Interests

Research

The main research interests of the Tax lab are to understand how short and long-range signaling are integrated during plant growth and development. Currently, our major project is to try to understand how environmental input from roots and metabolic information from shoots regulate how secondary roots initiate their development and control their length. We mainly use developmental genetic approaches and our research is mainly using the model system Arabidopsis.

Courses

Scholarly Contributions

Journals/Publications

• Xun, Q., Wu, Y., Li, H., Chang, J., Ou, Y., He, K., Gou, X., Tax, F. E., & Li, J. (2020). Two receptor-like protein kinases, MUSTACHES and MUSTACHES-LIKE, regulate lateral root development in Arabidopsis thaliana. The New phytologist, 227(4), 1157-1173.
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  Receptor-like protein kinases (RLKs) play key roles in regulating plant growth, development and stress adaptations. There are at least 610 RLKs (including receptor-like cytoplasmic kinases) in Arabidopsis. The functions of the majority of RLKs have not yet been determined. We previously generated promoter::GUS transgenic plants for all leucine-rich repeat (LRR)-RLKs in Arabidopsis and analyzed their expression patterns during various developmental stages. We found the expression of two LRR-RLKs, MUSTACHES (MUS) and MUSTACHES-LIKE (MUL), are overlapped in lateral root primordia. Independent mutants, mus-3 mul-1 and mus-4 mul-2, show a significantly decreased emerged lateral root phenotype. Our analyses indicate that the defects of the double mutant occur mainly at stage I of lateral root development. Exogenous application of auxin can dramatically enhance the transcription of MUS, which is largely dependent on AUXIN RESPONSE FACTOR 7 (ARF7) and ARF19. MUS and MUL are inactive kinases in vitro but are phosphorylated in planta, possibly by an unknown kinase. The kinase activity of MUS is dispensable for its function in lateral root development. Many cell wall related genes are down regulated in mus-3 mul-1. In conclusion, we identified MUS and MUL, two kinase-inactive RLKs, in controlling the early development of lateral root primordia likely via regulating cell wall synthesis and remodeling.
• Dimitrov, I., & Tax, F. E. (2018). Lateral root growth in Arabidopsis is controlled by short and long distance signaling through the LRR RLKs XIP1/CEPR1 and CEPR2. Plant signaling & behavior, 1-6.
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  Plants rely on lateral roots to explore their soil environment and to maximize their uptake of essential minerals and water. Here we present evidence that the receptor kinases XIP1/CEPR1 and CEPR2 regulate both the initiation of lateral root primordia and emergence of lateral roots locally in the root, while also controlling lateral root extension in response to shoot-derived sucrose in Arabidopsis plants. In addition, mutation of both of these receptors prevents seedlings from responding to sucrose in the media, resulting in longer lateral roots. These results, combined with previous data, establish XIP1/CEPR1 and CEPR2-dependent roles in short- and long-distance pathways regulating different stages of lateral root growth.
• Imkampe, J., Halter, T., Huang, S., Schulze, S., Mazzotta, S., Schmidt, N., Manstretta, R., Postel, S., Wierzba, M., Yang, Y., van Dongen, W. M., Stahl, M., Zipfel, C., Goshe, M. B., Clouse, S., de Vries, S. C., Tax, F., Wang, X., & Kemmerling, B. (2017). The Arabidopsis Leucine-Rich Repeat Receptor Kinase BIR3 Negatively Regulates BAK1 Receptor Complex Formation and Stabilizes BAK1. The Plant cell, 29(9), 2285-2303.
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  BAK1 is a coreceptor and positive regulator of multiple ligand binding leucine-rich repeat receptor kinases (LRR-RKs) and is involved in brassinosteroid (BR)-dependent growth and development, innate immunity, and cell death control. The BAK1-interacting LRR-RKs BIR2 and BIR3 were previously identified by proteomics analyses of in vivo BAK1 complexes. Here, we show that BAK1-related pathways such as innate immunity and cell death control are affected by BIR3 in Arabidopsis thaliana BIR3 also has a strong negative impact on BR signaling. BIR3 directly interacts with the BR receptor BRI1 and other ligand binding receptors and negatively regulates BR signaling by competitive inhibition of BRI1. BIR3 is released from BAK1 and BRI1 after ligand exposure and directly affects the formation of BAK1 complexes with BRI1 or FLAGELLIN SENSING2. Double mutants of bak1 and bir3 show spontaneous cell death and constitutive activation of defense responses. BAK1 and its closest homolog BKK1 interact with and are stabilized by BIR3, suggesting that bak1 bir3 double mutants mimic the spontaneous cell death phenotype observed in bak1 bkk1 mutants via destabilization of BIR3 target proteins. Our results provide evidence for a negative regulatory mechanism for BAK1 receptor complexes in which BIR3 interacts with BAK1 and inhibits ligand binding receptors to prevent BAK1 receptor complex formation.
• Racolta, A., Nodine, M. D., Davies, K., Lee, C., Rowe, S., Velazco, Y., Wellington, R., & Tax, F. E. (2018). A Common Pathway of Root Growth Control and Response to CLE Peptides Through Two Receptor Kinases in Arabidopsis. Genetics, 208(2), 687-704. doi:doi: 10.1534/genetics.117.300148.
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  Cell-cell communication is essential for plants to integrate developmental programs with external cues that affect their growth. Recent advances in plant signaling have uncovered similar molecular mechanisms in shoot, root and vascular meristem signaling that involve receptor-like kinases and small, secreted peptides. Here we report that the receptor-like kinases TOAD2/RPK2 and RPK1 regulate root growth by controlling cell proliferation and affecting meristem size. Two types of developmental alterations were observed upon exogenous CLE peptide application. The first type was detected in all plants treated and comprises increased proliferative activity of cells in the stem cell niche and a delay of progression in differentiation of daughter cells. The second type were changes specific to the genotypes that are sensitive to CLE-driven root meristem inhibition and include a large decrease in the occurrence of cell divisions in longitudinal files, correlating with shorter meristems and cessation of root growth. The root meristems of toad2/rpk2 mutant plants are insensitive to the inhibitory effect of CLE17 peptide treatment, consistent with TOAD2/RPK2 function as a receptor for CLE peptides. In addition, a strong reduction in the expression of RPK1 protein upon CLE treatment, dependent on TOAD2/RPK2, suggests these two RLKs mediate CLE signaling in a common pathway to control root growth.
• Sun, C., Yan, K., Han, J. T., Tao, L., Lv, M. H., Shi, T., He, Y. X., Wierzba, M., Tax, F. E., & Li, J. (2017). Scanning for New BRI1 Mutations via TILLING Analysis. Plant physiology, 174(3), 1881-1896.
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  The identification and characterization of a mutational spectrum for a specific protein can help to elucidate its detailed cellular functions. BRASSINOSTEROID INSENSITIVE1 (BRI1), a multidomain transmembrane receptor-like kinase, is a major receptor of brassinosteroids in Arabidopsis (Arabidopsis thaliana). Within the last two decades, over 20 different bri1 mutant alleles have been identified, which helped to determine the significance of each domain within BRI1. To further understand the molecular mechanisms of BRI1, we tried to identify additional alleles via targeted induced local lesions in genomes. Here, we report our identification of 83 new point mutations in BRI1, including nine mutations that exhibit an allelic series of typical bri1 phenotypes, from subtle to severe morphological alterations. We carried out biochemical analyses to investigate possible mechanisms of these mutations in affecting brassinosteroid signaling. A number of interesting mutations have been isolated via this study. For example, bri1-702, the only weak allele identified so far with a mutation in the activation loop, showed reduced autophosphorylation activity. bri1-705, a subtle allele with a mutation in the extracellular portion, disrupts the interaction of BRI1 with its ligand brassinolide and coreceptor BRI1-ASSOCIATED RECEPTOR KINASE1. bri1-706, with a mutation in the extracellular portion, is a subtle defective mutant. Surprisingly, root inhibition analysis indicated that it is largely insensitive to exogenous brassinolide treatment. In this study, we found that bri1-301 possesses kinase activity in vivo, clarifying a previous report arguing that kinase activity may not be necessary for the function of BRI1. These data provide additional insights into our understanding of the early events in the brassinosteroid signaling pathway.
• Wierzba, M. P., & Tax, F. E. (2016). An Allelic Series of bak1 Mutations Differentially Alter bir1 Cell-Death, Immune Response, Growth, and Root Development Phenotypes in Arabidopsis thaliana. Genetics, 202, 689-702.
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  Receptor-like kinases mediate cell-signaling pathways in Arabidopsis thaliana, including those controlling growth and development, immune response, and cell death. The RLK co-receptor BRI1-ASSOCIATED KINASE-1 (BAK1) partners with multiple ligand-binding RLKs and contributes to their signaling in diverse pathways. An additional RLK, BAK1-INTERACTING RECEPTOR-1 (BIR1), physically interacts with BAK1 and loss-of-function mutations in BIR1 display constitutive activation of cell-death and immune response pathways, dwarfism, and a reduction in lateral root number. Here we show that bir1 plants display defects in primary root growth, characterize bir1 lateral root defects, and analyze expression of BIR1 and BAK1 promoters within the root. Using an allelic series of bak1 mutations, we show that loss of BAK1 function in immune response pathways can partially suppress bir1 cell death, immune response, and lateral root phenotypes, and that null bak1 alleles enhance bir1 primary root phenotypes. Based upon our data we propose a model in which BIR1 functions to regulate BAK1 participation in multiple pathways.
• Shi, T., Dimitrov, I., Zhang, Y., Tax, F. E., Yi, J., Gou, X., & Li, J. (2015). Accelerated rates of protein evolution in barley grain and pistil biased genes might be legacy of domestication. Plant molecular biology, 89(3), 253-61.
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  Traits related to grain and reproductive organs in grass crops have been under continuous directional selection during domestication. Barley is one of the oldest domesticated crops in human history. Thus genes associated with the grain and reproductive organs in barley may show evidence of dramatic evolutionary change. To understand how artificial selection contributes to protein evolution of biased genes in different barley organs, we used Digital Gene Expression analysis of six barley organs (grain, pistil, anther, leaf, stem and root) to identify genes with biased expression in specific organs. Pairwise comparisons of orthologs between barley and Brachypodium distachyon, as well as between highland and lowland barley cultivars mutually indicated that grain and pistil biased genes show relatively higher protein evolutionary rates compared with the median of all orthologs and other organ biased genes. Lineage-specific protein evolutionary rates estimation showed similar patterns with elevated protein evolution in barley grain and pistil biased genes, yet protein sequences generally evolve much faster in the lowland barley cultivar. Further functional annotations revealed that some of these grain and pistil biased genes with rapid protein evolution are related to nutrient biosynthesis and cell cycle/division. Our analyses provide insights into how domestication differentially shaped the evolution of genes specific to different organs of a crop species, and implications for future functional studies of domestication genes.
• Chunli, M. a., Chunli, M. a., Guo, J., Guo, J., Kang, Y., Kang, Y., Doman, K., Doman, K., Bryan, A. C., Bryan, A. C., Tax, F. E., Tax, F. E., Yamaguchi, Y., Yamaguchi, Y., Zhi, Q. i., & Zhi, Q. i. (2014). AtPeptide RECEPTOR2 mediates the AtPeptide1-induced cytosolic Ca²⁺ rise, which is required for the suppression of glutamine dumper gene expression in arabidopsis roots. Journal of Integrative Plant Biology.
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  Abstract: AtPEPTIDE RECEPTOR2 (AtPEPR2) is a member of leucine-rich repeat receptor-like kinase family and binds to a group of AtPROPEP gene-encoded endogenous peptides, AtPeps. Previously, we found that AtPEPR2 plays a moderate role in the AtPep1-mediated innate immunity responses in Arabidopsis leaf. In this study, we found that AtPEPR2 promoter has strong activity in the vascular tissues of the roots and the atpepr2 mutants showed a moderate but significantly shorter root phenotype. AtPEPR2 partially mediated AtPep1-induced root elongation inhibition. AtPep1-triggered cytosolic Ca2+ transient rise in roots showed partial dependence on AtPEPR2 and fully on extracellular Ca2+ ([Ca2+]ext). Transcriptional profiling analysis found that expression of 75% of AtPep1-modulated genes in roots was fully dependent on AtPEPR2, of which two dramatically induced genes showed partial dependence on the [Ca2+]ext. Arabidopsis genome contains seven Glutamine Dumpers genes (AtGDUs), encoding amino acid exporters. Three of them (AtGDU2, 3, 5) were among the top 10 genes that were downregulated by AtPep1 through AtPEPR2 fully dependent pathway. Treatment with AtPep1 strongly suppressed promoter activity of AtGDU3 in roots, which was relieved by chelating [Ca2+]ext. Arabidopsis overexpressing AtGDU3 showed a shorter root phenotype and decreased sensitivity to the AtPep1-mediated inhibition of root elongation. Taken together, this study demonstrated a significant role of AtPEPR2 in the AtPep1-mediated signaling in the roots. © 2014 Institute of Botany, Chinese Academy of Sciences.
• Halter, T., Imkampe, J., Mazzotta, S., Wierzba, M., Postel, S., Bücherl, C., Kiefer, C., Stahl, M., Chinchilla, D., Wang, X., Nürnberger, T., Zipfel, C., Clouse, S., Borst, J. W., Boeren, S., C., S., Tax, F., & Kemmerling, B. (2014). The leucine-rich repeat receptor kinase BIR2 is a negative regulator of BAK1 in plant immunity. Current Biology, 24(2), 134-143.
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  Abstract: Background Transmembrane leucine-rich repeat (LRR) receptors are commonly used innate immune receptors in plants and animals but can also sense endogenous signals to regulate development. BAK1 is a plant LRR-receptor-like kinase (RLK) that interacts with several ligand-binding LRR-RLKs to positively regulate their functions. BAK1 is involved in brassinosteroid-dependent growth and development, innate immunity, and cell-death control by interacting with the brassinosteroid receptor BRI1, immune receptors, such as FLS2 and EFR, and the small receptor kinase BIR1, respectively. Results Identification of in vivo BAK1 complex partners by LC/ESI-MS/MS uncovered two novel BAK1-interacting RLKs, BIR2 and BIR3. Phosphorylation studies revealed that BIR2 is unidirectionally phosphorylated by BAK1 and that the interaction between BAK1 and BIR2 is kinase-activity dependent. Functional analyses of bir2 mutants show differential impact on BAK1-regulated processes, such as hyperresponsiveness to pathogen-associated molecular patterns (PAMP), enhanced cell death, and resistance to bacterial pathogens, but have no effect on brassinosteroid- regulated growth. BIR2 interacts constitutively with BAK1, thereby preventing interaction with the ligand-binding LRR-RLK FLS2. PAMP perception leads to BIR2 release from the BAK1 complex and enables the recruitment of BAK1 into the FLS2 complex. Conclusions Our results provide evidence for a new regulatory mechanism for innate immune receptors with BIR2 acting as a negative regulator of PAMP-triggered immunity by limiting BAK1-receptor complex formation in the absence of ligands. © 2014 Elsevier Ltd.
• Racolta, A., Bryan, A. C., & Tax, F. E. (2014). The receptor-like kinases GSO1 and GSO2 together regulate root growth in arabidopsis through control of cell division and cell fate specification. Developmental Dynamics, 243(2), 257-278.
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  Abstract: Background: The root apical meristem of Arabidopsis is established post-embryonically as the main source of root cells, and its activity is maintained by complex bidirectional signaling between stem cells and mature cells. The receptor-like kinases GASSHO1 (GSO1) and GSO2 have been shown to regulate aerial epidermal function and seedling growth in Arabidopsis. Results: Here we show that gso1; gso2 seedlings also have root growth and patterning defects. Analyses of mutant root morphology indicate abnormal numbers of cells in longitudinal files and radial cell layers, as well as aberrant stem cell division planes. gso1; gso2 double mutants misexpress markers for stem cells and differentiated root cell types. In addition, gso1; gso2 root growth defects, but not marker missexpression or patterning phenotypes, are rescued by growth on media containing metabolizable sugars. Conclusions: We conclude that GSO1 and GSO2 function together in intercellular signaling to positively regulate cell proliferation, differentiation of root cell types, and stem cell identity. In addition, GSO1 and GSO2 control seedling root growth by modulating sucrose response after germination. Developmental Dynamics 243:257-278, 2014. © 2013 Wiley Periodicals, Inc.
• Jia, L. i., Jia, L. i., Tax, F. E., & Tax, F. E. (2013). Receptor-Like Kinases: Key Regulators of Plant Development and Defense. Journal of Integrative Plant Biology, 55(12), 1184-1187.
• Mosher, S., Seybold, H., Rodriguez, P., Stahl, M., Davies, K. A., Dayaratne, S., Morillo, S. A., Wierzba, M., Favery, B., Keller, H., Tax, F. E., & Kemmerling, B. (2013). The tyrosine-sulfated peptide receptors PSKR1 and PSY1R modify the immunity of Arabidopsis to biotrophic and necrotrophic pathogens in an antagonistic manner. Plant Journal, 73(3), 469-482.
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  PMID: 23062058;Abstract: Summary The tyrosine-sulfated peptides PSKα and PSY1 bind to specific leucine-rich repeat surface receptor kinases and control cell proliferation in plants. In a reverse genetic screen, we identified the phytosulfokine (PSK) receptor PSKR1 as an important component of plant defense. Multiple independent loss-of-function mutants in PSKR1 are more resistant to biotrophic bacteria, show enhanced pathogen-associated molecular pattern responses and less lesion formation after infection with the bacterial pathogen Pseudomonas syringae pv. tomato DC3000. By contrast, pskr1 mutants are more susceptible to necrotrophic fungal infection with Alternaria brassicicola, show more lesion formation and fungal growth which is not observed on wild-type plants. The antagonistic effect on biotrophic and necrotrophic pathogen resistance is reflected by enhanced salicylate and reduced jasmonate responses in the mutants, suggesting that PSKR1 suppresses salicylate-dependent defense responses. Detailed analysis of single and multiple mutations in the three paralogous genes PSKR1, -2 and PSY1-receptor (PSY1R) determined that PSKR1 and PSY1R, but not PSKR2, have a partially redundant effect on plant immunity. In animals and plants, peptide sulfation is catalyzed by a tyrosylprotein sulfotransferase (TPST). Mutants lacking TPST show increased resistance to bacterial infection and increased susceptibility to fungal infection, mimicking the triple receptor mutant phenotypes. Feeding experiments with PSKα in tpst-1 mutants partially restore the defense-related phenotypes, indicating that perception of the PSKα peptide has a direct effect on plant defense. These results suggest that the PSKR subfamily integrates growth-promoting and defense signals mediated by sulfated peptides and modulates cellular plasticity to allow flexible adjustment to environmental changes. © 2012 The Authors The Plant Journal © 2012 Blackwell Publishing Ltd.
• Replogle, A., Wang, J., Paolillo, V., Smeda, J., Kinoshita, A., Durbak, A., Tax, F. E., Wang, X., Sawa, S., & Mitchum, M. G. (2013). Synergistic interaction of clavata1, clavata2, and receptor-like protein kinase 2 in cyst nematode parasitism of arabidopsis. Molecular Plant-Microbe Interactions, 26(1), 87-96.
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  PMID: 22835273;Abstract: Plant-parasitic cyst nematodes secrete CLAVATA3 (CLV3)/ ENDOSPERM SURROUNDING REGION (CLE)-like effector proteins. These proteins act as ligand mimics of plant CLE peptides and are required for successful nematode infection. Previously, we showed that the CLV2/ CORYNE (CRN) heterodimer receptor complex is required for nematode CLE signaling. However, there was only a partial reduction in nematode infection when this signaling was disrupted, indicating that there might be additional nematode CLE receptors. In this study, we demonstrate that CLV1 and RECEPTOR-LIKE PROTEIN KINASE 2/TOADSTOOL2 (RPK2), two additional receptors that can transmit the CLV3 signal independent of CLV2/CRN for shoot apical meristem maintenance, also play a role in nematode CLE perception. Localization studies showed that both receptors are expressed in nematode-induced syncytia. Infection assays with clv1 and rpk2 single mutants revealed a decrease in both nematode infection and syncytium size. Significantly, further reduction in nematode infection was observed when rpk2 was combined with clv1 and clv2 mutants. Taken together, our results indicate that parallel signaling pathways involving CLV1, CLV2, and RPK2 are important for nematode parasitism. © 2013 The American Phytopathological Society.
• Tax, F., Racolta, A., Bryan, A. C., & Tax, F. E. (2013). The receptor-like kinases GSO1 and GSO2 together regulate root growth in Arabidopsis through control of cell division and cell fate specification. Developmental dynamics : an official publication of the American Association of Anatomists.
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  Background: The root apical meristem of Arabidopsis is established post-embryonically as the main source of root cells, and its activity is maintained by complex bidirectional signaling between stem cells and mature cells. The receptor-like kinases GASSHO1 (GSO1) and GSO2 have been shown to regulate aerial epidermal function and seedling growth in Arabidopsis. Results: Here we show that gso1; gso2 seedlings also have root growth and patterning defects. Analyses of mutant root morphology indicate abnormal numbers of cells in longitudinal files and radial cell layers, as well as aberrant stem cell division planes. gso1; gso2 double mutants misexpress markers for stem cells and differentiated root cell types. Finally, gso1; gso2 root growth defects, but not marker missexpression or patterning phenotypes, are rescued by growth on media containing metabolizable sugars. Conclusions: We conclude that GSO1 and GSO2 function together in intercellular signaling to positively regulate cell proliferation, differentiation of root cell types, and stem cell identity. In addition, GSO1 and GSO2 control seedling root growth by modulating sucrose response after germination. Developmental Dynamics, 2013. © 2013 Wiley Periodicals, Inc.
• Tax, F., Wierzba, M. P., & Tax, F. E. (2013). Notes from the Underground: Receptor-Like Kinases in Arabidopsis Root Development. Journal of integrative plant biology.
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  During plant development, the frequency and context of cell division must be controlled, and cells must differentiate properly to perform their mature functions. In addition, stem cell niches need to be maintained as a reservoir for new cells. All of these processes require intercellular signaling, whether it is a cell relaying its position to other cells, or more mature cells signaling to the stem cell niche to regulate the rate of growth. Receptor-like kinases have emerged as a major component in these diverse roles, especially within the Arabidopsis root. In this review, the functions of receptor-like kinase signaling in regulating Arabidopsis root development will be examined in the areas of root apical meristem maintenance, regulation of epidermal cell fate, lateral root development and vascular differentiation. [Figure: see text] Frans E. Tax (Corresponding author).
• Wierzba, M. P., Wierzba, M. P., Tax, F. E., & Tax, F. E. (2013). Notes from the Underground: Receptor-like kinases in arabidopsis root development. Journal of Integrative Plant Biology, 55(12), 1224-1237.
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  Abstract: During plant development, the frequency and context of cell division must be controlled, and cells must differentiate properly to perform their mature functions. In addition, stem cell niches need to be maintained as a reservoir for new cells. All of these processes require intercellular signaling, whether it is a cell relaying its position to other cells, or more mature cells signaling to the stem cell niche to regulate the rate of growth. Receptor-like kinases have emerged as a major component in these diverse roles, especially within the Arabidopsis root. In this review, the functions of receptor-like kinase signaling in regulating Arabidopsis root development will be examined in the areas of root apical meristem maintenance, regulation of epidermal cell fate, lateral root development and vascular differentiation. © 2013 Institute of Botany, Chinese Academy of Sciences.
• Bryan, A. C., Obaidi, A., Wierzba, M., & Tax, F. E. (2012). XYLEM INTERMIXED WITH PHLOEM1, a leucine-rich repeat receptor-like kinase required for stem growth and vascular development in Arabidopsis thaliana. Planta, 235(1), 111-122.
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  PMID: 21853254;Abstract: The regulation of cell specification in plants is particularly important in vascular development. The vascular system is comprised two differentiated tissue types, the xylem and phloem, which form conductive elements for the transport of water, nutrients and signaling molecules. A meristematic layer, the procambium, is located between these two differentiated cell types and divides to initiate vascular growth. We report the identification of a receptor-like kinase (RLK) that is expressed in the vasculature. Histochemical analyses of mutants in this kinase display an aberrant accumulation of highly lignified cells, typical of xylem or fiber cells, within the phloem. In addition, phloem cells are sometimes located adjacent to xylem cells in these mutants. We, therefore, named this RLK XYLEM INTERMIXED WITH PHLOEM 1 (XIP1). Analyses of longitudinal profiles of xip1 mutant stems show malformed cell files, indicating defects in oriented cell divisions or cell morphology. We propose that XIP1 prevents ectopic lignification in phloem cells and is necessary to maintain the organization of cell files or cell morphology in conductive elements. © 2011 Springer-Verlag.
• Tax, F., Bryan, A. C., Obaidi, A., Wierzba, M., & Tax, F. E. (2012). XYLEM INTERMIXED WITH PHLOEM1, a leucine-rich repeat receptor-like kinase required for stem growth and vascular development in Arabidopsis thaliana. Planta, 235(1).
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  The regulation of cell specification in plants is particularly important in vascular development. The vascular system is comprised two differentiated tissue types, the xylem and phloem, which form conductive elements for the transport of water, nutrients and signaling molecules. A meristematic layer, the procambium, is located between these two differentiated cell types and divides to initiate vascular growth. We report the identification of a receptor-like kinase (RLK) that is expressed in the vasculature. Histochemical analyses of mutants in this kinase display an aberrant accumulation of highly lignified cells, typical of xylem or fiber cells, within the phloem. In addition, phloem cells are sometimes located adjacent to xylem cells in these mutants. We, therefore, named this RLK XYLEM INTERMIXED WITH PHLOEM 1 (XIP1). Analyses of longitudinal profiles of xip1 mutant stems show malformed cell files, indicating defects in oriented cell divisions or cell morphology. We propose that XIP1 prevents ectopic lignification in phloem cells and is necessary to maintain the organization of cell files or cell morphology in conductive elements.
• Brooks, E., Dolan, E., & Tax, F. (2011). Partnership for Research & Education in Plants (PREP): Involving high school students in authentic research in collaboration with scientists. American Biology Teacher, 73(3), 137-142.
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  Abstract: A partnership between scientists, high school teachers, and their students provides authentic research experiences to help students understand the nature and processes of science. The Partnership for Research and Education in Plants (PREP) engages students in a large-scale genomics research project using classroom-tested protocols that can help to find the function of a disabled gene in the widely studied plant Arabidopsis thaliana. Here, we describe the framework of PREP in the classroom within the context of the National Science Education Standards. © 2011 by National Association of Biology Teachers. All rights reserved.
• Durbak, A. R., & Tax, F. E. (2011). CLAVATA signaling pathway receptors of arabidopsis regulate cell proliferation in fruit organ formation as well as in meristems. Genetics, 189(1), 177-194.
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  PMID: 21705761;PMCID: PMC3176120;Abstract: The CLAVATA1 (CLV1), CLV2, and CORYNE (CRN) receptors in Arabidopsis thaliana maintain cell proliferation in shoot apical meristems by restricting expression of the transcription factor WUSCHEL (WUS). Previously characterized receptor mutants generate extra fruit and floral organs that are proposed to arise from enlarged floral meristems (FMs). We identified new alleles in clv1, clv2, and crn and found that most mutants produce only extra fruit organs and generate FMs of similar dimensions as wild type. Characterization of gynoecium development in receptor mutants revealed increased cell proliferation and ectopic fruit organ initiation after FM termination. These regions of increased cell division also display expanded expression of the cell proliferation-promoting transcription factor SHOOTMERISTEMLESS (STM), similar to the expansion of WUS expression in the shoot apical meristems of strong clv1 mutants. We also examined genetic interactions between the ERECTA (ER) and BARELY ANY MERISTEM 1 (BAM1) receptor-like kinases and CLV pathway receptors. Our results suggest a model in which CLV1/BAM1 and CLV2/CRN complexes act in separate, parallel pathways in shoot meristems, while the CLV1, CLV2, and CRN receptors function together in a linear pathway during fruit development. These results demonstrate the importance of regulating cell proliferation in plants that undergo organogenesis throughout their life cycle. © 2011 by the Genetics Society of America.
• Nodine, M. D., Bryan, A. C., Racolta, A., Jerosky, K. V., & Tax, F. E. (2011). A few standing for many: Embryo receptor-like kinases. Trends in Plant Science, 16(4), 211-217.
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  PMID: 21349757;Abstract: Development of plant embryos is a complex and highly organized process, and experimental evidence indicates that intercellular signaling plays a major role. The recent identification of Receptor-Like Kinases (RLKs) and related Receptor-Like Cytoplasmic Kinases (RLCKs) with specific roles in Arabidopsis thaliana embryo development suggest important functions of intercellular signaling during embryogenesis. Despite the characterization of only a few RLKs and RLCKs with embryonic roles, expression data indicate that many RLKs and RLCKs with either post-embryonic functions or unknown functions are transcribed in Arabidopsis embryos. The functional characterization of a few members of this large kinase family is likely to represent only the tip of the iceberg, and we predict that many RLKs and RLCKs play major roles throughout embryo development. © 2011 Elsevier Ltd.
• Tax, F., Durbak, A. R., & Tax, F. E. (2011). CLAVATA signaling pathway receptors of Arabidopsis regulate cell proliferation in fruit organ formation as well as in meristems. Genetics, 189(1).
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  The CLAVATA1 (CLV1), CLV2, and CORYNE (CRN) receptors in Arabidopsis thaliana maintain cell proliferation in shoot apical meristems by restricting expression of the transcription factor WUSCHEL (WUS). Previously characterized receptor mutants generate extra fruit and floral organs that are proposed to arise from enlarged floral meristems (FMs). We identified new alleles in clv1, clv2, and crn and found that most mutants produce only extra fruit organs and generate FMs of similar dimensions as wild type. Characterization of gynoecium development in receptor mutants revealed increased cell proliferation and ectopic fruit organ initiation after FM termination. These regions of increased cell division also display expanded expression of the cell proliferation-promoting transcription factor SHOOTMERISTEMLESS (STM), similar to the expansion of WUS expression in the shoot apical meristems of strong clv1 mutants. We also examined genetic interactions between the ERECTA (ER) and BARELY ANY MERISTEM 1 (BAM1) receptor-like kinases and CLV pathway receptors. Our results suggest a model in which CLV1/BAM1 and CLV2/CRN complexes act in separate, parallel pathways in shoot meristems, while the CLV1, CLV2, and CRN receptors function together in a linear pathway during fruit development. These results demonstrate the importance of regulating cell proliferation in plants that undergo organogenesis throughout their life cycle.
• Belkhadir, Y., Durbak, A., Wierzba, M., Schmitz, R. J., Aguirre, A., Michel, R., Rowe, S., Fujioka, S., & Tax, F. E. (2010). Intragenic suppression of a trafficking-defective brassinosteroid receptor mutant in arabidopsis. Genetics, 185(4), 1283-1296.
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  PMID: 20457881;PMCID: PMC2927756;Abstract: The cell surface receptor kinase BRASSINOSTEROID-INSENSITIVE-1 (BRI1) is the major receptor for steroid hormones in Arabidopsis. Plants homozygous for loss-of-function mutations in BRI1 display a reduction in the size of vegetative organs, resulting in dwarfism. The recessive bri1-5 mutation produces receptors that do not accumulate to wild-type levels and are retained mainly in the endoplasmic reticulum. We have isolated a dominant suppressor of the dwarf phenotype of bri1-5 plants. We show that this suppression is caused by a second-site mutation in BRI1, bri1-5R1. The bri1-5R1 mutation partially rescues the phenotypes of bri1-5 in many tissues and enhances bri1-5 phenotypes above wild-type levels in several other tissues. We demonstrate that the phenotypes of bri1-5R1 plants are due to both increased cell expansion and increased cell division. To test the mechanism of bri1-5 suppression, we assessed whether the phenotypic suppression in bri1-5R1 was dependent on ligand availability and the integrity of the signaling pathway. Our results indicate that the suppression of the dwarf phenotypes associated with bri1-5R1 requires both BR biosynthesis and the receptor kinase BRI1-ASSOCIATED KINASE-1 (BAK1). Finally, we show that bri1-5R1 partially restores the accumulation and plasma membrane localization of BRI1. Collectively, our results point toward a model in which bri1-R1 compensates for the protein-folding abnormalities caused by bri1-5, restoring accumulation of the receptor and its delivery to the cell surface. Copyright © 2010 by the Genetics Society of America.
• Yamaguchi, Y., Huffaker, A., Bryan, A. C., Tax, F. E., & Ryan, C. A. (2010). PEPR2 is a second receptor for the Pep1 and Pep2 peptides and contributes to defense responses in Arabidopsis. Plant Cell, 22(2), 508-522.
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  PMID: 20179141;PMCID: PMC2845411;Abstract: Pep1 is a 23-amino acid peptide that enhances resistance to a root pathogen, Pythium irregulare. Pep1 and its homologs (Pep2 to Pep7) are endogenous amplifiers of innate immunity of Arabidopsis thaliana that induce the transcription of defense-related genes and bind to PEPR1, a plasma membrane leucine-rich repeat (LRR) receptor kinase. Here, we identify a plasma membrane LRR receptor kinase, designated PEPR2, that has 76% amino acid similarity to PEPR1, and we characterize its role in the perception of Pep peptides and defense responses. Both PEPR1 and PEPR2 were transcriptionally induced by wounding, treatment with methyl jasmonate, Pep peptides, and pathogen-associated molecular patterns. The effects of Pep1 application on defense-related gene induction and enhancement of resistance to Pseudomonas syringae pv tomato DC3000 were partially reduced in single mutants of PEPR1 and PEPR2 and abolished completely in double mutants. Photoaffinity labeling and binding assays using transgenic tobacco (Nicotiana tabacum) cells expressing PEPR1 and PEPR2 clearly demonstrated that PEPR1 is a receptor for Pep1-6 and that PEPR2 is a receptor for Pep1 and Pep2. Our analysis demonstrates differential binding affinities of two receptors with a family of peptide ligands and the corresponding physiological effects of the specific receptor-ligand interactions. Therefore, we demonstrate that, through perception of Peps, PEPR1 and PEPR2 contribute to defense responses in Arabidopsis. © 2010 American Society of Plant Biologists.
• Nodine, M. D., & Tax, F. E. (2008). Two receptor-like kinases required together for the establishment of Arabidopsis cotyledon primordia. Developmental Biology, 314(1), 161-170.
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  PMID: 18158146;Abstract: Inter-regional signaling coordinates pattern formation in Arabidopsis thaliana embryos. However, little is known regarding the cells and molecules involved in inter-regional communication. We have characterized two related leucine-rich repeat receptor-like kinases (LRR-RLKs), RECEPTOR-LIKE PROTEIN KINASE1 (RPK1) and TOADSTOOL2 (TOAD2), which are required together for patterning the apical embryonic domain cell types that generate cotyledon primordia. Central domain protoderm patterning defects were always observed subjacent to the defective cotyledon primordia cell types in mutant embryos. In addition, RPK1-GFP and TOAD2-GFP translational fusions were both localized to the central domain protodermal cells when cotyledon primordia were first recognizable. We propose that RPK1 and TOAD2 are primarily required to maintain central domain protoderm cell fate and that the loss of this key embryonic cell type in mutant embryos results in patterning defects in other regions of the embryo including the failure to initiate cotyledon primordia. © 2007 Elsevier Inc. All rights reserved.
• Tax, F., Nodine, M. D., & Tax, F. E. (2008). Two receptor-like kinases required together for the establishment of Arabidopsis cotyledon primordia. Developmental biology, 314(1).
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  Inter-regional signaling coordinates pattern formation in Arabidopsis thaliana embryos. However, little is known regarding the cells and molecules involved in inter-regional communication. We have characterized two related leucine-rich repeat receptor-like kinases (LRR-RLKs), RECEPTOR-LIKE PROTEIN KINASE1 (RPK1) and TOADSTOOL2 (TOAD2), which are required together for patterning the apical embryonic domain cell types that generate cotyledon primordia. Central domain protoderm patterning defects were always observed subjacent to the defective cotyledon primordia cell types in mutant embryos. In addition, RPK1-GFP and TOAD2-GFP translational fusions were both localized to the central domain protodermal cells when cotyledon primordia were first recognizable. We propose that RPK1 and TOAD2 are primarily required to maintain central domain protoderm cell fate and that the loss of this key embryonic cell type in mutant embryos results in patterning defects in other regions of the embryo including the failure to initiate cotyledon primordia.
• Lally, D., Brooks, E., Tax, F. E., & Dolan, E. L. (2007). Sowing the seeds of dialogue: Public engagement through plant science. Plant Cell, 19(8), 2311-2319.
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  PMID: 17766406;PMCID: PMC2002607;
• Nodine, M. D., Yadegari, R., & Tax, F. E. (2007). RPK1 and TOAD2 Are Two Receptor-like Kinases Redundantly Required for Arabidopsis Embryonic Pattern Formation. Developmental Cell, 12(6), 943-956.
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  PMID: 17543866;Abstract: Although the basic plant body plan is established during embryogenesis, the molecular basis of embryonic patterning remains to be fully understood. We have identified two receptor-like kinases, RECEPTOR-LIKE PROTEIN KINASE1 (RPK1) and TOADSTOOL2 (TOAD2), required for Arabidopsis embryonic pattern formation. Genetic analysis indicates that RPK1 and TOAD2 have overlapping embryonic functions. The zygotic gene dosage of TOAD2 in an rpk1 background is of critical importance, suggesting that signaling mediated by RPK1 and TOAD2 must be above a threshold level for proper embryo development. The localization of RPK1 and TOAD2 translational fusions to GFP coupled with the analysis of cell-type-specific markers indicate that RPK1 and TOAD2 are redundantly required for both pattern formation along the radial axis and differentiation of the basal pole during early embryogenesis. We propose that RPK1 and TOAD2 receive intercellular signals and mediate intracellular responses that are necessary for embryonic pattern formation. © 2007 Elsevier Inc. All rights reserved.
• Tax, F., Nodine, M. D., Yadegari, R., & Tax, F. E. (2007). RPK1 and TOAD2 are two receptor-like kinases redundantly required for arabidopsis embryonic pattern formation. Developmental cell, 12(6).
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  Although the basic plant body plan is established during embryogenesis, the molecular basis of embryonic patterning remains to be fully understood. We have identified two receptor-like kinases, RECEPTOR-LIKE PROTEIN KINASE1 (RPK1) and TOADSTOOL2 (TOAD2), required for Arabidopsis embryonic pattern formation. Genetic analysis indicates that RPK1 and TOAD2 have overlapping embryonic functions. The zygotic gene dosage of TOAD2 in an rpk1 background is of critical importance, suggesting that signaling mediated by RPK1 and TOAD2 must be above a threshold level for proper embryo development. The localization of RPK1 and TOAD2 translational fusions to GFP coupled with the analysis of cell-type-specific markers indicate that RPK1 and TOAD2 are redundantly required for both pattern formation along the radial axis and differentiation of the basal pole during early embryogenesis. We propose that RPK1 and TOAD2 receive intercellular signals and mediate intracellular responses that are necessary for embryonic pattern formation.
• Morillo, S. A., & Tax, F. E. (2006). Functional analysis of receptor-like kinases in monocots and dicots. Current Opinion in Plant Biology, 9(5), 460-469.
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  PMID: 16877029;Abstract: Receptor-like kinases (RLKs) are signaling proteins that feature an extracellular domain connected via a transmembrane domain to a cytoplasmic kinase. This architecture indicates that RLKs perceive external signals, transducing them into the cell. In plants, RLKs were first implicated in the regulation of development, in pathogen responses, and in recognition events. RLKs comprise a major gene family in plants, with more than 600 encoded in the Arabidopsis genome and more than 1100 found in rice genomes. The greater number of RLKs in rice is mostly attributable to expansions in the clades that are involved in pathogen responses. Recent functional studies in both monocots and dicots continue to identify individual RLKs that have similar developmental and abiotic stress roles. Analysis of closely related RLKs reveals that family members might have overlapping roles but can also possess distinct functions. © 2006 Elsevier Ltd. All rights reserved.
• Tax, F. E., & Durbak, A. (2006). Meristems in the movies: Live imaging as a tool for decoding intercellular signaling in shoot apical meristems. Plant Cell, 18(6), 1331-1337.
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  PMID: 16741235;PMCID: PMC1475494;
• Tax, F., Morillo, S. A., & Tax, F. E. (2006). Functional analysis of receptor-like kinases in monocots and dicots. Current opinion in plant biology, 9(5).
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  Receptor-like kinases (RLKs) are signaling proteins that feature an extracellular domain connected via a transmembrane domain to a cytoplasmic kinase. This architecture indicates that RLKs perceive external signals, transducing them into the cell. In plants, RLKs were first implicated in the regulation of development, in pathogen responses, and in recognition events. RLKs comprise a major gene family in plants, with more than 600 encoded in the Arabidopsis genome and more than 1100 found in rice genomes. The greater number of RLKs in rice is mostly attributable to expansions in the clades that are involved in pathogen responses. Recent functional studies in both monocots and dicots continue to identify individual RLKs that have similar developmental and abiotic stress roles. Analysis of closely related RLKs reveals that family members might have overlapping roles but can also possess distinct functions.
• Kim, G., Fujioka, S., Kozuka, T., Tax, F. E., Takatsuto, S., Yoshida, S., & Tsukaya, H. (2005). CYP90C1 and CYP90D1 are involved in different steps in the brassinosteroid biosynthesis pathway in Arabidopsis thaliana. Plant Journal, 41(5), 710-721.
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  PMID: 15703058;Abstract: Brassinosteroids (BRs) are plant hormones that are essential for a wide range of developmental processes in plants. Many of the genes responsible for the early reactions in the biosynthesis of BRs have recently been identified. However, several genes for enzymes that catalyze late steps in the biosynthesis pathways of BRs remain to be identified, and only a few genes responsible for the reactions that produce bioactive BRs have been identified. We found that the ROTUNDIFOLIA3 (ROT3) gene, encoding the enzyme CYP90C1, which was specifically involved in the regulation of leaf length in Arabidopsis thaliana, was required for the late steps in the BR biosynthesis pathway. ROT3 appears to be required for the conversion of typhasterol to castasterone, an activation step in the BR pathway. We also analyzed the gene most closely related to ROT3, CYP90D1, and found that double mutants for ROT3 and CYP90D1 had a severe dwarf phenotype, whereas cyp90d1 single knockout mutants did not. BR profiling in these mutants revealed that CYP90D1 was also involved in BR biosynthesis pathways. ROT3 and CYP90D1 were expressed differentially in leaves of A. thaliana, and the mutants for these two genes differed in their defects in elongation of hypocotyls under light conditions. The expression of CYP90D1 was strongly induced in leaf petioles in the dark. The results of the present study provide evidence that the two cytochrome P450s, CYP90C1 and CYP90D1, play distinct roles in organ-specific environmental regulation of the biosynthesis of BRs. © 2005 Blackwell Publishing Ltd.
• Diévart, A., Dalal, M., Tax, F. E., Lacey, A. D., Huttly, A., Jianming, L. i., & Clark, S. E. (2003). CLAVATA1 dominant-negative alleles reveal functional overlap between multiple receptor kinases that regulate meristem and organ development. Plant Cell, 15(5), 1198-1211.
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  PMID: 12724544;PMCID: PMC153726;Abstract: The CLAVATA1 (CLV1) receptor kinase controls stem cell number and differentiation at the Arabidopsis shoot and flower meristems. Other components of the CLV1 signaling pathway include the secreted putative ligand CLV3 and the receptor-like protein CLV2. We report evidence indicating that all intermediate and strong clv1 alleles are dominant negative and likely interfere with the activity of unknown receptor kinase(s) that have functional overlap with CLV1. clv1 dominant-negative alleles show major differences from dominant-negative alleles characterized to date in animal receptor kinase signaling systems, including the lack of a dominant-negative effect of kinase domain truncation and the ability of missense mutations in the extracellular domain to act in a dominant-negative manner. We analyzed chimeric receptor kinases by fusing CLV1 and BRASSINOSTEROID INSENSITIVE1 (BRI1) coding sequences and expressing these in clv1 null backgrounds. Constructs containing the CLV1 extracellular domain and the BRI1 kinase domain were strongly dominant negative in the regulation of meristem development. Furthermore, we show that CLV1 expressed within the pedicel can partially replace the function of the ERECTA receptor kinase. We propose the presence of multiple receptors that regulate meristem development in a functionally related manner whose interactions are driven by the extracellular domains and whose activation requires the kinase domain.
• Choe, S., Schmitz, R. J., Fujioka, S., Takatsuto, S., Lee, M., Yoshida, S., Feldmann, K. A., & Tax, F. E. (2002). Arabidopsis brassinosteroid-insensitive dwarf12 mutants are semidominant and defective in a glycogen synthase kinase 3β-like kinase. Plant Physiology, 130(3), 1506-1515.
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  PMID: 12428015;PMCID: PMC166669;Abstract: Mutants defective in the biosynthesis or signaling of brassinosteroids (BRs), plant steroid hormones, display dwarfism. Loss-of-function mutants for the gene encoding the plasma membrane-located BR receptor BRI1 are resistant to exogenous application of BRs, and characterization of this protein has contributed significantly to the understanding of BR signaling. We have isolated two new BR-insensitive mutants (dwarf12-1D and dwf12-2D) after screening Arabidopsis ethyl methane-sulfonate mutant populations, dwf12 mutants displayed the characteristic morphology of previously reported BR dwarfs including short stature, short round leaves, infertility, and abnormal de-etiolation. In addition, dwf12 mutants exhibited several unique phenotypes, including severe downward curling of the leaves. Genetic analysis indicates that the two mutations are semidominant in that heterozygous plants show a semidwarf phenotype whose height is intermediate between wild-type and homozygous mutant plants. Unlike BR biosynthetic mutants, dwf12 plants were not rescued by high doses of exogenously applied BRs. Like bri1 mutants, dwf12 plants accumulated castasterone and brassinolide, 43- and 15-fold higher, respectively, providing further evidence that DWF12 is a component of the BR signaling pathway that includes BRI1. Map-based cloning of the DWF12 gene revealed that DWF12 belongs to a member of the glycogen synthase kinase 3β family. Unlike human glycogen synthase kinase 3β, DWF12 lacks the conserved serine-9 residue in the auto-inhibitory N terminus. In addition, dwf12-1D and dwf12-2D encode changes in consecutive glutamate residues in a highly conserved TREE domain. Together with previous reports that both bin2 and ucu1 mutants contain mutations in this TREE domain, this provides evidence that the TREE domain is of critical importance for proper function of DWF12/BIN2/UCU1 in BR signal transduction pathways.
• Jia, L. i., Wen, J., Lease, K. A., Doke, J. T., Tax, F. E., & Walker, J. C. (2002). BAK1, an Arabidopsis LRR receptor-like protein kinase, interacts with BRI1 and modulates brassinosteroid signaling. Cell, 110(2), 213-222.
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  PMID: 12150929;Abstract: Brassinosteroids regulate plant growth and development through a protein complex that includes the leucine-rich repeat receptor-like protein kinase (LRR-RLK) brassinosteroid-insensitive 1 (BRI1). Activation tagging was used to identify a dominant genetic suppressor of bri1, bak1-1D (bri1-associated receptor kinase 1-1Dominant), which encodes an LRR-RLK, distinct from BRI1. Overexpression of BAK1 results in elongated organ phenotypes, while a null allele of BAK1 displays a semidwarfed phenotype and has reduced sensitivity to brassinosteroids (BRs). BAK1 is a serine/threonine protein kinase, and BRI1 and BAK1 interact in vitro and in vivo. Expression of a dominant-negative mutant allele of BAK1 causes a severe dwarf phenotype, resembling the phenotype of null bri1 alleles. These results indicate BAK1 is a component of BR signaling.
• Zhao, J., Peng, P., Schmitz, R. J., Decker, A. D., Tax, F. E., & Jianming, L. i. (2002). Two putative BIN2 substrates are nuclear components of brassinosteroid signaling. Plant Physiology, 130(3), 1221-1229.
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  PMID: 12427989;PMCID: PMC166643;Abstract: GSK3 is a highly conserved kinase that negatively regulates many cellular processes by phosphorylating a variety of protein substrates. BIN2 is a GSK3-like kinase in Arabidopsis that functions as a negative regulator of brassinosteroid (BR) signaling. It was proposed that BR signals, perceived by a membrane BR receptor complex that contains the leucine (Leu)-rich repeat receptor-like kinase BRI1, inactivate BIN2 to relieve its inhibitory effect on unknown downstream BR-signaling components. Using a yeast (Saccharomyces cerevisiae) two-hybrid approach, we discovered a potential BIN2 substrate that is identical to a recently identified BR-signaling protein, BES1. BES1 and its closest homolog, BZR1, which was also uncovered as a potential BR-signaling protein, display specific interactions with BIN2 in yeast. Both BES1 and BZR1 contain many copies of a conserved GSK3 phosphorylation site and can be phosphorylated by BIN2 in vitro via a novel GSK3 phosphorylation mechanism that is independent of a priming phosphorylation ora scaffold protein. Five independent bes1 alleles containing the same proline-233-Leu mutation were identified as semidominant suppressors of two different bri1 mutations. Overexpression of the wild-type BZR1 gene partially complemented bin2/+ mutants and resulted in a BRI1 overexpression phenotype in a BIN2+ background, whereas overexpression of a mutated BZR1 gene containing the corresponding proline-234-Leu mutation rescued a weak bri1 mutation and led to a bes1-like phenotype. Confocal microscopic analysis indicated that both BES1 and BZR1 proteins were mainly localized in the nucleus. We propose that BES1/BZR1 are two nuclear components of BR signaling that are negatively regulated by BIN2 through a phosphorylation-initiated process.
• Bak, S., Tax, F. E., Feldmann, K. A., Galbraith, D. W., & Feyereisen, R. (2001). CYP83B1, a cytochrome P450 at the metabolic branch point in auxin and indole glucosinolate biosynthesis in Arabidopsis. Plant Cell, 13(1), 101-111.
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  PMID: 11158532;PMCID: PMC102201;Abstract: Auxins are growth regulators involved in virtually all aspects of plant development. However, little is known about how plants synthesize these essential compounds. We propose that the level of indole-3-acetic acid is regulated by the flux of indole-3-acetaldoxime through a cytochrome P450, CYP83B1, to the glucosinolate pathway. A T-DNA insertion in the CYP83B1 gene leads to plants with a phenotype that suggests severe auxin overproduction, whereas CYP83B1 overexpression leads to loss of apical dominance typical of auxin deficit. CYP83B1 N-hydroxylates indole-3-acetaldoxime to the corresponding aci-nitro compound, 1-aci-nitro-2-indolyl-ethane, with a Km of 3 μM and a turnover number of 53 min-1. The aci-nitro compound formed reacts non-enzymatically with thiol compounds to produce an N-alkyl-thiohy-droximate adduct, the committed precursor of glucosinolates. Thus, indole-3-acetaldoxime is the metabolic branch point between the primary auxin indole-3-acetic acid and indole glucosinolate biosynthesis in Arabidopsis.
• Gribskov, M., Fana, F., Harper, J., Hope, D. A., Harmon, A. C., Smith, D. W., Tax, F. E., & Zhang, G. (2001). PlantsP: A functional genomics database for plant phosphorylation. Nucleic Acids Research, 29(1), 111-113.
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  PMID: 11125063;PMCID: PMC29854;Abstract: The PlantsP database is a curated database that combines information derived from sequences with experimental functional genomics information. PlantsP focuses on plant protein kinases and protein phosphatases. The database will specifically provide a resource for information on a collection of T-DNA insertion mutants (knockouts) in each protein kinase and phosphatase in Arabidopsis thaliana. PlantsP also provides a curated view of each protein that includes a comprehensive annotation of functionally related sequence motifs, sequence family definitions, alignments and phylogenetic trees, and descriptive information drawn directly from the literature. PlantsP is available at http://PlantsP.sdsc.edu.
• Jia, L. i., Lease, K. A., Tax, F. E., & Walker, J. C. (2001). BRS1, a serine carboxypeptidase, regulates BRI1 signaling in Arabidopsis thaliana. Proceedings of the National Academy of Sciences of the United States of America, 98(10), 5916-5921.
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  PMID: 11320207;PMCID: PMC33313;Abstract: Brassinosteroid-insensitive 1 (BRI1) of Arabidopsis thaliana encodes a cell surface receptor for brassinosteroids. Mutations in BRI1 severely affect plant growth and development. Activation tagging of a weak bri1 allele (bri1-5) resulted in the identification of a new locus, brs1-1D. BRS1 is predicted to encode a secreted carboxypeptidase. Whereas a brs1 loss-of-function allele has no obvious mutant phenotype, overexpression of BRS1 can suppress bri1 extracellular domain mutants. Genetic analyses showed that brassinosteroids and a functional BRI1 protein kinase domain are required for suppression. In addition, overexpressed BRS1 missense mutants, predicted to abolish BRS1 protease activity, failed to suppress bri1-5. Finally, the effects of BRS1 are selective: over-expression in either wild-type or two other receptor kinase mutants resulted in no phenotypic alterations. These results strongly suggest that BRS1 processes a protein involved in an early event in the BRI1 signaling.
• Li, J., Lease, K. A., Tax, F. E., & Walker, J. C. (2001). Erratum: BRS1, a serine carboxypeptidase, regulates BRI1 signaling in Arabidopsis thaliana (Proceedings of the National Academy of Sciences of the United States of America (May 8, 2001) 98:10 (5916-5921)). Proceedings of the National Academy of Sciences of the United States of America, 98(12), 6981-.
• Tax, F. E., & Vernon, D. M. (2001). T-DNA-associated duplication/translocations in Arabidopsis. Implications for mutant analysis and functional genomics. Plant Physiology, 126(4), 1527-1538.
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  PMID: 11500551;PMCID: PMC117152;Abstract: T-DNA insertion mutants have become a valuable resource for studies of gene function in Arabidopsis. In the course of both forward and reverse genetic projects, we have identified novel interchromosomal rearrangements in two Arabidopsis T-DNA insertion lines. Both rearrangements were unilateral translocations associated with the left borders of T-DNA inserts that exhibited normal Mendelian segregation. In one study, we characterized the embryo-defective88 mutation. Although emb88 had been mapped to chromosome I, molecular analysis of DNA adjacent to the T-DNA left border revealed sequence from chromosome V. Simple sequence length polymorphism mapping of the T-DNA insertion demonstrated that a >40-kbp region of chromosome V had inserted with the T-DNA into the emb88 locus on chromosome I. A similar scenario was observed with a prospective T-DNA knockout allele of the LIGHT-REGULATED RECEPTOR PROTEIN KINASE (LRRPK) gene. Whereas wild-type LRRPK is on lower chromosome IV, mapping of the T-DNA localized the disrupted LRRPK allele to chromosome V. In both these cases, the sequence of a single T-DNA-flanking region did not provide an accurate picture of DNA disruption because flanking sequences had duplicated and inserted, with the T-DNA, into other chromosomal locations. Our results indicate that T-DNA insertion lines - even those that exhibit straightforward genetic behavior - may contain an unexpectedly high frequency of rearrangements. Such duplication/translocations can interfere with reverse genetic analyses and provide misleading information about the molecular basis of mutant phenotypes. Simple mapping and polymerase chain reaction methods for detecting such rearrangements should be included as a standard step in T-DNA mutant analysis.
• Choe, S., Tanaka, A., Noguchi, T., Fujioka, S., Takatsuto, S., Ross, A. S., Tax, F. E., Yoshida, S., & Feldmann, K. A. (2000). Lesions in the sterol Δ⁷ reductase gene of Arabidopsis cause dwarfism due to a block in brassinosteroid biosynthesis. Plant Journal, 21(5), 431-443.
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  PMID: 10758495;Abstract: The brassinosteroid (BR) biosynthetic pathway, and the sterol pathway which is prerequisite to the BR pathway, are rapidly being characterized because of the availability of a large number of characteristic dwarf mutants in Arabidopsis. Here we show that the Arabidopsis dwarf5 mutants are disrupted in a sterol Δ7 reduction step. dwf5 plants display the characteristic dwarf phenotype typical of other BR mutants. This phenotype includes small, round, dark-green leaves, and short stems, pedicels, and petioles. Metabolite tracing with 13C-labeled precursors in dwf5 verified a deficiency in a sterol Δ7 reductase activity. All six independent alleles contain loss-of-function mutations in the sterol Δ7 reductase gene. These include a putative mRNA instability mutation in dwf5-1, 3' and 5' splice-site mutations in dwf5-2 and dwf5-6, respectively, premature stop codons in dwf5-3 (R400Z) and dwf5-5 (R409Z), and a mis-sense mutation in dwf5-4 (D257N). The dwf5 plant could be restored to wild type by ectopic overexpression of the wild-type copy of the gene. Both the Arabidopsis dwf5 phenotype and the human Smith-Lemli-Opitz syndrome are caused by loss-of-function mutations in a sterol Δ7 reductase gene, indicating that it is required for the proper growth and development of these two organisms.
• Noguchi, T., Fujioka, S., Choe, S., Takatsuto, S., Tax, F. E., Yoshida, S., & Feldmann, K. A. (2000). Biosynthetic pathways of brassinolide in Arabidopsis. Plant Physiology, 124(1), 201-209.
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  PMID: 10982435;PMCID: PMC59135;Abstract: Our previous studies on the endogenous brassinosteroids (BRs) in Arabidopsis have provided suggestive evidence for the operation of the early C6-oxidation and the late C6-oxidation pathways, leading to brassinolide (BL) in Arabidopsis. However, to date the in vivo operation of these pathways has not been fully confirmed in this species. This paper describes metabolic studies using deuterium-labeled BRs in wild-type and BR-insensitive mutant (bri1) seedlings to establish the intermediates of the biosynthetic pathway of BL in Arabidopsis. The first evidence for the conversion of campestanol to 6-deoxocathasterone and the conversion of 6-deoxocathasterone to 6-deoxoteasterone is provided. The later biosynthetic steps (6-deoxoteasterone → 3-dehydro-6-deoxoteasterone → 6-deoxotyphasterol → 6-deoxocastasterone → 6α-hydroxycastasterone → castasterone → BL) were demonstrated by stepwise metabolic experiments. Therefore, these studies complete the documentation of the late C6-oxidation pathway. The biosynthetic sequence involved in the early C6-oxidation pathway (teasterone → 3-dehydroteasterone → typhasterol → castasterone → BL) was also demonstrated. These results show that both the early and late C6-oxidation pathways are functional in Arabidopsis. In addition we report two new observations: the presence of a new branch in the pathway, C6 oxidation of 6-deoxotyphasterol to typhasterol, and increased metabolic flow in BR-insensitive mutants.
• Noguchi, T., Fujioka, S., Choe, S., Takatsuto, S., Tax, F. E., Yoshida, S., & Feldmann, K. A. (2000). Erratum: Biosynthetic pathways of brassinolide in arabidopsis (Plant Physiology (2000) 124 (201-209)). Plant Physiology, 124(2), 920-.
• Choe, S., Dilkes, B. P., Gregory, B. D., Ross, A. S., Yuan, H., Noguchi, T., Fujioka, S., Takatsuto, S., Tanaka, A., Yoshida, S., Tax, F. E., & Feldmann, K. A. (1999). The Arabidopsis dwarf1 mutant is defective in the conversion of 24-methylenecholesterol to campesterol in brassinosteroid biosynthesis. Plant Physiology, 119(3), 897-907.
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  PMID: 10069828;PMCID: PMC32104;Abstract: Since the isolation and characterization of dwarf1-1 (dwf1-1) from a T-DNA insertion mutant population, phenotypically similar mutants, including deetiolated2 (det2), constitutive photomorphogenesis and dwarfism (cpd), brassinosteroid insensitive 1 (bri1), and dwf4, have been reported to be defective in either the biosynthesis or the perception of brassinosteroids. We present further characterization of dwf1-1 and additional dwf1 alleles. Feeding tests with brassinosteroid-biosynthetic intermediates revealed that dwf1 can be rescued by 22α-hydroxycampesterol and downstream intermediates in the brassinosteroid pathway. Analysis of the endogenous levels of brassinosteroid intermediates showed that 24-methylenecholesterol in dwf1 accumulates to 12 times the level of the wild type, whereas the level of campesterol is greatly diminished, indicating that the defective step is in C-24 reduction. Furthermore, the deduced amino acid sequence of DWF1 shows significant similarity to a flavin adenine dinucleotide-binding domain conserved in various oxidoreductases, suggesting an enzymatic role for DWF1. In support of this, 7 of 10 dwf1 mutations directly affected the flavin adenine dinucleotide-binding domain. Our molecular characterization of dwf1 alleles, together with our biochemical data, suggest that the biosynthetic defect in dwf1 results in reduced synthesis of bioactive brassinosteroids, causing dwarfism.
• Choe, S., Noguchi, T., Fujioka, S., Takatsuto, S., Tissier, C. P., Gregory, B. D., Ross, A. S., Tanaka, A., Yoshida, S., Tax, F. E., & Feldmann, K. A. (1999). The Arabidopsis dwf7/ste1 mutant is defective in the Δ⁷ sterol C-5 desaturation step leading to brassinosteroid biosynthesis. Plant Cell, 11(2), 207-221.
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  PMID: 9927639;PMCID: PMC144158;Abstract: Lesions in brassinosteroid (BR) biosynthetic genes result in characteristic dwarf phenotypes in plants. Understanding the regulation of BR biosynthesis demands continued isolation and characterization of mutants corresponding to the genes involved in BR biosynthesis. Here, we present analysis of a novel BR biosynthetic locus, dwarf7(dwf7). Feeding studies with BR biosynthetic intermediates and analysis of endogenous levels of BR and sterol biosynthetic intermediates indicate that the defective step in dwf7-1 resides before the production of 24-methylenecholesterol in the sterol biosynthetic pathway. Furthermore, results from feeding studies with 13C-labeled mevalonic acid and compactin show that the defective step is specifically the Δ7 sterol C-5 desaturation, suggesting that dwf7 is an allele of the previously cloned STEROL1 (STE1) gene. Sequencing of the STE1 locus in two dwf7 mutants revealed premature stop codons in the first (dwf7-2) and the third (dwf7-1) exons. Thus, the reduction of BRs in dwf7 is due to a shortage of substrate sterols and is the direct cause of the dwarf phenotype in dwf7.
• Noguchi, T., Fujioka, S., Choe, S., Takatsuto, S., Yoshida, S., Yuan, H., Feldmann, K. A., & Tax, F. E. (1999). Brassinosteroid-insensitive dwarf mutants of Arabidopsis accumulate brassinosteroids. Plant Physiology, 121(3), 743-752.
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  PMID: 10557222;PMCID: PMC59436;Abstract: Seven dwarf mutants resembling brassinosteroid (BR)-biosynthetic dwarfs were isolated that did not respond significantly to the application of exogenous BRs. Genetic and molecular analyses revealed that these were novel alleles of BRI1 (Brassinosteroid-Insensitive 1), which encodes a receptor kinase that may act as a receptor for BRs or be involved in downstream signaling. The results of morphological and molecular analyses indicated that these represent a range of alleles from weak to null. The endogenous BRs were examined from 5-week-old plants of a null allele (bri1-4) and two weak alleles (bri1-5 and bri1-6). Previous analysis of endogenous BRs in several BR-biosynthetic dwarf mutants revealed that active BRs are deficient in these mutants. However, bril-4 plants accumulated very high levels of brassinolide, castasterone, and typhasterol (57-, 128-, and 33-fold higher, respectively, than those of wild-type plants). Weaker alleles (bri1-5 and bri1-6) also accumulated considerable levels of brassinolide, castasterone, and typhasterol, but less than the null allele (bri1-4). The levels of 6-deoxoBRs in bri1 mutants were comparable to that of wild type. The accumulation of biologically active BRs may result from the inability to utilize these active BRs, the inability to regulate BR biosynthesis in bri1 mutants, or both. Therefore, BRI-1 is required for the homeostasis of endogenous BR levels.
• Tax, F. E., Thomas, J. H., Ferguson, E. L., & Horvitz, H. R. (1997). Identification and characterization of genes that interact with lin-12 in Caenorhabditis elegans. Genetics, 147(4), 1675-1695.
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  PMID: 9409830;PMCID: PMC1208340;Abstract: We identified and characterized 14 extragenic mutations that suppressed the dominant egg-laying defect of certain lin-12 gain-of-function mutations. These suppressors defined seven genes: sup-17, lag-2, sel-4, sel-5, sel-6, sel-7 and sel-8. Mutations in six of the genes are recessive suppressors, whereas the two mutations that define the seventh gene, lag-2, are semi- dominant suppressors. These suppressor mutations were able to suppress other lin-12 gain-of-function mutations. The suppressor mutations arose at a very low frequency per gene, 10-50 times below the typical loss-of-function mutation frequency. The suppressor mutations in sup-17 and lag-2 were shown to be rare non-null alleles, and we present evidence that null mutations in these two genes cause lethality. Temperature-shift studies for two suppressor genes, sup-17 and lag-2, suggest that both genes act at approximately the same time as lin-12 in specifying a cell fate. Suppressor alleles of six of these genes enhanced a temperature-sensitive loss-of-function allele of glp- 1, a gene related to lin-12 in structure and function. Our analysis of these suppressors suggests that the majority of these genes are part of a shared lin-12/glp-1 signal transduction pathway, or act to regulate the expression or stability of lin-12 and glp-1.
• Krysan, P. J., Young, J. C., Tax, F., & Sussman, M. R. (1996). Identification of transferred DNA insertions within Arabidopsis genes involved in signal transduction and ion transport. Proceedings of the National Academy of Sciences of the United States of America, 93(15), 8145-8150.
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  PMID: 8755618;PMCID: PMC38890;Abstract: The transferred DNA (T-DNA) of Agrobacterium tumefaciens serves as an insertional mutagen once integrated into a host plant's genome. As a means of facilitating reverse genetic analysis in Arabidopsis thaliana, we have developed a method that allows one to search for plants carrying T-DNA insertions within any sequenced Arabidopsis gene. Using PCR, we screened a collection of 9100 independent T-DNA-transformed Arabidopsis lines and found 17 T-DNA insertions within the 63 genes analyzed. The genes surveyed include members of various gene families involved in signal transduction and ion transport. As an example, data are shown for a T-DNA insertion that was found within CPK-9, a member of the gene family encoding calmodulin-domain protein kinases.
• Tax, F. E., & Thomas, J. H. (1994). Receiving signals in the nematode embryo. Current Biology, 4(10), 914-916.
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  PMID: 7850427;Abstract: Two molecules involved in an inductive cell-cell interaction in the C. elegans early embryo have been identified. The apx-1 gene seems to encode the ligand and glp-1 the receptor responsible for the induction.
• Tax, F. E., Yeargers, J. J., & Thomas, J. H. (1994). Sequence of C. elegans lag-2 reveals a cell-signalling domain shared with Delta and Serrate of Drosophila. Nature, 368(6467), 150-154.
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  PMID: 8139658;Abstract: THE lin-12 and glp-1 genes of Caenorhabditis elegans encode members of the Notch family of transmembrane proteins. Genetic studies indicate that the lin-12 and glp-1 proteins act as receptors in specific developmental cell interactions and that their functions are partially redundant. lin-12 glp-1 double mutants display certain embryonic defects not found in either single mutant. The phenotype of this double mutant is called Lag, and recessive mutations in either of the genes lag-1 or lag-2 can also result in the Lag phenotype, indicating that these two genes may participate in the same cell interactions that require lin-12 or glp-1. We report here that lag-2 encodes a predicted transmembrane protein of 402 amino acids. The predicted extracellular region of lag-2 is similar to amino-terminal regions of Delta and Serrate, two Drosophila proteins that are thought to function as ligands for Notch. The region of similarity includes sequences related to epidermal growth factor (EGF) repeats. We have isolated lag-2(sa37), a dominant allele that shows specific genetic interactions with lin-12. The sa37 mutation causes a Gly→Asp change in a conserved residue of an EGF motif. Because of its overall structure, its sequence similarity to Delta and Serrate, and its genetic interactions, we suggest that lag-2 encodes an intercellular signal for the lin-12 and glp-1 receptors.
• Bowerman, B., Tax, F. E., Thomas, J. H., & Priess, J. R. (1992). Cell interactions involved in development of the bilaterally symmetrical intestinal valve cells during embryogenesis in Caenorhabditis elegans. Development, 116(4), 1113-1122.
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  PMID: 1295733;Abstract: We describe two different cell interactions that appear to be required for the proper development of a pair of bilaterally symmetrical cells in Caenorhabditis elegans called the intestinal valve cells. Previous experiments have shown that at the beginning of the 4-cell stage of embryogenesis, two sister blastomeres called ABa and ABp are equivalent in developmental potential. We show that cell interactions between ABp and a neighboring 4-cell-stage blastomere called P2 distinguish the fates of ABa and ABp by inducing descendants of ABp to produce the intestinal valve cells, a cell type not made by ABa. A second cell interaction appears to occur later in embryogenesis when two bilaterally symmetrical descendants of ABp, which both have the potential to produce valve cells, contact each other; production of the valve cells subsequently becomes limited to only one of the two descendants. This second interaction does not occur properly if the two symmetrical descendants of ABp are prevented from contacting each other. Thus the development of the intestinal valve cells appears to require both an early cell interaction that establishes a bilaterally symmetrical pattern of cell fate and a later interaction that breaks the symmetrical cell fate pattern by restricting to only one of two cells the ability to produce a pair of valve cells.
• Golumbeski, G. S., Bardsley, A., Tax, F., & Boswell, R. E. (1991). tudor, a posterior-group gene of Drosophila melanogaster, encodes a novel protein and an mRNA localized during mid-oogenesis. Genes and Development, 5(11), 2060-2070.
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  PMID: 1936993;Abstract: The tudor (tud) locus of Drosophila melanogaster is required during oogenesis for the formation of primordial germ cells and for normal abdominal segmentation. The tud locus was cloned, and its product was identified by Northern analysis of wild-type and tud mutant RNAs. The locus encodes a single mRNA of ∼8.0 kb that is expressed throughout the life cycle, beginning in the early stages of germ-line development in the female. During oogenesis, tud mRNA appears to be present in the oocyte precursor within the germarial cysts, and in stages 1-3 it accumulates within the developing oocyte. The transcript is localized to the posterior half of the oocyte during oogenetic stages 4-7 but is not detectable within the ooplasm by egg deposition and throughout early embryogenesis. The tud protein has a predicted molecular mass of 285,000 daltons and has no distinctive sequence similarity to known proteins or protein structural motifs. Taken together, these results indicate that the tud product is a novel protein required during oogenesis for establishment of a functional center of morphogenetic activity in the posterior tip of the Drosophila embryo.

Presentations

• Tax, F. E. (2016, April). Notes to the underground:understanding how and where roots grow. seminar. NMSU.

Reviews

• Tax, F. E., Honey, S. H., & Oh, M. (2020. The Control of Cell Expansion, Cell Division, and Vascular Development by Brassinosteroids: a Historical Perspective.