Plant Molecular Biology

, Volume 93, Issue 1–2, pp 109–120 | Cite as

Arabidopsis thaliana methionine sulfoxide reductase B8 influences stress-induced cell death and effector-triggered immunity

  • Shweta Roy
  • Ashis Kumar Nandi


Key message

Reactive oxygen species (ROS) oxidize methionine to methionine sulfoxide (MetSO) and thereby inactivate proteins. Methionine sulfoxide reductase (MSR) enzyme converts MetSO back to the reduced form and thereby detoxifies the effect of ROS. Our results show that Arabidopsis thaliana MSR enzyme coding gene MSRB8 is required for effector-triggered immunity and containment of stress-induced cell death in Arabidopsis.


Plants activate pattern-triggered immunity (PTI), a basal defense, upon recognition of evolutionary conserved molecular patterns present in the pathogens. Pathogens release effector molecules to suppress PTI. Recognition of certain effector molecules activates a strong defense, known as effector-triggered immunity (ETI). ETI induces high-level accumulation of reactive oxygen species (ROS) and hypersensitive response (HR), a rapid programmed death of infected cells. ROS oxidize methionine to methionine sulfoxide (MetSO), rendering several proteins nonfunctional. The methionine sulfoxide reductase (MSR) enzyme converts MetSO back to the reduced form and thereby detoxifies the effect of ROS. Though a few plant MSR genes are known to provide tolerance against oxidative stress, their role in plant–pathogen interaction is not known. We report here that activation of cell death by avirulent pathogen or UV treatment induces expression of MSRB7 and MSRB8 genes. The T-DNA insertion mutant of MSRB8 exaggerates HR-associated and UV-induced cell death and accumulates a higher level of ROS than wild-type plants. The negative regulatory role of MSRB8 in HR is further supported by amiRNA and overexpression lines. Mutants and overexpression lines of MSRB8 are susceptible and resistant respectively, compared to the wild-type plants, against avirulent strains of Pseudomonas syringae pv. tomato DC3000 (Pst) carrying AvrRpt2, AvrB, or AvrPphB genes. However, the MSRB8 gene does not influence resistance against virulent Pst or P. syringae pv. maculicola (Psm) pathogens. Our results altogether suggest that MSRB8 function is required for ETI and containment of stress-induced cell death in Arabidopsis.


Arabidopsis Hypersensitive response Incompatible interaction MSRB7 MSRB8 Pseudomonas syringae 



Artificial microRNA




Cauliflower mosaic virus 35S


Effector-triggered immunity


Hours post inoculation


Hypersensitive response






Methionine sulfoxide reductase


Pathogenesis related


Pseudomonas syringae pv. tomato


Pattern triggered immunity


Quantitative real-time PCR


RPM1 interacting protein 13



We thank Zeeshan Z. Banday for comments on the manuscript. We acknowledge Arabidopsis Biological Resource Center, Ohio State University, USA for the mutant seeds. This work is supported by financial assistance from DST projects (F. No.SERB/SR/SO/PS/150/2012). SR is a recipient of a Council for Scientific and Industrial Research (CSIR) fellowship.

Author contributions

SR performed the experiments, analyzed data, and wrote the manuscript. AKN conceptualized the project, designed the experiments, and wrote the manuscript.

Compliance with ethical standards

Conflict of interest

The authors have no conflict of interest to declare.

Supplementary material

11103_2016_550_MOESM1_ESM.pdf (242 kb)
Supplementary material 1 (PDF 242 KB)


  1. Al-Daoude A, de Torres Zabala M, Ko JH, Grant M (2005) RIN13 is a positive regulator of the plant disease resistance protein RPM1. Plant Cell 17:1016–1028CrossRefPubMedPubMedCentralGoogle Scholar
  2. Alvarez ME, Pennell RI, Meijer PJ, Ishikawa A, Dixon RA, Lamb C (1998) Reactive oxygen intermediates mediate a systemic signal network in the establishment of plant immunity. Cell 92:773–784CrossRefPubMedGoogle Scholar
  3. Baker CJ, Orlandi EW (1995) Active oxygen in plant pathogenesis. Annu Rev Phytopathol 33:299–321CrossRefPubMedGoogle Scholar
  4. Bari R, Jones JD (2009) Role of plant hormones in plant defence responses. Plant Mol Biol 69:473–488CrossRefPubMedGoogle Scholar
  5. Bechtold U, Murphy DJ, Mullineaux PM (2004) Arabidopsis peptide methionine sulfoxide reductase2 prevents cellular oxidative damage in long nights. Plant Cell 16:908–919CrossRefPubMedPubMedCentralGoogle Scholar
  6. Bechtold U, Rabbani N, Mullineaux PM, Thornalley PJ (2009) Quantitative measurement of specific biomarkers for protein oxidation, nitration and glycation in Arabidopsis leaves. Plant J 59:661–671CrossRefPubMedGoogle Scholar
  7. Chandra S, Martin GB, Low PS (1996) The Pto kinase mediates a signaling pathway leading to the oxidative burst in tomato. Proc Natl Acad Sci USA 93:13393–13397CrossRefPubMedPubMedCentralGoogle Scholar
  8. Chen S, Songkumarn P, Liu J, Wang GL (2009) A versatile zero background T-vector system for gene cloning and functional genomics. Plant Physiol 150:1111–1121CrossRefPubMedPubMedCentralGoogle Scholar
  9. Davies MJ (2005) The oxidative environment and protein damage. Biochim Biophys Acta 1703:93–109CrossRefPubMedGoogle Scholar
  10. Gao J, Yin D, Yao Y, Williams TD, Squier TC (1998) Progressive decline in the ability of calmodulin isolated from aged brain to activate the plasma membrane Ca-ATPase. BioChemistry 37:9536–9548CrossRefPubMedGoogle Scholar
  11. Giri MK, Swain S, Gautam JK, Singh S, Singh N, Bhattacharjee L, Nandi AK (2014) The Arabidopsis thaliana At4g13040 gene, a unique member of the AP2/EREBP family, is a positive regulator for salicylic acid accumulation and basal defense against bacterial pathogens. J Plant Physiol 171:860–867CrossRefPubMedGoogle Scholar
  12. Grant JJ, Loake GJ (2000) Role of reactive oxygen intermediates and cognate redox signaling in disease resistance. Plant Physiol 124:21–29CrossRefPubMedPubMedCentralGoogle Scholar
  13. Grant JJ, Yun BW, Loake GJ (2000) Oxidative burst and cognate redox signalling reported by luciferase imaging: identification of a signal network that functions independently of ethylene, SA and Me-JA but is dependent on MAPKK activity. Plant J 24:569–582CrossRefPubMedGoogle Scholar
  14. Guo X, Wu Y, Wang Y, Chen Y, Chu C (2009) OsMSRA4.1 and OsMSRB1.1, two rice plastidial methionine sulfoxide reductases, are involved in abiotic stress responses. Planta 230:227–238CrossRefPubMedGoogle Scholar
  15. Heath MC (2000) Hypersensitive response-related death. Plant Mol Biol 44:321–334CrossRefPubMedGoogle Scholar
  16. Hein I, Gilroy EM, Armstrong MR, Birch PR (2009) The zig-zag-zig in oomycete-plant interactions. Mol Plant Pathol 10:547–562CrossRefPubMedGoogle Scholar
  17. Jones JD, Dangl JL (2006) The plant immune system. Nature 444:323–329CrossRefPubMedGoogle Scholar
  18. Kumar RA, Koc A, Cerny RL, Gladyshev VN (2002) Reaction mechanism, evolutionary analysis, and role of zinc in Drosophila methionine-R-sulfoxide reductase. J Biol Chem 277:37527–37535CrossRefPubMedGoogle Scholar
  19. Lamb C, Dixon RA (1997) The oxidative burst in plant disease resistance. Ann Rev Plant Physiol Plant Mol Biol 48:251–275CrossRefGoogle Scholar
  20. Laugier E, Tarrago L, Vieira Dos Santos C, Eymery F, Havaux M, Rey P (2010) Arabidopsis thaliana plastidial methionine sulfoxide reductases B, MSRBs, account for most leaf peptide MSR activity and are essential for growth under environmental constraints through a role in the preservation of photosystem antennae. Plant J 61:271–282CrossRefPubMedGoogle Scholar
  21. Laugier E et al (2013) Involvement of thioredoxin y2 in the preservation of leaf methionine sulfoxide reductase capacity and growth under high light. Plant Cell Environ 36:670–682CrossRefPubMedGoogle Scholar
  22. Li CW, Lee SH, Chieh PS, Lin CS, Wang YC, Chan MT (2012) Arabidopsis root-abundant cytosolic methionine sulfoxide reductase B genes MsrB7 and MsrB8 are involved in tolerance to oxidative stress. Plant Cell Physiol 53:1707–1719CrossRefPubMedGoogle Scholar
  23. Moskovitz J (2005) Methionine sulfoxide reductases: ubiquitous enzymes involved in antioxidant defense, protein regulation, and prevention of aging-associated diseases. Biochim Biophys Acta 1703:213–219CrossRefPubMedGoogle Scholar
  24. Mur LA, Kenton P, Lloyd AJ, Ougham H, Prats E (2008) The hypersensitive response; the centenary is upon us but how much do we know? J Exp Bot 59:501–520CrossRefPubMedGoogle Scholar
  25. Mushegian AR, Koonin EV (1996) A minimal gene set for cellular life derived by comparison of complete bacterial genomes. Proc Natl Acad Sci USA 93:10268–10273CrossRefPubMedPubMedCentralGoogle Scholar
  26. Nandi A, Krothapalli K, Buseman CM, Li M, Welti R, Enyedi A, Shah J (2003) Arabidopsis sfd mutants affect plastidic lipid composition and suppress dwarfing, cell death, and the enhanced disease resistance phenotypes resulting from the deficiency of a fatty acid desaturase. Plant Cell 15:2383–2398CrossRefPubMedPubMedCentralGoogle Scholar
  27. Nandi A, Welti R, Shah J (2004) The Arabidopsis thaliana dihydroxyacetone phosphate reductase gene SUPPRESSOR OF FATTY ACID DESATURASE DEFICIENCY1 is required for glycerolipid metabolism and for the activation of systemic acquired resistance. Plant Cell 16:465–477CrossRefPubMedPubMedCentralGoogle Scholar
  28. Neiers F, Sonkaria S, Olry A, Boschi-Muller S, Branlant G (2007) Characterization of the amino acids from Neisseria meningitidis methionine sulfoxide reductase B involved in the chemical catalysis and substrate specificity of the reductase step. J Biol Chem 282:32397–32405CrossRefPubMedGoogle Scholar
  29. Neužil J, Gebicki JM, Stocker R (1993) Radical-induced chain oxidation of proteins and its inhibition by chain-breaking antioxidants. Biochem J 293:601–606CrossRefPubMedPubMedCentralGoogle Scholar
  30. Nimchuk Z, Eulgem T, Holt BF 3rd, Dangl JL (2003) Recognition and response in the plant immune system. Annu Rev Genet 37:579–609CrossRefPubMedGoogle Scholar
  31. Oh SK et al (2010) CaMsrB2, pepper methionine sulfoxide reductase B2, is a novel defense regulator against oxidative stress and pathogen attack. Plant Physiol 154:245–261CrossRefPubMedPubMedCentralGoogle Scholar
  32. Ozgur R, Uzilday B, Sekmen AH, Turkan I (2015) The effects of induced production of reactive oxygen species in organelles on endoplasmic reticulum stress and on the unfolded protein response in Arabidopsis. Ann Bot 116:541–553CrossRefPubMedPubMedCentralGoogle Scholar
  33. Romero HM, Berlett BS, Jensen PJ, Pell EJ, Tien M (2004) Investigations into the role of the plastidial peptide methionine sulfoxide reductase in response to oxidative stress in Arabidopsis. Plant Physiol 136:3784–3794CrossRefPubMedPubMedCentralGoogle Scholar
  34. Schwab R, Ossowski S, Riester M, Warthmann N, Weigel D (2006) Highly specific gene silencing by artificial microRNAs in Arabidopsis. Plant Cell 18:1121–1133CrossRefPubMedPubMedCentralGoogle Scholar
  35. Sharov VS, Ferrington DA, Squier TC, Schoneich C (1999) Diastereoselective reduction of protein-bound methionine sulfoxide by methionine sulfoxide reductase. FEBS Lett 455:247–250CrossRefPubMedGoogle Scholar
  36. Singh S, Giri MK, Singh PK, Siddiqui A, Nandi AK (2013a) Down-regulation of OsSAG12-1 results in enhanced senescence and pathogen-induced cell death in transgenic rice plants. J Biosci 38:583–592Google Scholar
  37. Singh V, Roy S, Giri MK, Chaturvedi R, Chowdhury Z, Shah J, Nandi AK (2013b) Arabidopsis thaliana FLOWERING LOCUS D is required for systemic acquired resistance. Mol Plant Microbe Interact 26:1079–1088Google Scholar
  38. Spoel SH, Dong X (2012) How do plants achieve immunity? Defence without specialized immune cells. Nat Rev Immunol 12:89–100CrossRefPubMedGoogle Scholar
  39. Stadtman ER, Moskovitz J, Levine RL (2003) Oxidation of methionine residues of proteins: biological consequences. Antioxid Redox Signal 5:577–582CrossRefPubMedGoogle Scholar
  40. Stakman EC (1915) Relation between Puccina graminis and plants highly resistant to its attack. J Agric Res 4:193–199Google Scholar
  41. Swain S, Roy S, Shah J, Van Wees S, Pieterse CM, Nandi AK (2011) Arabidopsis thaliana cdd1 mutant uncouples the constitutive activation of salicylic acid signalling from growth defects. Mol Plant Pathol 12:855–865CrossRefPubMedGoogle Scholar
  42. Torres MA, Dangl JL, Jones JD (2002) Arabidopsis gp91phox homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response. Proc Natl Acad Sci USA 99:517–522CrossRefPubMedGoogle Scholar
  43. Torres MA, Jones JD, Dangl JL (2006) Reactive oxygen species signaling in response to pathogens. Plant Physiol 141:373–378CrossRefPubMedPubMedCentralGoogle Scholar
  44. Van Poecke RM, Sato M, Lenarz-Wyatt L, Weisberg S, Katagiri F (2007) Natural variation in RPS2-mediated resistance among Arabidopsis accessions: correlation between gene expression profiles and phenotypic responses. Plant Cell 19:4046–4060CrossRefPubMedPubMedCentralGoogle Scholar
  45. Vieira Dos Santos C, Cuine S, Rouhier N, Rey P (2005) The Arabidopsis plastidic methionine sulfoxide reductase B proteins. Sequence and activity characteristics, comparison of the expression with plastidic methionine sulfoxide reductase A, and induction by photooxidative stress. Plant Physiol 138:909–922CrossRefPubMedGoogle Scholar
  46. Zhang J, Zhou JM (2010) Plant immunity triggered by microbial molecular signatures. Mol Plant 3:783–793CrossRefPubMedGoogle Scholar
  47. Zhang X, Henriques R, Lin SS, Niu QW, Chua NH (2006) Agrobacterium-mediated transformation of Arabidopsis thaliana using the floral dip method. Nat Protoc 1:641–646CrossRefPubMedGoogle Scholar
  48. Zhu J, Ding P, Li Q, Gao Y, Chen F, Xia G (2015) Molecular characterization and expression profile of methionine sulfoxide reductase gene family in maize (Zea mays) under abiotic stresses. Gene 562:159–168CrossRefPubMedGoogle Scholar
  49. Zipfel C (2008) Pattern-recognition receptors in plant innate immunity. Curr Opin Immunol 20:10–16CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  1. 1.415, School of Life ScienceJawaharlal Nehru UniversityNew DelhiIndia

Personalised recommendations