Cold priming on pathogen susceptibility in the Arabidopsis eds1 mutant background requires a functional stromal Ascorbate Peroxidase

References

• Hilker M, Schwachtje J, Baier M, Balazadeh S, Bäurle I, Geiselhardt S, Hincha DK, Kunze R, Mueller-Roeber B, Rillig MC, et al. Priming and memory of stress responses in organisms lacking a nervous system. Biol Rev. 2016;91(4):1118–4. doi:10.1111/brv.12215.
   PubMed Web of Science ®Google Scholar
• Conrath U. Molecular aspects of defence priming. Trends Plant Sci. 2011;16(10):524–531. doi:10.1016/j.tplants.2011.06.004.
   PubMed Web of Science ®Google Scholar
• Conrath U, Beckers GJM, Langenbach CJG, Jaskiewicz MR. Priming for Enhanced Defense. Annu Rev Phytopathol. 2015;53(1):97–119. doi:10.1146/annurev-phyto-080614-120132.
   PubMed Web of Science ®Google Scholar
• Hönig M, Roeber VM, Schmülling T, Cortleven A. Chemical priming of plant defense responses to pathogen attacks. Front Plant Sci. 2023;14:1146577. doi:10.3389/fpls.2023.1146577.
   PubMed Web of Science ®Google Scholar
• Singh P, Yekondi S, Chen P-W, Tsai C-H, Yu C-W, Wu K, Zimmerli L. Environmental history modulates Arabidopsis pattern-triggered immunity in a HISTONE ACETYLTRANSFERASE1–dependent manner. Plant Cell. 2014;26(6):2676–2688. doi:10.1105/tpc.114.123356.
   PubMed Web of Science ®Google Scholar
• Cortleven A, Roeber VM, Frank M, Bertels J, Lortzing V, Beemster GTS, Schmülling T. Photoperiod stress in Arabidopsis thaliana induces a transcriptional response resembling that of pathogen infection. Front Plant Sci. 2022;13:838284. doi:10.3389/fpls.2022.838284.
   PubMed Web of Science ®Google Scholar
• Lajeunesse G, Roussin-Léveillée C, Boutin S, Fortin É, Laforest-Lapointe I, Moffett P. Light prevents pathogen-induced aqueous microenvironments via potentiation of salicylic acid signaling. Nat Commun. 2023;14:713. doi:10.1038/s41467-023-36382-7.
   PubMedGoogle Scholar
• Griebel T, Zeier J. Light regulation and daytime dependency of inducible plant defenses in Arabidopsis: phytochrome signaling controls systemic acquired resistance rather than local defense. Plant Physiol. 2008;147(2):790–801. doi:10.1104/pp.108.119503.
   PubMed Web of Science ®Google Scholar
• Griebel T, Schütte D, Ebert A, Nguyen HH, Baier M. Cold exposure memory reduces pathogen susceptibility in Arabidopsis based on a functional plastid peroxidase system. Mol Plant-Microbe Interact. 2022;35(7):627–637. doi:10.1094/MPMI-11-21-0283-FI.
   PubMed Web of Science ®Google Scholar
• Hinsch M, Staskawicz B. Identification of a new Arabidopsis disease resistance locus, RPS4, and cloning of the corresponding avirulence gene, avrRps4, from Pseudomonas syringae pv. pisi. Mol Plant Microbe Interact. 1996;9(1):55–61. doi:10.1094/MPMI-9-0055.
   PubMed Web of Science ®Google Scholar
• Cui H, Tsuda K, Parker JE. Effector-Triggered Immunity: From Pathogen Perception to Robust Defense. Annu Rev Plant Biol. 2015;66(1):487–511. doi:10.1146/annurev-arplant-050213-040012.
   PubMed Web of Science ®Google Scholar
• Mackey D, Holt BF, Wiig A, Dangl JL. RIN4 interacts with Pseudomonas syringae type III effector molecules and is required for RPM1-mediated resistance in arabidopsis. Cell. 2002;108(6):743–754. doi:10.1016/S0092-8674(02)00661-X.
   PubMed Web of Science ®Google Scholar
• Bisgrove SR, Simonich MT, Smith NM, Sattler A, Innes RW. A disease resistance gene in Arabidopsis with specificity for two different pathogen avirulence genes. Plant Cell. 1994;6(7):927–933. doi:10.1105/tpc.6.7.927.
   PubMed Web of Science ®Google Scholar
• Aarts N, Metz M, Holub E, Staskawicz BJ, Daniels MJ, Parker JE. Different requirements for EDS1 and NDR1 by disease resistance genes define at least two R gene-mediated signaling pathways in Arabidopsis. Proc Natl Acad Sci U S A. 1998;95(17):10306–10311. doi:10.1073/pnas.95.17.10306.
   PubMed Web of Science ®Google Scholar
• Wiermer M, Feys BJ, Parker JE. Plant immunity: the EDS1 regulatory node. Curr Opin Plant Biol. 2005;8(4):383–389. doi:10.1016/j.pbi.2005.05.010.
   PubMed Web of Science ®Google Scholar
• Lapin D, Bhandari DD, Parker JE. Origins and Immunity Networking Functions of EDS1 Family Proteins. Annu Rev Phytopathol. 2020;58(1):253–276. doi:10.1146/annurev-phyto-010820-012840.
   PubMedGoogle Scholar
• Wagner S, Stuttmann J, Rietz S, Guerois R, Brunstein E, Bautor J, Niefind K, Parker JE. Structural basis for signaling by exclusive EDS1 heteromeric complexes with SAG101 or PAD4 in plant innate immunity. Cell Host & Microbe. 2013;14(6):619–630. doi:10.1016/j.chom.2013.11.006.
   PubMed Web of Science ®Google Scholar
• Falk A, Feys BJ, Frost LN, Jones JD, Daniels MJ, Parker JE. EDS1, an essential component of R gene-mediated disease resistance in Arabidopsis has homology to eukaryotic lipases. Proc Natl Acad Sci USA. 1999;96(6):3292–3297. doi:10.1073/pnas.96.6.3292.
   PubMed Web of Science ®Google Scholar
• Breitenbach HH, Wenig M, Wittek F, Jordá L, Maldonado-Alconada AM, Sarioglu H, Colby T, Knappe C, Bichlmeier M, Pabst E, et al. Contrasting roles of the apoplastic aspartyl protease APOPLASTIC, ENHANCED DISEASE SUSCEPTIBILITY1-DEPENDENT1 and LEGUME LECTIN-LIKE PROTEIN1 in Arabidopsis systemic acquired resistance. Plant Physiology. 2014;165(2):791–809. doi:10.1104/pp.114.239665.
   PubMed Web of Science ®Google Scholar
• Dongus JA, Parker JE. EDS1 signalling: at the nexus of intracellular and surface receptor immunity. Curr Opin Plant Biol. 2021;62:102039. doi:10.1016/j.pbi.2021.102039.
   PubMed Web of Science ®Google Scholar
• Zeier J. Metabolic regulation of systemic acquired resistance. Curr Opin Plant Biol. 2021;62:102050. doi:10.1016/j.pbi.2021.102050.
   PubMed Web of Science ®Google Scholar
• Chai J, Song W, Parker JE. New biochemical principles for NLR immunity in plants. MPMI. 2023;36(8):468–475. doi:10.1094/MPMI-05-23-0073-HH.
   PubMed Web of Science ®Google Scholar
• Huang S, Jia A, Song W, Hessler G, Meng Y, Sun Y, Xu L, Laessle H, Jirschitzka J, Ma S, et al. Identification and receptor mechanism of TIR-catalyzed small molecules in plant immunity. Sci. 2022;377(6605):eabq3297. doi:10.1126/science.abq3297.
   PubMed Web of Science ®Google Scholar
• Jia A, Huang S, Song W, Wang J, Meng Y, Sun Y, Xu L, Laessle H, Jirschitzka J, Hou J, et al. TIR-catalyzed ADP-ribosylation reactions produce signaling molecules for plant immunity. Sci. 2022;377(6605):eabq8180. doi:10.1126/science.abq8180.
   PubMed Web of Science ®Google Scholar
• Dongus JA, Bhandari DD, Penner E, Lapin D, Stolze SC, Harzen A, Patel M, Archer L, Dijkgraaf L, Shah J, et al. Cavity surface residues of PAD4 and SAG101 contribute to EDS1 dimer signaling specificity in plant immunity. Plant Journal. 2022;110(5):1415–1432. doi:10.1111/tpj.15747.
   PubMed Web of Science ®Google Scholar
• Cui H, Gobbato E, Kracher B, Qiu J, Bautor J, Parker JE. A core function of EDS1 with PAD4 is to protect the salicylic acid defense sector in Arabidopsis immunity. New Phytol. 2017;213(4):1802–1817. doi:10.1111/nph.14302.
   PubMed Web of Science ®Google Scholar
• Asada K. The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Annu Rev Plant Biol. 1999;50(1):601–639. doi:10.1146/annurev.arplant.50.1.601.
   Google Scholar
• Jardim-Messeder D, Zamocky M, Sachetto-Martins G, Margis-Pinheiro M. Chloroplastic ascorbate peroxidases targeted to stroma or thylakoid membrane: the chicken or egg dilemma. FEBS Lett. 2022;596(23):2989–3004. doi:10.1002/1873-3468.14438.
   PubMed Web of Science ®Google Scholar
• Jespersen HM, Kjærsgård IVH, Østergaard L, Welinder KG. From sequence analysis of three novel ascorbate peroxidases from Arabidopsis thaliana to structure, function and evolution of seven types of ascorbate peroxidase. Biochem J. 1997;326(2):305–310. doi:10.1042/bj3260305.
   PubMedGoogle Scholar
• Chew O, Whelan J, Millar AH. Molecular definition of the ascorbate-glutathione cycle in Arabidopsis mitochondria reveals dual targeting of antioxidant defenses in plants. J Biol Chem. 2003;278(47):46869–46877. doi:10.1074/jbc.M307525200.
   PubMed Web of Science ®Google Scholar
• Xu L, Carrie C, Law SR, Murcha MW, Whelan J. Acquisition, conservation, and loss of dual-targeted proteins in land plants. Plant Physiol. 2013;161(2):644–662. doi:10.1104/pp.112.210997.
   PubMed Web of Science ®Google Scholar
• Kieselbach T, Bystedt M, Hynds P, Robinson C, Schröder WP. A peroxidase homologue and novel plastocyanin located by proteomics to the Arabidopsis chloroplast thylakoid lumen. FEBS Lett. 2000;480(2–3):271–276. doi:10.1016/S0014-5793(00)01890-1.
   PubMed Web of Science ®Google Scholar
• Granlund I, Storm P, Schubert M, García-Cerdán JG, Funk C, Schröder WP. The TL29 protein is lumen located, associated with PSII and not an ascorbate peroxidase. Plant Cell Physiol. 2009;50(11):1898–1910. doi:10.1093/pcp/pcp134.
   PubMed Web of Science ®Google Scholar
• Maruta T, Tanouchi A, Tamoi M, Yabuta Y, Yoshimura K, Ishikawa T, Shigeoka S. Arabidopsis chloroplastic ascorbate peroxidase isoenzymes play a dual role in Photoprotection and Gene Regulation under photooxidative stress. Plant Cell Physiol. 2010;51(2):190–200. doi:10.1093/pcp/pcp177.
   PubMed Web of Science ®Google Scholar
• Kangasjarvi S, Lepisto A, Hannikainen K, Piippo M, Luomala E-M, Aro E-M, Rintamaki E. Diverse roles for chloroplast stromal and thylakoid-bound ascorbate peroxidases in plant stress responses. Biochem J. 2008;412(2):275–285. doi:10.1042/BJ20080030.
   PubMed Web of Science ®Google Scholar
• Maruta T, Sawa Y, Shigeoka S, Ishikawa T. Diversity and evolution of ascorbate peroxidase functions in chloroplasts: more than just a classical antioxidant enzyme? Plant Cell Physiol. 2016;57:1377–1386. doi:10.1093/pcp/pcv203.
   PubMed Web of Science ®Google Scholar
• van Buer J, Cvetkovic J, Baier M. Cold regulation of plastid ascorbate peroxidases serves as a priming hub controlling ROS signaling in Arabidopsis thaliana. BMC Plant Biol. 2016;16(1):163. doi:10.1186/s12870-016-0856-7.
   PubMedGoogle Scholar
• van Buer J, Prescher A, Baier M. Cold-priming of chloroplast ROS signalling is developmentally regulated and is locally controlled at the thylakoid membrane. Sci Rep. 2019;9(1):3022. doi:10.1038/s41598-019-39838-3.
   PubMedGoogle Scholar
• Seiml-Buchinger V, Reifschneider E, Bittner A, Baier M. Ascorbate peroxidase post-cold regulation of chloroplast NADPH dehydrogenase activity controls cold memory. Plant Physiol. 2022;190(3):1997–2016. doi:10.1093/plphys/kiac355.
   PubMed Web of Science ®Google Scholar
• Bartsch M, Gobbato E, Bednarek P, Debey S, Schultze JL, Bautor J, Parker JE. Salicylic acid–Independent ENHANCED DISEASE SUSCEPTIBILITY1 signaling in Arabidopsis immunity and cell death is regulated by the monooxygenase FMO1 and the Nudix Hydrolase NUDT7. Plant Cell. 2006;18(4):1038–1051. doi:10.1105/tpc.105.039982.
   PubMed Web of Science ®Google Scholar