Jesse D Woodson

Interests

No activities entered.

Courses

Scholarly Contributions

Chapters

• Woodson, J. D., Lemke, M. D., Tano, D. W., & Rai, S. (2024).

  Chloroplast stress signals: control of retrograde signaling, chloroplast turn-over, and cell fate decisions

  . In Nucleic Acids and Molecular Biology - Chloroplast gene expression(pp 133-169). Springer. doi:10.1007/978-3-031-70098-9_5
• Escalante-semerena, J. C., Woodson, J. D., Buan, N. R., & Zayas, C. L. (2009). Conversion of Cobinamide into Coenzyme B12. In Tetrapyrroles: Birth, Life, and Death(pp 300-316). Springer, New York, NY. doi:10.1007/978-0-387-78518-9_19
  More info

  Cobamides are unique cyclic tetrapyrroles because their structures include an upper (Coβ) and a lower (Coα) axial ligand. The Coα and Coβ ligands are important for the interaction of the cobamide with enzymes, and for the chemistry of the reaction catalyzed by the enzyme. B12 (5,6-dimethylbenzimidazolylcobamide, cobalamin) is the best-known cobamide, which in its vitamin form has a cyano group as Coβ ligand, and in its coenzymic form it has a 5′-deoxyadenosine group as Coβ ligand (Fig. 1). In this chapter we review the current understanding of upper and lower ligand attachment to the ring macrocycle. Most of the knowledge reviewed here was obtained using bacterial systems; we add to the discussion recent work from our laboratory that uncovered variations in the conversion of cobinamide to B12 in archaea.

Journals/Publications

• Lemke, M., & Woodson, J. (2024). A genetic screen for dominant chloroplast reactive oxygen species signaling mutants reveals life stage-specific singlet oxygen signaling networks. Frontiers in Plant Science, 14, 1331346. doi:10.3389/fpls.2023.1331346
  More info

  Introduction: Plants employ intricate molecular mechanisms to respond to abiotic stresses, which often lead to the accumulation of reactive oxygen species (ROS) within organelles such as chloroplasts. Such ROS can produce stress signals that regulate cellular response mechanisms. One ROS, singlet oxygen (1O2), is predominantly produced in the chloroplast during photosynthesis and can trigger chloroplast degradation, programmed cell death (PCD), and retrograde (organelle-to-nucleus) signaling. However, little is known about the molecular mechanisms involved in these signaling pathways or how many different signaling 1O2 pathways may exist. Methods: The Arabidopsis thaliana plastid ferrochelatase two (fc2) mutant conditionally accumulates chloroplast 1O2, making fc2 a valuable genetic system for studying chloroplast 1O2-initiated signaling. Here, we have used activation tagging in a new forward genetic screen to identify eight dominant fc2 activation-tagged (fas) mutations that suppress chloroplast 1O2-initiated PCD. Results: While 1O2-triggered PCD is blocked in all fc2 fas mutants in the adult stage, such cellular degradation in the seedling stage is blocked in only two mutants. This differential blocking of PCD suggests that life-stage-specific 1O2-response pathways exist. In addition to PCD, fas mutations generally reduce 1O2-induced retrograde signals. Furthermore, fas mutants have enhanced tolerance to excess light, a natural mechanism to produce chloroplast 1O2. However, general abiotic stress tolerance was only observed in one fc2 fas mutant (fc2 fas2). Together, this suggests that plants can employ general stress tolerance mechanisms to overcome 1O2 production but that this screen was mostly specific to 1O2 signaling. We also observed that salicylic acid (SA) and jasmonate (JA) stress hormone response marker genes were induced in 1O2-stressed fc2 and generally reduced by fas mutations, suggesting that SA and JA signaling is correlated with active 1O2 signaling and PCD. Discussion: Together, this work highlights the complexity of 1O2 signaling by demonstrating that multiple pathways may exist and introduces a suite of new 1O2 signaling mutants to investigate the mechanisms controlling chloroplast-initiated degradation, PCD, and retrograde signaling.
• Lemke, M., Abate, A., & Woodson, J. (2024). Investigating the mechanism of chloroplast singlet oxygen signaling in the Arabidopsis thaliana accelerated cell death 2 mutant. Plant Signaling and Behavior, 19(1), 2347783. doi:10.1080/15592324.2024.2347783
  More info

  As sessile organisms, plants have evolved complex signaling mechanisms to sense stress and acclimate. This includes the use of reactive oxygen species (ROS) generated during dysfunctional photosynthesis to initiate signaling. One such ROS, singlet oxygen (1O2), can trigger retrograde signaling, chloroplast degradation, and programmed cell death. However, the signaling mechanisms are largely unknown. Several proteins (e.g. PUB4, OXI1, EX1) are proposed to play signaling roles across three Arabidopsis thaliana mutants that conditionally accumulate chloroplast 1O2 (fluorescent in blue light (flu), chlorina 1 (ch1), and plastid ferrochelatase 2 (fc2)). We previously demonstrated that these mutants reveal at least two chloroplast 1O2 signaling pathways (represented by flu and fc2/ch1). Here, we test if the 1O2-accumulating lesion mimic mutant, accelerated cell death 2 (acd2), also utilizes these pathways. The pub4–6 allele delayed lesion formation in acd2 and restored photosynthetic efficiency and biomass. Conversely, an oxi1 mutation had no measurable effect on these phenotypes. acd2 mutants were not sensitive to excess light (EL) stress, yet pub4–6 and oxi1 both conferred EL tolerance within the acd2 background, suggesting that EL-induced 1O2 signaling pathways are independent from spontaneous lesion formation. Thus, 1O2 signaling in acd2 may represent a third (partially overlapping) pathway to control cellular degradation.
• Goloubinoff, P., Woodson, J. D., Strader, L. C., & Fu, Z. Q. (2022). Important questions and future directions in plant biochemistry. Trends in biochemical sciences, 47(10), 811-813.
• Tano, D. W., Kozlowska, M. A., Easter, R. A., & Woodson, J. D. (2023). Multiple pathways mediate chloroplast singlet oxygen stress signaling. Plant molecular biology, 111(1-2), 167-187.
  More info

  Chloroplast singlet oxygen initiates multiple pathways to control chloroplast degradation, cell death, and nuclear gene expression. Chloroplasts can respond to stress and changes in the environment by producing reactive oxygen species (ROS). Aside from being cytotoxic, ROS also have signaling capabilities. For example, the ROS singlet oxygen (O) can initiate nuclear gene expression, chloroplast degradation, and cell death. To unveil the signaling mechanisms involved, researchers have used several O-producing Arabidopsis thaliana mutants as genetic model systems, including plastid ferrochelatase two (fc2), fluorescent in blue light (flu), chlorina 1 (ch1), and accelerated cell death 2 (acd2). Here, we compare these O-producing mutants to elucidate if they utilize one or more signaling pathways to control cell death and nuclear gene expression. Using publicly available transcriptomic data, we demonstrate fc2, flu, and ch1 share a core response to O accumulation, but maintain unique responses, potentially tailored to respond to their specific stresses. Subsequently, we used a genetic approach to determine if these mutants share O signaling pathways by testing the ability of genetic suppressors of one O producing mutant to suppress signaling in a different O producing mutant. Our genetic analyses revealed at least two different chloroplast O signaling pathways control cellular degradation: one specific to the flu mutant and one shared by fc2, ch1, and acd2 mutants, but with life-stage-specific (seedling vs. adult) features. Overall, this work reveals chloroplast stress signaling involving O is complex and may allow cells to finely tune their physiology to environmental inputs.
• Woodson, J. D. (2022). Control of chloroplast degradation and cell death in response to stress.. Trends in biochemical sciences. doi:10.1016/j.tibs.2022.03.010
  More info

  Chloroplasts are the sites of photosynthesis in plants and algae and, by extension, are essential for most life on Earth. Their maintenance is costly and complex due to the inherent photo-oxidative damage incurred by photosynthetic chemistry. Chloroplast degradation and cell death are mechanisms by which plants acclimate to such stress and serve a dual purpose: protecting cells and organs by removing reactive oxygen species-producing chloroplasts and redistributing nutrients to other tissues. Here I review recent progress in understanding the molecular mechanisms initiating and facilitating such degradation and show these are complex processes involving multiple pathways. Due to the links to photosynthesis and nitrogen metabolism, there is great potential to manipulate these pathways to increase crop yield and quality under stressful environments.
• Woodson, J. D., & Lemke, M. D. (2022). Targeted for destruction: degradation of singlet oxygen-damaged chloroplasts. Plant Signaling & Behavior, 17(1). doi:10.1080/15592324.2022.2084955
• Woodson, J. D., & Tano, D. W. (2022). Putting the brakes on chloroplast stress signaling.. Molecular plant, 15(3), 388-390. doi:10.1016/j.molp.2022.02.009
• Woodson, J. D., Fisher, K. E., Krishnamoorthy, P., Joens, M. S., Chory, J., & Fitzpatrick, J. A. (2022). Singlet Oxygen Leads to Structural Changes to Chloroplasts during their Degradation in the Arabidopsis thaliana plastid ferrochelatase two Mutant. Plant and Cell Physiology, 63(2), 248-264. doi:10.1093/pcp/pcab167
• Woodson, J. D., Tano, D. W., Kozlowska, M. A., & Easter, R. A. (2022). Multiple pathways mediate chloroplast singlet oxygen stress signaling. bioRxiv. doi:https://doi.org/10.1101/2022.08.01.502416
  More info

  Chloroplasts can respond to stress and changes in the environment by producing reactive oxygen species (ROS). Aside from being cytotoxic, ROS also have signaling capabilities. For example, the ROS singlet oxygen (1O2) can initiate nuclear gene expression, chloroplast degradation, and cell death. To unveil the signaling mechanisms involved, researchers have used several 1O2-producing Arabidopsis thaliana mutants as genetic model systems, including plastid ferrochelatase two (fc2), fluorescent in blue light (flu), chlorina 1 (ch1), and accelerated cell death 2 (acd2). Here, we compare these 1O2-producing mutants to elucidate if they utilize one or more signaling pathways to control cell death and nuclear gene expression. Using publicly available transcriptomic data, we demonstrate fc2, flu, and ch1 share a core response to 1O2 accumulation, but maintain unique responses, potentially tailored to respond to their specific stresses. Subsequently, we used a genetic approach to determine if these mutants share 1O2 signaling pathways by testing the ability of genetic suppressors of one 1O2 producing mutant to suppress signaling in a different 1O2 producing mutant. Our genetic analyses revealed at least two different chloroplast 1O2 signaling pathways control cellular degradation: one specific to the flu mutant and one shared by fc2, ch1, and acd2 mutants, but with life-stage-specific (seedling vs. adult) features. Overall, this work reveals chloroplast stress signaling involving 1O2 is complex and may allow cells to finely tune their physiology to environmental inputs.
• Fisher, K. E., Krishnamoorthy, P., Joens, M. S., Chory, J., Fitzpatrick, J. A., & Woodson, J. D. (2021). Singlet oxygen leads to structural changes to chloroplasts during degradation in the Arabidopsis thaliana plastid ferrochelatase two mutant.. bioRxiv. doi:10.1101/2021.07.19.452378
• Woodson, J. D. (2021). All in the timing: epigenetic control of greening. New Phytologist, 231(3), 907-909. doi:10.1111/nph.17454
• Woodson, J. D., Lemke, M. D., Fisher, K. E., Kozlowska, M. A., & Tano, D. W. (2021). Singlet oxygen-dependent chloroplast degradation is independent of macroautophagy in the Arabidopsis ferrochelatase two mutant. bioRxiv. doi:https://doi.org/10.1101/2021.02.17.431731
  More info

  Background Chloroplasts respond to stress and changes in the environment by producing reactive oxygen species (ROS) that have specific signaling abilities. The ROS singlet oxygen (1O2) is unique in that it can signal to initiate selective degradation of damaged chloroplasts and then cell death. This chloroplast quality control pathway can be monitored in the Arabidopsis mutant plastid ferrochelatase two (fc2) that conditionally accumulates chloroplast 1O2 under diurnal light cycling conditions leading to rapid chloroplast degradation and eventual cell death. The cellular machinery involved in such degradation, however, remains unknown. Recently it has been demonstrated that whole damaged chloroplasts can be transported to the central vacuole via a process requiring autophagosomes and core components of the autophagy machinery. The relationship between this process, referred to as chlorophagy, and the degradation of 1O2-stressed chloroplasts and cells has remained unexplored.Results To further understand 1O2-induced cellular degradation and determine what role autophagy may play, the expression of autophagy-related genes were monitored in 1O2-stressed fc2 seedlings and found to be induced. Although autophagosomes were present in fc2 cells, they did not associate with chloroplasts during 1O2 stress. Mutations blocking the core autophagy machinery (atg5, atg7, and atg10) were unable to suppress 1O2-induced chloroplast degradation or cell death in the fc2 mutant, suggesting autophagosome formation and macroautophagy are dispensable for 1O2–mediated cellular degradation. However, both atg5 and atg7 led to specific defects in chloroplast ultrastructure and photosynthetic efficiencies, suggesting macroautophagy may be involved in protecting chloroplasts from photo-oxidative damage. Finally, genes predicted to be involved in microautophagy were shown to be induced in stressed fc2 seedlings, indicating a possible role for an alternate form of autophagy in the dismantling of 1O2-damaged chloroplasts.Conclusions Our results support the hypothesis that 1O2-dependent chloroplast degradation is independent from autophagosome formation, canonical macroautophagy, and chlorophagy. Instead, ATG-independent microautophagy may be involved in such degradation. However, canonical macroautophagy may still play a role in protecting chloroplasts from 1O2-induced photo-oxidative stress. Together, this suggests chloroplast function and degradation is a complex process that utilizes multiple autophagy and degradation machineries, possibly depending on the type of stress or damage incurred.
• Woodson, J. D., Tano, D. W., Lemke, M. D., Kozlowska, M. A., & Fisher, K. E. (2021). The core autophagy machinery is not required for chloroplast singlet oxygen-mediated cell death in the Arabidopsis thaliana plastid ferrochelatase two mutant.. BMC plant biology, 21(1), 342. doi:10.1186/s12870-021-03119-x
  More info

  Chloroplasts respond to stress and changes in the environment by producing reactive oxygen species (ROS) that have specific signaling abilities. The ROS singlet oxygen (1O2) is unique in that it can signal to initiate cellular degradation including the selective degradation of damaged chloroplasts. This chloroplast quality control pathway can be monitored in the Arabidopsis thaliana mutant plastid ferrochelatase two (fc2) that conditionally accumulates chloroplast 1O2 under diurnal light cycling conditions leading to rapid chloroplast degradation and eventual cell death. The cellular machinery involved in such degradation, however, remains unknown. Recently, it was demonstrated that whole damaged chloroplasts can be transported to the central vacuole via a process requiring autophagosomes and core components of the autophagy machinery. The relationship between this process, referred to as chlorophagy, and the degradation of 1O2-stressed chloroplasts and cells has remained unexplored..To further understand 1O2-induced cellular degradation and determine what role autophagy may play, the expression of autophagy-related genes was monitored in 1O2-stressed fc2 seedlings and found to be induced. Although autophagosomes were present in fc2 cells, they did not associate with chloroplasts during 1O2 stress. Mutations affecting the core autophagy machinery (atg5, atg7, and atg10) were unable to suppress 1O2-induced cell death or chloroplast protrusion into the central vacuole, suggesting autophagosome formation is dispensable for such 1O2-mediated cellular degradation. However, both atg5 and atg7 led to specific defects in chloroplast ultrastructure and photosynthetic efficiencies, suggesting core autophagy machinery is involved in protecting chloroplasts from photo-oxidative damage. Finally, genes predicted to be involved in microautophagy were shown to be induced in stressed fc2 seedlings, indicating a possible role for an alternate form of autophagy in the dismantling of 1O2-damaged chloroplasts..Our results support the hypothesis that 1O2-dependent cell death is independent from autophagosome formation, canonical autophagy, and chlorophagy. Furthermore, autophagosome-independent microautophagy may be involved in degrading 1O2-damaged chloroplasts. At the same time, canonical autophagy may still play a role in protecting chloroplasts from 1O2-induced photo-oxidative stress. Together, this suggests chloroplast function and degradation is a complex process utilizing multiple autophagy and degradation machineries, possibly depending on the type of stress or damage incurred.
• Woodson, J. D., Tano, D. W., Rai, S., Palos, K., Nelson, A. D., Fisher, K. E., & Alamdari, K. (2021). Chloroplast quality control pathways are dependent on plastid DNA synthesis and nucleotides provided by cytidine triphosphate synthase two.. The New phytologist, 231(4), 1431-1448. doi:10.1111/nph.17467
  More info

  Reactive oxygen species (ROS) produced in chloroplasts cause oxidative damage, but also signal to initiate chloroplast quality control pathways, cell death, and gene expression. The Arabidopsis thaliana plastid ferrochelatase two (fc2) mutant produces the ROS singlet oxygen in chloroplasts that activates such signaling pathways, but the mechanisms are largely unknown. Here we characterize one fc2 suppressor mutation and map it to CYTIDINE TRIPHOSPHATE SYNTHASE TWO (CTPS2), which encodes one of five enzymes in Arabidopsis necessary for de novo cytoplasmic CTP (and dCTP) synthesis. The ctps2 mutation reduces chloroplast transcripts and DNA content without similarly affecting mitochondria. Chloroplast nucleic acid content and singlet oxygen signaling are restored by exogenous feeding of the dCTP precursor deoxycytidine, suggesting ctps2 blocks signaling by limiting nucleotides for chloroplast genome maintenance. An investigation of CTPS orthologs in Brassicaceae showed CTPS2 is a member of an ancient lineage distinct from CTPS3. Complementation studies confirmed this analysis; CTPS3 was unable to compensate for CTPS2 function in providing nucleotides for chloroplast DNA and signaling. Our studies link cytoplasmic nucleotide metabolism with chloroplast quality control pathways. Such a connection is achieved by a conserved clade of CTPS enzymes that provide nucleotides for chloroplast function, thereby allowing stress signaling to occur.
• Alamdari, K. D., Alamdari, K., Fisher, K. E., Sinson, A. B., & Chory, J. (2020). Plastid gene expression is required for singlet oxygen-induced chloroplast degradation and cell death. bioRxiv. doi:https://doi.org/10.1101/2020.02.24.961144
  More info

  Chloroplasts constantly experience photo-oxidative stress while performing photosynthesis. This is particularly true under abiotic stresses that lead to the accumulation of reactive oxygen species (ROS). While ROS leads to the oxidation of DNA, proteins, and lipids, it can also act as a signal to induce acclimation through chloroplast degradation, cell death, and nuclear gene expression. Although the mechanisms behind ROS signaling from chloroplasts remain mostly unknown, several genetic systems have been devised in the model plant Arabidopsis to understand their signaling properties. One system uses the plastid ferrochelatase two (fc2) mutant that conditionally accumulates the ROS singlet oxygen (1O2) leading to chloroplast degradation and eventually cell death. Here we have mapped three mutations that suppress chloroplast degradation in the fc2 mutant and demonstrate that they affect two independent loci (PPR30 and mTERF9) encoding chloroplast proteins predicted to be involved in post-transcriptional gene expression. Mutations in either gene were shown to lead to broadly reduced chloroplast gene expression, impaired chloroplast development, and reduced chloroplast stress signaling. In these mutants, however, 1O2 levels were uncoupled to chloroplast degradation suggesting that PPR30 and mTERF9 are involved in ROS signaling pathways. In the wild type background, ppr30 and mTERF9 mutants were also observed to be less susceptible to cell death induced by excess light stress. Together these results suggest that plastid gene expression (or the expression of specific plastid genes) is a necessary prerequisite for chloroplasts to activate 1O2 signaling pathways to induce chloroplast degradation and/or cell death.
• Woodson, J. D., Alamdari, K., Fisher, K. E., Sinson, A. B., & Chory, J. (2020). Roles for the chloroplast‐localized pentatricopeptide repeat protein 30 and the ‘mitochondrial’ transcription termination factor 9 in chloroplast quality control. The Plant Journal, 104(3), 735-751. doi:10.1111/tpj.14963
• Woodson, J. D., Alamdari, K., Fisher, K. E., Welsh, D. W., Rai, S., Palos, K. R., & Nelson, A. D. (2020). Chloroplast quality control pathways are dependent on plastid DNA synthesis and nucleotides provided by cytidine triphosphate synthase two. bioRxiv. doi:10.1101/2020.10.28.360057
• Woodson, J. D., Kikuchi, Y., Nakamura, S., Ishida, H., Ling, Q., Hidema, J., Jarvis, R. P., Hagihara, S., & Izumi, M. (2020). Chloroplast Autophagy and Ubiquitination Combine to Manage Oxidative Damage and Starvation Responses. Plant Physiology, 183(4), 1531-1544. doi:10.1104/pp.20.00237
• Woodson, J. D. (2019). Chloroplast stress signals: regulation of cellular degradation and chloroplast turnover. Current opinion in plant biology, 52, 30-37.
  More info

  For 40 years, it has been known that chloroplasts signal to the nucleus and the cell to coordinate gene expression, maximize photosynthesis, and avoid stress. However, the signaling mechanisms have been challenging to uncover due to the complexity of these signals and the stresses that induce them. New research has shown that many signals are induced by singlet oxygen, a natural by-product of inefficient photosynthesis. Chloroplast singlet oxygen not only regulates nuclear gene expression, but also cellular degradation and cell death. Stressed chloroplasts also induce post-translational mechanisms, including autophagy, that allows individual chloroplasts to regulate their own degradation and turnover. Such chloroplast quality control pathways may allow cells to maintain healthy populations of chloroplasts and to avoid cumulative photo-oxidative stress in stressful environments.
• Woodson, J. D. (2016). Chloroplast quality control - balancing energy production and stress.. The New phytologist, 212(1), 36-41. doi:10.1111/nph.14134
  More info

  Contents 36 I. 36 II. 37 III. 37 IV. 38 V. 39 VI. 40 VII. 40 40 References 40 SUMMARY: All organisms require the ability to sense their surroundings and adapt. Such capabilities allow them to thrive in a wide range of habitats. This is especially true for plants, which are sessile and have to be genetically equipped to withstand every change in their environment. Plants and other eukaryotes use their energy-producing organelles (i.e. mitochondria and chloroplasts) as such sensors. In response to a changing cellular or external environment, these organelles can emit 'retrograde' signals that alter gene expression and/or cell physiology. This signaling is important in plants, fungi, and animals and impacts diverse cellular functions including photosynthesis, energy production/storage, stress responses, growth, cell death, ageing, and tumor progression. Originally, chloroplast retrograde signals in plants were known to lead to the reprogramming of nuclear transcription. New research, however, has pointed to additional posttranslational mechanisms that lead to chloroplast regulation and turnover in response to stress. Such mechanisms involve singlet oxygen, ubiquitination, the 26S proteasome, and cellular degradation machinery.
• Woodson, J. D., Chory, J., Woodson, J. D., Weigel, D., Sinson, A. B., Salome, P. A., Joens, M. S., Gilkerson, J., Fitzpatrick, J. A., & Chory, J. (2015). Ubiquitin facilitates a quality-control pathway that removes damaged chloroplasts.. Science (New York, N.Y.), 350(6259), 450-4. doi:10.1126/science.aac7444
  More info

  Energy production by chloroplasts and mitochondria causes constant oxidative damage. A functioning photosynthetic cell requires quality-control mechanisms to turn over and degrade chloroplasts damaged by reactive oxygen species (ROS). Here, we generated a conditionally lethal Arabidopsis mutant that accumulated excess protoporphyrin IX in the chloroplast and produced singlet oxygen. Damaged chloroplasts were subsequently ubiquitinated and selectively degraded. A genetic screen identified the plant U-box 4 (PUB4) E3 ubiquitin ligase as being necessary for this process. pub4-6 mutants had defects in stress adaptation and longevity. Thus, we have identified a signal that leads to the targeted removal of ROS-overproducing chloroplasts.
• Woodson, J. D., Chory, J., Woodson, J. D., & Chory, J. (2014). Sense and adaptation: Signalling between the nucleus and genomecontaining organelles. The Biochemist, 36(5), 6-10. doi:10.1042/bio03605006
  More info

  All organisms require the ability to sense their surroundings and adapt. From bacteria to humans, these abilities ensure that an organism can thrive and grow in a wide range of habitats. This is especially true for plants, which are sessile organisms that have to be genetically equipped to withstand every change in the environment in which they live. Recently, it is becoming clear that plants and many other eukaryotes use their energy-producing organelles (chloroplasts and mitochondria) as endogenous and environmental sensors (Figure 1). These organelles allow the organism to respond and adapt to changing conditions by sending signals to the nucleus to alter gene expression and cell physiology. This organelle-to-nucleus (retrograde) signalling is important in plants, fungi and animals and affects various cellular functions including growth, metabolism, stress responses, cell death, photosynthesis, energy production/storage, aging and tumour progression. Here, we summarize what is known of these pathways in photosynthetic plants that contain both chloroplasts and mitochondria.
• Woodson, J. D., Ecker, J. R., Chory, J., Woodson, J. D., Schmitz, R. J., Perez-ruiz, J. M., Ecker, J. R., & Chory, J. (2013). Sigma factor-mediated plastid retrograde signals control nuclear gene expression.. The Plant journal : for cell and molecular biology, 73(1), 1-13. doi:10.1111/tpj.12011
  More info

  Retrograde signalling from plastids to the nucleus is necessary to regulate the organelle's proteome during the establishment of photoautotrophy and fluctuating environmental conditions. Studies that used inhibitors of chloroplast biogenesis have revealed that hundreds of nuclear genes are regulated by retrograde signals emitted from plastids. Plastid gene expression is the source of at least one of these signals, but the number of signals and their mechanisms used to regulate nuclear gene expression are unknown. To further examine the effects of plastid gene expression on nuclear gene expression, we analyzed Arabidopsis mutants that were defective in each of the six sigma factor (SIG) genes that encode proteins utilized by plastid-encoded RNA polymerase to transcribe specific sets of plastid genes. We showed that SIG2 and SIG6 have partially redundant roles in plastid transcription and retrograde signalling to control nuclear gene expression. The loss of GUN1 (a plastid-localized pentatricopeptide repeat protein) is able to restore nuclear (but not plastid) gene expression in both sig2 and sig6, whereas an increase in heme synthesis is able to restore nuclear gene expression in sig2 mutants only. These results demonstrate that sigma factor function is the source of at least two retrograde signals to the nucleus; one likely to involve the transcription of tRNA(Glu) . A microarray analysis showed that these two signals accounted for at least one subset of the nuclear genes that are regulated by the plastid biogenesis inhibitors norflurazon and lincomycin. Together these data suggest that such inhibitors can induce retrograde signalling by affecting transcription in the plastid.
• Woodson, J. D., Chory, J., Woodson, J. D., & Chory, J. (2012). Organelle signaling: how stressed chloroplasts communicate with the nucleus.. Current biology : CB, 22(17), R690-2. doi:10.1016/j.cub.2012.07.028
  More info

  Plastids are able to relay information to the nucleus to regulate stress responses. A new genetic screen has identified an isoprenoid intermediate that accumulates in stressed plastids and acts as a novel retrograde signal.
• Woodson, J. D., Chory, J., Woodson, J. D., Perez-ruiz, J. M., & Chory, J. (2011). Heme synthesis by plastid ferrochelatase I regulates nuclear gene expression in plants.. Current biology : CB, 21(10), 897-903. doi:10.1016/j.cub.2011.04.004
  More info

  Chloroplast signals regulate hundreds of nuclear genes during development and in response to stress, but little is known of the signals or signal transduction mechanisms of plastid-to-nucleus (retrograde) signaling. In Arabidopsis thaliana, genetic studies using norflurazon (NF), an inhibitor of carotenoid biosynthesis, have identified five GUN (genomes uncoupled) genes, implicating the tetrapyrrole pathway as a source of a retrograde signal. Loss of function of any of these GUN genes leads to increased expression of photosynthesis-associated nuclear genes (PhANGs) when chloroplast development has been blocked by NF. Here we present a new Arabidopsis gain-of-function mutant, gun6-1D, with a similar phenotype. The gun6-1D mutant overexpresses the conserved plastid ferrochelatase 1 (FC1, heme synthase). Genetic and biochemical experiments demonstrate that increased flux through the heme branch of the plastid tetrapyrrole biosynthetic pathway increases PhANG expression. The second conserved plant ferrochelatase, FC2, colocalizes with FC1, but FC2 activity is unable to increase PhANG expression in undeveloped plastids. These data suggest a model in which heme, specifically produced by FC1, may be used as a retrograde signal to coordinate PhANG expression with chloroplast development.
• Woodson, J. D., Chory, J., Woodson, J. D., & Chory, J. (2008). Coordination of gene expression between organellar and nuclear genomes.. Nature reviews. Genetics, 9(5), 383-95. doi:10.1038/nrg2348
  More info

  Following the acquisition of chloroplasts and mitochondria by eukaryotic cells during endosymbiotic evolution, most of the genes in these organelles were either lost or transferred to the nucleus. Encoding organelle-destined proteins in the nucleus allows for host control of the organelle. In return, organelles send signals to the nucleus to coordinate nuclear and organellar activities. In photosynthetic eukaryotes, additional interactions exist between mitochondria and chloroplasts. Here we review recent advances in elucidating the intracellular signalling pathways that coordinate gene expression between organelles and the nucleus, with a focus on photosynthetic plants.
• Otte, M. M., Woodson, J. D., & Escalante-semerena, J. C. (2007). The thiamine kinase (YcfN) enzyme plays a minor but significant role in cobinamide salvaging in Salmonella enterica.. Journal of bacteriology, 189(20), 7310-5. doi:10.1128/jb.00822-07
  More info

  Cobinamide (Cbi) salvaging is impaired, but not abolished, in a Salmonella enterica strain lacking a functional cobU gene. CobU is a bifunctional enzyme (NTP:adenosylcobinamide [NTP:AdoCbi] kinase, GTP:adenosylcobinamide-phosphate [GTP:AdoCbi-P] guanylyltransferase) whose AdoCbi kinase activity is necessary for Cbi salvaging in this bacterium. Inactivation of the ycfN gene in a DeltacobU strain abrogated Cbi salvaging. Introduction of a plasmid carrying the ycfN(+) allele into a DeltacobU DeltaycfN strain substantially restored Cbi salvaging. Mass spectrometry data indicate that when YcfN-enriched cell extracts were incubated with AdoCbi and ATP, the product of the reaction was AdoCbi-P. Results from bioassays confirmed that YcfN converted AdoCbi to AdoCbi-P in an ATP-dependent manner. YcfN is a good example of enzymes that are used by the cell in multiple pathways to ensure the salvaging of valuable precursors.
• Woodson, J. D., & Escalante-semerena, J. C. (2006). The cbiS gene of the archaeon Methanopyrus kandleri AV19 encodes a bifunctional enzyme with adenosylcobinamide amidohydrolase and alpha-ribazole-phosphate phosphatase activities.. Journal of bacteriology, 188(12), 4227-35. doi:10.1128/jb.00227-06
  More info

  Here we report the initial biochemical characterization of the bifunctional alpha-ribazole-P (alpha-RP) phosphatase, adenosylcobinamide (AdoCbi) amidohydrolase CbiS enzyme from the hyperthermophilic methanogenic archaeon Methanopyrus kandleri AV19. The cbiS gene encodes a 39-kDa protein with two distinct segments, one of which is homologous to the AdoCbi amidohydrolase (CbiZ, EC 3.5.1.90) enzyme and the other of which is homologous to the recently discovered archaeal alpha-RP phosphatase (CobZ, EC 3.1.3.73) enzyme. CbiS function restored AdoCbi salvaging and alpha-RP phosphatase activity in strains of the bacterium Salmonella enterica where either step was blocked. The two halves of the cbiS genes retained their function in vivo when they were cloned separately. The CbiS enzyme was overproduced in Escherichia coli and was isolated to >95% homogeneity. High-performance liquid chromatography, UV-visible spectroscopy, and mass spectroscopy established alpha-ribazole and cobyric acid as the products of the phosphatase and amidohydrolase reactions, respectively. Reasons why the CbiZ and CobZ enzymes are fused in some archaea are discussed.
• Zayas, C. L., Woodson, J. D., & Escalante-semerena, J. C. (2006). The cobZ gene of Methanosarcina mazei Go1 encodes the nonorthologous replacement of the alpha-ribazole-5'-phosphate phosphatase (CobC) enzyme of Salmonella enterica.. Journal of bacteriology, 188(7), 2740-3. doi:10.1128/jb.188.7.2740-2743.2006
  More info

  Open reading frame (ORF) Mm2058 of the methanogenic archaeon Methanosarcina mazei strain Gö1 was shown in vivo and in vitro to encode the nonorthologous replacement of the alpha-ribazole-phosphate phosphatase (CobC; EC 3.1.3.73) enzyme of Salmonella enterica serovar Typhimurium LT2. Bioinformatics analysis of sequences available in databases tentatively identified ORF Mm2058, which was cloned under the control of an inducible promoter and was used to support growth of an S. enterica strain under conditions that demanded CobC-like activity. The Mm2058 protein was expressed with a decahistidine tag at its N terminus and was purified to homogeneity using nickel affinity chromatography. High-performance liquid chromatography followed by electrospray ionization mass spectrometry showed that the Mm2058 protein had phosphatase activity that converted alpha-ribazole-5'-phosphate to alpha-ribazole, as reported for the bacterial CobC enzyme. On the basis of the data reported here, we refer to ORF Mm2058 as cobZ. We tested the prediction by Rodionov et al. (D. A. Rodionov, A. G. Vitreschak, A. A. Mironov, and M. S. Gelfand, J. Biol. Chem. 278:41148-41159, 2003) that ORF HSL01294 (also called Vng1577) encoded the nonorthologous replacement of the bacterial CobC enzyme in the extremely halophilic archaeon Halobacterium sp. strain NRC-1. A strain of the latter carrying an in-frame deletion of ORF Vng1577 was not a cobalamin auxotroph, suggesting that either there is redundancy of this function in Halobacterium or the gene was misannotated.
• Woodson, J. D., Reynolds, A. A., & Escalante-semerena, J. C. (2005). ABC transporter for corrinoids in Halobacterium sp. strain NRC-1.. Journal of bacteriology, 187(17), 5901-9. doi:10.1128/jb.187.17.5901-5909.2005
  More info

  We report evidence for the existence of a putative ABC transporter for corrinoid utilization in the extremely halophilic archaeon Halobacterium sp. strain NRC-1. Results from genetic and nutritional analyses of Halobacterium showed that mutants with lesions in open reading frames (ORFs) Vng1370G, Vng1371Gm, and Vng1369G required a 10(5)-fold higher concentration of cobalamin for growth than the wild-type or parent strain. The data support the conclusion that these ORFs encode orthologs of the bacterial cobalamin ABC transporter permease (btuC; Vng1370G), ATPase (btuD; Vng1371Gm), and substrate-binding protein (btuF; Vng1369G) components. Mutations in the Vng1370G, Vng1371Gm, and Vng1369G genes were epistatic, consistent with the hypothesis that their products work together to accomplish the same function. Extracts of btuF mutant strains grown in the presence of cobalamin did not contain any cobalamin molecules detectable by a sensitive bioassay, whereas btuCD mutant strain extracts did. The data are consistent with the hypothesis that the BtuF protein is exported to the extracellular side of the cell membrane, where it can bind cobalamin in the absence of BtuC and BtuD. Our data also provide evidence for the regulation of corrinoid transport and biosynthesis. Halobacterium synthesized cobalamin in a chemically defined medium lacking corrinoid precursors. To the best of our knowledge, this is the first genetic analysis of an archaeal corrinoid transport system.
• Woodson, J. D., & Escalante-semerena, J. C. (2004). CbiZ, an amidohydrolase enzyme required for salvaging the coenzyme B12 precursor cobinamide in archaea.. Proceedings of the National Academy of Sciences of the United States of America, 101(10), 3591-6. doi:10.1073/pnas.0305939101
  More info

  The existence of a pathway for salvaging the coenzyme B(12) precursor dicyanocobinamide (Cbi) from the environment was established by genetic and biochemical means. The pathway requires the function of a previously unidentified amidohydrolase enzyme that converts adenosylcobinamide to adenosylcobyric acid, a bona fide intermediate of the de novo coenzyme B(12) biosynthetic route. The cbiZ gene of the methanogenic archaeon Methanosarcina mazei strain Göl was cloned, was overproduced in Escherichia coli, and the recombinant protein was isolated to homogeneity. HPLC, UV-visible spectroscopy, MS, and bioassay data established adenosylcobyric as the corrinoid product of the CbiZ-catalyzed reaction. Inactivation of the cbiZ gene in the extremely halophilic archaeon Halobacterium sp. strain NRC-1 blocked the ability of this archaeon to salvage Cbi. cbiZ function restored Cbi salvaging in a strain of the bacterium Salmonella enterica, whose Cbi-salvaging pathway was blocked. The salvaging of Cbi through the CbiZ enzyme appears to be an archaeal strategy because all of the genomes of B(12)-producing archaea have a cbiZ ortholog. Reasons for the evolution of two distinct pathways for Cbi salvaging in prokaryotes are discussed.
• Woodson, J. D., Peck, R. F., Krebs, M. P., & Escalante-semerena, J. C. (2003). The cobY gene of the archaeon Halobacterium sp. strain NRC-1 is required for de novo cobamide synthesis.. Journal of bacteriology, 185(1), 311-6. doi:10.1128/jb.185.1.311-316.2003
  More info

  Genetic and nutritional analyses of mutants of the extremely halophilic archaeon Halobacterium sp. strain NRC-1 showed that open reading frame (ORF) Vng1581C encodes a protein with nucleoside triphosphate:adenosylcobinamide-phosphate nucleotidyltransferase enzyme activity. This activity was previously associated with the cobY gene of the methanogenic archaeon Methanobacterium thermoautotrophicum strain DeltaH, but no evidence was obtained to demonstrate the direct involvement of this protein in cobamide biosynthesis in archaea. Computer analysis of the Halobacterium sp. strain NRC-1 ORF Vng1581C gene and the cobY gene of M. thermoautotrophicum strain DeltaH showed the primary amino acid sequence of the proteins encoded by these two genes to be 35% identical and 48% similar. A strain of Halobacterium sp. strain NRC-1 carrying a null allele of the cobY gene was auxotrophic for cobinamide-GDP, a known intermediate of the late steps of cobamide biosynthesis. The auxotrophic requirement for cobinamide-GDP was corrected when a wild-type allele of cobY was introduced into the mutant strain, demonstrating that the lack of cobY function was solely responsible for the observed block in cobamide biosynthesis in this archaeon. The data also show that Halobacterium sp. strain NRC-1 possesses a high-affinity transport system for corrinoids and that this archaeon can synthesize cobamides de novo under aerobic growth conditions. To the best of our knowledge this is the first genetic and nutritional analysis of cobalamin biosynthetic mutants in archaea.
• Woodson, J. D., Zayas, C. L., & Escalante-semerena, J. C. (2003). A new pathway for salvaging the coenzyme B12 precursor cobinamide in archaea requires cobinamide-phosphate synthase (CbiB) enzyme activity.. Journal of bacteriology, 185(24), 7193-201. doi:10.1128/jb.185.24.7193-7201.2003
  More info

  The ability of archaea to salvage cobinamide has been under question because archaeal genomes lack orthologs to the bacterial nucleoside triphosphate:5'-deoxycobinamide kinase enzyme (cobU in Salmonella enterica). The latter activity is required for cobinamide salvaging in bacteria. This paper reports evidence that archaea salvage cobinamide from the environment by using a pathway different from the one used by bacteria. These studies demanded the functional characterization of two genes whose putative function had been annotated based solely on their homology to the bacterial genes encoding adenosylcobyric acid and adenosylcobinamide-phosphate synthases (cbiP and cbiB, respectively) of S. enterica. A cbiP mutant strain of the archaeon Halobacterium sp. strain NRC-1 was auxotrophic for adenosylcobyric acid, a known intermediate of the de novo cobamide biosynthesis pathway, but efficiently salvaged cobinamide from the environment, suggesting the existence of a salvaging pathway in this archaeon. A cbiB mutant strain of Halobacterium was auxotrophic for adenosylcobinamide-GDP, a known de novo intermediate, and did not salvage cobinamide. The results of the nutritional analyses of the cbiP and cbiB mutants suggested that the entry point for cobinamide salvaging is adenosylcobyric acid. The data are consistent with a salvaging pathway for cobinamide in which an amidohydrolase enzyme cleaves off the aminopropanol moiety of adenosylcobinamide to yield adenosylcobyric acid, which is converted by the adenosylcobinamide-phosphate synthase enzyme to adenosylcobinamide-phosphate, a known intermediate of the de novo biosynthetic pathway. The existence of an adenosylcobinamide amidohydrolase enzyme would explain the lack of an adenosylcobinamide kinase in archaea.

Presentations

• Woodson, J. D. (2024, March). Understanding the Photo-Oxidative Stress Signals That Initiate Chloroplast Degradation and Cell Death. Donald Danforth Plant Science Center Seminar Series. Donald Danforth Plant Science Center, St. Louis, MO: Donald Danforth Plant Science Center, Committee for Scientific Training and Mentoring.
• Woodson, J. D. (2023, April).

  Control of chloroplast degradation and cell death in response to reactive oxygen species

  . 32nd Western Photosynthesis Meeting. Bodega Bay, CA: University of California, Berkeley.
• Woodson, J. D. (2023, August).

  Control of chloroplast turn-over and cell death by reactive oxygen species

  . The American Society of Plant Biologists (ASPB) annual meeting. Savannah, GA: The American Society of Plant Biologists (ASPB).
• Woodson, J. D. (2023, December).

  Signal transduction pathways for chloroplast quality control

  . Photosynthetic Systems Principal Investigators Meeting. Rockville, MD: United State Department of Energy (DOE).
• Woodson, J. D. (2023, March).

  Photo- Oxidative Stress Signals to Initiate Chloroplast Degradation and Cell Death

  . Gordon Research Conference – Chloroplast Biotechnology. Ventura, CA: Gordon Research Conference.
• Woodson, J. D. (2022, July). Chloroplast stress signals and the control of organelle degradation and cell death. State Key Laboratory of Plant Physiology and Biochemistry, College of Biological Sciences, China Agricultural University. 2022 Symposium on Plant Responses to Abiotic Stresses and Environmental Signals.. Beijing, China (remote): China Agricultural University.
• Woodson, J. D. (2022, July). Control of cellular degradation pathways by chloroplast stress signals. The American Society of Plant Biologists Annual Meeting. Portland, OR: The American Society of Plant Biologists.
• Woodson, J. D., Gu, A., Gore, M., Lang, M., & Lewenstein, B. (2022, October). Research Visions Workshop - Programmable Biology. NSF Science and Technology Center, Center for Research on Programmable Plant Systems (CROPPS), Annual Meeting. Cornell University, Ithaca, NY: Cornell University.
• Woodson, J. D., Lemke, M. D., & Salazar De Leon, C. (2022, June). Optogenetics. NSF Science and Technology Center, Center for Research on Programmable Plant Systems (CROPPS), Cornell University, Vision Seminar Series. Cornell University (remote): Cornell University.
• Woodson, J. D. (2021). Chloroplast quality control and stress signaling pathways. TRR 175 (Chloroplasts – the green hub) International Conference. Germany: TRR 175.
• Woodson, J. D. (2021). Chloroplast stress signaling and the regulation of cellular degradation. University of Nebraska, Dept. of Biochemistry Seminar Series. University of Nebraska: University of Nebraska, Dept. of Biochemistry.
• Woodson, J. D. (2021). Control of cellular degradation pathways by chloroplast signaling. U. of California, Riverside, Institute for Integrative Genome Biology Seminar Series. U. of California, Riverside: U. of California, Riverside, Institute for Integrative Genome Biology.
• Woodson, J. D. (2021). Control of photo-oxidative stress by chloroplast quality control pathways. KAUST and the U. of Arizona Summer Seminar Series. Online remote: KAUST and the U. of Arizona.
• Woodson, J. D. (2021, January). A link between chloroplast gene expression and organelle quality control pathways. 30th Annual Western Photosynthesis Conference. Oracle, AZ (online): Western Photosynthesis Conference.
• Woodson, J. D. (2019, August). A Genetic Screen for Chloroplast Stress Signaling Mutants. The American Society of Plant Biologists annual meeting. San Jose, CA: The American Society of Plant Biologists.
• Woodson, J. D. (2019, October). Signal Transduction Pathways of Chloroplast Quality Control. Photosynthetic Systems PI Meeting. Gaithersburg, MD: United States Department of Energy.
• Woodson, J. D. (2019, September). Chloroplast stress signaling: environmental sensors for the cell. University of Arizona, School of Plant Sciences Seminar Series. Tucson, AZ: University of Arizona, School of Plant Sciences.
• Woodson, J. D. (2018, January). Signal Transduction Pathways of Chloroplast Quality Control. Western Photosynthesis Conference. Oracle, AZ: Western Photosynthesis Conference.
• Woodson, J. D. (2018, July). Signal Transduction Pathways of Chloroplast Quality Control. Gordon Research Conference (Mitochondria and Chloroplasts). Lucca, Italy: Gordon Research Conference.
• Woodson, J. D. (2018, July). Signal Transduction Pathways of Chloroplast Quality Control. International Society on Photosynthesis Research Annual Meeting. Montreal, Canada: International Society on Photosynthesis Research.
• Woodson, J. D. (2018, September). Balancing energy production and stress. University of Arizona, Molecular and Cellular Biology Seminar Series. Tucson, AZ: University of Arizona.
• Woodson, J. D. (2018, September). Signal Transduction Pathways of Chloroplast Quality Control. Arizona State University Center for Bioenergy and Photosynthesis Seminar Series. Tempe, AZ: Arizona State University Center for Bioenergy and Photosynthesis.

Poster Presentations

• Woodson, J. D. (2018, July). Signal Transduction Pathways Of Chloroplast Quality Control. The American Society of Plant Biologists annual meeting. Montreal, Canada: The American Society of Plant Biologists.