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retrograde signaling in plants: A critical review focusing on the GUN pathway and beyond

Plant Communications 2023年第1期4卷 304-323页

作者： Andreas S.Richter Thomas Nägele Bernhard Grimm Kerstin Kaufmann Michael Schroda Dario Leister Tatjana Kleine Physiology of Plant Metabolism Institute for BiosciencesUniversity of RostockAlbert-Einstein-Str.318059 RostockGermany Plant Evolutionary Cell Biology Faculty of BiologyLudwig-Maximilians-Universität München82152 Planegg-MartinsriedGermany Institute of Biology/Plant Physiology Humboldt-Universität zu BerlinPhilippstr.1310115 BerlinGermany Plant Cell and Molecular Biology Institute of BiologyHumboldt-Universität zu BerlinPhilippstr.1310115 BerlinGermany Molecular Biotechnology and Systems Biology TU KaiserslauternKaiserslauternGermany Plant Molecular Biology(Botany) Faculty of BiologyLudwig-Maximilians-Universität München82152 Planegg-MartinsriedGermany

Plastids communicate their developmental and physiological status to the nucleus via retrograde signaling,allowing nuclear gene expression to be adjusted appropriately.signaling during plastid biogenesis and responses of mature chloroplasts to environmental changes are designated“biogenic”and“operational”controls,respectively.A prominent example of the investigation of biogenic signaling is the screen for gun(genomes uncoupled)mutants.Although the first five gun mutants were identified 30 years ago,the functions of GUN proteins in retrograde signaling remain controversial,and that of GUN1 is hotly disputed.Here,we provide background information and critically discuss recently proposed concepts that address GUN-related signaling and some novel gun mutants.Moreover,considering heme as a candidate in retrograde signaling,we revisit the spatial organization of heme biosynthesis and export from plastids.Although this review focuses on GUN pathways,we also highlight recent progress in the identification and elucidation of chloroplast-derived signals that regulate the acclimation response in green algae and plants.Here,stress-induced accumulation of unfolded/misassembled chloroplast proteins evokes a chloroplast-specific unfolded protein response,which leads to changes in the expression levels of nucleus-encoded chaperones and proteases to restore plastid protein homeostasis.We also address the importance of chloroplast-derived signals for activation of flavonoid biosynthesis leading to production of anthocyanins during stress acclimation through sucrose non-fermenting 1-related protein kinase 1.Finally,a framework for identification and quantification of intercompartmental signaling cascades at the proteomic and metabolomic levels is provided,and we discuss future directions of dissection of organelle-nucleus communication.

关键词： chloroplast chloroplast unfolded protein response genomes uncoupled gun retrograde signaling subcellular proteomes subcellular metabolomes

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retrograde signaling and Photoprotection in a gun4 Mutant of Chlamydomonas reinhardtii

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Molecular Plant 2012年第6期5卷 1242-1262页

作者： Cinzia Formighieri Mauro Ceol Giulia Bonente Jean-David Rochaix Roberto Bassi Dipartimento di Biotecnologie Universita di Verona Strada Le Grazie 15 1-37134 Verona Italy Departments of Molecular Biology and Plant Biology University of Geneva Sciences Ⅲ 30 Quai Ernest-Ansermet CH-1211 Geneva 4 Switzerland

GUN4 is a regulatory subunit of Mg-chelatase involved in the control of tetrapyrrole synthesis in plants and cyanobacteria. Here, we report the first characterization of a gun4 insertion mutant of the unicellular green alga Chlamydomonas reinhardtii. The mutant contains 50% of chlorophyll as compared to wild-type and accumulates ProtolX. In contrast to the increase in LHCtranscription, the accumulation of most LHC proteins is drastically diminished, implying posttranscriptional down-regulation in the absence of transcriptional coordination. We found that 803 genes change their expression level in gun4 as compared to wild-type, by RNA-Seq, and this wide-ranging effect on transcription is apparent under physiological conditions. Besides LHCs, we identified transcripts encoding enzymes of the tetrapyrrole pathway and factors involved in signal transduction, transcription, and chromatin remodeling. Moreover, we observe perturbations in electron transport with a strongly decreased PSI-to-PSII ratio. This is accompanied by an enhanced activ- ity of the plastid terminal oxidase （PTOX） that could have a physiological role in decreasing photosystem II excitation pressure.

关键词： green algae Chlamydomonas genome uncoupled （gun） mutants gun4 retrograde signaling PTOX.

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Role of Reactive Oxygen Species in the Initiation of Plant retrograde signaling

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Phyton-International Journal of Experimental Botany 2022年第5期91卷 905-913页

作者： Eduardo-Antonio Trillo-Hernández Arturo Duarte Sierra Martín Ernesto Tiznado-Hernández Centro de Investigación en Alimentación y Desarrollo A.C.Tecnología de Alimentos de Origen VegetalLaboratorio de Fisiología y Biología Molecular de PlantasHermosillo83304México Department of Food Science and Plant Research and Innovation Center Laval UniversityQuebecQCG1V 0A6Canada

The interaction between the nucleus and the different organelles is important in the physiology of the plant.Reac-tive oxygen species(ROS)are a by-product of the oxidation of organic molecules to obtain energy by the need to carry out the electron transfer between the different enzymatic complexes.However,they also have a role in the generation of what is known as retrograde signaling.This signal comes from the different organelles in which the oxidation of molecules or the electron transference is taking place such as mitochondria and chloroplasts.Furthermore,ROS can also induce the release of signals from the apoplast.It seems that these signals plays a role communicating to the nucleus the current status of the different parts of the plant cell to induce a changes in gene expression.In this review,the molecular mechanism of ROS retrograde signaling is described.

关键词： Reactive oxygen species retrograde signaling mitochondria chloroplast

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nitiation of ER Body Formation and Indole Glucosinolate Metabolism by the Plastidia retrograde signaling Metabolite, MEcPP

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Molecular Plant 2017年第11期10卷 1400-1416页

作者： Jin-Zheng Wang Baohua Li Yanmei Xiao Yu Ni Haiyan Ke Panyu Yang Amancio de Souza Marta Bjornson Xiang He Zhouxin Shen Gerd Ulrich Balcke Steve P. Briggs Alain Tissier Daniel J. Kliebenstein Katayoon Dehesh Institute for Integrative Genome Biology and Department of Botany and Plant Sciences University of California Riverside CA 92521 USA Department of Plant Biology University of California Davis CA 95616 USA Department of Plant Sciences University of California Davis CA 95616 USA Division of Biological Sciences University of California San Diego La Jolla CA 92093 USA Department of Cell and Metabolic Biology Leibniz-lnstitute of Plant Biochemistry Halle Germany Present address: College of Agronomy and Biotechnology Southwest University Chongqing P.R. China Present address: Rice Research Institute Sichuan Agricultural University Changdu Sichuan 611130 China

Plants have evolved tightly regulated signaling networks to respond and adapt to environmental perturbations, but the nature of the signaling hub（s） involved have remained an enigma. We have previously established that methylerythritol cyclodiphosphate （MEcPP）, a precursor of plastidial isoprenoids and a stress- specific retrograde signaling metabolite, enables cellular readjustments for high-order adaptive functions. Here, we specifically show that MEcPP promotes two Brassicaceae-specific traits, namely endoplasmic reticulum （ER） body formation and induction of indole glucosinolate （IGs） metabolism selectively, via tran- scriptional regulation of key regulators NAIl for ER body formation and MYB51/122 for IGs biosynthesis）. The specificity of MEcPP is further confirmed by the lack of induction of wound-inducible ER body genes as well as IGs by other altered methylerythritol phosphate pathway enzymes. Genetic analyses revealed MEcPP-mediated COil-dependent induction of these traits. Moreover, MEcPP signaling integrates the biosynthesis and hydrolysis of IGs through induction of nitrile-specifier protein1 and reduction of the sup- pressor, ESM1, and production of simple nitriles as the bioactive end product. The findings position the plastidial metabolite, MEcPP, as the initiation hub, transducing signals to adjust the activity of hard- wired gene circuitry to expand phytochemical diversity and alter the associated subcellular structure required for functionality of the secondary metabolites, thereby tailoring plant stress responses.

关键词： glucosinolates ER body retrograde signaling MEP pathway MEcPP stress

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Meta-Analysis of retrograde signaling in Arabidopsis thaliana Reveals a Core Module of Genes Embedded in Complex Cellular signaling Networks

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Molecular Plant 2014年第7期7卷 1167-1190页

作者： Christine GlaiBer Georg Haberer Iris Finkemeier Thomas Pfannschmidt Tatjana Kleine Dario Leister KarI-Josef Dietz Rainer Erich Haiusler Bernhard Grimm Klaus Franz Xaver Mayer Helmholtz Zentrum Munchen German Research Center for Environmental Health Institute of Bioinformatics and Systems Biology(IBIS) Ingolstadter Landstr. 1 D-85764 Neuherberg Germany Biozentrum der LMU Munchen Department of Biologie I-Botanik Groβhaderner Str. 2-4 D-82152 Planegg-Martinsried Germany Friedrich-Schiller-Universitat Jena Institut fur AIIgemeine Botanik und Pflanzenphysiologie Dornburger Str. 159 D-07743 JenaGermany Laboratoire de Physiologie Cellulaire Vegetale (LPCV) CEA/CNRS/UJF iRTSV CEA Grenoble 17 rue des Martyrs 38054 Grenoble cedex 9France Biochemistry and Physiology of Plants Faculty of Biology Bielefeld University Universit~tsstrai3e 25 D-33615 Bielefeld Germany University of Cologne Botanical Institute Cologne Biocenter Zu1picher Str. 47B D-50674 Cologne Germany Humboldt-Universitat zu Berlin Institut fur Biologie AG Pflanzenphysiologie Philippstrasse 13 D-10115 Berlin Germany

Plastid-to-nucleus signaling is essential for the coordination and adjustment of cellular metabolism in response to environmental and developmental cues of plant cells. A variety of operational retrograde signaling path- ways have been described that are thought to be triggered by reactive oxygen species, photosynthesis redox imbalance, tetrapyrrole intermediates, and other metabolic traits. Here we report a meta-analysis based on transcriptome and pro- tein interaction data. Comparing the output of these pathways reveals the commonalities and peculiarities stimulated by six different sources impinging on operational retrograde signaling. Our study provides novel insights into the interplay of these pathways, supporting the existence of an as-yet unknown core response module of genes being regulated under all conditions tested. Our analysis further highlights affiliated regulatory cis-elements and classifies abscisic acid and auxin-based signaling as secondary components involved in the response cascades following a plastidial signal. Our study provides a global analysis of structure and interfaces of different pathways involved in plastid-to-nucleus signaling and a new view on this complex cellular communication network.

关键词： retrograde signaling meta-analysis abscisic acid auxin.

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Identification of Target Genes and Transcription Factors Implicated in Translation-Dependent retrograde Sig- naling in Arabidopsis

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Molecular Plant 2014年第7期7卷 1228-1247页

作者： Dario Leister Isidora Romani Lukas Mittermayr Francesca Paieri Elena Fenino Tatjana Kleine Plant Molecular Biology (Botany) Department Biology I Ludwig-Maximilians-University Munich Gro0haderner Str. 2 D-82152Martinsried Germany

Changes in organellar gene expression （OGE） trigger retrograde signaling. The molecular dissection of OGE-dependent retrograde signaling based on analyses of mutants with altered OGE is complicated by compensatory responses that mask the primary signaling defect and by secondary effects that influence other retrograde signaling pathways. Therefore, to identify the earliest effects of altered OGE on nuclear transcript accumulation, we have induced OGE defects in adult plants by ethanol-dependent repression of PRORS1, which encodes a prolyl-tRNA synthetase located in chloroplasts and mitochondria. After 32 h of PRORS1 repression, the translational capacity of chloroplasts was reduced, and this effect subsequently intensified, while basic photosynthetic parameters were still unchanged at 51 h. Analysis of changes in whole-genome transcriptomes during exposure to ethanol revealed that induced PRORS1 silencing affects the expression of 1020 genes in all. Some of these encode photosynthesis-related proteins, including several down-regulated light-harvesting chlorophyll a/b binding （LHC） proteins. Interestingly, genes for presumptive endoplasmic reticulum pro- teins are transiently up-regulated. Furthermore, several NAC-domain-containing proteins are among the transcription factors regulated. Candidate cis-acting elements which may coordinate the transcriptional co-regulation of genes sets include both G-box variants and sequence motifs with no similarity to known plant c/s-elements.

关键词： Arabidopsis chloroplast mitochondrion retrograde signaling target genes transcription factors cis-elements.

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1O2-Mediated and EXECUTER-Dependent retrograde Plastid-to-Nucleus signaling in Norflurazon-Treated Seedlings of Arabidopsis thaliana

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Molecular Plant 2013年第5期6卷 1580-1591页

作者： Chanhong Kim Klaus Apel Boyce Thompson Institute for Plant Research Ithaca NY 14853-1801 USA

Chloroplast development depends on the synthesis and import of a large number of nuclear-encoded pro- teins. The synthesis of some of these proteins is affected by the functional state of the plastid via a process known as retrograde signaling. retrograde plastid-to-nucleus signaling has been often characterized in seedlings of Arabidopsis thaliana exposed to norflurazon （NF）, an inhibitor of carotenoid biosynthesis. Results of this work suggested that, throughout seedling development, a factor is released from the plastid to the cytoplasm that indicates a perturbation of plastid homeostasis and represses nuclear genes required for normal chloroplast development. The identity of this factor is still under debate. Reactive oxygen species （ROS） were among the candidates discussed as possible retrograde signals in NF-treated plants. In the present work, this proposed role of ROS has been analyzed. In seedlings grown from the very beginning in the presence of NF, ROS-dependent signaling was not detectable, whereas, in seedlings first exposed to NF after light-dependent chloroplast formation had been completed, enhanced ROS production occurred and, among oth- ers, 1O2-mediated and EXECUTER-dependent retrograde signaling was induced. Hence, depending on the developmental stage at which plants are exposed to NF, different retrograde signaling pathways may be activated, some of which are also active in non-treated plants under light stress.

关键词： retrograde signaling singlet oxygen Executer norflurazon programmed cell death photo-oxidative stress.

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EXECUTER2 modulates the EXECUTER1 signalosome through its singlet oxygen-dependent oxidation

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Molecular Plant 2022年第3期15卷 438-453页

作者： Vivek Dogra Rahul Mohan Singh Mengping Li Mingyue Li Somesh Singh Chanhong Kim Shanghai Center for Plant Stress Biology CAS Center for Excellence in Molecular Plant SciencesChinese Academy of SciencesShanghai 200032China University of the Chinese Academy of Sciences Beijing 100049China Present address:Biotechnology Division CSIR-Institute of Himalayan Bioresource TechnologyPalampur 176061India

Oxidative post-translational modifications of specific chloroplast proteins contribute to the initiation of retrograde signaling.The Arabidopsis thaliana EXECUTER1(EX1)protein,a chloroplast-localized singlet oxygen(^(1)O_(2))sensor,undergoes tryptophan(Trp)643 oxidation by^(1)O_(2),a chloroplast-derived and light-dependent reactive oxygen species.The indole side chain of Trp is vulnerable to^(1)O_(2),leading to the generation of oxidized Trp variants and priming EX1 for degradation by a membrane-bound FtsH protease.The perception of^(1)O_(2)via Trp643 oxidation and subsequent EX1 proteolysis facilitate chloroplast-to-nucleus retrograde signaling.In this study,we discovered that the EX1-like protein EX2 also undergoes^(1)O_(2)-dependent Trp530 oxidation and FtsH-dependent turnover,which attenuates^(1)O_(2)signaling by decelerating EX1-Trp643 oxidation and subsequent EX1 degradation.Consistent with this finding,the loss of EX2 function reinforces EX1-dependent retrograde signaling by accelerating EX1-Trp643 oxidation and subsequent EX1 proteolysis,whereas overexpression of EX2 produces molecular phenotypes opposite to those observed in the loss-of-function mutants of EX2.Intriguingly,phylogenetic analysis suggests that EX2 may have emerged evolutionarily to attenuate the sensitivity of EX1 toward^(1)O_(2).Collectively,these results suggest that EX2 functions as a negative regulator of the EX1 signalosome through its own^(1)O_(2)-dependent oxidation,providing a new mechanistic insight into the regulation of EX1-mediated^(1)O_(2)signaling.

关键词： EXECUTER1 EXECUTER2 singlet oxygen retrograde signaling Trp oxidation FtsH protease

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An update on the function and regulation of methylerythritol phosphate and mevalonate pathways and their evolutionary dynamics

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Journal of Integrative Plant Biology 2021年第7期63卷 1211-1226页

作者： Xiaojun Pu Xiumei Dong Qing Li Zexi Chen Li Liu State Key Laboratory of Biocatalysis and Enzyme Engineering Hubei Collaborative Innovation Center for Green Transformation of BioResourcesHubei Key Laboratory of Industrial BiotechnologySchool of Life SciencesHubei UniversityWuhan 434200China Key Laboratory for Economic Plants and Biotechnology Kunming Institute of Botanythe Chinese Academy of Sciencesand Yunnan Key Laboratory for Wild Plant ResourcesKunming 650201China School of Life Sciences Yunnan UniversityKunming 650091China University of the Chinese Academy of Sciences Beijing 100049China

Isoprenoids are among the largest and most chemically diverse classes of organic compounds in nature and are involved in the processes of photosynthesis, respiration, growth, development,and plant responses to stress. The basic building block units for isoprenoid synthesis-isopentenyl diphosphate and its isomer dimethylallyl diphosphate-are generated by the mevalonate (MVA) and methylerythritol phosphate(MEP) pathways. Here, we summarize recent advances on the roles of the MEP and MVA pathways in plant growth, development and stress responses, and attempt to define the underlying gene networks that orchestrate the MEP and MVA pathways in response to developmental or environmental cues.Through phylogenomic analysis, we also provide a new perspective on the evolution of the plant isoprenoid pathway. We conclude that the presence of the MVA pathway in plants may be associated with the transition from aquatic to subaerial and terrestrial environments, as lineages for its core components are absent in green algae. The emergence of the MVA pathway has acted as a key evolutionary event in plants that facilitated land colonization and subsequent embryo development, as well as adaptation to new and varied environments.

关键词： evolutionary innovation MEP pathway MVA pathway retrograde signaling stress

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The Translational Apparatus of Plastids and Its Role in Plant Development

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Molecular Plant 2014年第7期7卷 1105-1120页

作者： Nadine Tiller Ralph Bock Max-Planck-Institut for Molekulare Pflanzenphysiologie Am Muhlenberg 1 D-14476 Potsdam-Golm Germany

Chloroplasts （plastids） possess a genome and their own machinery to express it. Translation in plastids occurs on bacterial-type 70S ribosomes utilizing a set of tRNAs that is entirely encoded in the plastid genome. In recent years, the components of the chloroplast translational apparatus have been intensely studied by proteomic approaches and by reverse genetics in the model systems tobacco （plastid-encoded components） and Arabidopsis （nucleus-encoded components）. This work has provided important new insights into the structure, function, and biogenesis of chloroplast ribosomes, and also has shed fresh light on the molecular mechanisms of the translation process in plastids. In addition, mutants affected in plastid translation have yielded strong genetic evidence for chloroplast genes and gene products influencing plant develop- ment at various levels, presumably via retrograde signaling pathway（s）. In this review, we describe recent progress with the functional analysis of components of the chloroplast translational machinery and discuss the currently available evidence that supports a significant impact of plastid translational activity on plant anatomy and morphology.

关键词： plastid translation ribosome ribosomal protein evolution plastid transformation retrograde signaling leaf development palisade cell.

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