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Summary Tomato fruit ripening is a complex developmental process that is important for fruit quality and shelf life. Many factors, including ethylene and several key transcription factors, have been shown to play important roles in the regulation of tomato fruit ripening. However, our understanding of the regulation of tomato fruit ripening is still limited. Here, we describe mut26, an EMS‐induced tomato (Solanum lycopersicum) mutant that exhibits chlorophyll‐deficient phenotypes in various organs, including fruits. Genetic mapping and functional analyses revealed that a single‐nucleotide substitution and a corresponding Pro398–>Ser mis‐sense mutation in SlChlH (GENOMES UNCOUPLED 5, GUN5), which encodes the H subunit of magnesium chelatase, are responsible for the defects in the mut26 strain. Transcript analyses towards the expression of many SlPhANGs revealed that mut26 is defective in plastid retrograde signalling during tomato fruit ripening initiation, namely the transition from mature green to breaker stage. mut26 exhibits delayed progression of fruit ripening characterized by reduced fruit ethylene emission, increased fruit firmness, reduced carotenoid content and delayed plastid conversion from chloroplast to chromoplast. Given that fruit ripening requires signalling from plastids to nucleus, these data support the hypothesis that GUN5‐mediated plastid retrograde signalling promotes tomato fruit ripening. We further showed that the delayed fruit ripening of mut26 is not likely caused by reduced chlorophyll content. Taken together, we identified a new function of SlChlH in the promotion of tomato fruit ripening and ethylene biosynthesis, suggesting that GUN5‐mediated plastid retrograde signalling plays a promotive role in tomato fruit ripening. [ABSTRACT FROM AUTHOR]

SUMMARY: In the course of their life, plants continuously experience a wide range of unfavourable environmental conditions in the form of biotic and abiotic stress factors. The perception of stress via various organelles and rapid, tailored cellular responses are essential for the establishment of plant stress resilience. Mitochondria as the biosynthetic sites of energy equivalents in the form of ATP—provided in order to enable a multitude of biological processes in the cell—are often directly impacted by external stress factors. At the same time, mitochondrial function may fluctuate to a tolerable extent without the need to activate downstream retrograde signalling cascades for stress adaptation. In this Focus Review, we summarise the current state of knowledge on the perception and processing of stress signals by mitochondria and show which layers of retrograde signalling, that is, those involving transcription factors, metabolites, but also enzymes with moonlighting functions, enable communication with the nucleus. Also, light is shed on signal integration between mitochondria and chloroplasts as part of retrograde signalling. With this Focus Review, we aim to show ways in which organelle‐specific communication can be further researched and the collected data used in the long‐term to strengthen plant resilience in the context of climate change. [ABSTRACT FROM AUTHOR]

Reactive oxygen species (ROS) and defence hormones like salicylic acid (SA) and jasmonic acid (JA) play pivotal roles in triggering cell death. However, the precise mechanism governing the interaction between ROS and SA/JA remains elusive. Recently, our research revealed that RNAi mutants with suppressed expression of PROGRAMMED CELL DEATH8 (PCD8) exhibit an overabundance of tetrapyrrole intermediates, particularly uroporphyrinogen III (Uro III), leading to the accumulation of singlet oxygen (1O2) during the transition from darkness to light, thereby instigating leaf necrosis. In this investigation, we uncovered that 1O2 stimulates biosynthesis of SA and JA, activating SA/JA signalling and the expression of responsive genes in PCD8 RNAi (pcd8) mutants. Introducing NahG or knocking out PAD4 or NPR1 significantly alleviates the cell death phenotype of pcd8 mutants, while coi1 partially mitigates the pcd8 phenotype. Further exploration revealed that EX1 and GUN1 can partially rescue the pcd8 phenotype by reducing the levels of Uro III and 1O2. Notably, mutations in EX1 mutations but not GUN1, substantially diminish SA content in pcd8 mutants compared to the wild type, implying that EX1 acts as the primary mediator of 1O2 signalling‐mediated SA biosynthesis. Moreover, the triple ex1 gun1 pcd8 displays a phenotype similar to ex1. Overall, our findings underscore that the 1O2‐induced cell death phenotype requires EX1/GUN1‐mediated retrograde signalling in pcd8 mutants, providing novel insights into the interplay between ROS and SA/JA. Summary statement: We uncovered that 1O2 stimulates biosynthesis of SA and JA, activating SA/JA signalling in Arabidopsis PCD8 RNAi mutants; and 1O2 burst‐triggered PCD requires SA and JA; interestingly, EX1 senses 1O2 and initiates the signalling of 1O2 to SA/JA, while GUN1 acts upstream of EX1 and mediates the signal from 1O2 to JA. Overall, it establishes the relationship between chlorophyll metabolism, hormone biosynthesis, and retrograde signalling pathways and provides a new perspective for the interaction between ROS and hormone. [ABSTRACT FROM AUTHOR]

Chloroplast function is essential for growth, development, and plant adaptation to stress. Organelle stress and plant defence responses were examined here using noxy8 (nonresponding to oxylipins 8) from a series of Arabidopsis mutants. The noxy8 mutation was located at the CLPC2 gene, encoding a chloroplast chaperone of the protease complex CLP. Although its CLPC1 paralogue is considered to generate redundancy, our data reveal significant differences distinguishing CLPC2 and CLPC1 functions. As such, clpc1 mutants displayed a major defect in housekeeping chloroplast proteostasis, leading to a pronounced reduction in growth and pigment levels, enhanced accumulation of chloroplast and cytosol chaperones, and resistance to fosmidomycin. Conversely, clpc2 mutants showed severe susceptibility to lincomycin inhibition of chloroplast translation and resistance to Antimycin A inhibition of mitochondrial respiration. In the response to Pseudomonas syringae pv. tomato, clpc2 but not clpc1 mutants were resistant to bacterial infection, showing higher salicylic acid levels, defence gene expression and 9‐LOX pathway activation. Our findings suggest CLPC2 and CLPC1 functional specificity, with a preferential involvement of CLPC1 in housekeeping processes and of CLPC2 in stress responses. Summary statement: The CLPC1 and CLPC2 chaperones participate in protein unfolding prior degradation by the chloroplast CLP protease. In contrast to previous data indicating functional redundancy, our results suggest CLPC2 and CLPC1 specificity, with a preferential involvement of CLPC1 in housekeeping processes and of CLPC2 in stress responses. [ABSTRACT FROM AUTHOR]

Singlet oxygen (SO) is among the most potent reactive oxygen species, and readily oxidizes proteins, lipids and DNA. It can be generated at the plant surface by phototoxins in the epidermis, acting as a direct defense against pathogens and herbivores (including humans). SO can also accumulate within mitochondria, peroxisomes, cytosol and the nucleus through multiple enzymatic and nonenzymatic processes. However, the majority of research on intracellular SO generation in plants has focused on transfer of light energy to triplet oxygen by photopigments from the chloroplast. SO accumulates in response to diverse stresses that perturb chloroplast metabolism, and while its high reactivity limits diffusion distances, it participates in retrograde signalling through the EXECUTER1 sensor, generation of carotenoid metabolites and possibly other unknown pathways. SO thereby reprogrammes nuclear gene expression and modulates hormone signalling and programmed cell death. While SO signalling has long been known to regulate plant responses to high‐light stress, recent literature also suggests a role in plant interactions with insects, bacteria and fungi. The goals of this review are to provide a brief overview of SO, summarize evidence for its involvement in biotic stress responses and discuss future directions for the study of SO in defense signalling. Summary statement: This review summarizes the evidence for a role of singlet oxygen (SO) in mediating plant responses to herbivores and pathogens, and makes a case for the importance of further studies on this potent molecule for signalling and defense. Evidence reviewed here is primarily from Arabidopsis thaliana, although other species are covered where information is available. [ABSTRACT FROM AUTHOR]

Integration of reactive oxygen species (ROS)-mediated signal transduction pathways via redox sensors and the thiol-dependent signalling network is of increasing interest in cell biology for their implications in plant growth and productivity. Redox regulation is an important point of control in protein structure, interactions, cellular location, and function, with thioredoxins (TRXs) and glutaredoxins (GRXs) being key players in the maintenance of cellular redox homeostasis. The crosstalk between second messengers, ROS, thiol redox signalling, and redox homeostasis-related genes controls almost every aspect of plant development and stress response. We review the emerging roles of TRXs and GRXs in redox-regulated processes interacting with other cell signalling systems such as organellar retrograde communication and gene expression, especially in plants during their development and under stressful environments. This approach will cast light on the specific role of these proteins as redox signalling components, and their importance in different developmental processes during abiotic stress. [ABSTRACT FROM AUTHOR]

Balanced photosynthesis is essential for improved plant survival and agricultural benefits in terms of biomass and yield. Photosynthesis is the hub of energy metabolism in plants; however, drought stress (DS) strongly perturbs photosynthetic efficiency due to biochemical and diffusive limitations that reduce key photosynthetic components and close stomata. This review describes photosynthetic responses, chloroplast retrograde signalling, and genetic imprints that curtail DS damage to photosynthetic machinery. While stomatal closure, disrupted photosynthetic systems, over‐reduced electron transport rates (ETR), partial hindrance of the Calvin cycle, and reduced pigment contents strongly affect the repertoire of photosynthetic processes under DS, chloroplast retrograde signalling also has a plausible role in preserving photosynthetic capacity. Progress in agronomic, genetic engineering approaches and isoprene regulation would help to rescue photosynthetic apparatus under DS. [ABSTRACT FROM AUTHOR]

Most retrograde signalling research in plants was performed using Arabidopsis, so an evolutionary perspective on mitochondrial retrograde regulation (MRR) is largely missing. Here, we used phylogenetics to track the evolutionary origins of factors involved in plant MRR. In all cases, the gene families can be traced to ancestral green algae or earlier. However, the specific subfamilies containing factors involved in plant MRR in many cases arose during the transition to land. NAC transcription factors with C-terminal transmembrane domains, as observed in the key regulator ANAC017, can first be observed in non-vascular mosses, and close homologs to ANAC017 can be found in seed plants. Cyclin-dependent kinases (CDKs) are common to eukaryotes, but E-type CDKs that control MRR also diverged in conjunction with plant colonization of land. AtWRKY15 can be traced to the earliest land plants, while AtWRKY40 only arose in angiosperms and AtWRKY63 even more recently in Brassicaceae. Apetala 2 (AP2) transcription factors are traceable to algae, but the ABI4 type again only appeared in seed plants. This strongly suggests that the transition to land was a major driver for developing plant MRR pathways, while additional fine-tuning events have appeared in seed plants or later. Finally, we discuss how MRR may have contributed to meeting the specific challenges that early land plants faced during terrestrialization. [ABSTRACT FROM AUTHOR]

Summary: The pentatricopeptide repeat protein GENOMES UNCOUPLED1 (GUN1) is required for chloroplast‐to‐nucleus signalling when plastid translation becomes inhibited during chloroplast development in Arabidopsis thaliana, but its exact molecular function remains unknown.We analysed GUN1 sequences in land plants and streptophyte algae. We tested functional conservation by complementation of the Arabidopsis gun1 mutant with GUN1 genes from the streptophyte alga Coleochate orbicularis or the liverwort Marchantia polymorpha. We also analysed the transcriptomes of M. polymorpha gun1 knockout mutant lines during chloroplast development.GUN1 evolved within the streptophyte algal ancestors of land plants and is highly conserved among land plants but missing from the Rafflesiaceae that lack chloroplast genomes. GUN1 genes from C. orbicularis and M. polymorpha suppress the cold‐sensitive phenotype of the Arabidopsis gun1 mutant and restore typical retrograde responses to treatments with inhibitors of plastid translation, even though M. polymorpha responds very differently to such treatments.Our findings suggest that GUN1 is an ancient protein that evolved within the streptophyte algal ancestors of land plants before the first plants colonized land more than 470 million years ago. Its primary role is likely to be in chloroplast gene expression and its role in chloroplast retrograde signalling probably evolved more recently. [ABSTRACT FROM AUTHOR]

Abstract Background In Saccharomyces cerevisiae, the retrograde signalling pathway is activated in ρ0/− cells, which lack mitochondrial DNA. Within this pathway, the activation of the transcription factor Pdr3 induces transcription of the ATP-binding cassette (ABC) transporter gene, PDR5, and causes pleiotropic drug resistance (PDR). Although a histone deacetylase, Rpd3, is also required for cycloheximide resistance in ρ0/− cells, it is currently unknown whether Rpd3 and its DNA binding partners, Ume6 and Ash1, are involved in the activation of PDR5 transcription and PDR in ρ0/− cells. This study investigated the roles of RPD3, UME6, and ASH1 in the activation of PDR5 transcription and PDR by retrograde signalling in ρ0 cells. Results ρ0 cells in the rpd3∆ and ume6∆ strains, with the exception of the ash1∆ strain, were sensitive to fluconazole and cycloheximide. The PDR5 mRNA levels in ρ0 cells of the rpd3∆ and ume6∆ strains were significantly reduced compared to the wild-type and ash1∆ strain. Transcriptional expression of PDR5 was reduced in cycloheximide-exposed and unexposed ρ0 cells of the ume6∆ strain; the transcriptional positive response of PDR5 to cycloheximide exposure was also impaired in this strain. Conclusions RPD3 and UME6 are responsible for enhanced PDR5 mRNA levels and PDR by retrograde signalling in ρ0 cells of S. cerevisiae.

Summary: Some canonical plant hormones such as auxins and gibberellins have precursors that are biogenic volatiles (indole, indole acetonitrile, phenylacetaldoxime and ent‐kaurene). Cytokinins, abscisic acid and strigolactones are hormones comprising chemical moieties that have distinct volatile analogues, and are synthesised alongside constitutively emitted volatiles (isoprene, sesquiterpenes, lactones, benzenoids and apocarotenoid volatiles). Nonvolatile hormone analogues and biogenic volatile organic compounds (BVOCs) evolved in tandem as growth and behavioural regulators in unicellular organisms. In plants, however, nonvolatile hormones evolved as regulators of growth, development and differentiation, while endogenous BVOCs (often synthesised lifelong) became subtle regulators of hormone synthesis, availability, activity and turnover, all supported by functionally redundant components of hormone metabolism. Reciprocal changes in the abundance and activity of hormones, nitric oxide, and constitutive plant volatiles constantly bridge retrograde and anterograde signalling to maintain hormone equilibria even in unstressed plants. This is distinct from transient interference in hormone signalling by stress‐induced and exogenously received volatiles. [ABSTRACT FROM AUTHOR]

His research chiefly focuses on identifying and characterising new factors involved in the regulation of anthocyanin biosynthesis during high light acclimation. Keywords: acclimation; anthocyanin; early career researcher; flavonoid biosynthesis; high light; Profile; retrograde signalling; stress response EN acclimation anthocyanin early career researcher flavonoid biosynthesis high light Profile retrograde signalling stress response 2016 2018 3 11/21/22 20221215 NES 221215 Galileo Estopare Araguirang's poster 'When plants paint their leaves purple: analyses of new factors involved in the regulation of anthocyanin biosynthesis in Arabidopsis during high light' won first prize at the Next Generations Scientists meeting 2022 in Tartu, Estonia. Under the supervision of Professor Dr Alfred Batschauer, he carried out his MSc thesis on the photobiochemistry of a cryptochrome 2 mutant at Philipps-Universität Marburg, Germany (2017). Anthocyanin, early career researcher, acclimation, Profile, stress response, flavonoid biosynthesis, high light, retrograde signalling. [Extracted from the article]

The response of chloroplasts to adverse environmental cues, principally increases in light intensity, stimulates chloroplast-to-nucleus retrograde signalling, which leads to the induction of immediate protective responses and longer-term acclimation. Hydrogen peroxide (H2O2), generated during photosynthesis, is proposed to both initiate and transduce a retrograde signal in response to photoinhibitory light intensities. Signalling specificity achieved by chloroplast-sourced H2O2 for signal transduction may be dependent upon the oft-observed close association of a proportion of these organelles with the nucleus. In this review, we consider more precisely the nature of the close association between a chloroplast appressed to the nucleus and the requirement for H2O2 to cross both the double membranes of the chloroplast and nuclear envelopes. Of particular relevance is that the endoplasmic reticulum (ER) has close physical contact with chloroplasts and is contiguous with the nuclear envelope. Therefore, the perinuclear space, which transducing H2O2 molecules would have to cross, may have an oxidising environment the same as the ER lumen. Based on studies in animal cells, the ER lumen may be a significant source of H2O2 in plant cells arising from the oxidative folding of proteins. If this is the case, then there is potential for the ER lumen/perinuclear space to be an important location to modify chloroplast-to-nucleus H2O2 signal transduction and thereby introduce modulation of it by additional different environmental cues. These would include for example, heat stress and pathogen infection, which induce the unfolded protein response characterised by an increased H2O2 level in the ER lumen. [ABSTRACT FROM AUTHOR]

Background: In Saccharomyces cerevisiae, the retrograde signalling pathway is activated in ρ0/− cells, which lack mitochondrial DNA. Within this pathway, the activation of the transcription factor Pdr3 induces transcription of the ATP-binding cassette (ABC) transporter gene, PDR5, and causes pleiotropic drug resistance (PDR). Although a histone deacetylase, Rpd3, is also required for cycloheximide resistance in ρ0/− cells, it is currently unknown whether Rpd3 and its DNA binding partners, Ume6 and Ash1, are involved in the activation of PDR5 transcription and PDR in ρ0/− cells. This study investigated the roles of RPD3, UME6, and ASH1 in the activation of PDR5 transcription and PDR by retrograde signalling in ρ0 cells. Results: ρ0 cells in the rpd3∆ and ume6∆ strains, with the exception of the ash1∆ strain, were sensitive to fluconazole and cycloheximide. The PDR5 mRNA levels in ρ0 cells of the rpd3∆ and ume6∆ strains were significantly reduced compared to the wild-type and ash1∆ strain. Transcriptional expression of PDR5 was reduced in cycloheximide-exposed and unexposed ρ0 cells of the ume6∆ strain; the transcriptional positive response of PDR5 to cycloheximide exposure was also impaired in this strain. Conclusions: RPD3 and UME6 are responsible for enhanced PDR5 mRNA levels and PDR by retrograde signalling in ρ0 cells of S. cerevisiae. [ABSTRACT FROM AUTHOR]

The inducible carbon concentration mechanism (CCM) in Chlamydomonas reinhardtii has been well defined from a molecular and ultrastructural perspective. Inorganic carbon transport proteins, and strategically located carbonic anhydrases deliver CO2 within the chloroplast pyrenoid matrix where Rubisco is packaged. However, there is little understanding of the fundamental signalling and sensing processes leading to CCM induction. While external CO2 limitation has been believed to be the primary cue, the coupling between energetic supply and inorganic carbon demand through regulatory feedback from light harvesting and photorespiration signals could provide the original CCM trigger. Key questions regarding the integration of these processes are addressed in this review. We consider how the chloroplast functions as a crucible for photosynthesis, importing and integrating nuclear-encoded components from the cytoplasm, and sending retrograde signals to the nucleus to regulate CCM induction. We hypothesize that induction of the CCM is associated with retrograde signals associated with photorespiration and/or light stress. We have also examined the significance of common evolutionary pressures for origins of two co-regulated processes, namely the CCM and photorespiration, in addition to identifying genes of interest involved in transcription, protein folding, and regulatory processes which are needed to fully understand the processes leading to CCM induction. [ABSTRACT FROM AUTHOR]

Plant life relies on complex arrays of environmental stress sensing and signalling mechanisms. Extremophile plants develop and grow in harsh environments with extremes of cold, heat, drought, desiccation, or salinity, which have resulted in original adaptations. In accordance with their polyphyletic origins, extremophile plants likely possess core mechanisms of plant abiotic stress signalling. However, novel properties or regulations may have emerged in the context of extremophile adaptations. Comparative omics of extremophile genetic models, such as Arabidopsis lyrata , Craterostigma plantagineum , Eutrema salsugineum , and Physcomitrella patens , reveal diverse strategies of sensing and signalling that lead to a general improvement in abiotic stress responses. Current research points to putative differences of sensing and emphasizes significant modifications of regulatory mechanisms, at the level of secondary messengers (Ca2+, phospholipids, reactive oxygen species), signal transduction (intracellular sensors, protein kinases, transcription factors, ubiquitin-mediated proteolysis) or signalling crosstalk. Involvement of hormone signalling, especially ABA signalling, cell homeostasis surveillance, and epigenetic mechanisms, also shows that large-scale gene regulation, whole-plant integration, and probably stress memory are important features of adaptation to extreme conditions. This evolutionary and functional plasticity of signalling systems in extremophile plants may have important implications for plant biotechnology, crop improvement, and ecological risk assessment under conditions of climate change. [ABSTRACT FROM AUTHOR]

SUMMARY: Chloroplast perturbations activate retrograde signalling pathways, causing dynamic changes of gene expression. Besides transcriptional control of gene expression, different classes of small non‐coding RNAs (sRNAs) act in gene expression control, but comprehensive analyses regarding their role in retrograde signalling are lacking. We performed sRNA profiling in response to norflurazon (NF), which provokes retrograde signals, in Arabidopsis thaliana wild type (WT) and the two retrograde signalling mutants gun1 and gun5. The RNA samples were also used for mRNA and long non‐coding RNA profiling to link altered sRNA levels to changes in the expression of their cognate target RNAs. We identified 122 sRNAs from all known sRNA classes that were responsive to NF in the WT. Strikingly, 142 and 213 sRNAs were found to be differentially regulated in both mutants, indicating a retrograde control of these sRNAs. Concomitant with the changes in sRNA expression, we detected about 1500 differentially expressed mRNAs in the NF‐treated WT and around 900 and 1400 mRNAs that were differentially regulated in the gun1 and gun5 mutants, with a high proportion (~30%) of genes encoding plastid proteins. Furthermore, around 20% of predicted miRNA targets code for plastid‐localised proteins. Among the sRNA–target pairs, we identified pairs with an anticorrelated expression as well pairs showing other expressional relations, pointing to a role of sRNAs in balancing transcriptional changes upon retrograde signals. Based on the comprehensive changes in sRNA expression, we assume a considerable impact of sRNAs in retrograde‐dependent transcriptional changes to adjust plastidic and nuclear gene expression. Significance Statement: Perturbations of plastid functions trigger retrograde signalling to adjust plastidic and nuclear gene expression; however, the role of small non‐coding RNAs acting as regulators in these pathways is not well understood. We analysed small non‐coding RNA expression in response to retrograde signals in Arabidopsis thaliana wild type and two retrograde signalling mutants and identified members of all known small non‐coding RNA classes, pointing to a functional role of these RNA classes in retrograde pathways. [ABSTRACT FROM AUTHOR]

SUMMARY: Mitochondria have critical functions in the acclimation to abiotic and biotic stresses. Adverse environmental conditions lead to increased demands in energy supply and metabolic intermediates, which are provided by mitochondrial ATP production and the tricarboxylic acid (TCA) cycle. Mitochondria also play a role as stress sensors to adjust nuclear gene expression via retrograde signalling with the transcription factor (TF) ANAC017 and the kinase CDKE1 key components to integrate various signals into this pathway. To determine the importance of mitochondria as sensors of stress and their contribution in the tolerance to adverse growth conditions, a comparative phenotypical, physiological and transcriptomic characterisation of Arabidopsis mitochondrial signalling mutants (cdke1/rao1 and anac017/rao2) and a set of contrasting accessions was performed after applying the complex compound stress of submergence. Our results showed that impaired mitochondrial retrograde signalling leads to increased sensitivity to the stress treatments. The multi‐factorial approach identified a network of 702 co‐expressed genes, including several WRKY TFs, overlapping in the transcriptional responses in the mitochondrial signalling mutants and stress‐sensitive accessions. Functional characterisation of two WRKY TFs (WRKY40 and WRKY45), using both knockout and overexpressing lines, confirmed their role in conferring tolerance to submergence. Together, the results revealed that acclimation to submergence is dependent on mitochondrial retrograde signalling, and underlying transcriptional re‐programming is used as an adaptation mechanism. Significance Statement: Mitochondria provide the energy and metabolic building blocks allowing plants to respond to adverse environmental conditions. Our results show that plant mitochondria also have a function as stress sensors, and that corresponding signalling pathways that lead to the adjustment of gene expression are used for the adaptation to stress. [ABSTRACT FROM AUTHOR]

• Each kingdom has apparently developed its specific UPRmt regulators. • However, UPRmt activation induces nuclear gene expression of many similar genes. • Strategies to resolve mitochondrial dysfunctions are thus partially conserved. • We identified conserved genes across kingdoms as candidates for future research. Mitochondria are key components of eukaryotic cells, so their proper functioning is monitored via different mitochondrial signalling responses. One of these mitochondria-to-nuclear 'retrograde' responses to maintain mitochondrial homeostasis is the mitochondrial unfolded protein response (UPRmt), which can be activated by a variety of defects including blocking mitochondrial translation, respiration, protein import or transmembrane potential. Although UPRmt was first reported in cultured mammalian cells, this signalling pathway has also been extensively studied in the nematode Caenorhabditis elegans. In yeast, there are no published studies focusing on UPRmt in a strict sense, but other unfolded protein responses (UPR) that appear related to UPRmt have been described, such as the UPR activated by protein mistargeting (UPRam) and mitochondrial compromised protein import response (mitoCPR). In plants, very little is known about UPRmt and only recently some of the regulators have been identified. In this paper, we summarise and compare the current knowledge of the UPRmt and related responses across eukaryotic kingdoms: animals, fungi and plants. Our comparison suggests that each kingdom has evolved its own specific set of regulators, however, the functional categories represented among UPRmt–related target genes appear to be largely overlapping. This indicates that the strategies for preserving proper mitochondrial functions are partially conserved, targeting mitochondrial chaperones, proteases, import components, dynamics and stress response, but likely also non-mitochondrial functions including growth regulators/hormone balance and amino acid metabolism. We also identify homologs of known UPRmt regulators and responsive genes across kingdoms, which may be interesting targets for future research. [ABSTRACT FROM AUTHOR]

• Plant UCPs biochemical properties, 3D structure, and physiological role are reviewed. • UCPs transcriptional regulation and co-expression networks across species is revisited. • Plant UCPs play a major role in cell signaling towards cellular bioenergetics and stress response. The biological function of plant mitochondrial uncoupling proteins (pUCPs) has been a matter of considerable controversy. For example, the pUCP capacity to uncouple respiration from ATP synthesis in vivo has never been fully acknowledged, in contrast to the mammalian UCP1 (mUCP1) role in uncoupling respiration-mediated thermogenesis. Interestingly, both pUCPs and mUCPs have been associated with stress response and metabolic perturbations. Some central questions that remain are how pUCPs and mUCPs compare in biochemical properties, molecular structure and cell biology under physiological and metabolically perturbed conditions. This review takes advantage of the large amount of data available for mUCPs to review the biochemical properties, 3D structure models and potential physiological roles of pUCPs during plant development and response to stress. The biochemical properties and structure of pUCPs are revisited in light of the recent findings that pUCPs catalyse the transport of metabolites across the mitochondrial inner membrane and the resolved mUCP2 protein structure. Additionally, transcriptional regulation and co-expression networks of UCP orthologues across species are analysed, taking advantage of publicly available curated experimental datasets. Taking these together, the biological roles of pUCPs are analysed in the context of their potential roles in thermogenesis, ROS production, cell signalling and the regulation of plant cellular bioenergetics. Finally, pUCPs biological function is discussed in the context of their potential role in protecting against environmental stresses. [ABSTRACT FROM AUTHOR]

Chloroplasts compose about one-quarter of the mesophyll cell volume and contain about 60% of the cell protein. Photosynthetic carbon assimilation is the dominating metabolism in illuminated leaves. To optimize the resource expenditure in these costly organelles and to control and adjust chloroplast metabolism, an intensive transfer of information between nucleus-cytoplasm and chloroplasts occurs in both directions as anterograde and retrograde signalling. Recent research identified multiple retrograde pathways that use metabolite transfer and include reaction products of lipids and carotenoids with reactive oxygen species (ROS). Other pathways use metabolites of carbon, sulfur and nitrogen metabolism, low molecular weight antioxidants and hormone precursors to carry information between the cell compartments. This reviewfocuses on redox- and ROS-related retrograde signalling pathways. In analogy to the microbe-associated molecular pattern, we propose the term 'chloroplast-associated molecular pattern' which connects chloroplast performance to extrachloroplast processes such as nuclear gene transcription, posttranscriptional processing, including translation, andRNAand protein fate. [ABSTRACT FROM AUTHOR]

Neuronal mitochondrial dysfunction causes primary mitochondrial diseases and likely contributes to neurodegenerative diseases including Parkinson's and Alzheimer's disease. Mitochondrial dysfunction has also been documented in neurodevelopmental disorders such as tuberous sclerosis complex and autism spectrum disorder. Only symptomatic treatments exist for neurodevelopmental disorders, while neurodegenerative diseases are largely untreatable. Altered mitochondrial function activates mitochondrial retrograde signalling pathways, which enable signalling to the nucleus to reprogramme nuclear gene expression. In this review, we discuss the role of mitochondrial retrograde signalling in neurological diseases. We summarize how mitochondrial dysfunction contributes to neurodegenerative disease and neurodevelopmental disorders. Mitochondrial signalling mechanisms that have relevance to neurological disease are discussed. We then describe studies documenting retrograde signalling pathways in neurons and glia, and in animal models of neuronal mitochondrial dysfunction and neurological disease. Finally, we suggest how specific retrograde signalling pathways can be targeted to develop novel treatments for neurological diseases. [ABSTRACT FROM AUTHOR]

Lifespan in eukaryotic species can be prolonged by shifting fromcellular states favouring growth to those favouring maintenance and stress resistance. For instance, perturbations in mitochondrial oxidative phosphorylation (OXPHOS) can shift cells into this latter state and extend lifespan. Because mitochondria rely on proteins synthesized from nuclear as well as mitochondrial DNA, they need to constantly send and receive messages from other compartments of the cell in order to function properly andmaintain homeostasis, and lifespan extension is often dependent on this cross-compartmental signalling. Here, we describe the mechanisms of bi-directional mitochondrial cross-compartmental signalling resulting in proteostasis and longevity. These proteostasis mechanisms are highly context-dependent, governed by the origin and extent of stress. Furthermore, we discuss the translatability of these mechanisms and explore therapeutic developments, such as the antibiotic studies targeting mitochondria or mitochondria-derived peptides as therapies for age-related diseases such as neurodegeneration and cancer. [ABSTRACT FROM AUTHOR]

The Arabidopsis mutant rcd1 is tolerant to methyl viologen (MV). MV enhances the Mehler reaction, i.e. electron transfer from Photosystem I (PSI) to O2, generating reactive oxygen species (ROS) in the chloroplast. To study the MV tolerance of rcd1, we first addressed chloroplast thiol redox enzymes potentially implicated in ROS scavenging. NADPH-thioredoxin oxidoreductase type C (NTRC) was more reduced in rcd1. NTRC contributed to the photosynthetic and metabolic phenotypes of rcd1, but did not determine its MV tolerance. We next tested rcd1 for alterations in the Mehler reaction. In rcd1, but not in the wild type, the PSI-to-MV electron transferwas abolished by hypoxic atmosphere. A characteristic feature of rcd1 is constitutive expression of mitochondrial dysfunction stimulon (MDS) genes that affect mitochondrial respiration. Similarly to rcd1, in other MDS-overexpressing plants hypoxia also inhibited the PSI-to-MV electron transfer. One possible explanation is that the MDS gene products may affect the Mehler reaction by altering the availability of O2. In green tissues, this putative effect is masked by photosynthetic O2 evolution. However, O2 evolution was rapidly suppressed in MV-treated plants. Transcriptomic meta-analysis indicated that MDS gene expression is linked to hypoxic response not only under MV, but also in standard growth conditions. [ABSTRACT FROM AUTHOR]

Impaired mitochondrial translation or reduced mitochondrial protein import can lead to imbalances in mitochondrial protein composition. Such mitochondrial proteotoxic stresses can trigger a nuclear transcriptional response commonly described as the mitochondrial unfolded protein response (UPRmt). Despite extensive studies of UPRmt pathways in animal and fungal systems, very little is known about how the UPRmt is regulated in plants. Through comparison of Arabidopsis thaliana whole-genome transcriptome data, it was found that most genes induced bymitochondrial ribosome inhibitor doxycycline are also induced by Complex III inhibitor antimycin A. We demonstrate that transcriptional responses to a wide range of mitochondrial proteotoxic stress-triggers are regulated by the transcription factor ANAC017, which was shown to reside in the endoplasmic reticulum (ER). By contrast, no consistent evidence was found for genes that are specifically induced by doxycycline but not antimycin A. Furthermore, ANAC017 gainand loss-of-function mutants showed marked resistance or susceptibility, respectively, to mitochondrial stress-inducing treatments, demonstrating the physiological importance of ANAC017 during mitochondrial proteotoxic stress. Finally, it was shown that ethylene signalling promotes mitochondriato- nucleus signalling, most likely independently of ANAC017. Overall, this study showsthat in plants, the UPRmt is largely overlapping with, and perhaps identical to, 'classical' mitochondrial retrograde signalling, and is mediated by ER-anchored transcription factor ANAC017. [ABSTRACT FROM AUTHOR]

Retrograde signalling refers to the regulation of nuclear gene expression in response to functional changes in organelles. In plants, the two energyconverting organelles, mitochondria and chloroplasts, are tightly coordinated to balance their activities. Although our understanding of components involved in retrograde signalling has greatly increased in the last decade, studies on the regulation of the two organelle signalling pathways have been largely independent. Thus, the mechanism of how mitochondrial and chloroplastic retrograde signals are integrated is largely unknown. Here, we summarize recent findings on the function of mitochondrial signalling components and their links to chloroplast retrograde responses. From this, a picture emerges showing that the major regulators are integrators of both organellar retrograde signalling pathways. [ABSTRACT FROM AUTHOR]

The signalling pathways that regulate intercellular trafficking via plasmodesmata (PD) remain largely unknown. Analyses of mutants with defects in intercellular trafficking led to the hypothesis that chloroplasts are important for controlling PD, probably by retrograde signalling to the nucleus to regulate expression of genes that influence PD formation and function, an idea encapsulated in the organelle-nucleus-PD signalling (ONPS) hypothesis. ONPS is supported by findings that point to chloroplast redox state as also modulating PD. Here, we have attempted to further elucidate details of ONPS. Through reverse genetics, expression of select nucleus-encoded genes with known or predicted roles in chloroplast gene expression was knocked down, and the effects on intercellular trafficking were then assessed. Silencing most genes resulted in chlorosis, and the expression of several photosynthesis and tetrapyrrole biosynthesis associated nuclear genes was repressed in all silenced plants. PD-mediated intercellular trafficking was changed in the silenced plants, consistent with predictions of the ONPS hypothesis. One striking observation, best exemplified by silencing the PNPase homologues, was that the degree of chlorosis of silenced leaves was not correlated with the capacity for intercellular trafficking. Finally, we measured the distribution of PD in silenced leaves and found that intercellular trafficking was positively correlated with the numbers of PD. Together, these results not only provide further support for ONPS but also point to a genetic mechanism for PD formation, clarifying a longstanding question about PD and intercellular trafficking. [ABSTRACT FROM AUTHOR]

Communication between chloroplasts and the nucleus in response to various environmental cues may be mediated by various small molecules. Signalling specificity could be enhanced if the physical contact between these organelles facilitates direct transfer and prevents interference from other subcellular sources of the same molecules. Plant cells have plastid-nuclear complexes, which provide close physical contact between these organelles. Plastid-nuclear complexes have been proposed to facilitate transfer of photosynthesis- derived H2O2 to the nucleus in high light. Stromules (stroma filled tubular plastid extensions) may provide an additional conduit for transfer of a wider range of signalling molecules, including proteins. However, plastid- nuclear complexes and stromules have been hitherto treated as distinct phenomena. We suggest that plastid-nuclear complexes and stromules work in a coordinated manner so that, according to environmental conditions or developmental state, the two modes of connection contribute to varying extents. We hypothesize that this association is dynamic and that there may be a link between plastid-nuclear complexes and the development of stromules. Furthermore, the changes in contact could alter signalling specificity by allowing an extended or different range of signalling molecules to be delivered to the nucleus. [ABSTRACT FROM AUTHOR]

Chloroplast-to-nucleus retrograde signalling (RS) is known to impact plant growth and development. In Arabidopsis, we and others have shown that RS affects seedling establishment by inhibiting deetiolation. In the presence of lincomycin, a chloroplast protein synthesis inhibitor that triggers RS, Arabidopsis light-grown seedlings display partial skotomorphogenesis with undeveloped plastids and closed cotyledons. By contrast, RS in monocotyledonous has been much less studied. Here, we show that emerging rice seedlings exposed to lincomycin do not accumulate chlorophyll but otherwise remain remarkably unaffected. However, by using high red (R) and blue (B) monochromatic lights in combination with lincomycin, we have uncovered a RS inhibition of length and a reduction in the B light-induced declination of the second leaf. Furthermore, we present data showing that seedlings grown in high B and R light display different non-photochemical quenching capacity. Our findings support the view that excess B and R light impact seedling photomorphogenesis differently to photoprotect and optimize the response to high-light stress. [ABSTRACT FROM AUTHOR]

Defects in chloroplast development are 'retrograde-signalled' to the nucleus, reducing synthesis of photosynthetic or related proteins. The Arabidopsis cue8 mutant manifests virescence, a slow-greening phenotype, and is defective at an early stage in plastid development. Greening cotyledons or early leaf cells of cue8 exhibit immature chloroplasts which fail to fill the available cellular space. Such chloroplasts show reduced expression of genes of photosynthetic function, dependent on the plastid-encoded polymerase (PEP), while the expression of genes of housekeeping function driven by the nucleusencoded polymerase (NEP) is elevated, a phenotype shared with mutants in plastid genetic functions. We attribute this phenotype to reduced expression of specific PEP-controlling sigma factors, elevated expression of RPOT (NEP) genes and maintained replication of plastid genomes (resulting in densely coalesced nucleoids in the mutant), i.e. it is due to an anterograde nucleus-to-chloroplast correction, analogous to retention of a juvenile plastid state. Mutants in plastid protein import components, particularly those involved in housekeeping protein import, also show this 'retro-anterograde' correction. Loss of CUE8 also causes changes in mRNA editing. The overall response has strong fitness value: loss of GUN1, an integrator of retrograde signalling, abolishes elements of it (albeit not others, including editing changes), causing bleaching and eventual seedling lethality upon cue8 gun1. This highlights the adaptive significance of virescence and retrograde signalling. [ABSTRACT FROM AUTHOR]

We previously showed that Arabidopsis mda1 and mterf9 mutants, defective in the chloroplast‐targeted mitochondrial transcription termination factors mTERF5 and mTERF9, respectively, display altered responses to abiotic stresses and abscisic acid (ABA), as well as perturbed development, likely through abnormal chloroplast biogenesis.To advance the functional analysis of mTERF5 and mTERF9, we obtained and characterized overexpression (OE) lines. Additionally, we studied genetic interactions between sca3‐2, affected in the plastid‐RNA polymerase RpoTp, and the mda1‐1 and mterf9 mutations. We also investigated the role of mTERF5 and mTERF9 in plastid translation and plastid‐to‐nucleus signalling.We found that mTERF9 OE reduces salt and ABA tolerance, while mTERF5 or mTERF9 OE alter expression of nuclear and plastid genes. We determined that mda1‐1 and mterf9 mutations genetically interact with sca3‐2. Further, plastid 16S rRNA levels were reduced in mda1‐1 and mterf9 mutants, and mterf9 was more sensitive to chemical inhibitors of chloroplast translation. Expression of the photosynthesis gene LHCB1, a retrograde signalling marker, was differentially affected in mda1‐1 and/or mterf9 compared to wild‐type Col‐0, after treatments with inhibitors of carotenoid biosynthesis (norflurazon) or chloroplast translation (lincomycin). Moreover, mterf9, but not mda1‐1, synergistically interacts with gun1‐1, defective in GUN1, a central integrator of plastid retrograde signals.Our results show that mTERF9, and to a lesser extent mTERF5, are negative regulators of salt tolerance and that both genes are functionally related to RpoTp, and that mTERF9 is likely required for plastid ribosomal stability and/or assembly. Furthermore, our findings support a role for mTERF9 in retrograde signalling. [ABSTRACT FROM AUTHOR]

VIPP proteins aid thylakoid biogenesis and membrane maintenance in cyanobacteria, algae, and plants. Some members of the Chlorophyceae contain two VIPP paralogs termed VIPP1 and VIPP2, which originate from an early gene duplication event during the evolution of green algae. VIPP2 is barely expressed under nonstress conditions but accumulates in cells exposed to high light intensities or H2O2, during recovery from heat stress, and in mutants with defective integration (alb3.1) or translocation (secA) of thylakoid membrane proteins. Recombinant VIPP2 forms rod‐like structures in vitro and shows a strong affinity for phosphatidylinositol phosphate. Under stress conditions, >70% of VIPP2 is present in membrane fractions and localizes to chloroplast membranes. A vipp2 knock‐out mutant displays no growth phenotypes and no defects in the biogenesis or repair of photosystem II. However, after exposure to high light intensities, the vipp2 mutant accumulates less HSP22E/F and more LHCSR3 protein and transcript. This suggests that VIPP2 modulates a retrograde signal for the expression of nuclear genes HSP22E/F and LHCSR3. Immunoprecipitation of VIPP2 from solubilized cells and membrane‐enriched fractions revealed major interactions with VIPP1 and minor interactions with HSP22E/F. Our data support a distinct role of VIPP2 in sensing and coping with chloroplast membrane stress. The VIPP2 protein from Chlamydomonas reinhardtii localizes predominantly to chloroplast membranes under stresses inducing protein mistargeting and misfolding. VIPP2 interacts with VIPP1 as major partner and with HSP22E/F as minor partner and modulates a retrograde signal for HSP22E/F gene expression in high light. [ABSTRACT FROM AUTHOR]

Background Mitochondria play a diversity of physiological and metabolic roles under conditions of abiotic or biotic stress. They may be directly subjected to physico-chemical constraints, and they are also involved in integrative responses to environmental stresses through their central position in cell nutrition, respiration, energy balance and biosyntheses. In plant cells, mitochondria present various biochemical peculiarities, such as cyanide-insensitive alternative respiration, and, besides integration with ubiquitous eukaryotic compartments, their functioning must be coupled with plastid functioning. Moreover, given the sessile lifestyle of plants, their relative lack of protective barriers and present threats of climate change, the plant cell is an attractive model to understand the mechanisms of stress/organelle/cell integration in the context of environmental stress responses. Scope The involvement of mitochondria in this integration entails a complex network of signalling, which has not been fully elucidated, because of the great diversity of mitochondrial constituents (metabolites, reactive molecular species and structural and regulatory biomolecules) that are linked to stress signalling pathways. The present review analyses the complexity of stress signalling connexions that are related to the mitochondrial electron transport chain and oxidative phosphorylation system, and how they can be involved in stress perception and transduction, signal amplification or cell stress response modulation. Conclusions Plant mitochondria are endowed with a diversity of multi-directional hubs of stress signalling that lead to regulatory loops and regulatory rheostats, whose functioning can amplify and diversify some signals or, conversely, dampen and reduce other signals. Involvement in a wide range of abiotic and biotic responses also implies that mitochondrial stress signalling could result in synergistic or conflicting outcomes during acclimation to multiple and complex stresses, such as those arising from climate change. [ABSTRACT FROM AUTHOR]

Summary: Correct chloroplast development and function require co‐ordinated expression of chloroplast and nuclear genes. This is achieved through chloroplast signals that modulate nuclear gene expression in accordance with the chloroplast's needs. Genetic evidence indicates that GUN1, a chloroplast‐localized pentatricopeptide repeat (PPR) protein with a C‐terminal Small MutS‐Related (SMR) domain, is involved in integrating multiple developmental and stress‐related signals in both young seedlings and adult leaves. Recently, GUN1 was found to interact physically with factors involved in chloroplast protein homeostasis, and with enzymes of tetrapyrrole biosynthesis in adult leaves that function in various retrograde signalling pathways. Here we show that following perturbation of chloroplast protein homeostasis: (i) by growth in lincomycin‐containing medium; or (ii) in mutants defective in either the FtsH protease complex (ftsh), plastid ribosome activity (prps21‐1 and prpl11‐1) or plastid protein import and folding (cphsc70‐1), GUN1 influences NEP‐dependent transcript accumulation during cotyledon greening and also intervenes in chloroplast protein import. Significance Statement: Correct chloroplast development and function require co‐ordinated regulation of chloroplast and nuclear gene expression. Here, we propose that GUN1, a main player of chloroplast‐to‐nucleus retrograde communication, influences NEP‐dependent transcript accumulation during cotyledon greening and also intervenes in chloroplast protein import. [ABSTRACT FROM AUTHOR]

The response of chloroplasts to adverse environmental cues, principally increases in light intensity, stimulates chloroplast-to-nucleus retrograde signalling, which leads to the induction of immediate protective responses and longer-term acclimation. Hydrogen peroxide (H2O2), generated during photosynthesis, is proposed to both initiate and transduce a retrograde signal in response to photoinhibitory light intensities. Signalling specificity achieved by chloroplast-sourced H2O2 for signal transduction may be dependent upon the oft-observed close association of a proportion of these organelles with the nucleus. In this review, we consider more precisely the nature of the close association between a chloroplast appressed to the nucleus and the requirement for H2O2 to cross both the double membranes of the chloroplast and nuclear envelopes. Of particular relevance is that the endoplasmic reticulum (ER) has close physical contact with chloroplasts and is contiguous with the nuclear envelope. Therefore, the perinuclear space, which transducing H2O2 molecules would have to cross, may have an oxidising environment the same as the ER lumen. Based on studies in animal cells, the ER lumen may be a significant source of H2O2 in plant cells arising from the oxidative folding of proteins. If this is the case, then there is potential for the ER lumen/perinuclear space to be an important location to modify chloroplast-to-nucleus H2O2 signal transduction and thereby introduce modulation of it by additional different environmental cues. These would include for example, heat stress and pathogen infection, which induce the unfolded protein response characterised by an increased H2O2 level in the ER lumen.

As a light-harvesting organelle, the chloroplast inevitably produces a substantial amount of reactive oxygen species (ROS) primarily through the photosystems. These ROS, such as superoxide anion, hydrogen peroxide, hydroxyl radical, and singlet oxygen, are potent oxidizing agents, thereby damaging the photosynthetic apparatus. On the other hand, it became increasingly clear that ROS act as beneficial tools under photo-oxidative stress conditions by stimulating chloroplast-nucleus communication, a process called retrograde signaling (RS). These ROS-mediated RS cascades appear to participate in a broad spectrum of plant physiology, such as acclimation, resistance, programmed cell death (PCD), and growth. Recent reports imply that ROS-driven oxidation of RS-associated components is essential in sensing and responding to an increase in ROS contents. ROS appear to activate RS pathways via reversible or irreversible oxidation of sensor molecules. This review provides an overview of the emerging perspective on the topic of “oxidative modification-associated retrograde signaling.”

As a light-harvesting organelle, the chloroplast inevitably produces a substantial amount of reactive oxygen species (ROS) primarily through the photosystems. These ROS, such as superoxide anion, hydrogen peroxide, hydroxyl radical, and singlet oxygen, are potent oxidizing agents, thereby damaging the photosynthetic apparatus. On the other hand, it became increasingly clear that ROS act as beneficial tools under photo-oxidative stress conditions by stimulating chloroplast-nucleus communication, a process called retrograde signaling (RS). These ROS-mediated RS cascades appear to participate in a broad spectrum of plant physiology, such as acclimation, resistance, programmed cell death (PCD), and growth. Recent reports imply that ROS-driven oxidation of RS-associated components is essential in sensing and responding to an increase in ROS contents. ROS appear to activate RS pathways via reversible or irreversible oxidation of sensor molecules. This review provides an overview of the emerging perspective on the topic of "oxidative modification-associated retrograde signaling." [ABSTRACT FROM AUTHOR]

With the increasing impact of climate instability on agricultural and ecological systems has come a heightened sense of urgency to understand plant adaptation mechanisms in more detail. Plant species have a remarkable ability to disperse their progeny to a wide range of environments, demonstrating extraordinary resiliency mechanisms that incorporate epigenetics and transgenerational stability. Surprisingly, some of the underlying versatility of plants to adapt to abiotic and biotic stress emerges from the neofunctionalization of organelles and organellar proteins. We describe evidence of possible plastid specialization and multi-functional organellar protein features that serve to enhance plant phenotypic plasticity. These features appear to rely on, for example, spatio-temporal regulation of plastid composition, and unusual interorganellar protein targeting and retrograde signalling features that facilitate multi-functionalization. Although we report in detail on three such specializations, involving MSH1, WHIRLY1 and CUE1 proteins in Arabidopsis, there is ample reason to believe that these represent only a fraction of what is yet to be discovered as we begin to elaborate cross-species diversity. Recent observations suggest that plant proteins previously defined in one context may soon be rediscovered in new roles and that much more detailed investigation of proteins that show subcellular multi-targeting may be warranted. This article is part of the theme issue 'Linking the mitochondrial genotype to phenotype: a complex endeavour'. [ABSTRACT FROM AUTHOR]

Summary: Hypoxia regularly occurs during plant development and can be induced by the environment through, for example, flooding.To understand how plant tissue physiology responds to progressing oxygen restriction, we aimed to monitor subcellular physiology in real time and in vivo. We establish a fluorescent protein sensor‐based system for multiparametric monitoring of dynamic changes in subcellular physiology of living Arabidopsis thaliana leaves and exemplify its applicability for hypoxia stress.By monitoring cytosolic dynamics of magnesium adenosine 5'‐triphosphate, free calcium ion concentration, pH, NAD redox status, and glutathione redox status in parallel, linked to transcriptional and metabolic responses, we generate an integrated picture of the physiological response to progressing hypoxia. We show that the physiological changes are surprisingly robust, even when plant carbon status is modified, as achieved by sucrose feeding or extended night. Inhibition of the mitochondrial respiratory chain causes dynamics of cytosolic physiology that are remarkably similar to those under oxygen depletion, highlighting mitochondrial electron transport as a key determinant of the cellular consequences of hypoxia beyond the organelle.A broadly applicable system for parallel in vivo sensing of plant stress physiology is established to map out the physiological context under which both mitochondrial retrograde signalling and low oxygen signalling occur, indicating shared upstream stimuli. [ABSTRACT FROM AUTHOR]

The sulfur metabolism pathway in plants produces a variety of compounds that are central to the acclimation response to oxidative stresses such as drought and high light. Primary sulfur assimilation provides the amino acid cysteine, which is utilized in protein synthesis and as a precursor for the cellular redox buffer glutathione. In contrast, the secondary sulfur metabolism pathway produces sulfated compounds such as glucosinolates and sulfated peptides, as well as a corresponding by-product 3′-phosphoadenosine 5′-phosphate (PAP). Emerging evidence over the past decade has shown that secondary sulfur metabolism also has a crucial engagement during oxidative stress. This occurs across various cellular, tissue, and organismal levels including chloroplast-to-nucleus retrograde signalling events mediated by PAP, modulation of hormonal signalling by sulfated compounds and PAP, control of physiological responses such as stomatal closure, and potential regulation of plant growth. In this review, we examine the contribution of the different components of plant secondary metabolism to oxidative stress homeostasis, and how this pathway is metabolically regulated. We further outline the key outstanding questions in the field that are necessary to understand how and why this 'specialized' metabolic pathway plays significant roles in plant oxidative stress tolerance. [ABSTRACT FROM AUTHOR]

Summary: GUN1 integrates retrograde signals in chloroplasts but the underlying mechanism is elusive. FUG1, a chloroplast translation initiation factor, and GUN1 are co‐expressed at the transcriptional level, and FUG1 co‐immunoprecipitates with GUN1. We used mutants of GUN1 (gun1‐103) and FUG1 (fug1‐3) to analyse their functional relationship at the physiological and system‐wide level, the latter including transcriptome and proteome analyses. Absence of GUN1 aggravates the effects of decreased FUG1 levels on chloroplast protein translation, resulting in transiently more pronounced phenotypes regarding photosynthesis, leaf colouration, growth and cold acclimation. The gun1‐103 mutation also enhances variegation in the var2 mutant, increasing the fraction of white sectors, while fug1‐3 suppresses the var2 phenotype. The transcriptomes of fug1‐3 and gun1‐103 plants are very similar, but absence of GUN1 alone has almost no effect on protein levels, whereas steady‐state levels of chloroplast proteins are markedly decreased in fug1‐3. In fug1 gun1 double mutants, effects on transcriptomes and particularly on proteomes are enhanced. Our results show that GUN1 function becomes critical when chloroplast proteostasis is perturbed by decreased rates of synthesis (fug1) or degradation (var2) of chloroplast proteins, or by low temperatures. The functions of FUG1 and GUN1 appear to be related, corroborating the view that GUN1 helps to maintain chloroplast protein homeostasis (proteostasis). Significance Statement: GUN1 coordinates retrograde signalling in chloroplasts but the underlying mechanism is elusive. We shed light on the function of GUN1 in plastid proteostasis, revealing that its role is closely related to one of the chloroplast translation initiation factors FUG1 and finding that GUN1 is required for effective cold tolerance. [ABSTRACT FROM AUTHOR]

Feeding by insect herbivores such as caterpillars and aphids induces plant resistance mechanisms that are mediated by the phytohormones jasmonic acid (JA) and salicylic acid (SA). These phytohormonal pathways often crosstalk. Besides phytohormones, methyl‐D‐erythriol‐2,4‐cyclodiphosphate (MEcPP), the penultimate metabolite in the methyl‐D‐erythritol‐4‐phosphate pathway, has been speculated to regulate transcription of nuclear genes in response to biotic stressors such as aphids. Here, we show that MEcPP uniquely enhances the SA pathway without attenuating the JA pathway. Arabidopsis mutant plants that accumulate high levels of MEcPP (hds3) are highly resistant to the cabbage aphid (Brevicoryne brassicae), whereas resistance to the large cabbage white caterpillar (Pieris brassicae) remains unaltered. Thus, MEcPP is a distinct signalling molecule that acts beyond phytohormonal crosstalk to induce resistance against the cabbage aphid in Arabidopsis. We dissect the molecular mechanisms of MEcPP mediating plant resistance against the aphid B. brassicae. This shows that MEcPP induces the expression of genes encoding enzymes involved in the biosynthesis of several primary and secondary metabolic pathways contributing to enhanced resistance against this aphid species. A unique ability to regulate multifaceted molecular mechanisms makes MEcPP an attractive target for metabolic engineering in Brassica crop plants to increase resistance to cabbage aphids. The plastidial metabolite methyl‐D‐erythriol‐2,4‐cyclodiphosphate is a positive regulator of genes in SA signalling and biosynthetic genes in various metabolic pathways that confer resistance to aphids without compromising resistance to caterpillars. [ABSTRACT FROM AUTHOR]

Sucrose non-fermenting 1 (SNF1)-related protein kinase 1.1 (SnRK1.1; also known as KIN10 or SnRK1α) has been identified as the catalytic subunit of the complex SnRK1, the Arabidopsis thaliana homologue of a central integrator of energy and stress signalling in eukaryotes dubbed AMPK/Snf1/SnRK1. A nuclear localization of SnRK1.1 has been previously described and is in line with its function as an integrator of energy and stress signals. Here, using two biological models (Nicotiana benthamiana and Arabidopsis thaliana), native regulatory sequences, different microscopy techniques, and manipulations of cellular energy status, it was found that SnRK1.1 is localized dynamically between the nucleus and endoplasmic reticulum (ER). This distribution was confirmed at a spatial and temporal level by co-localization studies with two different fluorescent ER markers, one of them being the SnRK1.1 phosphorylation target HMGR. The ER and nuclear localization displayed a dynamic behaviour in response to perturbations of the plastidic electron transport chain. These results suggest that an ER-associated SnRK1.1 fraction might be sensing the cellular energy status, being a point of crosstalk with other ER stress regulatory pathways. [ABSTRACT FROM AUTHOR]

Reactive oxygen species (ROS) are key signalling intermediates in plant metabolism, defence, and stress adaptation. In plants, both the chloroplast and mitochondria are centres of metabolic control and ROS production, which coordinate stress responses in other cell compartments. The herbicide and experimental tool, methyl viologen (MV) induces ROS generation in the chloroplast under illumination, but is also toxic in non-photosynthetic organisms. We used MV to probe plant ROS signalling in compartments other than the chloroplast. Taking a genetic approach in the model plant Arabidopsis (Arabidopsis thaliana), we used natural variation, QTL mapping, and mutant studies with MV in the light, but also under dark conditions, when the chloroplast electron transport is inactive. These studies revealed a light-independent MV-induced ROS-signalling pathway, suggesting mitochondrial involvement. Mitochondrial Mn SUPEROXIDE DISMUTASE was required for ROS-tolerance and the effect of MV was enhanced by exogenous sugar, providing further evidence for the role of mitochondria. Mutant and hormone feeding assays revealed roles for stress hormones in organellar ROS-responses. The radical-induced cell death1 mutant, which is tolerant to MV-induced ROS and exhibits altered mitochondrial signalling, was used to probe interactions between organelles. Our studies suggest that mitochondria are involved in the response to ROS induced by MV in plants. Image 1 • The herbicide methyl viologen (MV) induces ROS production in plant chloroplasts. • MV inhibited Arabidopsis growth in the dark when chloroplasts were inactive. • Mitochondrial MnSOD was required for protection against MV. • Results with the MV-tolerant rcd1 mutant implicate interorganellar communication. • This suggests MV acts in plant mitochondria, as in non-photosynthetic organisms. [ABSTRACT FROM AUTHOR]

Abstract: Singlet oxygen (1O2) is a prime cause of photo‐damage of the photosynthetic apparatus. The chlorophyll molecules in the photosystem II reaction center and in the light‐harvesting antenna complex are major sources of 1O2 generation. It has been thought that the generation of 1O2 mainly takes place in the appressed regions of the thylakoid membranes, namely, the grana core, where most of the active photosystem II complexes are localized. Apart from being a toxic molecule, new evidence suggests that 1O2 significantly contributes to chloroplast‐to‐nucleus retrograde signalling that primes acclimation and cell death responses. Interestingly, recent studies reveal that chloroplasts operate two distinct 1O2‐triggered retrograde signalling pathways in which β‐carotene and a nuclear‐encoded chloroplast protein EXECUTER1 play essential roles as signalling mediators. The coexistence of these mediators raises several questions: their crosstalk, source(s) of 1O2, downstream signalling components, and the perception and reaction mechanism of these mediators towards 1O2. In this review, we mainly discuss the molecular genetic basis of the mode of action of these two putative 1O2 sensors and their corresponding retrograde signalling pathways. In addition, we also propose the possible existence of an alternative source of 1O2, which is spatially and functionally separated from the grana core. [ABSTRACT FROM AUTHOR]

Abstract In the last decade plant mitochondria have emerged as a target, sensor and initiator of signalling cascades to a variety of stress and adverse growth conditions. A combination of various ‘omic profiling approaches combined with forward and reverse genetic studies have defined how mitochondria respond to stress and the signalling pathways and regulators of these responses. Reactive oxygen species (ROS)-dependent and -independent pathways, specific metabolites, complex I dysfunction, and the mitochondrial unfolded protein response (UPR) pathway have been proposed to date. These pathways are regulated by kinases (sucrose non-fermenting response like kinase; cyclin dependent protein kinase E 1) and transcription factors from the abscisic acid-related, WRKY and NAC families. A number of independent studies have revealed that these mitochondrial signalling pathways interact with a variety of phytohormone signalling pathways. While this represents significant progress in the last decade there are more pathways to be uncovered. Post-transcriptional/translational regulation is also a likely determinant of the mitochondrial stress response. Unbiased analyses of the expression of genes encoding mitochondrial proteins in a variety of stress conditions reveal a modular network exerting a high degree of anterograde control. As abiotic and biotic stresses have significant impact on the yield of important crops such as rice, wheat and barley we will give an outlook of how knowledge gained in Arabidopsis may help to increase crop production and how emerging technologies may contribute. Graphical abstract fx1 Highlights • Abiotic and biotic stresses are major constraints of crop production. • Energy generated in plant mitochondria is important for plant stress responses. • Plant mitochondria are targets, sources and initiators of signalling cascades. • Regulators of mitochondrial (dys)function have been identified in Arabidopsis. • Transcriptional and Post-transcriptional/translational regulation play a major role. [ABSTRACT FROM AUTHOR]