Martha C Hawes

Interests

Research

My research focuses on fundamental new insights into mechanisms of plant and animal immune responses, and their potential applications in controlling infectious and autoimmune diseases among eukaryotes.

Teaching

Student research projects center on plant-microbe recognition and defense, and their implications in understanding human disease as well .

Courses

Scholarly Contributions

Journals/Publications

• Huskey, D. A., Curlango-Rivera, G., Root, R. A., Wen, F., Amistadi, M. K., Chorover, J., & Hawes, M. C. (2018). Trapping of lead (Pb) by corn and pea root border cells. PLANT AND SOIL, 430(1-2), 205-217.
• Wang, W., Curlango-Rivera, G., Xiong, Z., Turgeon, B. G., Hawes, M. C., & Huskey, D. (2018). A DNase from a fungal phytopathogen is a virulence factor likely deployed as counter defense against host-secreted extracellular DNA.. MBIO-02805, 18(R1), 10-25.
• Wen, F., Curlango-Rivera, G., Huskey, D. A., Xiong, Z., & Hawes, M. C. (2017). Visualization of extracellular DNA released during border cell separation from the root cap. AMERICAN JOURNAL OF BOTANY, 104(7), 970-978.
• Wen, F., Rivera, G. C., Huskey, D. A., Xiong, Z., & Hawes, M. C. (2017). Visualization of extracellular DNA released during border cell separation from the root cap. American Journal of botany, 104(5), 1-9. doi:doi.org/10.3732/ajb.1700142
• Hawes, M. C., McLain, J., Ramirez-Andreotta, M., Curlango-Rivera, G., Flores-Lara, Y., & Brigham, L. A. (2016). Extracellular Trapping of Soil Contaminants by Root Border Cells: New Insights into Plant Defense. AGRONOMY-BASEL, 6(1).
• Hawes, M. C., Tran, T., Allen, C., & McIntyre, A. (2016). Extracellular DNases of Ralstonia solanacearum modulate biofilms and facilitate bacterial wilt virulence. Environmental Microbiology, 252(5), 1-15. doi:doi:10.1111
• Hawes, M. C., Tran, T., McIntyre, A., & Allen, C. (2016). Escaping underground NETs : extracellular DNases degrade plant extracellular traps and contribute to virulence of the plant pathogenic bacterium Ralstonia solanacearum.. Plos Pathogens, 12(6), PLoS Pathog. 12(6):e1005686. doi:doi: 10.1371
• Hawes, M., Allen, C., Turgeon, B. G., Curlango-Rivera, G., Tran, T. M., Huskey, D. A., & Xiong, Z. (2016). Root Border Cells and Their Role in Plant Defense. ANNUAL REVIEW OF PHYTOPATHOLOGY, VOL 54, 54, 143-161.
• Tran, T. M., MacIntyre, A., Hawes, M., & Allen, C. (2016). Escaping Underground Nets: Extracellular DNases Degrade Plant Extracellular Traps and Contribute to Virulence of the Plant Pathogenic Bacterium Ralstonia solanacearum. PLOS PATHOGENS, 12(6).
• Tran, T. M., MacIntyre, A., Khokhani, D., Hawes, M., & Allen, C. (2016). Extracellular DNases of Ralstonia solanacearum modulate biofilms and facilitate bacterial wilt virulence. ENVIRONMENTAL MICROBIOLOGY, 18(11), 4103-4117.
• Hawes, M. C., Curlango-Rivera, G., Cho, I., Huskey, D., & Xiong, Z. (2014). Signals Controlling Extracellular Trap Formation in Plant and Animal Immune Responses. . Clinical Microbiology 3: 5-.. Clinical Microbiology, 3(5), 8-10.
• Hawes, M. C., Elquza, E., & Wen, F. (2015). Extracellular DNA: a bridge to cancer. Cancer Research, 15, 46-52.
• Hawes, M. C., Tollefson, S., Curlango-Rivera, G., Huskey, D., Pew, T., & Giacomelli, g. (2014). Altered carbon delivery from roots: rapid, sustained inhibition of border cell dispersal in response to compost water extracts. Tollefson SJ, Curlango-Rivera G, Huskey DA, Pew T, Giacomelli G, .. Plant and Soil.
• Hawes, M. C., Wen, F., & Elquza, E. (2015). Extracellular DNA: A Bridge to Cancer. CANCER RESEARCH, 75(20), 4260-4264.
• Tollefson, S. J., Curlango-Rivera, G., Huskey, D. A., Pew, T., Giacomelli, G., & Hawes, M. C. (2015). Altered carbon delivery from roots: rapid, sustained inhibition of border cell dispersal in response to compost water extracts. PLANT AND SOIL, 389(1-2), 145-156.
• Hawes, M. C., Wen, F., Curlango-rivera, G., & Brigham, L. (2014). Altered growth and root tip morphology in Pisum sativum L. in response to altered expression of a gene expressed in border cells.. Plant and Soil Volume: 377 Issue: 1-2 Pages: 179-187 Published: APR 2014, 377(1-2), 179-187.
• Wen, F., Brigham, L. A., Curlango-Rivera, G., Xiong, Z., & Hawes, M. C. (2014). Altered growth and root tip morphology in Pisum sativum L. in response to altered expression of a gene expressed in border cells. PLANT AND SOIL, 377(1-2), 179-187.
• Curlango-Rivera, G., Huskey, D. A., Mostafa, A., Kessler, J. O., Xiong, Z., & Hawes, M. C. (2013). INTRASPECIES VARIATION IN COTTON BORDER CELL PRODUCTION: RHIZOSPHERE MICROBIOME IMPLICATIONS. AMERICAN JOURNAL OF BOTANY, 100(9), 1706-1712.
• Curlango-Rivera, G., Huskey, D. A., Mostafa, A., Kessler, J. O., Xiong, Z., & Hawes, M. C. (2013). Intraspecies variation in cotton border cell production: Rhizosphere microbiome implications. American Journal of Botany, 100(9), 1706-1712.
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  PMID: 23942085;Abstract: Premise of the study: Border cells, which separate from the root cap, can comprise >90% of carbon-based exudates released into the rhizosphere, but may not provide a general source of nutrients for soil microorganisms. Instead, this population of specialized cells appears to function in defense of the root tip by an extracellular trapping process similar to that of mammalian white blood cells. Border cell production is tightly regulated, and direct tests of their impact on crop production have been hindered by lack of intraspecies variation. Methods: Border cell number, viability, and clumping were compared among 22 cotton cultivars. Slime layer "extracellular trap" production by border cells in response to copper chloride, an elicitor of plant defenses, was compared in two cultivars with divergent border cell production. Trapping of bacteria by border cells in these lines also was measured. Key results: Emerging roots of some cultivars produced more than 20 000 border cells per root, a 100% increase over previously reported values for this species. No differences in border cell morphology, viability, or clumping were found. Copper chloride-induced extracellular trap formation by border cells from a cultivar that produced 27 921 ± 2111 cells per root was similar to that of cells from a cultivar with 10 002 ± 614 cells, but bacterial trapping was reduced. Conclusions: Intraspecific variation in border cell production provides a tool to measure their impact on plant development in the laboratory, greenhouse, and field. Further research is needed to determine the basis for this variation, and its impact on rhizosphere community structure. © 2013 Botanical Society of America.
• Curlango-Rivera, G., Pew, T., D., H., Zhongguo, X., Naitong, Y. u., & Hawes, M. C. (2013). Measuring root disease suppression in response to a compost water extract. Phytopathology, 103(3), 255-260.
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  PMID: 23402629;Abstract: Commercial application of compost to prevent plant disease is hindered by variable performance. Here, we describe the use of a growth pouch assay to measure impact of a compost water extract (CWE) on root infection under controlled conditions. Most pea roots (≥95%) inoculated with Fusarium solani or Phoma pinodella spores rapidly develop a single local lesion in the region of elongation. In the presence of CWE, infection of pea roots grown in pouches was reduced by 93 to 100%. CWE used as a drench on pea seedlings grown in sand also resulted in 100% protection but, in a heavy clay soil, infection was reduced by
• Curlango-Rivera, G., Pew, T., VanEtten, H. D., Xiong, Z., Yu, N., & Hawes, M. C. (2013). Curlango-Rivera G, Pew T, VanEtten HD, Xiong Z, Yu N, Hawes MC (2013) Measuring root disease suppression in response to a compost water extract. Phytopathology 103:255-260.. Phytopathology, 103(1), 255-260.
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  research paper
• Curlango-Rivera, G., Pew, T., VanEtten, H. D., Zhongguo, X., Yu, N., & Hawes, M. C. (2013). Measuring Root Disease Suppression in Response to a Compost Water Extract. PHYTOPATHOLOGY, 103(3), 255-260.
• Driouich, A., Follet-Gueye, M., Vicre-Gibouin, M., & Hawes, M. (2013). Root border cells and secretions as critical elements in plant host defense. CURRENT OPINION IN PLANT BIOLOGY, 16(4), 489-495.
• Driouich, A., Follet-Gueye, M., Vicré-Gibouin, M., & Hawes, M. (2013). Root border cells and secretions as critical elements in plant host defense. Current Opinion in Plant Biology, 16(4), 489-495.
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  PMID: 23856080;Abstract: Border cells and border-like cells are released from the root tip as individual cells and small aggregates, or as a group of attached cells. These are viable components of the root system that play a key role in controlling root interaction with living microbes of the rhizosphere. As their separation from root tip proceeds, the cells synthesize and secrete a hydrated mucilage that contains polysaccharides, secondary metabolites, antimicrobial proteins and extracellular DNA (exDNA). This exDNA-based matrix seems to function in root defense in a way similar to that of recently characterized neutrophil extracellular traps (NETs) in mammalian cells. This review discusses the role of the cells and secreted compounds in the protection of root tip against microbial infections. © 2013 Elsevier Ltd.
• Hawes, M. C., Wen, F., Brigham, L. A., Curlango-Rivera, G., & Xiong, Z. (2013). Wen F, Brigham LA, Curlango-Rivera G, Xiong Z, Hawes MC (2013) Altered growth and root tip morphology in response to altered expression of a gene expressed in border cells.. Plant and Soil, 373(5), 13-18.
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  Research paper
• Wen, F., Brigham, L. A., Curlango-Rivera, G., Xiong, Z., & Hawes, M. C. (2013). Altered growth and root tip morphology in Pisum sativum L. in response to altered expression of a gene expressed in border cells. Plant and Soil, 1-9.
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  Abstract: Background and aims: Recent studies suggest that root border cells function in defense of the root by an extracellular DNA-based trapping mechanism similar to that described in mammalian white blood cells. Genes controlling the specialized properties of border cells as they detach from the root tip therefore are of interest. Methods: mRNA differential display was used to identify Brd13, a sequence expressed in border cells but not other root tissues. RNase protection and mRNA Northern blot analyses, and reporter gene expression under the control of the Brd13 promoter in transgenic hairy roots were used to confirm localized expression. Phenotype analysis of transgenic hairy roots expressing Brd13 antisense mRNA was carried out. Results: Brd13 was expressed constitutively in border cells but not in leaves, stems, or roots without border cells. The predicted protein shares sequence similarity with flavin-binding proteins. Transgenic hairy roots expressing Brd13 antisense mRNA exhibited abnormal growth and morphology. Conclusions: We report here that altered expression of a putative flavin-binding protein in border cells resulted in altered root development. Flavin-binding proteins play key roles in development, defense, and local auxin biosynthesis. The Brd13 gene and its promoter may be useful in creating defined changes in root development and defense. © 2013 Springer Science+Business Media Dordrecht.
• Hawes, M. C., Curlango-Rivera, G., Xiong, Z., & Kessler, J. O. (2012). Roles of root border cells in plant defense and regulation of rhizosphere microbial populations by extracellular DNA 'trapping'. PLANT AND SOIL, 355(1-2), 1-16.
• Hawes, M. C., Curlango-Rivera, G., Xiong, Z., & Kessler, J. O. (2012). Roles of root border cells in plant defense and regulation of rhizosphere microbial populations by extracellular DNA 'trapping'. Plant and Soil, 355(1-2), 1-16.
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  Abstract: Background: As roots penetrate soil, specialized cells called 'border cells' separate from root caps and contribute a large proportion of exudates forming the rhizosphere. Their function has been unclear. Recent findings suggest that border cells act in a manner similar to that of white blood cells functioning in defense. Histone-linked extracellular DNA (exDNA) and proteins operate as 'neutrophil extracellular traps' to attract and immobilize animal pathogens. DNase treatment reverses trapping and impairs defense, and mutation of pathogen DNase results in loss of virulence. Scope: Histones are among a group of proteins secreted from living border cells. This observation led to the discovery that exDNA also functions in defense of root caps. Experiments revealed that exDNA is synthesized and exported into the surrounding mucilage which attracts, traps and immobilizes pathogens in a host-microbe specific manner. When this plant exDNA is degraded, the normal resistance of the root cap to infection is abolished. Conclusions: Research to define how exDNA may operate in plant immunity is needed. In the meantime, the specificity and stability of exDNA and its association with distinct microbial species may provide an important new tool to monitor when, where, and how soil microbial populations become established as rhizosphere communities. © 2012 Springer Science+Business Media B.V.
• Hawes, M., Curlango-Rivera, G., Xiong, Z., & Kessler, J. O. (2012). Extracellular DNA in defense of plant cells: rooting out novel discoveries.. International Innovation, 3, 15.
• Cannesan, M. A., Gangneux, C., Lanoue, A., Giron, D., Laval, K., Hawes, M., Driouich, A., & Vicré-Gibouin, M. (2011). Association between border cell responses and localized root infection by pathogenic Aphanomyces euteiches. Annals of Botany, 108(3), 459-469.
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  PMID: 21807690;PMCID: PMC3158693;Abstract: •Background and Aims: The oomycete Aphanomyces euteiches causes up to 80% crop loss in pea (Pisum sativum). Aphanomyces euteiches invades the root system leading to a complete arrest of root growth and ultimately to plant death. To date, disease control measures are limited to crop rotation and no resistant pea lines are available. The present study aims to get a deeper understanding of the early oomyceteplant interaction at the tissue and cellular levels. •Methods: Here, the process of root infection by A. euteiches on pea is investigated using flow cytometry and microscopic techniques. Dynamic changes in secondary metabolism are analysed with high-performance liquid chromatography with diode-array detection. •Key Results: Root infection is initiated in the elongation zone but not in the root cap and border cells. Border-cell production is significantly enhanced in response to root inoculation with changes in their size and morphology. The stimulatory effect of A. euteiches on border-cell production is dependent on the number of oospores inoculated. Interestingly, border cells respond to pathogen challenge by increasing the synthesis of the phytoalexin pisatin. •Conclusions: Distinctive responses to A. euteiches inoculation occur at the root tissue level. The findings suggest that root border cells in pea are involved in local defence of the root tip against A. euteiches. Root border cells constitute a convenient quantitative model to measure the molecular and cellular basis of plantmicrobe interactions. © The Author 2011. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved.
• Cannesan, M., Gangneux, C., Lanoue, A., Hawes, M., Driouich, A., & VicreM, . (2011). Association between border cell responses and localized root infection by pathogenic Aphanomyces euteiches. ANNALS OF BOTANY, 108(3), 459-469.
• Curlango-Rivera, G., & Hawes, M. (2011). Root tips moving through soil: an intrinsic vulnerability.. Plant Signal Behav, 6(6), 726-727.
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  DOI: 10.1016/j.plantsci.2011.02.007
• Curlango-Rivera, G., & Hawes, M. C. (2011). Root tips moving through soil: An intrinsic vulnerability. Plant Signaling and Behavior, 6(5), 726-727.
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  PMID: 21455030;PMCID: PMC3172849;Abstract: Root elongation occurs by the generation of new cells from meristematic tissue within the apical 1-2 mm region of root tips. Therefore penetration of the soil environment is carried out by newly synthesized plant tissue, whose cells are inherently vulnerable to invasion by pathogens. This conundrum, on its face, would seem to reflect an intolerable risk to the successful establishment of root systems needed for plant life. Yet root tip regions housing the meristematic tissues repeatedly have been found to be free of microbial infection and colonization. Even when spore germination, chemotaxis, and/or growth of pathogens are stimulated by signals from the root tip, the underlying root tissue can escape invasion. Recent insights into the functions of root border cells, and the regulation of their production by transient exposure to external signals, may shed light on long-standing observations. © 2011 Landes Bioscience.
• Hawes, M. C., Curlango-Rivera, G., Wen, F., White, G. J., VanEtten, H. D., & Xiong, Z. (2011). Extracellular DNA: The tip of root defenses?. PLANT SCIENCE, 180(6), 741-745.
• Hawes, M. C., Curlango-Rivera, G., Wen, F., White, G. J., VanEtten, H. D., & Xiong, Z. (2011). Extracellular DNA: The tip of root defenses?. Plant Science, 180(6), 741-745.
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  PMID: 21497709;Abstract: This review discusses how extracellular DNA (exDNA) might function in plant defense, and at what level(s) of innate immunity this process might operate. A new role for extracellular factors in mammalian defense has been described in a series of studies. These studies reveal that cells including neutrophils, eosinophils, and mast cells produce 'extracellular traps' (ETs) consisting of histone-linked exDNA. When pathogens are attracted to such ETs, they are trapped and killed. When the exDNA component of ETs is degraded, trapping is impaired and resistance against invasion is reduced. Conversely, mutation of microbial genes encoding exDNases that degrade exDNA results in loss of virulence. This discovery that exDNases are virulence factors opens new avenues for disease control. In plants, exDNA is required for defense of the root tip. Innate immunity-related proteins are among a group of >100 proteins secreted from the root cap and root border cell populations. Direct tests revealed that exDNA also is rapidly synthesized and exported from the root tip. When this exDNA is degraded by the endonuclease DNase 1, root tip resistance to fungal infection is lost; when the polymeric structure is degraded more slowly, by the exonuclease BAL31, loss of resistance to fungal infection is delayed accordingly. The results suggest that root border cells may function in a manner analogous to that which occurs in mammalian cells. © 2011.
• Hawes, M., Curlango-Rivera, G., WenF, ., & et, a. l. (2011). Extracellular DNA: The tip of root defenses. Plant Science, 180(6), 741-745.
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  DOI: 10.1093/aob/mcr177
• Curlango-Rivera, G., Duclos, D. V., Ebolo, J. J., & Hawes, M. C. (2010). Transient exposure of root tips to primary and secondary metabolites: Impact on root growth and production of border cells. PLANT AND SOIL, 332(1-2), 267-275.
• Curlango-Rivera, G., Duclos, D. V., Ebolo, J. J., & Hawes, M. C. (2010). Transient exposure of root tips to primary and secondary metabolites: Impact on root growth and production of border cells. Plant and Soil, 332(1), 267-275.
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  Abstract: Here we describe the use of Pisum sativum L. as a model system to measure how short-term treatment of root tips with soluble metabolites can influence root growth and release of root exudates. The results revealed that even a 3-minute exposure of root tips to metabolites normally released from roots into the rhizosphere (e. g. rhamnose, ferulic acid, salicylic acid) can significantly influence root growth without affecting production of border cells and associated exudates. Conversely, products including caffeine, saccharide lactone, and pisatin alter production of border cells, without affecting root growth. Understanding how root-derived and exogenous metabolites can selectively impact root function may yield benefits in crop production, especially in greenhouse agriculture systems where growing roots can be exposed to a significant accumulation of plant exudates. © 2010 Springer Science+Business Media B.V.
• Brooks, W. J., Krupinski, E. A., & Hawes, M. C. (2009). Reversal of childhood idiopathic scoliosis in an adult, without surgery: A case report and literature review. Scoliosis, 4.
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  PMID: 20003501;PMCID: PMC2808297;Abstract: Background: Some patients with mild or moderate thoracic scoliosis (Cobb angle 10 degree decrease in Cobb angle magnitude of the primary thoracic curvature.Conclusion: This report documents improved chest wall function and resolution of respiratory symptoms in response to nonsurgical approaches in an adult female, diagnosed at age eleven years with idiopathic scoliosis. © 2009 Brooks et al; licensee BioMed Central Ltd.
• Curlango-Rivera, G., Albala, G., Kemp, J. P., Duclos, D. V., & Hawes, M. C. (2009). Contribution of the root cap to soil fertility: Extracellular plant lectins. Soil Fertility, 65-79.
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  Abstract: Lectins are proteins with multiple sites that bind specific sugars and therefore can agglutinate cells or other substrates with those sugars on the surface. This property is exploited in detecting human ABO blood type, defined based on the presence of distinct surface sugars that result in agglutination of blood cells in response to appropriate lectins. This capacity to bind to specific sites on cell surfaces is of interest for its potential in treating human diseases including cancer, AIDS, and diabetes. In plants, species-specific lectins are secreted from root tips into the extracellular environment of agronomically important crops including legumes and cereals. The function, stability and distribution of these proteins after export from root cells into the extracellular environment remain unexplored. Experiments to examine predictions of the hypothesis that root-secreted lectins influence soil structure and fertility, rhizosphere microbial communities, and root nutrient cycling are warranted. © 2009 by Nova Science Publishers, Inc. All rights reserved.
• Hawes, M., & Ronald, P. (2009). Focus: Plant Interactions with Bacterial Pathogens. PLANT PHYSIOLOGY, 150(4), 1621-1622.
• Hawes, M., & Ronald, P. (2009). Focus: Plant interactions with bacterial pathogens. Plant Physiology, 150(4), 1621-1622.
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  PMID: 19656918;PMCID: PMC2719114;
• Wen, F., White, G. J., VanEtten, H. D., Xiong, Z., & Hawes, M. C. (2009). Extracellular DNA Is Required for Root Tip Resistance to Fungal Infection. PLANT PHYSIOLOGY, 151(2), 820-829.
• Wen, F., White, G. J., Vanetten, H. D., Xiong, Z., & Hawes, M. C. (2009). Extracellular DNA is required for root tip resistance to fungal infection. Plant Physiology, 151(2), 820-829.
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  PMID: 19700564;PMCID: PMC2754639;Abstract: Plant defense involves a complex array of biochemical interactions, many of which occur in the extracellular environment. The apical 1- to 2-mm root tip housing apical and root cap meristems is resistant to infection by most pathogens, so growth and gravity sensing often proceed normally even when other sites on the root are invaded. The mechanism of this resistance is unknown but appears to involve a mucilaginous matrix or "slime" composed of proteins, polysaccharides, and detached living cells called "border cells." Here, we report that extracellular DNA (exDNA) is a component of root cap slime and that exDNA degradation during inoculation by a fungal pathogen results in loss of root tip resistance to infection. Most root tips (.95%) escape infection even when immersed in inoculum from the root-rotting pathogen Nectria haematococca. By contrast, 100% of inoculated root tips treated with DNase I developed necrosis. Treatment with BAL31, an exonuclease that digests DNA more slowly than DNase I, also resulted in increased root tip infection, but the onset of infection was delayed. Control root tips or fungal spores treated with nuclease alone exhibited normal morphology and growth. Pea (Pisum sativum) root tips incubated with [32P]dCTP during a 1-h period when no cell death occurs yielded root cap slime containing 32P-labeled exDNA. Our results suggest that exDNA is a previously unrecognized component of plant defense, an observation that is in accordance with the recent discovery that exDNA from white blood cells plays a key role in the vertebrate immune response against microbial pathogens. © 2009 American Society of Plant Biologists.
• Wen, F., Woo, H. H., Pierson, E. A., Eldhuset, T. D., Fossdal, C. G., Nagy, N. E., & Hawes, M. C. (2009). Synchronous elicitation of development in root caps induces transient gene expression changes common to legume and gymnosperm species. Plant Molecular Biology Reporter, 27(1), 58-68.
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  Abstract: Root cap development in cereals and legumes is self-regulated by a repressor that accumulates in the extracellular environment, and immersing the root tip into water results in renewed cap development. By exploiting this phenomenon, root cap mitosis and differentiation can be synchronously induced among populations. In Pisum sativum L., messenger RNA (mRNA) differential display revealed changes in expression of approximately 1% of the sample mRNA population within minutes of induced cap turnover. This profile changes sequentially over a period of 30 min, then stabilizes. Microarray analysis of Medicago truncatula root caps confirmed changes in expression of approximately 1% of the target population, within minutes. A cell specific marker for cap turnover exhibited the same temporal and spatial expression profile in the gymnosperm species Norway spruce (Picea abies) as in pea. Induced cap development provides a means to profile cell-specific gene expression among phylogenetically diverse species from the early moments of mitosis and cellular differentiation. © Springer Science + Business Media, LLC 2008.
• Hawes, M. C., & O'Brien, J. P. (2008). A century of spine surgery: What can patients expect?. DISABILITY AND REHABILITATION, 30(10), 808-817.
• Hawes, M. C., & O'Brien, J. P. (2008). A century of spine surgery: What can patients expect?. Disability and Rehabilitation, 30(10), 808-817.
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  PMID: 18432439;Abstract: Purpose. To evaluate the hypothesis that spinal fusion surgery is an effective method to address spinal deformity-associated clinical problems, including magnitude of curvature (Cobb angle), pulmonary dysfunction, and pain. Method. A systematic review was carried out using Science Citation Index (SCI) Expanded (1900 - present), Social Sciences Citation Index (1956 - present), Arts and Humanities Citation Index (1965 - present), Medline (1950 - present) and PubMed Central databases (1887 - present) to access information regarding efficacy of spine surgery in preventing or improving the health and function of patients diagnosed with scoliosis in adolescence. Results. Since 1950, more than 12,600 articles on scoliosis have been published, and nearly 50% (5721) focus on methods, rationale, outcome, and complications of surgical intervention. Among these, 82 articles have documented outcome for groups of ≥10 patients, treated for adolescent idiopathic scoliosis, and followed for at least 2 years after treatment. These data provide an overview of the impact of spine surgery on scoliosis for 5780 patients as surgery methods and approaches have evolved. Conclusions. For most patients, a reduced magnitude of spinal curvature can be achieved through one or more spinal fusion surgeries. There is no evidence to support the premise that this result is correlated with improved pulmonary function or reduced pain.
• Hawes, M. C., & O'Brien, J. P. (2008). Scoliosis and the human genome project.. Studies in health technology and informatics, 135, 97-111.
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  PMID: 18401084;Abstract: Understanding the cause of a disease or disorder is key to developing effective and humane strategies for early intervention and treatment. School screening programs have made it possible to demonstrate the high prevalence of childhood scoliosis, worldwide, and to reliably identify spinal curvatures early in the disease process before progression to a fixed structural deformity. Unfortunately, effective early interventions have not been established. Developing strategies to prevent scoliosis has been compromised, in general, by lack of understanding of its causes on a case by case basis. Information about genetic loci associated with disorders including scoliosis is emerging rapidly, since completion of the human genome sequence in 2003. These data can be used to identify children at high risk for developing spinal deformities and to design strategies for prevention.
• Weiss, H., Negrini, S., Rigo, M., Kotwicki, T., Hawes, M. C., Grivas, T. B., Maruyama, T., & Landauer, F. (2008). Indications for conservative management of scoliosis (SOSORT guidelines).. Studies in health technology and informatics, 135, 164-170.
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  PMID: 18401089;Abstract: This guideline has been discussed by the SOSORT guideline committee prior to the SOSORT consensus meeting in Milan, January 2005 and published in its first version on the SOSORT homepage: http://www.sosort.org/meetings.php. After the meeting it again has been discussed by the members of the SOSORT guideline committee to establish the final 2005 version submitted to Scoliosis, the official Journal of the society, in December 2005. This chapter is a republication from the original paper published in "Scoliosis" BioMed journal and it is included in this book due to its high importance.
• Wen, F., Celoy, R. M., Nguyen, T., Zeng, W., Keegstra, K., Immerzeel, P., Pauly, M., & Hawes, M. C. (2008). Inducible expression of Pisum sativum xyloglucan fucosyltransferase in the pea root cap meristem, and effects of antisense mRNA expression on root cap cell wall structural integrity. Plant Cell Reports, 27(7), 1125-1135.
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  PMID: 18347802;PMCID: PMC2755773;Abstract: Mitosis and cell wall synthesis in the legume root cap meristem can be induced and synchronized by the nondestructive removal of border cells from the cap periphery. Newly synthesized cells can be examined microscopically as they differentiate progressively during cap development, and ultimately detach as a new population of border cells. This system was used to demonstrate that Pisum sativum L. fucosyl transferase (PsFut1) mRNA expression is strongly expressed in root meristematic tissues, and is induced >2-fold during a 5-h period when mitosis in the root cap meristem is increased. Expression of PsFut1 antisense mRNA in pea hairy roots under the control of the CaMV35S promoter, which exhibits meristem localized expression in pea root caps, resulted in a 50-60% reduction in meristem localized endogenous PsFut1 mRNA expression measured using whole mount in situ hybridization. Changes in gross levels of cell wall fucosylated xyloglucan were not detected, but altered surface localization patterns were detected using whole mount immunolocalization with CCRC-M1, an antibody that recognizes fucosylated xyloglucan. Emerging hairy roots expressing antisense PsFut1 mRNA appeared normal macroscopically but scanning electron microscopy of tissues with altered CCRC-M1 localization patterns revealed wrinkled, collapsed cell surfaces. As individual border cells separated from the cap periphery, cell death occurred in correlation with extrusion of cellular contents through breaks in the wall. © 2008 Springer-Verlag.
• Wen, F., Celoy, R., Price, I., Ebolo, J. J., & Hawes, M. C. (2008). Identification and characterization of a rhizosphere β-galactosidase from Pisum sativum L.. Plant and Soil, 304(1-2), 133-144.
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  Abstract: Plant enzyme activities in the rhizosphere potentially are a resource for improved plant nutrition, soil fertility, bioremediation, and disease resistance. Here we report that a border cell specific β-galactosidase is secreted into the acidic extracellular environment surrounding root tips of pea, as well as bean, alfalfa, barrel medic, sorghum, and maize. No enzyme activity was detected in radish and Arabidopsis, species that do not produce viable border cells. The secreted enzyme activity was inhibited by galactose and 2-phenylethyl 1-thio-β-d-galactopyranoside (PETG) at concentrations that altered root growth without causing cell death. A tomato galactanase encoding gene was used as a probe to isolate a full length pea cDNA clone (BRDgal1) from a root cap-border cell cDNA library. Southern blot analysis using full length BRDgal1 as a probe revealed 1-2 related sequences within the pea genome. BRDgal1 mRNA expression was analysed by whole mount in situ hybridization (WISH) and found to occur in the outermost peripheral layer of the cap and in suspensions of detached border cells. No expression was detected within the body of the root cap. Repeated efforts to develop viable hairy root clones expressing BRDgal1 antisense mRNA under the control of the CaMV35S promoter, whose expression in the root cap is limited to cells at the root cap periphery only during root emergence, were unsuccessful. These data suggest that altered expression of this enzyme is deleterious to early root development. © 2007 Springer Science+Business Media B.V.
• Grivas, T. B., Wade, M. H., Negrini, S., O'Brien, J. P., Maruyama, T., Hawes, M. C., Rigo, M., Weiss, H. R., Kotwicki, T., Vasiliadis, E. S., Sulam, L., & Neuhous, T. (2007). SOSORT consensus paper: School screening for scoliosis. Where are we today?. Scoliosis, 2(1).
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  PMID: 18039374;PMCID: PMC2228277;Abstract: This report is the SOSORT Consensus Paper on School Screening for Scoliosis discussed at the 4th International Conference on Conservative Management of Spinal Deformities, presented by SOSORT, on May 2007. The objectives were numerous, 1) the inclusion of the existing information on the issue, 2) the analysis and discussion of the responses by the meeting attendees to the twenty six questions of the questionnaire, 3) the impact of screening on frequency of surgical treatment and of its discontinuation, 4) the reasons why these programs must be continued, 5) the evolving aim of School Screening for Scoliosis and 6) recommendations for improvement of the procedure. © 2007 Grivas et al; licensee BioMed Central Ltd.
• Wen, F., Curlango-Rivera, G., & Hawes, M. C. (2007). Proteins among the polysaccharides: A new perspective on root cap Slime. Plant Signaling and Behavior, 2(5), 410-412.
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  PMID: 19704617;PMCID: PMC2634230;
• Wen, F., VanEtten, H. D., Tsaprailis, G., & Hawes, M. C. (2007). Extracellular proteins in pea root tip and border cell exudates. PLANT PHYSIOLOGY, 143(2), 773-783.
• Wen, F., Vanetten, H. D., Tsaprailis, G., & Hawes, M. C. (2007). Extracellular proteins in pea root tip and border cell exudates. Plant Physiology, 143(2), 773-783.
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  PMID: 17142479;PMCID: PMC1803736;Abstract: Newly generated plant tissue is inherently sensitive to infection. Yet, when pea (Pisum sativum) roots are inoculated with the pea pathogen, Nectria haematococca, most newly generated root tips remain uninfected even though most roots develop lesions just behind the tip in the region of elongation. The resistance mechanism is unknown but is correlated spatially with the presence of border cells on the cap periphery. Previously, an array of >100 extracellular proteins was found to be released while border cell separation proceeds. Here we report that protein secretion from pea root caps is induced in correlation with border cell separation. When this root cap secretome was proteolytically degraded during inoculation of pea roots with N. haematococca, the percentage of infected root tips increased from 4% ± 3% to 100%. In control experiments, protease treatment of conidia or roots had no effect on growth and development of the fungus or the plant. A complex of >100 extracellular proteins was confirmed, by multidimensional protein identification technology, to comprise the root cap secretome. In addition to defense-related and signaling enzymes known to be present in the plant apoplast were ribosomal proteins, 14-3-3 proteins, and others typically associated with intracellular localization but recently shown to be extracellular components of microbial biofilms. We conclude that the root cap, long known to release a high molecular weight polysaccharide mucilage and thousands of living cells into the incipient rhizosphere, also secretes a complex mixture of proteins that appear to function in protection of the root tip from infection. © 2006 American Society of Plant Biologists.
• Woo, H., Jeong, B. R., Hirsch, A. M., & Hawes, M. C. (2007). Characterization of Arabidopsis AtUGT85A and AtGUS gene families and their expression in rapidly dividing tissues. GENOMICS, 90(1), 143-153.
• Woo, H., Jeong, B. R., Hirsch, A. M., & Hawes, M. C. (2007). Characterization of Arabidopsis AtUGT85A and AtGUS gene families and their expression in rapidly dividing tissues. Genomics, 90(1), 143-153.
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  PMID: 17498920;PMCID: PMC2064910;Abstract: In humans, uridine 5′-diphosphate glucuronosyltransferase (UGT) operates in opposition to glucuronidase (GUS) to control activity of diverse metabolites such as hormones by reversible conjugation with glucuronic acid. Previous data revealed that, as in mammals, these enzymes are required for plant life in that a UGT from Pisum sativum (PsUGT1) controls plant development by opposing endogenous GUS activity thereby modulating the duration of the cell cycle. Here we report that a small family of genes (AtUGT85A1, 2, 3, 4, 5, and 7) homologous to pea PsUGT1 exists in the Arabidopsis genome. The AtUGT85A-encoded proteins are predicted to be membrane-associated enzymes. Three genes (AtGUS1, AtGUS2, and AtGUS3) that are homologous to a GUS-encoding gene from Scutellaria baicalensis were identified. The AtGUS-encoded proteins are predicted to be secretory (AtGUS1) and membrane-associated (AtGUS2 and AtGUS3) enzymes. Both AtUGT85A and AtGUS genes, like PsUGT1, exhibit localized, tissue-specific expression, mainly in areas of active cell division with possible involvement in cell cycle regulation. © 2007 Elsevier Inc. All rights reserved.
• Woo, H., Jeong, B. R., Koo, K. B., Choi, J. W., Hirsch, A. M., & Hawes, M. C. (2007). Modifying expression of closely related UDP-glycosyltransferases from pea and Arabidopsis results in altered root development and function. Physiologia Plantarum, 130(2), 250-260.
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  Abstract: Glycosyltransferases (GTs) play diverse roles in cellular metabolism by modifying the activities of structural and regulatory metabolites. Previous studies indicated that a Pisum sativum UDP-glycosyltransferase (PsUGT1) is essential for plant development, and suggested a role for this enzyme in the regulation of the cell division cycle. Here we report that recombinant PsUGT1 expressed in vitro exhibits activity on diverse flavonoids including kaempferol. In Arabidopsis expressing PsUGT1, gravity sensing is impaired, and this loss of function is corrected by exogenous addition of kaempferol. HPLC of tissue extracts of Arabidopsis expressing PsUGT1 revealed the accumulation of glycosides of kaempferol, but not of other related flavonoids. A search of the NCBI gene bank (http://www.ncbi.nlm.nih.gov/) using PsUGT1 revealed that six genes from the Arabidopsis AtUGT85A subfamily show similarities both in DNA and protein sequences (Woo et al. 2007). In the current study, we examined the hypothesis that one or more members of this family, like PsUGT1, is required for Arabidopsis development. Altered expression of AtUGT85A7, but not other AtUGT85A subfamily members, resulted in changes in life cycle, leaf morphology, auxin response, and root development, including loss of gravity sensing. The phenotypes of plants where AtUGT85A7 gene expression was suppressed, by RNAi mutagenesis, were very similar to those occurring in plants with altered expression of PsUGT1. © Physiologia Plantarum 2007.
• Hamamoto, L., Hawes, M. C., & Rost, T. L. (2006). The production and release of living root cap border cells is a function of root apical meristem type in dicotyledonous angiosperm plants. Annals of Botany, 97(5), 917-923.
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  PMID: 16488922;PMCID: PMC2803423;Abstract: • Background and Aims: The root apical meristems (RAM) of flowering plant roots are organized into recognizable pattern types. At present, there are no known ecological or physiological benefits to having one RAM organization type over another. Although there are phylogenetic distribution patterns in plant groups, the possible evolutionary advantages of different RAM organization patterns are not understood. Root caps of many flowering plant roots are known to release living border cells into the rhizosphere, where the cells are believed to have the capacity to alter conditions in the soil and to interact with soil micro-organisms. Consequently, high rates of border cell production may have the potential to benefit plant growth and development greatly, and to provide a selective advantage in certain soil environments. This study reports the use of several approaches to elucidate the anatomical and developmental relationships between RAM organization and border cell production. • Methods: RAM types from many species were compared with numbers of border cells released in those species. In addition, other species were grown, fixed and sectioned to verify their organization type and capacity to produce border cells. Root tips were examined microscopically to characterize their pattern and some were stained to determine the viability of root cap cells. • Key Results: The first report of a correlation between RAM organization type and the production and release of border cells is provided: species exhibiting open RAM organization produce significantly more border cells than species exhibiting closed apical organization. Roots with closed apical organization release peripheral root cap cells in sheets or large groups of dead cells, whereas root caps with open organization release individual living border cells. • Conclusions: This study, the first to document a relationship between RAM organization, root cap behaviour and a possible ecological benefit to the plant, may yield a framework to examine the evolutionary causes for the diversification of RAM organization types across taxa. © The Author 2006. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved.
• Hawes, M. (2006). Impact of spine surgery on signs and symptoms of spinal deformity. Developmental Neurorehabilitation, 9(4), 318-339.
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  Abstract: Paediatric scoliosis is associated with signs and symptoms including reduced pulmonary function, increased pain and impaired quality of life, all of which worsen during adulthood, even when the curvature remains stable. Spinal fusion has been used as a treatment for nearly 100 years. In 1941, the American Orthopedic Association reported that for 70% of patients treated surgically, outcome was fair or poor: an average 65% curvature correction was reduced to 27% at>2 year follow-up and the torso deformity was unchanged or worse. Outcome was worse in children treated surgically before age 10, despite earlier intervention. Today, a reduced magnitude of curvature obtained by spinal fusion in adolescence can be maintained for decades. However, successful surgery still does not eliminate spinal curvature and it introduces irreversible complications whose long-term impact is poorly understood. For most patients there is little or no improvement in pulmonary function. Some report improved pain after surgery, some report no improvement and some report increased pain. The rib deformity is eliminated only by rib resection which can dramatically reduce respiratory function even in healthy adolescents. Outcome for pulmonary function and deformity is worse in patients treated surgically before the age of 10 years, despite earlier intervention. Research to develop effective non-surgical methods to prevent progression of mild, reversible spinal curvatures into complex, irreversible structural deformities, is long overdue. © 2006 Informa UK Ltd All rights reserved.
• Hawes, M. (2006). Impact of spine surgery on signs and symptoms of spinal deformity. Pediatric Rehabilitation, 318-339.
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  PMID: 17111548;Abstract: Paediatric scoliosis is associated with signs and symptoms including reduced pulmonary function, increased pain and impaired quality of life, all of which worsen during adulthood, even when the curvature remains stable. Spinal fusion has been used as a treatment for nearly 100 years. In 1941, the American Orthopedic Association reported that for 70% of patients treated surgically, outcome was fair or poor: an average 65% curvature correction was reduced to 27% at >2 year follow-up and the torso deformity was unchanged or worse. Outcome was worse in children treated surgically before age 10, despite earlier intervention. Today, a reduced magnitude of curvature obtained by spinal fusion in adolescence can be maintained for decades. However, successful surgery still does not eliminate spinal curvature and it introduces irreversible complications whose long-term impact is poorly understood. For most patients there is little or no improvement in pulmonary function. Some report improved pain after surgery, some report no improvement and some report increased pain. The rib deformity is eliminated only by rib resection which can dramatically reduce respiratory function even in healthy adolescents. Outcome for pulmonary function and deformity is worse in patients treated surgically before the age of 10 years, despite earlier intervention. Research to develop effective non-surgical methods to prevent progression of mild, reversible spinal curvatures into complex, irreversible structural deformities, is long overdue. © 2006 Informa UK Ltd.
• Hawes, M. C., & O'Brien, J. P. (2006). The transformation of spinal curvature into spinal deformity: Pathological processes and implications for treatment. Scoliosis, 1(1).
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  Abstract: Background: This review summarizes what is known about the pathological processes (e.g. structural and functional changes), by which spinal curvatures develop and evolve into spinal deformities. Methods: Comprehensive review of articles (English language only) published on 'scoliosis,' whose content yielded data on the pathological changes associated with spinal curvatures. Medline, Science Citation Index and other searches yielded > 10,000 titles each of which was surveyed for content related to 'pathology' and related terms such as 'etiology,' 'inheritance,' 'pathomechanism,' 'signs and symptoms.' Additional resources included all books published on 'scoliosis' and available through the Arizona Health Sciences Library, Interlibrary Loan, or through direct contact with the authors or publishers. Results: A lateral curvature of the spine-'scoliosis'-can develop in association with postural imbalance due to genetic defects and injury as well as pain and scarring from trauma or surgery. Irrespective of the factor that triggers its appearance, a sustained postural imbalance can result, over time, in establishment of a state of continuous asymmetric loading relative to the spinal axis. Recent studies support the longstanding hypothesis that spinal deformity results directly from such postural imbalance, irrespective of the primary trigger, because the dynamics of growth within vertebrae are altered by continuous asymmetric mechanical loading. These data suggest that, as long as growth potential remains, evolution of a spinal curvature into a spinal deformity can be prevented by reversing the state of continuous asymmetric loading. Conclusion: Spinal curvatures can routinely be diagnosed in early stages, before pathological deformity of the vertebral elements is induced in response to asymmetric loading. Current clinical approaches involve 'watching and waiting' while mild reversible spinal curvatures develop into spinal deformities with potential to cause symptoms throughout life. Research to define patient-specific mechanics of spinal loading may allow quantification of a critical threshold at which curvature establishment and progression become inevitable, and thereby yield strategies to prevent development of spinal deformity. © 2006 Hawes and O'Brien; licensee BioMed Central Ltd.
• Weiss, H., Negrini, S., Hawes, M. C., Rigo, M., Kotwicki, T., Grivas, T. B., & Maruyama, T. (2006). Physical exercises in the treatment of idiopathic scoliosis at risk of brace treatment - SOSORT consensus paper 2005. Scoliosis, 1(1).
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  Abstract: Background: Based on a recognized need for research to examine the premise that nonsurgical approaches can be used effectively to treat signs and symptoms of scoliosis, a scientific society on scoliosis orthopaedic and rehabilitation treatment (SOSORT) was established in Barcelona in 2004. SOSORT has a primary goal of implementing multidisciplinary research to develop quantitative, objective data to address the role of conservative therapies in the treatment of scoliosis. This international working group of clinicians and scientists specializing in treatment of scoliosis met in Milan, Italy in January 2005. Methods: As a baseline for developing a consensus for language and goals for proposed multicenter clinical studies, we developed questionnaires to examine current beliefs, before and after the meeting, regarding (1) the aims of physical exercises; (2) standards of treatment; and (3) the impact of such treatment performed by specialists in the field. Results: The responses to the questionnaires show that, in principle, specialists in scoliosis physiotherapy do not disagree and that several features can be regarded, currently, as standard features in the rehabilitation of scoliosis patients. These features include autocorrection in 3D, training in ADL, stabilizing the corrected posture, and patient education. © 2006 Weiss et al; licensee BioMed Central Ltd.
• Weiss, H., Negrini, S., Rigo, M., Kotwicki, T., Hawes, M. C., Grivas, T. B., Maruyama, T., & Landauer, F. (2006). Indications for conservative management of scoliosis (guidelines). Scoliosis, 1(1).
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  Abstract: This guideline has been discussed by the SOSORT guideline committee prior to the SOSORT consensus meeting in Milan, January 2005 and published in its first version on the SOSORT homepage: http://www.sosort.org/meetings.php. After the meeting it again has been discussed by the members of the SOSORT guideline committee to establish the final 2005 version submitted to Scoliosis, the official Journal of the society, in December 2005. © 2006 Weiss et al; licensee BioMed Central Ltd.
• Gunawardena, U., Rodriguez, M., Straney, D., Romeo, J. T., VanEtten, H. D., & Hawes, M. C. (2005). Tissue-specific localization of pea root infection by Nectria haematococca. Mechanisms and consequences. Plant Physiology, 137(4), 1363-1374.
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  PMID: 15778461;PMCID: PMC1088327;Abstract: Root infection in susceptible host species is initiated predominantly in the zone of elongation, whereas the remainder of the root is resistant. Nectria haematococca infection of pea (Pisum sativum) was used as a model to explore possible mechanisms influencing the localization of root infection. The failure to infect the root tip was not due to a failure to induce spore germination at this site, suppression of pathogenicity genes in the fungus, or increased expression of plant defense genes. Instead, exudates from the root tip induce rapid spore germination by a pathway that is independent of nutrient-induced germination. Subsequently, a factor produced during fungal infection and death of border cells at the root apex appears to selectively suppress fungal growth and prevent sporulation. Host-specific mantle formation in response to border cells appears to represent a previously unrecognized form of host-parasite relationship common to diverse species. The dynamics of signal exchange leading to mantle development may play a key role in fostering plant health, by protecting root meristems from pathogenic invasion. © 2005 American Society of Plant Biologists.
• Woo, H., Jeong, B. R., & Hawes, M. C. (2005). Flavonoids: From cell cycle regulation to biotechnology. Biotechnology Letters, 27(6), 365-374.
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  PMID: 15834800;Abstract: Flavonoids have been proposed to play diverse roles in plant growth and development, including defense, symbiosis, pollen development and male fertility, polar auxin transport, and protection against ultraviolet radiation. Recently, a new role in cell cycle regulation has emerged. Genetic alteration of glucuronide metabolism by altered expression of a Pisum sativum UDP-glucuronosyltransferase (PsUGT1) results in an altered cell cycle in pea, alfalfa, and Arabidopsis. In alfalfa, altered expression of PsUGT1 results in accumulation of a flavonoid-like compound that suppresses growth of cultured cells. The results are consistent with the hypothesis that PsUGT1 functions by controlling cellular levels of a factor controlling cell cycle (FCC). © Springer 2005.
• Weiss, H., & Hawes, M. C. (2004). Adolescent idiopathic scoliosis, bracing and the Hueter-Volkmann principle.. The spine journal : official journal of the North American Spine Society, 4(4), 484-485; author reply 485-486.
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  PMID: 15246310;
• Weiss, H., Hawes, M. C., & Castro Jr., F. P. (2004). Letter to the Editor (multiple letters) [1]. Spine Journal, 4(4), 484-486.
• Wen, F., Woo, H., Hirsch, A. M., & Hawes, M. C. (2004). Lethality of inducible, meristem-localized ectopic β-glucuronidase expression in plants. Plant Molecular Biology Reporter, 22(1), 7-14.
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  Abstract: GUSA from Escherichia coli, encoded by the uidA gene, has been successfully used as a plant reporter system for more than a decade with no reported deleterious effects. However, when expressed in coordination with a UDP-glucuronosyltransferase isolated from the root cap meristem of Pisum sativum (PsUGT1) at the onset of mitosis, GUSA expression was lethal in pea, alfalfa, and Arabidopsis thaliana. These unexpected results indicate that, under some circumstances, using GUSA in plants is incompatible with life and suggest that the cell-specific lethal phenotype might be useful in selecting for genes specifically involved in regulating the G2-M phase of the cell cycle. © 2004 International Society for Plant Molecular Biology.
• Woo, H. -., Hirsch, A. M., & Hawes, M. C. (2004). Altered susceptibility to infection by Sinorhizobium meliloti and Nectria haematococca in alfalfa roots with altered cell cycle. Plant Cell Reports, 22(12), 967-973.
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  PMID: 15042410;Abstract: Most infections of plant roots are initiated in the region of elongation; the mechanism for this tissue-specific localization pattern is unknown. In alfalfa expressing PsUGT1 antisense mRNA under the control of the cauliflower mosaic virus (CaMV) 35S promoter, the cell cycle in roots is completed in 48 h instead of 24 h, and border cell number is decreased by more than 99%. These plants were found to exhibit increased root-tip infection by a fungal pathogen and reduced nodule formation by a bacterial symbiont. Thus, the frequency of infection in the region of elongation by Nectria haematocca was unaffected, but infection of the root tip was increased by more than 90%; early stages of Sinorhizobium meliloti infection and nodule morphology were normal, but the frequency of nodulation was fourfold lower than in wild-type roots. © Springer-Verlag 2004.
• Zhu, Y., Wen, F., Zhao, X., & Hawes, M. C. (2004). Isolation of the promoter of a root cap expressed pectinmethylesterase gene from Pisum sativum L. (rcpme1) and its use in the study of gene activity. Plant and Soil, 265(1-2), 47-59.
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  Abstract: A genomic clone of a pea pectinmethylesterase encoding gene, rcpme1, was isolated; the promoter region was found to include regions of homology to phenylalanine ammonia lyase (PAL) and nodulin gene promoters. Agrobacterium rhizogenes mediated hairy roots were used for rcpme1 expression and functional analysis in pea. Patterns of rcpme1 expression in cultured hairy roots, measured using uidA encoding β-glucuronidase (GUS) as a reporter gene, were distinct from patterns which occur in normal pea roots. No reporter gene expression occurred in transgenic Arabidopsis thaliana, whose roots do not produce border cells. Border cell number from transgenic hairy roots expressing rcpme1 anti-sense mRNA under the control of its 2.75 kb 5prime; flanking sequence was reduced by > 50%. Nodulation genes of Rhizobium leguminosarum were used as a marker to document that roots with reduced production of border cells and other root cap exudates have a corresponding reduction in levels of biologically active signal molecules. Direct measurements were used to confirm that most of the exudate harvested from young, unwounded roots of normal pea plants is derived from the root tip region where rcpme1 is expressed. The potential application of the rcpme1 gene as a molecular marker for root exudate production is discussed. © 2004 Kluwer Academic Publishers.
• Farrar, J., Hawes, M., Jones, D., & Lindow, S. (2003). How roots control the flux of carbon to the rhizosphere. Ecology, 84(4), 827-837.
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  Abstract: What determines the way in which roots provide carbon to and interact with other components of the soil? Roots lose metabolites and signal molecules to the soil at rates of significance to soil organisms, and we need to know if the mechanisms of passive diffusion identified in hydroponics apply in soil, and whether other, active mechanisms complement them. New insights from biosensors into the heterogeneity and localization of exudation are transforming our understanding of root-microorganism relations. We need to know more about compounds that are exuded at subnutritional rates in soil and may act as signal molecules modifying the biology of soil organisms. Insights into one suite of such compounds is coming from studies of border cells. These cells are lost from the root cap at a rate regulated by the root and secrete compounds that alter the environment of and gene expression in soil microorganisms and fauna. The amount of root places an upper limit on the effect roots can have; carbon flow to the rhizosphere is a function of root growth. Top-down metabolic control analysis shows that the control over the rate at which roots grow is shared between root and shoot, with most control being in the shoot.
• Hawes, M. C. (2003). The use of exercises in the treatment of scoliosis: An evidence-based critical review of the literature. Developmental Neurorehabilitation, 6(3-4), 171-182.
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  Abstract: The loss of flexibility in a spinal curvature defines it as a structural spinal deformity; a curvature sufficiently mobile to resolve with a change in posture is a non-structural or 'functional' scoliosis which is within the normal limits of movement for a human spine. It, therefore, seems logical that exercise-based therapies designed to improve and/or maintain flexibility and range of motion of the spine and thorax would be useful in the treatment of scoliosis. Recognition of the importance of maintaining flexibility of the thoracic spinal column to avoid scoliosis-associated pulmonary dysfunction made the use of exercise-based therapies a topic of clinical interest in ancient Greece. In recent years, successful prevention of polio epidemics has resulted in a stable change in patient populations such that most individuals diagnosed with scoliosis do not suffer from irreversible central nervous system compromise. As a result, realistic opportunities to examine the role of exercise in treatment of scoliosis are available for the first time in history. A growing body of evidence from independent sources is consistent with the hypothesis that exercise-based approaches can be used effectively to reverse the signs and symptoms of spinal deformity and to prevent progression in children and adults. © 2003 Informa UK Ltd All rights reserved.
• Hawes, M. C. (2003). The use of exercises in the treatment of scoliosis: An evidence-based critical review of the literature. Pediatric Rehabilitation, 6(3-4), 171-182.
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  PMID: 14713583;Abstract: The loss of flexibility in a spinal curvature defines it as a structural spinal deformity; a curvature sufficiently mobile to resolve with a change in posture is a non-structural or 'functional' scoliosis which is within the normal limits of movement for a human spine. It, therefore, seems logical that exercise-based therapies designed to improve and/or maintain flexibility and range of motion of the spine and thorax would be useful in the treatment of scoliosis. Recognition of the importance of maintaining flexibility of the thoracic spinal column to avoid scoliosis-associated pulmonary dysfunction made the use of exercise-based therapies a topic of clinical interest in ancient Greece. In recent years, successful prevention of polio epidemics has resulted in a stable change in patient populations such that most individuals diagnosed with scoliosis do not suffer from irreversible central nervous system compromise. As a result, realistic opportunities to examine the role of exercise in treatment of scoliosis are available for the first time in history. A growing body of evidence from independent sources is consistent with the hypothesis that exercise-based approaches can be used effectively to reverse the signs and symptoms of spinal deformity and to prevent progression in children and adults.
• Hawes, M. C., & Weinstein, S. L. (2003). Health and Function of Patients with Untreated Idiopathic Scoliosis [2] (multiple letters). Journal of the American Medical Association, 289(20), 2644-2645.
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  PMID: 12771105;
• Woo, H., Faull, K. F., Hirsch, A. M., & Hawes, M. C. (2003). Altered Life Cycle in Arabidopsis Plants Expressing PsUGT1, a UDP-Glucuronosyltransferase-Encoding Gene from Pea. Plant Physiology, 133(2), 538-548.
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  PMID: 12972656;PMCID: PMC219030;Abstract: Alfalfa (Medicago sativa) and Arabidopsis were used as model systems to examine molecular mechanisms underlying developmental effects of a microsomal UDP-glucuronosyltransferase-encoding gene from pea (Pisum sativum; PsUGT1). Alfalfa expressing PsUGT1 antisense mRNA under the control of the cauliflower mosaic virus (CaMV) 35S promoter exhibited delayed root emergence, reduced root growth, and increased lateral root development. The timing of root emergence in wild-type and antisense plants was correlated with the transient accumulation of auxin at the site of root emergence. Cell suspension cultures derived from the antisense alfalfa plants exhibited a delay in cell cycle from 24-h in the wild-type plants to 48-h in the antisense plants. PsUGT1::uidA was introduced into Arabidopsis to demonstrate that, as in alfalfa and pea, PsUGT1 expression occurs in regions of active cell division. This includes the root cap and root apical meristems, leaf primordia, tips of older leaves, and the transition zone between the hypocotyl and the root. Expression of PsUGT1::uidA colocalized with the expression of the auxin-responding reporter DR5::uidA. Co-expression of DR5::uidA in transgenic Arabidopsis lines expressing CaMV35S::PsUGT1 revealed that ectopic expression of CaMV35S::PsUGT1 is correlated with a change in endogenous auxin gradients in roots. Roots of ecotype Columbia expressing CaMV35S::PsUGT1 exhibited distinctive responses to exogenous naphthalene acetic acid. Completion of the life cycle occurred in 4 to 6 weeks compared with 6 to 7 weeks for wild-type Columbia. Inhibition of endogenous ethylene did not correct this early senescence phenotype.
• Gunawardena, U., & Hawes, M. C. (2002). Tissue specific localization of root infection by fungal pathogens: Role of root border cells. Molecular Plant-Microbe Interactions, 15(11), 1128-1136.
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  PMID: 12423018;Abstract: When roots of pea seedlings were inoculated uniformly with spores of Nectria haematocca or other pea pathogenic fungi, more than 90% developed lesions in the region of elongation within 3 days. More mature regions of most roots as well as the tip showed no visible signs of infection. Yet, microscopic observation revealed that 'mantles,' comprised of fungal hyphae intermeshed with populations of border cells, covered the tips of most roots. After physical detachment of the mantle, the underlying tip of most roots was found to be free of infection. Mantle-covered root tips did not respond to invasion of their border cells by activation of known defense genes unless there was invasion of the tip itself, as revealed by the presence of a lesion. Concomitant with the activation of defense genes was the induction of a cell-wall degrading enzyme whose expression is a marker for renewed production of border cells. Mantle formation did not occur in response to nonpathogens. The data are consistent with the hypothesis that border cells serve as a host-specific 'decoy' that protects root meristems by inhibiting fungal infection of the root tip.
• Hawes, M. C., & Brooks, W. J. (2002). Reversal of the signs and symptoms of moderately severe idiopathic scoliosis in response to physical methods. Studies in Health Technology and Informatics, 91, 365-368.
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  PMID: 15457757;Abstract: This report describes improved signs and symptoms of previously untreated symptomatic spinal deformity in an adult female diagnosed with moderately severe thoracic scoliosis at the age of.7 years. Current treatment initiated at the age of forty included massage therapy, manual traction, ischemic pressure, and comprehensive manipulative medicine (CMM). A left-right chest circumference inequity was reduced by >10 cm, in correlation with improved appearance of the ribcage deformity and a 40% reduction in magnitude of Cobb angle, which had been stable for 30 years. The changes occurred gradually over an eight-year period, with the most rapid improvement occurring during two periods when CMM was employed.
• Hawes, M. C., Bengough, G., Cassab, G., & Ponce, G. (2002). Root caps and rhizosphere. Journal of Plant Growth Regulation, 21(4), 352-367.
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  Abstract: In this paper we discuss recent work on the physiological, molecular, and mechanical mechanisms that underlie the capacity of root caps to modulate the properties of the rhizosphere and thereby foster plant growth and development. The root cap initially defines the rhizosphere by its direction of growth, which in turn occurs in response to gradients in soil conditions and gravity. The ability of the root cap to modulate its environment is largely a result of the release of exudates and border cells, and so provides a potential method to engineer the rhizosphere. Factors affecting the release of border cells from the outer surface of the root cap, and function of these cells and their exudates in the rhizosphere, are considered in detail. Release of border cells into the rhizosphere depends on soil matric potential and mechanical impedance, in addition to a host of other environmental conditions. There is good evidence of unidentified feedback signals between border cells and the root cap meristem, and some potential mechanisms are discussed. Root border cells play a significant mechanical role in decreasing frictional resistance to root penetration, and a conceptual model for this function is discussed. Root and border cell exudates influence specific interactions between plant hosts and soil organisms, including pathogenic fungi. The area of exudates and border cell function in soil is an exciting and developing one that awaits the production of appropriate mutant and transgenic lines for further study in the soil environment.
• Woo, H., Kuleck, G., Hirsch, A. M., & Hawes, M. C. (2002). Flavonoids: Signal molecules in plant development. Advances in Experimental Medicine and Biology, 505, 51-60.
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  PMID: 12083466;
• Hawes, M. C. (2001). Improved chest expansion in idiopathic scoliosis. Psychosomatic Medicine, 63(6), 994-995.
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  PMID: 11719639;
• Hawes, M. C., & Brooks, W. J. (2001). Improved chest expansion in idiopathic scoliosis after intensive, multiple-modality, nonsurgical treatment in an adult. Chest, 120(2), 672-674.
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  PMID: 11502678;Abstract: This case report documents a substantial increase in chest wall expansion in a middle-aged woman with stable right thoracic spinal curvature due to idiopathic scoliosis. Treatment involved intensive psychological and mobilization therapies, including comprehensive manipulative medicine treatments and daily manual traction. Over an 8-year period, a 6-cm increase in resting chest circumference (in the absence of weight gain) and a 7.5-cm increase in chest expansion were correlated with a substantial reduction of incidence of respiratory infections.
• Miyasaka, S. C., & Hawes, M. C. (2001). Possible role of root border cells in detection and avoidance of aluminum toxicity. Plant Physiology, 125(4), 1978-1987.
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  PMID: 11299377;PMCID: PMC88853;Abstract: Root border cells are living cells that surround root apices of most plant species and are involved in production of root exudates. We tested predictions of the hypothesis that they participate in detection and avoidance of aluminum (Al) toxicity by comparing responses of two snapbean (Phaseolus vulgaris) cultivars (cv Dade and cv Romano) known to differ in Al resistance at the whole-root level. Root border cells of these cultivars were killed by excess Al in agarose gels or in simple salt solutions. Percent viability of Al-sensitive cv Romano border cells exposed in situ for 96 h to 200 μM total Al in an agarose gel was significantly less than that of cv Dade border cells; similarly, relative viability of harvested cv Romano border cells was significantly less than that of cv Dade cells after 24 h in 25 μM total Al in a simple salt solution. These results indicate that Al-resistance mechanisms that operate at the level of whole roots also operate at the cellular level in border cells. Al induced a thicker mucilage layer around detached border cells of both cultivars. Cultivar Dade border cells produced a thicker mucilage layer in response to 25 μM Al compared with that of cv Romano cells after 8 h of treatment and this phenomenon preceded that of observed cultivar differences in relative cell viability. Release of an Al-binding mucilage by border cells could play a role in protecting root tips from Al-induced cellular damage.
• Hawes, M. C., Gunawardena, U., Miyasaka, S., & Zhao, X. (2000). The role of root border cells in plant defense. Trends in Plant Science, 5(3), 128-133.
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  PMID: 10707079;Abstract: The survival of a plant depends upon the capacity of root tips to sense and move towards water and other nutrients in the soil. Perhaps because of the root tip's vital role in plant health, it is ensheathed by large populations of detached somatic cells - root 'border' cells - which have the ability to engineer the chemical and physical properties of the external environment. Of particular significance, is the production by border cells of specific chemicals that can dramatically alter the behavior of populations of soilborne microflora. Molecular approaches are being used to identify and manipulate the expression of plant genes that control the production and the specialized properties of border cells in transgenic plants. Such plants can be used to test the hypothesis that these unusual cells act as a phalanx of biological 'goalies', which neutralize dangers to newly generated root tissue as the root tip makes its way through soil.
• Zhao, X., Misaghi, I. J., & Hawes, M. C. (2000). Stimulation of border cell production in response to increased carbon dioxide levels. Plant Physiology, 122(1), 181-188.
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  PMID: 10631261;PMCID: PMC58856;Abstract: Field soil atmospheres have higher CO2 and lower O2 concentrations compared with ambient atmosphere, hut little is known about the impact of such conditions on root exudation patterns. We used altered levels of CO2 and O2 relative to ambient conditions to examine the influence of the atmosphere on the production of root border cells by pea (Pisum sativum) root tips. During germination, atmospheres with high CO2 and low O2 inhibited root development and border cell separation in pea seedlings. Later in development, the same atmospheric composition stimulated border cell separation without significantly influencing root growth, increased CO2, not low O2, was responsible for the observed stimulation of border cell number. High CO2 apparently can override endogenous signals that regulate the number of border cells released from pea roots into the rhizosphere. The same conditions that stimulated border cell production in pea had no such effect in alfalfa (Medicago sativa).
• Zhao, X., Schmitt, M., & Hawes, M. C. (2000). Species-dependent effects of border cell and root tip exudates on nematode behavior. Phytopathology, 90(11), 1239-1245.
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  PMID: 18944426;Abstract: Effects of border cell and root tip exudates on root knot nematode (Meloidogyne incognita) behavior were examined. In whole-plant assays using pea, M. incognita second-stage juveniles (J2) accumulated rapidly around the 1- to 2-mm apical region ensheathed by border cells, but not in the region of elongation. Within 15 to 30 min, J2 which had accumulated within detached clumps of border cells lost motility and entered into a quiescent state. When border cells (and associated root tip exudates) were washed from pea roots prior to challenge with nematodes, no such accumulation and quiescence was induced. Attraction of nematodes by roots was species dependent: no attraction or accumulation occurred in snap bean. Using a quantitative assay, three categories of chemotaxis responses occurred: attraction (pea and alfalfa cv. Thor), repulsion (alfalfa cv. Moapa 69), and no response (snap bean and alfalfa cv. Lahonton). In contrast, total root tip exudates from all three plant species acted as a repellent for M. incognita in the sand assay. An in vitro assay was developed to characterize the induced quiescence response. When total root tip exudate from the tested legumes (as well as corn) was incubated with J2 populations, >80% of the nematodes lost motility. A similar response occurred in Caenorhabditis elegans. Border cell exudates did not induce or contribute to the induction of quiescence. Cocultivation of pea border cells with M. incognita resulted in changes in border cell shape similar to those observed in response to exogenous plant hormones. No such changes occurred in snap bean border cells. Understanding the cell- and host-specific extracellular recognition that occurs between roots and pathogenic nematodes in the early stages before infection occurs could lead to new avenues for disease control.
• Wen, F., Zhu, Y., & Hawes, M. C. (1999). Effect of pectin methylesterase gene expression on pea root development. Plant Cell, 11(6), 1129-1140.
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  PMID: 10368183;PMCID: PMC144245;Abstract: Expression of an inducible gene with sequences common to genes encoding pectin methylesterase (PME) was found to be tightly correlated, both spatially and temporally, with border cell separation in pea root caps. Partial inhibition of the gene's expression by antisense mRNA in transgenic pea hairy roots prevented the normal separation of root border cells from the root tip into the external environment. This phenotype was correlated with an increase in extracellular pH, reduced root elongation, and altered cellular morphology. The translation product of the gene exhibited PME activity in vitro. These results are consistent with the long-standing hypothesis that the demethylation of pectin by PME plays a key role in cell wall metabolism.
• Woo, H., Orbach, M. J., Hirsch, A. M., & Hawes, M. C. (1999). Meristem-localized inducible expression of a UDP-glycosyltransferase gene is essential for growth and development in pea and alfalfa. Plant Cell, 11(12), 2303-2315.
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  PMID: 10590160;PMCID: PMC144138;Abstract: PsUGT1, which encodes a microsomal UDP-glucuronosyltransferase, was cloned from root tips of Pisum sativum. PsUGT1 expression is correlated with mitosis and strongly induced in dividing cells. A region at the C terminus of the encoded protein is closely related to the UDP-glucuronic acid binding site consensus sequence, and the protein encoded by PsUGT1 catalyzes conjugation of UDP-glucuronic acid to an unknown compound. Overexpression of PsUGT1 sense mRNA has no detectable effect on transgenic pea hairy root cultures or regenerated alfalfa. However, inhibiting PsUGT1 expression by the constitutive expression of antisense mRNA (under the control of the cauliflower mosaic virus 35S promoter) markedly retards growth and development of transgenic alfalfa. Cell structure and organization in the antisense plants are similar to those of controls, but plant growth is reduced and development is delayed. This inhibition in growth is correlated with a twofold delay in the time required for completion of a cell cycle and with a >99% inhibition of border cell production. Inhibition of PsUGT1 expression by meristem-localized inducible expression of PsUGT1 antisense mRNA (under the control of its own promoter) is lethal both in pea hairy roots and in transgenic alfalfa plants. These results indicate that PsUGT1 expression is required for normal plant growth and development, and they are consistent with the hypothesis that this UDP-glycosyltransferase regulates activity of a ligand(s) needed for cell division.
• Hawes, M. C., Brigham, L. A., Wen, F., Woo, H. H., & Zhu, Y. (1998). Function of root border cells in plant health: Pioneers in the rhizosphere. Annual Review of Phytopathology, 36, 311-327.
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  PMID: 15012503;Abstract: Plants dedicate a large amount of energy to the regulated production of living cells programmed to separate from roots into the external environment. This unusual process may be worth the cost because it enables the plant to dictate which species will share its ecological niche. For example, border cells can rapidly attract and stimulate growth in some microorganisms and repel and inhibit the growth of others. Such specificity may provide a way to control the dynamics of adjacent microbial populations in the soil to foster beneficial associations and inhibit pathogenic invasion. Plant genes controlling the delivery of border cells and the expression of their unique properties provide tools to genetically engineer plants with altered border cell quality and quantity. Such variants are being used to test the hypothesis that the function of border cells is to protect plant health by controlling the ecology of the root system.
• Woo, H., & Hawes, M. C. (1997). Cloning of genes whose expression is correlated with mitosis and localized in dividing cells in root caps of Pisum sativum L.. Plant Molecular Biology, 35(6), 1045-1051.
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  PMID: 9426627;Abstract: Removal of border cells from pea roots synchronizes and induces root cap cell division, wall biogenesis and differentiation. Three messages which are expressed differentially in such induced root caps have been cloned. Sequence analyses showed that the PsHRGP1-encoded protein has high homology with a hydroxyproline-rich glycoprotein. The PsCaP23-encoded protein has high homology with an alfalfa callus protein or translationally controlled human or mouse tumor protein P23. The PsRbL41-encoded protein has high homology with a highly basic 60S ribosomal protein L41. In situ hybridization showed that PsHRGP1, PsCaP23 and PsRbL41 messages are localized within dividing cells of the root cap. PsHRGP1 is highly expressed in uninduced root caps, but its message is repressed by 10-11 times as soon as cell division and differentiation begin. Expression of PsHRGP1 recovers to higher than (180%) its initial level in 30 min. PsHRGP1 is root-specific. PsCaP23 and PsRbL41 messages increase ca. 3-fold within 15 min after root cap induction. All three genes represent small families of 3-5 closely related genes in the pea genome.
• Woo, H., & Hawes, M. C. (1997). Rapid mapping and subcloning of genomic clones in bacteriophage lambda by PCR. BioTechniques, 22(5), 822-824.
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  PMID: 9149854;
• Zhu, Y., S., L., & Hawes, M. C. (1997). Induction of microbial genes for pathogenesis and symbiosis by chemicals from root border cells. Plant Physiology, 115(4), 1691-1698.
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  PMID: 9414568;PMCID: PMC158635;Abstract: Reporter strains of soil-borne bacteria were used to test the hypothesis that chemicals released by root border cells can influence the expression of bacterial genes required for the establishment of plant-microbe associations. Promoters from genes known to be activated by plant factors included virE, required for Agrobacterium tumefaciens pathogenesis, and common nod genes from Rhizobium leguminosarum bv viciae and Rhizobium meliloti, required for nodulation of pea (Pisum sativum) and alfalfa (Medicago sativum), respectively. Also included was phzB, an autoinducible gene encoding the biosynthesis of antibiotics by Pseudomonas aureofaciens. The virE and nod genes were activated to different degrees, depending on the source of border cells, whereas phzB activity remained unaffected. The homologous interaction between R. leguminosarum bv viciae and its host, pea, was examined in detail. Nod gene induction by border cells was dosage dependent and responsive to environmental signals. The highest levels of gene induction by pea (but not alfalfa) border cells occurred at low temperatures, when little or no bacterial growth was detected. Detached border cells cultured in distilled water exhibited increased nod gene induction (ini) in response to signals from R. leguminosarum bv viciae.
• Brigham, L. A., Woo, H. H., & Hawes, M. C. (1995). Root border cells as tools in plant cell studies.. Methods in cell biology, 49, 377-387.
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  PMID: 8531770;
• Brigham, L. A., Woo, H., Nicoll, S. M., & Hawes, M. C. (1995). Differential expression of proteins and mRNAs from border cells and root tips of pea. Plant Physiology, 109(2), 457-463.
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  Abstract: Many plants release large numbers of metabolically active root border cells into the rhizosphere. We have proposed that border cells, cells produced by the root cap meristem that separate from the rest of the root upon reaching the periphery of the cap, are a singularly differentiated part of the root system that modulates the environment of the plant root by producing specific substances to be released into the rhizosphere. Proteins synthesized in border cells exhibit profiles that are very distinct from those of the root tip (root cap, root meristem, and adjacent cells). In vivo-labeling experiments demonstrate that 13% of the proteins that are abundant in preparations from border cells are undetectable in root tip preparations. Twenty-five percent of the proteins synthesized by border cells in a 1-h period are rapidly excreted into the incubation medium. Quantitative variation in levels of specific marker proteins, including glutamine synthetase, heat-shock protein 70, and isoflavone reductase, also occurs between border cells and cells in the root tip. mRNA differential-display assays demonstrate that these large qualitative and quantitative differences in protein expression are correlated with similarly distinct patterns of gene expression. These observations are consistent with the hypothesis that a major switch in gene expression accompanies differentiation into root border cells, as expected for cells with specialized functions in plant development.
• Nicoll, S. M., Brigham, L. A., Wen, F., & Hawes, M. C. (1995). Expression of transferred genes during hairy root development in pea. Plant Cell, Tissue and Organ Culture, 42(1), 57-66.
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  Abstract: Root border cell development and expression of reporter genes were evaluated in transgenic pea hairy roots. Successful induction of hairy roots in pea is conditioned by bacterial strain and plant genotype, as well as by developmental and environmental factors. Morphological changes sometimes occur when hairy roots are transferred from infected plants to tissue culture media, but such changes are confined to specific clones. Expression of reporter genes under the control of promoters from bean (Phaseolus vulgaris L.) "stress" genes encoding phenylalanine ammonia lyase and chalcone synthase were evaluated. Expression patterns vary between hairy roots taken directly from infected plants, and those grown in culture; most hairy roots taken from infected plants exhibit expression throughout all tissues, whereas expression in cultured hairy roots is most often localized to specific tissues. Patterns of expression that occur during different stages of hairy root development are very similar to those observed in transgenic plants expressing the same fusion genes. Border cell separation and release in hairy roots is normal, and expression of glucuronidase in border cells of some transgenic roots resulted in development of bright blue single cells. Cultured hairy roots should provide a very useful model for studying the effect of defined changes in root border cells on microbial associations with roots of this important legume. © 1995 Kluwer Academic Publishers.
• Pan, S. Q., Jin, S., Boulton, M. I., Hawes, M., Gordon, M. P., & Nester, E. W. (1995). An Agrobacterium virulence factor encoded by a Ti plasmid gene or a chromosomal gene is required for T-DNA transfer into plants. Molecular Microbiology, 17(2), 259-269.
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  PMID: 7494475;Abstract: Mutagenesis of the vir region on the Ti plasmid of Agrobacterium tumefaciens revealed a new locus, virJ, that is induced by the plant-wound signal molecule, acetosyringone (AS). virJ lies between virA and virB, and is transcribed in the same direction. The amino acid sequence of virJ is similar to a region of a previously characterized chromosomal gene, acvB, required for virulence, virJ can complement the avirulent phenotype of an acvB mutant, indicating that virJ and acvB encode the same factor required for tumorigenesis. Southern analysis revealed that virJ is present on the Ti plasmid of an octopine but not a nopaline strain whereas acvB is present on the chromosomes of both octopine and nopaline strains. White virJ is regulated by AS under the control of the virA/virG two-component regulatory system, acvB is not induced by AS. VirJ possesses a putative signal peptide and was found predominantly in the periplasmic fraction. The strain lacking both acvB and virJ had an impaired ability to transfer T-DNA into plant cells, suggesting that the factor encoded by virJ or acvB is required for T-DNA transfer from A. tumefaciens to plant cells. acvB is the first chromosomal gene implicated in T-DNA transfer, but whether it functions specifically for this process is not clear. We hypothesize that virJ evolved from acvB, presumably for a more specialized role in tumorigenesis.
• Woo, H. -., Brigham, L. A., & Hawes, M. C. (1995). Detection of low-abundance messages by a combination of PCR and ribonuclease protection. BioTechniques, 18(5), 778-779.
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  PMID: 7619476;
• Woo, H., Brigham, L. A., & Hawes, M. C. (1995). In-cell RT-PCR in a single, detached plant cell. Plant Molecular Biology Reporter, 13(4), 355-362.
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  Abstract: A procedure is presented for the detection of mRNA in a single root border cell of pea seedlings using RT-PCR (reverse transcription-polymerase chain reaction) and direct incorporation of digoxigenin-dUTP. It includes cell preservation with aldehyde. Signal is detected using a conjugate of anti-DIG and alkaline phosphatase. © 1995 Kluwer Academic Publishers.
• Woo, H., Brigham, L. A., & Hawes, M. C. (1995). Molecular cloning and expression of mRNAs encoding H1 histone and an H1 histone-like sequences in root tips of pea (Pisum sativum L.). Plant Molecular Biology, 28(6), 1143-1147.
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  PMID: 7548832;Abstract: Two cDNA clones representing mRNAs, highly expressed in pea root tips, were isolated by mRNA differential display. Ribonuclease protection analyses showed different patterns of expression of these two messages in several pea tissues. Sequence analysis showed that the first clone, PsH1b-40, has 100% homology with a previously isolated H1 histone cDNA, PsH1b. However, it has an additional 30 nt at the 3′ end which is absent in PsH1b, suggesting possible multiple polyadenylation sites in the same mRNA. The second clone, PsH1b-41, encodes a deduced 19.5 kDa protein of 185 amino acids with an isoelectric point of 11.5. The putative globular domain of the encoded protein showed 67-71% residue identity with globular domains of 28 kDa pea PsH1b H1 histone and Arabidopsis thaliana H1-1 H1 histone. It has 9 repeating motifs of (T/S)XXK. In the C-terminal domain, there are four lysine-rich repeating motifs of SXK(T/S)PXKKXK which may be involved in chromatin condensation and decondensation. Southern blot analysis of nuclear DNA shows that PsH1-41 belongs to a multigene family. © 1995 Kluwer Academic Publishers.
• Ho-Hyung, W., Brigham, L. A., & Hawes, M. C. (1994). Primary structure of the mRNA encoding a 16.5-kDa ubiquitin-conjugating enzyme of Pisum sativum. Gene, 148(2), 369-370.
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  PMID: 7958971;Abstract: The complementary DNA (PsUBC4) representing an mRNA encoding an ubiquitin-conjugating enzyme (UBC) of Pisum sativum has been cloned. The coding region is 444 nucleotides (nt) in length and capable of specifying a 16.5-kDa protein of 148 amino acids (aa) with an isoelectric point of 7.95. The deduced aa sequence showed 97% identity with Arabidopsis thaliana AtUBC8-12 families and tomato ERT17, and 80% identity with yeast ScUBC4 and ScUBC5 and Drosophila melanogaster DmUBC4. The active site cysteine (Cys85) found in UBCs so far described is also conserved in the P. sativum sequence. © 1994.
• Stephenson, M. B., & Hawes, M. C. (1994). Correlation of pectin methylesterase activity in root caps of pea with root border cell separation. Plant Physiology, 106(2), 739-745.
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  Abstract: We tested predictions of the hypothesis that pectin methylesterase in the root cap plays a role in cell wall solubilization leading to separation of root border cells from the root tip. Root cap pectin methylesterase activity was detected only in species that release large numbers of border cells daily. In pea (Pisum sativum) root caps, enzyme activity is correlated with border cell separation during development: 6-fold more activity occurs during border cell separation than after cell separation is complete. Higher levels of enzyme activity are restored by experimental induction of border cell separation. A corresponding increase in transcription of a gene encoding root cap pectin methylesterase precedes the increase in enzyme activity. A dramatic increase in the level of soluble, deesterified pectin in the root tip also is correlated with pectin methylesterase activity during border cell development. This increase in acidic, de-esterified pectin during development occurs in parallel with a decrease in cell wall/apoplastic pH of cells in the periphery of the root cap.
• Hawes, M. C., Smith, L. Y., & Stephenson, M. (1991). Root organogenesis from single cells released from the root cap of Medicago sp.. Plant Cell, Tissue and Organ Culture, 27(3), 303-308.
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  Abstract: Root border cells were isolated from alfalfa seedlings, and incubated in culture medium with growth regulators. Alfalfa seedlings yielded 1500±100 cells per root, and initial viability of the cells was 95±5%. Multiple cell divisions occurred in the border cells within two weeks. Cell clusters transferred to solidified medium containing growth regulators developed into rapidly growing, friable callus. When transferred to growth regulator-free medium, some of the calluses generated normal roots. © 1991 Kluwer Academic Publishers.
• Robbs, S. L., Hawes, M. C., Lin, H., Pueppke, S. G., & Smith, L. Y. (1991). Inheritance of resistance to crown gall in Pisum sativum. Plant Physiology, 95(1), 52-57.
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  PMID: 16667980;PMCID: PMC1077484;Abstract: We screened a total of 1365 pea (Pisum sativum) lines for response to inoculation with Agrobacterium tumefaciens, strain B6, and characterized resistance in one cultivar, Sweet Snap. Sweet Snap seedlings were highly resistant to tumorigenesis under most conditions. Resistance was overcome at inoculum concentrations of greater than 109 bacteria per milliliter. At such high concentrations, very small tumors developed on Sweet Snap in response to four wide-host-range Agrobacterium strains, but tumors on other cultivars were two- to sevenfold larger than those that formed on Sweet Snap. The hypervirulent strain A281 induced larger tumors on Sweet Snap than did other Agrobacterium strains, but tumors on other genotypes were more than 100% larger than those on Sweet Snap. Physiological experiments suggested that tumorigenesis in Sweet Snap is not blocked in early stages of infection, and genetic analysis indicated that inheritance of resistance to crown gall is a quantitative trait. In addition to the observed resistance in Sweet Snap, three 'supersusceptible' genotypes, which developed very large tumors, also were identified.
• Hawes, M. C. (1990). Living plant cells released from the root cap: A regulator of microbial populations in the rhizosphere?. Plant and Soil, 129(1), 19-27.
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  Abstract: A group of cells at the periphery of the root cap separate from plant roots as they move through the soil. Experimentally, these cells can be separated from the root by gentle agitation in water. Detached root cap cells provide a convenient system for comparing cellular and whole-plant responses to fungal and bacterial pathogens. Results with several hos-parasite combinations indicate that these cells express host-specific traits with respect to chemotaxis, binding, and infection. Mutants of Agrobacterium tumefaciens were used to test the hypothesis that recognition of the cells plays a role in establishment of microbial-plant associations. Tn 5 mutants deficient in chemotaxis to the cells exhibit reduced ability to colonize the rhizosphere and to induce crown gall tumorigenesis on pea plants grown in soil. The discovery that cells shed from the cap express hos-specific genes suggests that some microorganisms may have greater access to constituents of the cells than others. This cellular selectivity could have a significant impact on rhizosphere populations. © 1990 Kluwer Academic Publishers.
• Hawes, M. C., & Lin, H. (1990). Correlation of pectolytic enzyme activity with the programmed release of cells from root caps of pea (Pisum sativum). Plant Physiology, 94(4), 1855-1859.
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  PMID: 16667927;PMCID: PMC1077464;Abstract: In many plant species, the daily release of hundreds to thousands of healthy cells from the root cap into the soil is a normal process, whose function is unknown. We studied the separation of the cells in pea (Pisum sativum) using an aeroponic system in which separated cells were retained on the root until they were washed off for counting. We found that cell separation is a developmentally regulated, temperature-sensitive process that appears to be regulated independently of root growth. No cells were released from very young roots. When plants were grown aeroponically, cell numbers increased with increasing root length to a mean of 3400 cells per root, at which point the release of new cells ceased. The process could be reset and synchronized by washing the root in water to remove shed cells. Cell separation from the root cap was correlated with pectolytic enzyme activity in root cap tissue. Because these cells that separate from the root cap ensheath the root as it grows and thus provide a cellular interface between the root surface and the soil, we propose to call the cells "root border cells.".
• Rong, L., Karcher, S. J., O'Neal, K., Hawes, M. C., Yerkes, C. D., Jayaswal, R. K., Hallberg, C. A., & Gelvin, S. B. (1990). picA, a novel plant-inducible locus on the Agrobacterium tumefaciens chromosome. Journal of Bacteriology, 172(10), 5828-5836.
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  PMID: 2170328;PMCID: PMC526900;Abstract: We used the transposon Mu dI1681 to identify genes on the Agrobacterium tumefaciens chromosome that are inducible by extracts from carrot roots. One such locus (picA, for plant inducible chromosomal), harbored by A. tumefaciens At156, was inducible 10- to 50-fold by these extracts. Mutation of picA had no detectable effect upon bacterial growth or virulence under laboratory assay conditions. However, A. tumefaciens cells harboring a mutated picA locus aggregated into long 'ropes' when incubated with pea root tip cells. Such aggregation was not displayed by the parental strain A. tumefaciens A136. A preliminary characterization of the inducing compound in the carrot root extract suggests that the active substance is an acidic polysaccharide that is most likely derived from the pectic portion of the plant cell wall.
• Hawes, M. C., & Pueppke, S. G. (1989). Reduced rhizosphere colonization ability of Agrobacterium tumefaciens chromosomal virulence (chv) mutants. Plant and Soil, 113(1), 129-132.
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  Abstract: Mutations in the chromosomal virulence (chv) region of A. tumefaciens strain A723 reduce virulence, motility, and ability of the bacteria to bind to plant cells. We conducted experiments to assess the ability of chv mutants to colonize the rhizosphere of Pisum sativum. The mutation had no effect on ability of bacteria to grow with a defined number of root cap cells as the sole carbon and nitrogen source. Ten days after inoculation, there were up to 103-fold more wild type than chv mutant bacteria present in the rhizosphere of inoculated plants. © 1989 Kluwer Academic Publishers.
• Hawes, M. C., & Smith, L. Y. (1989). Requirement for chemotaxis in pathogenicity of Agrobacterium tumefaciens on roots of soil-grown pea plants.. Journal of Bacteriology, 171(10), 5668-5671.
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  PMID: 2793831;PMCID: PMC210412;Abstract: Agrobacterium tumefaciens Tn5 mutants deficient in chemotaxis to root exudates were used to study the significance of chemotaxis in crown gall pathogenesis. Mutants deficient in motility and in chemotaxis were fully virulent when inoculated by direct immersion in inoculum, followed by growth for 2 weeks in moist growth pouches. Ability of mutant bacteria to move through soil to infect roots was tested by planting wounded seedlings into air-dried soil or sand that had been infested with inoculum. Mutant bacteria were almost as virulent as the parent on plants grown in sand but were avirulent on soil-grown plants.
• Kanemoto, R. H., Powell, A. T., Akiyoshi, D. E., Regier, D. A., Kerstetter, R. A., Nester, E. W., Hawes, M. C., & Gordon, M. P. (1989). Nucleotide sequence and analysis of the plant-inducible locus pinF from Agrobacterium tumefaciens.. Journal of Bacteriology, 171(5), 2506-2512.
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  PMID: 2708311;PMCID: PMC209927;Abstract: Several loci on the tumor-inducing plasmid from Agrobacterium tumefaciens were transcriptionally activated in the presence of wounded plant tissue or extracts. The inducible virulence loci were required for efficient tumor formation. In contrast, the plant-inducible locus pinF was not observed to be absolutely essential for virulence. Mutants in pinF showed an attenuated virulence on a variety of dicotyledonous hosts, and this attenuation became more pronounced with decreasing numbers of bacterial cells in the inoculum. The DNA sequence of a 5.5-kilobase region which included the pinF locus from the octopine-type tumor-inducing plasmid A6 was determined. Four open reading frames consistent with the observed transcription of pinF were observed. Two of the open reading frames, pinF1 and pinF2, coded for polypeptides with relative molecular weights of 47,519 (pinF1) and 46,740 (pinF2). A comparison of the amino acid sequences of pinF1 and pinF2 indicated that they were similar to each other and to known polypeptide sequences for cytochrome P-450 enzymes.
• Hawes, M. C., & Pueppke, S. G. (1987). Correlation between binding of Agrobacterium tumefaciens by root cap cells and susceptibility of plants to crown gall. Plant Cell Reports, 6(4), 287-290.
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  PMID: 24248761;Abstract: We compared the binding of Agrobacterium tumefaciens by freshly isolated root cap cells with susceptibility of plants to crown gall tumorigenesis. A high binding reaction was strongly correlated with susceptibility to tumorigenesis in a survey of the binding of strain B6 to cells from 48 species in 17 families. In reciprocal experiments with nine virulent A. tumefaciens strains, tumors developed in plant-bacteria combinations that gave a high binding response in the root cap cell assay. Binding was quantified by direct measurement of the number of bacteria bound to the periphery of individual cells. Root cap cells from six susceptible species bound significantly more bacteria than did cells from five resistant species. © 1987 Springer-Verlag.
• Hawes, M. C., Z.Sharpe, D., Plata, M., Pueppke, S. G., & Chourey, P. S. (1985). Auxin-independent growth of maize tissue culture cells. Plant Science, 40(3), 197-202.
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  Abstract: Wall-regenerating protoplasts and suspension culture cells of Zea mays L. 'Black Mexican Sweet' were co-cultivated] with Ti plasmid-containing Agrobacterium tumefaciens strain ACH5. After elimination of the bacteria, putative transformants were selected for their ability to grow in the absence of added auxin. Althoug some of the treated cells grew, untreated controls and cells treated with the Ti plsmidless strain ACH5C3 also proliferated. The frequency of auxin-independent growth was similar in all treatments. Because none of 75 candidate transforms contained detectable T-DNA, the hormone-independent phenotype appears to be a consequence of habituation. Although some of the habituated colonies grew as undifferentiated callus, others produced rootlike structures. Miaze cells subcultured in liquid media containing progressively reduced concentrations of 2,4-dichlorophenoxyacetic acid (2,4-D) also became habituated. © 1985.
• Pueppke, S. G., & Hawes, M. C. (1985). Understanding the binding of bacteria to plant surfaces. Trends in Biotechnology, 3(12), 311-313.
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  Abstract: Many of the bacteria that associate with plants bind tenaciously to plant cells. This characteristic appears to have important functional implications for the inception of disease-causing and symbiotic interactions. Although binding is complex and as yet poorly understood, experimental manipulation of this process holds promise for improved plant productivity. © 1985.
• Hawes, M. C., & Wheeler, H. (1984). Detection of effects of nuclear genes on susceptibility to Helminthosporium maydis race T by a root cap cell bioassay for HMT-toxin. Physiological Plant Pathology, 24(2), 163-168.
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  Abstract: Previous attempts to detect effects of nuclear genes on susceptibility of corn to Helminthosporium maydis, race T, with several bioassays for the pathotoxin produced by this pathogen (HMT-toxin) have yielded conflicting results. Ten Texas male sterile corn lines, differing in susceptibility to H. maydis race T, were tested for sensitivity to HMT-toxin using a recently developed bioassay based on lethal effects on isolated root-cap cells. Susceptibility to H. maydis, race T, was found to be generally correlated with sensitivity to HMT-toxin. Preliminary results with two other phytotoxins suggest that this root cap cell bioassay should provide a rapid, accurate and economical method of testing agricultural chemicals or other agents for phytotoxicity. © 1984.
• Hawes, M. C., & Wheeler, H. (1982). Factors affecting victorin-induced root cap cell death: temperature and plasmolysist. Physiological Plant Pathology, 20(2), 137-138,IN4,139-144.
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  Abstract: Victorin, the pathotoxin produced by Helminthosporium victoriae, causes false plasmolysis and death of root cap cells, and this effect is selective for oat cultivars susceptible to the fungus. The development of a procedure for the isolation of root cap cells made possible a study of victorin's effects on populations of intact cells uniformly exposed to the toxin. Isolated root cap cells from resistant and susceptible cultivars were used to examine the effects of temperature and plasmolysis on victorin-induced cell death. Cell viability was determined by the ability to stain with fluorescein diacetate. Victorin-induced cell death was highly temperature dependent with a temperature coefficient of 3·5. At 10°C 96 to 98% of the cells remained alive for over 30 days when incubated in up to 50 units of toxin per ml. Plasmolysis also inhibited cell death; this protective effect was dependent upon solution tonicity. Non-permeating media, mannitol and sorbitol, protected more than sucrose in which cells slowly deplasmolyzed. Urea, a rapidly-permeating osmoticum, did not delay victorin-induced cell death. The modification of victorin's lethal effects by temperature and plasmolysis may explain variability in reported effects of the toxin on isolated protoplasts. © 1982.

Proceedings Publications

• Hawes, M. C., Allen, C., Tran, T., Huerta, A., & Prior, P. (2014, summer). The Battle of the Rhizosphere: How Ralstonia solanacearum defeats competitors and overcomes plant defenses to invade host roots.. In ICPPB.
• Hawes, M. C., Pietramellara, G., Ascher, J., & Ceccerini, M. (2013, Summer). Pietramellara G, Ascher J, Ceccerini M, Hawes MC (2013) Relevance of extracellular DNA in rhizosphere.. In EGU General Assembly2013, Vienna Austria, 1, 6.

Presentations

• Hawes, M. C. (2017, September 29). Extracellular DNA Traps in Plant and Animal Cells: A Dynamic Interface Between Disease and Health. Controlled Environment Agriculture Center, invited seminar. Tucson: CEAC.
• Hawes, M. C. (2013, October). Extracellular trapping in plant defense: a new target for disease control. Invited talk. Department of Plant Pathology and Plant-Microbe Biology: Cornell University.
• Hawes, M. C. (2013, September). Extracellular DNA trapping in plant defense. invited seminar. Columbia Missouri: Interdisciplinary Plant Group, University of Missouri.
• Hawes, M. C. (2013, spring). Compost at the leading edge of the rhizosphere. Compost workship. Tucson: University of Arizona.
• Hawes, M. C., & Curlango-Rivera, G. (2013, Fall). Compost in root disease control. Glenstone conference. Glenstone Maryland.
• Hawes, M. C., Cochran, A. M., Huskey, D. A., Curlango-Rivera, G., Kessler, J. O., & Xiong, Z. (2013, Spring). Huskey DA, Curlango-Rivera G, Kessler JO, Xiong Z, Hawes MC,Biological control by extracellular trapping in root systems.. American Society for Microbiology annual meeting. Tucson: ASM.
• Hawes, M. C., Huskey, D., Curlango-Rivera, G., VanEtten, H., & Xiong, Z. (2013, spring). A new look at plant immune responses: extracellular DNA-based trapping in defense. Fungal Genetics Meeting, Asilomar CA. Asilomar CA: Fungal Genetics Assn..
• Hawes, M. C., Tran, T., & Allen, C. (2013, Fall). Tran TM, Hawes MC, Allen C (2013) Extracellular DNases contribute to virulence of Ralstonia solanacearum.. American Phytopathological Society. Phytopathology 103:147-148: American Phytopathological Society.

Poster Presentations

• D’Agostini, B. A., deCastro, L. V., Ramirez, B., Curlango-Rivera, G., Huskey, D., Root, R. A., Chorover, J., & Hawes, M. C. (2018, spring). Impact of soil contaminants on the viability and production of plant root border cells: Implications for phytoremediation. CALS. University of Arizona: CALS.
• Hawes, M. C., & xiong, z. (2018, Spring). Battles in the outer space: extracellular DNases secreted by Pectobacterium carotovorum and its host planst. Internation Congress of Plant PathologyICPP.
• Knox, O., Wen, F., Curlango-Rivera, G., Huskey, D., & Hawes, M. C. (2018, october 2018). Cotton root tip Exogenous DNA response to wilts. Cotton Hub Annual Disease Forum (FUSCOM). Australia: FUSCOM.
• Wen, F., Xiong, Z., & Hawes, M. C. (2018, April). Living, not Dead Root Border Cells Release Extracellular DNA in Plant Defense. CALS. University of Arizona: CALS.
• Hawes, M. C., Huskey, D. A., Rivera, G. C., Root, R., & Chorover, J. (2017, April). Extracellular trapping of metals by root border cells.. 12th Keele Meeting on Aluminum, Vancouver, BC. Vancouver BC: Keele.
• Hawes, M. C., Huskey, D. A., Rivera, G. C., Root, R., Chorover, J., Ramirez, B., & Riba, C. M. (2017, March). Specificity in extracellular trapping of metals by plant root border cells?. CALS. Tucson AZ: University of Arizona, CALS.
• Hawes, M. C., Huskey, D., Rivera, G. C., Ramirez, B., Riba, C., Root, R., & Chorover, J. (2017, Spring). Trapping of metals by root border cells. SWESX. Tucson AZ: University of Arizona, CALS.
• Wen, F., Rivera, G. C., Huskey, D. A., Riba, C., Ramirez, B., & Hawes, M. C. (2017, April). Extracellular DNA traps in eucaryotic defense. 56th ASM ARIZONA/S. NEVADA ANNUAL MEETING, April 1st, TUCSON, AZ. Tucson: ASM.
• Hawes, M. C., & Huskey, D. A. (2016, summer). Border cells: from root rot to cancer. SWESx. University of Arizona: UA.
• Hawes, M. C., Curlango-Rivera, G., Huskey, D., Riba, C., & Ramirez, B. (2016, spring). Extracellular traps in animal and plant defense. WRRC conference. UA: WRRC.
• Hawes, M. C., Allen, C., & Tran, T. (2014, summer). BACTERIAL EXTRACELLULAR DNASE: A NOVEL VIRULENCE FACTOR.. MPMI, Hellas, Greece. Hellas, Greece: MPMI.
• Hawes, M. C., Curlango-Rivera, G., Flores-Lara, Y., Knight, N., & Lee, T. (2014, November). Signals controlling extracellular trap formation in plant and animal immune responses. .. CALS forum. Tucson AZ: CALS.
• Hawes, M. C., Curlango-Rivera, G., Huskey, D., Tollefson, S., Pew, T., & Giacomelli, G. (2014, spring). Understanding Root-Microbe Interactions at the Leading Edge of the Rhizosphere: Harnessing the Plant's ‘White Blood Cells' to Increase Efficacy of Compost Applications.. Sustainability Conference, UA. Tucson AZ: University of Arizona.
• Hawes, M. C., Curlango-Rivera, G., McLain, J., & Flores-Lara, Y. (2014, November 2014). Extracellular trapping by root border cells as a tool for water recycling. Martha Hawes, Gilberto Curlango-Rivera, Jean McLain, Yolanda Flores-Lara... CALS forum. Tucson AZ: CALS.
• Hawes, M. C., Curlango-Rivera, G., Tollefson, S., Pew, T., & Giacomelli, G. (2014, November). Understanding root-microbe interactions at the leading edge of the rhizosphere to increase efficacy of compost applications. Martha C. Hawes, Gilberto Curlango-Rivera, Stacy Tollefson, Thomas Pew, Gene Giacomelli.. CALS Forum. Tucson AZ: University of Arizona, College of Agriculture.
• Mclain, J. E., Hawes, M. C., Curlango-Rivera, G., & Flores-Lara, Y. (2014, May). Extracellular trapping by root border cells as a tool for water recycling. CALS Poster Forum. Tucson, Arizona: College of Agriculture and Life Sciences.
• Hawes, M. C., Huskey, D. A., Cochran, A. M., Curlango-Rivera, G., & Xiong, Z. (2013, spring). David A. Huskey, Alicia Cochran, Gilberto Curlango-Rivera, Martha C. Hawes, Zhongguo Xiong ) Root border cells of higher plants: shaping the rhizosphere.. SWESX 2013. Tucson: University of Arizona.
• Hawes, M. C., Huskey, D. A., Curlango-Rivera, G., VanEtten, H. D., Cochran, A., & Xiong, Z. (2013, summer). A new look at plant immune responses: extracellular DNA-based trapping in defense.. Meeting of the American Society for Microbiology.. tucson: ASM.
• Hawes, M. C., Tollefson, S., Curlango-Rivera, G., Pew, T., & Giacomelli, G. (2013, Fall). Tollefson S, Curlango-Rivera G, Pew T, Giacomelli G, Hawes MC (2013) Environmental factors influencing disease suppression by compost water extracts under controlled conditions.. International Symposium on Growing Media and Soilless Cultivation, Netherlands, GroSci2013.. Netherlands: GroSci.
• Hawes, M. C., Tollefson, S., Curlango-rivera, G., & Giacomelli, G. (2013, Summer). Tollefson S, Curlango-Rivera G, Giacomelli G, Hawes MC Root disease inhibition by compost water extracts.. American Phytopathological Society, Joint Caribbean-Pacific Meeting.. Tucson: APS.

Reviews

• Hawes, M. C. (2016. Invited review: Extracellular Trapping of Soil Contaminants by Root Border Cells: New Insights into Plant Defense(pp 10-19). Agronomy.
• Hawes, M. C. (2016. Root border cells and their role in plant defense(pp 6-30).
• Hawes, M. C., Driouich, A., Vicre-Gibouin, M., & Follet-Gueye, M. (2013. Driouich A, Follet-Gueye M, Vicre-Gibouin M, Hawes MC (2013) Root border cells and secretions as critical elements in plant host defense.(pp 1-5). 16.
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Others

• Hawes, M. C. (2017, November). Extracellular traps in plant and animal defense: new insights into mechanisms of eukaryote immunity. Neutrophil Extracellular Traps, Berlin, Germany, November 11-13, 2017, special invited talk.
• Hawes, M. C. (2016, August). The role of the extracellular matrix in defense: New insights into plant and animal immune responses. Botanical Society of America, special event seminar.
• Hawes, M. C. (2016, January). Invited special seminar. University of California, Davis CA. Extracellular traps in plant and animal defense: new insights into mechanisms of eucaryote immunity.
• Hawes, M. C. (2016, January). Invited special seminar: New insights into eucaryotic immunity. Stanford University.
• Hawes, M. C. (2016, March). Invited special seminar: Plant and animal parallels in extracellular DNA trapping responses. Texas A&M University.
• Hawes, M. C. (2016, March). Special invited seminar: Extracellular DNA in plant and animal defense. University of Wisconsin, Department of Plant Pathology.
• Hawes, M. C. (2016, November). Extracellular traps in plant and animal defense: new insights into mechanisms of eucaryote immunity. Auburn University, Department of Entomology and Plant Pathology.
• Hawes, M. C. (2016, September). Extracellular DNA in plant immunity. UK-US Plant Health Workshop, British Embassy.
• Hawes, M. C. (2016, September). Extracellular trapping in defense: New insights into plant and animal immune responses. Max Planck Institute for Microbiology, Berlin Germany.