A novel pathway linking plasma membrane and chloroplasts is co-opted by pathogens to suppress salicylic acid-dependent defences

Chloroplasts are crucial players in the activation of defensive hormonal responses during plant-pathogen interactions. Here, we show that a plant virus-encoded protein re-localizes from the plasma membrane to chloroplasts upon triggering plant defence, interfering with the chloroplast-dependent activation of anti-viral salicylic acid (SA) biosynthesis. Strikingly, we have found that plant pathogens from different kingdoms seem to have convergently evolved to target chloroplasts and impair SA-dependent defences following an association with membranes, which is based on the co-existence of two subcellular targeting signals, an N-myristoylation site and a chloroplast transit peptide. This pattern is also present in plant proteins, at least one of which conversely activates SA defences from the chloroplast. Taken together, our results suggest that a pathway linking plasma membrane to chloroplasts and activating defence exists in plants, and that such pathway has been co-opted by plant pathogens during host-pathogen co-evolution to promote virulence through suppression of SA responses.

[1]  A. Macho,et al.  Intra-strain Elicitation and Suppression of Plant Immunity by Ralstonia solanacearum Type-III Effectors in Nicotiana benthamiana , 2019, bioRxiv.

[2]  Xin Li,et al.  Salicylic acid: biosynthesis, perception, and contributions to plant immunity. , 2019, Current opinion in plant biology.

[3]  W. Weckwerth,et al.  The High Light Response in Arabidopsis Requires the Calcium Sensor Protein CAS, a Target of STN7- and STN8-Mediated Phosphorylation , 2019, Front. Plant Sci..

[4]  Rosa Lozano-Durán,et al.  Chloroplast clustering around the nucleus is a general response to pathogen perception in Nicotiana benthamiana , 2019, Molecular plant pathology.

[5]  V. Dogra,et al.  Oxidative post-translational modification of EXECUTER1 is required for singlet oxygen sensing in plastids , 2019, Nature Communications.

[6]  A. Xiong,et al.  Salicylic acid-induced differential resistance to the Tomato yellow leaf curl virus among resistant and susceptible tomato cultivars , 2019, BMC Plant Biology.

[7]  S. Chakraborty,et al.  A geminivirus betasatellite encoded βC1 protein interacts with PsbP and subverts PsbP‐mediated antiviral defence in plants , 2019, Molecular plant pathology.

[8]  Rosa Lozano-Durán,et al.  The receptor-like kinases BAM1 and BAM2 promote the cell-to-cell movement of miRNA in the root stele to regulate xylem patterning , 2019, bioRxiv.

[9]  Daowen Wang,et al.  Pandemonium Breaks Out: Disruption of Salicylic Acid-Mediated Defense by Plant Pathogens. , 2018, Molecular plant.

[10]  Xueping Zhou,et al.  Functional Scanning of Apple Geminivirus Proteins as Symptom Determinants and Suppressors of Posttranscriptional Gene Silencing , 2018, Viruses.

[11]  W. Sakamoto,et al.  The Photosystem II Repair Cycle Requires FtsH Turnover through the EngA GTPase1[OPEN] , 2018, Plant Physiology.

[12]  I. Dry,et al.  In Planta Functional Analysis and Subcellular Localization of the Oomycete Pathogen Plasmopara viticola Candidate RXLR Effector Repertoire , 2018, Front. Plant Sci..

[13]  L. Miozzi,et al.  The interaction of Lolium latent virus major coat protein with ankyrin repeat protein NbANKr redirects it to chloroplasts and modulates virus infection. , 2018, The Journal of general virology.

[14]  S. Chakraborty,et al.  Chloroplast: the Trojan horse in plant-virus interaction. , 2018, Molecular plant pathology.

[15]  Weiman Xing,et al.  A virus-targeted plant receptor-like kinase promotes cell-to-cell spread of RNAi , 2018, Proceedings of the National Academy of Sciences.

[16]  Yaru Wang,et al.  The Ralstonia solanacearum type III effector RipAY targets plant redox regulators to suppress immune responses. , 2018, Molecular plant pathology.

[17]  Renyi Liu,et al.  Inference of a Geminivirus−Host Protein−Protein Interaction Network through Affinity Purification and Mass Spectrometry Analysis , 2017, Viruses.

[18]  Yongliang Zhang,et al.  Three-Dimensional Analysis of Chloroplast Structures Associated with Virus Infection1 , 2017, Plant Physiology.

[19]  K. Dehesh,et al.  Retrograde Signals: Integrators of Interorganellar Communication and Orchestrators of Plant Development. , 2017, Annual review of plant biology.

[20]  Dong Yeol Lee,et al.  Bacillus aryabhattai SRB02 tolerates oxidative and nitrosative stress and promotes the growth of soybean by modulating the production of phytohormones , 2017, PloS one.

[21]  Jian‐Kang Zhu.  Abiotic Stress Signaling and Responses in Plants , 2016, Cell.

[22]  Jinping Zhao,et al.  Chloroplast in Plant-Virus Interaction , 2016, Front. Microbiol..

[23]  K. Apel,et al.  Singlet oxygen- and EXECUTER1-mediated signaling is initiated in grana margins and depends on the protease FtsH2 , 2016, Proceedings of the National Academy of Sciences.

[24]  C. Audran,et al.  Chloroplasts at work during plant innate immunity. , 2016, Journal of experimental botany.

[25]  Peter A. Crisp,et al.  Learning the Languages of the Chloroplast: Retrograde Signaling and Beyond. , 2016, Annual review of plant biology.

[26]  S. Chakraborty,et al.  A geminivirus betasatellite damages the structural and functional integrity of chloroplasts leading to symptom formation and inhibition of photosynthesis , 2015, Journal of experimental botany.

[27]  George R. Littlejohn,et al.  Chloroplasts play a central role in plant defence and are targeted by pathogen effectors , 2015, Nature Plants.

[28]  S. Duplessis,et al.  Rust fungal effectors mimic host transit peptides to translocate into chloroplasts , 2015, bioRxiv.

[29]  Hengmu Zhang,et al.  P5-2 of rice black-streaked dwarf virus is a non-structural protein targeted to chloroplasts , 2015, Archives of Virology.

[30]  Springer-Verlag Wien.  P5-2 of rice black-streaked dwarf virus is a non-structural protein targeted to chloroplasts , 2015 .

[31]  Christian G Elowsky,et al.  Distinct Pseudomonas type-III effectors use a cleavable transit peptide to target chloroplasts. , 2014, The Plant journal : for cell and molecular biology.

[32]  K. Dehesh,et al.  Review of stress specific organelles-to-nucleus metabolic signal molecules in plants. , 2013, Plant science : an international journal of experimental plant biology.

[33]  S. Sano,et al.  Chloroplast-mediated activation of plant immune signalling in Arabidopsis , 2012, Nature Communications.

[34]  J. C. del Pozo,et al.  A bacterial cysteine protease effector protein interferes with photosynthesis to suppress plant innate immune responses , 2012, Cellular microbiology.

[35]  S. Bischof,et al.  FLU, a negative feedback regulator of tetrapyrrole biosynthesis, is physically linked to the final steps of the Mg++‐branch of this pathway , 2012, FEBS letters.

[36]  C. Zipfel,et al.  Hierarchy and Roles of Pathogen-Associated Molecular Pattern-Induced Responses in Nicotiana benthamiana1[W] , 2011, Plant Physiology.

[37]  Roman G. Bayer,et al.  Protein N‐acylation overrides differing targeting signals , 2011, FEBS letters.

[38]  J. Jeleńska,et al.  Pseudomonas syringae hijacks plant stress chaperone machinery for virulence , 2010, Proceedings of the National Academy of Sciences.

[39]  C. Wege,et al.  A plastid-targeted heat shock cognate 70kDa protein interacts with the Abutilon mosaic virus movement protein. , 2010, Virology.

[40]  Yiyue Zhang,et al.  Technical summary , 2007 .

[41]  Masaki Iwabuchi,et al.  Genome-wide identification of a large repertoire of Ralstonia solanacearum type III effector proteins by a new functional screen. , 2010, Molecular plant-microbe interactions : MPMI.

[42]  A. A. Borges,et al.  Selection of internal control genes for quantitative real-time RT-PCR studies during tomato development process , 2008, BMC Plant Biology.

[43]  H. Yoshioka,et al.  Induction of a Small Heat Shock Protein and Its Functional Roles in Nicotiana Plants in the Defense Response against Ralstonia solanacearum1[W] , 2007, Plant Physiology.

[44]  J. Brodsky,et al.  Supplemental Data S 1 A J Domain Virulence Effector of Pseudomonas syringae Remodels Host Chloroplasts and Suppresses Defenses , 2022 .

[45]  Cheng Lu,et al.  The consensus N-myristoylation motif of a geminivirus AC4 protein is required for membrane binding and pathogenicity. , 2007, Molecular plant-microbe interactions : MPMI.

[46]  B. Boisson,et al.  Unexpected Protein Families Including Cell Defense Components Feature in the N-Myristoylome of a Higher Eukaryote* , 2003, Journal of Biological Chemistry.

[47]  S. Ding,et al.  The suppressor of transgene RNA silencing encoded by Cucumber mosaic virus interferes with salicylic acid-mediated virus resistance. , 2001, Molecular plant-microbe interactions : MPMI.

[48]  T. Boller,et al.  FLS2: an LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis. , 2000, Molecular cell.

[49]  D. Klessig,et al.  Resistance to Turnip Crinkle Virus in Arabidopsis Is Regulated by Two Host Genes and Is Salicylic Acid Dependent but NPR1, Ethylene, and Jasmonate Independent , 2000, Plant Cell.

[50]  T. Boller,et al.  Plants have a sensitive perception system for the most conserved domain of bacterial flagellin. , 1999, The Plant journal : for cell and molecular biology.

[51]  A. Nairn,et al.  Regulation by phosphorylation of reversible association of a myristoylated protein kinase C substrate with the plasma membrane , 1991, Nature.

[52]  D F Klessig,et al.  Salicylic Acid: A Likely Endogenous Signal in the Resistance Response of Tobacco to Viral Infection , 1990, Science.