scholarly journals TheArabidopsisSAFEGUARD1 suppresses singlet oxygen-induced stress responses by protecting grana margins

2020 ◽  
Vol 117 (12) ◽  
pp. 6918-6927 ◽  
Author(s):  
Liangsheng Wang ◽  
Dario Leister ◽  
Li Guan ◽  
Yi Zheng ◽  
Katja Schneider ◽  
...  
Keyword(s):  
Singlet Oxygen ◽  
Signaling Pathway ◽  
Stress Responses ◽  
Double Mutant ◽  
Nuclear Gene ◽  
Oxygen Species ◽  
Nuclear Gene Expression ◽  
Induced Stress ◽  
Transcriptional Rewiring ◽  
Chloroplast Stroma

Singlet oxygen (1O2), the major reactive oxygen species (ROS) produced in chloroplasts, has been demonstrated recently to be a highly versatile signal that induces various stress responses. In thefluorescent(flu) mutant, its release causes seedling lethality and inhibits mature plant growth. However, these drastic phenotypes are suppressed when EXECUTER1 (EX1) is absent in theflu ex1double mutant. We identified SAFEGUARD1 (SAFE1) in a screen of ethyl methanesulfonate (EMS) mutagenizedflu ex1plants for suppressor mutants with aflu-like phenotype. Influ ex1 safe1, all1O2-induced responses, including transcriptional rewiring of nuclear gene expression, return to levels, such as, or even higher than, those influ. Without SAFE1, grana margins (GMs) of chloroplast thylakoids (Thys) are specifically damaged upon1O2generation and associate with plastoglobules (PGs). SAFE1 is localized in the chloroplast stroma, and release of1O2induces SAFE1 degradation via chloroplast-originated vesicles. Our paper demonstrates thatflu-produced1O2triggers an EX1-independent signaling pathway and proves that SAFE1 suppresses this signaling pathway by protecting GMs.

scholarly journals Plastid gene expression is required for singlet oxygen-induced chloroplast degradation and cell death

2020 ◽  
Author(s):  
Kamran Alamdari ◽  
Karen E. Fisher ◽  
Andrew B. Sinson ◽  
Joanne Chory ◽  
Jesse D. Woodson
Keyword(s):  
Gene Expression ◽  
Reactive Oxygen Species ◽  
Cell Death ◽  
Singlet Oxygen ◽  
Chloroplast Development ◽  
Nuclear Gene ◽  
Oxygen Species ◽  
Plastid Gene ◽  
Plastid Gene Expression ◽  
Nuclear Gene Expression

SummaryChloroplasts 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.Significance summaryReactive oxygen species accumulate in the chloroplast (photosynthetic plastids) and signal for stress acclimation by inducing chloroplast degradation, cell death, and changes in nuclear gene expression. We have identified two chloroplast-localized proteins involved in gene regulation that are required to transmit these signals, suggesting that proper plastid gene expression and chloroplast development is necessary to activate chloroplast controlled cellular degradation and nuclear gene expression pathways.

scholarly journals Dual-targeted transcription factors are required for optimal photosynthesis and stress responses in Arabidopsis thaliana

2019 ◽  
Author(s):  
Piotr Gawroński ◽  
Paweł Burdiak ◽  
Lars B. Scharff ◽  
Jakub Mielecki ◽  
Magdalena Zaborowska ◽  
...  
Keyword(s):  
Transcription Factors ◽  
Stress Responses ◽  
Environmental Changes ◽  
Cell Function ◽  
Nuclear Gene ◽  
Transit Peptide ◽  
Protein Translation ◽  
Retrograde Signaling ◽  
Nuclear Gene Expression ◽  
Chloroplast Translation

SummaryChloroplast to nucleus retrograde signaling is essential for cell function, acclimation to fluctuating environmental conditions, plant growth and development. The vast majority of chloroplast proteins are nuclear-encoded and must be imported into the organelle after synthesis in the cytoplasm. This import is essential for the development of fully functional chloroplasts. On the other hand, functional chloroplasts act as sensors of environmental changes and can trigger acclimatory responses that influence nuclear gene expression. Signaling via mobile transcription factors (TFs) has been recently recognized as a way of communication between organelles and the nucleus. In this study, we performed a targeted reverse genetic screen to identify novel dual-localized TFs involved in chloroplast retrograde signaling during stress responses. We found that CHLOROPLAST IMPORT APPARATUS 2 (CIA2), a TF with putative plastid transit peptide can be detected in chloroplasts and the nucleus. Further, we found that CIA2, along with its homolog CIA2-like (CIL) act in an unequally redundant manner and are involved in the regulation of Arabidopsis responses to UV-AB, high light, and heat shock. Finally, our results suggest that both CIA2 and CIL are crucial for chloroplast translation. Our results contribute to a deeper understanding of signaling events in the chloroplast-nucleus cross-talk.SignificanceWe found that a transcription factor CIA2 can be located in chloroplasts and nucleus. CIA2 and is close homolog CIL are involved in protein translation and abiotic stress responses, and we suggest that they play an essential role in retrograde signaling between these organelles.

scholarly journals Mitochondrial redox systems as central hubs in plant metabolism and signalling

2021 ◽  
Author(s):  
Olivier Van Aken
Keyword(s):  
Stress Responses ◽  
Plant Mitochondria ◽  
Nuclear Gene ◽  
Tca Cycle ◽  
Cellular Damage ◽  
Future Research ◽  
Antioxidant Systems ◽  
Plant Metabolism ◽  
Redox Systems ◽  
Glutathione Cycle

Abstract Plant mitochondria are indispensable for plant metabolism and are tightly integrated into cellular homeostasis. This review provides an update on the latest research concerning the organisation and operation of plant mitochondrial redox systems, and how they affect cellular metabolism and signalling, plant development and stress responses. New insights into the organisation and operation of mitochondrial energy systems such as the tricarboxylic acid (TCA) cycle and mitochondrial electron chain (mtETC) are discussed. The mtETC produces reactive oxygen and nitrogen species, which can act as signals or lead to cellular damage, and are thus efficiently removed by mitochondrial antioxidant systems, including Mn-superoxide dismutase, ascorbate-glutathione cycle and thioredoxin-dependent peroxidases. Plant mitochondria are tightly connected with photosynthesis, photorespiration and cytosolic metabolism, thereby providing redox-balancing. Mitochondrial proteins are targets of extensive post-translational modifications, but their functional significance and how they are added or removed remains unclear. To operate in sync with the whole cell, mitochondria can communicate their functional status via mitochondrial retrograde signalling to change nuclear gene expression, and several recent breakthroughs here are discussed. At a whole organism level, plant mitochondria thus play crucial roles from the first minutes after seed imbibition, supporting meristem activity, growth and fertility, until senescence of darkened and aged tissue. Finally, plant mitochondria are tightly integrated with cellular and organismal responses to environmental challenges such as drought, salinity, heat and submergence, but also threats posed by pathogens. Both the major recent advances and outstanding questions are reviewed, which may help future research efforts on plant mitochondria.

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