The arabidopsis transcription factor brassinosteroid insensitive1-ethyl methanesulfonate-suppressor1 is a direct substrate of mitogen-activated protein kinase6 and regulates immunity

Plant Physiology

Volumn 167, Issue 3, 2015, Pages 1076-1086

  Kang, Sining ^a   Yang, Fan ^a,b   Li, Lin ^c   Chen, Huamin ^d   Chen, She ^c   Zhang, Jie ^a  

^a INSTITUTE OF GENETICS AND DEVELOPMENTAL BIOLOGY   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c NATIONAL INSTITUTE OF BIOLOGICAL SCIENCES   (China)

^d INSTITUTE OF PLANT PROTECTION   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA; BACTERIA (MICROORGANISMS); LYCOPERSICON ESCULENTUM; PSEUDOMONAS SYRINGAE;

ARABIDOPSIS PROTEIN; BES1 PROTEIN, ARABIDOPSIS; BRASSINOSTEROID; FLAGELLIN; MITOGEN ACTIVATED PROTEIN KINASE; MPK6 PROTEIN, ARABIDOPSIS; NUCLEAR PROTEIN; PHOSPHOSERINE; PROTEIN BINDING;

ARABIDOPSIS; DISEASE RESISTANCE; DRUG EFFECTS; ENZYME ACTIVATION; ENZYME SPECIFICITY; ENZYMOLOGY; GROWTH, DEVELOPMENT AND AGING; HYPOCOTYL; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; PHOSPHORYLATION; PLANT DISEASE; PLANT IMMUNITY; PLANT ROOT; PSEUDOMONAS SYRINGAE;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; BRASSINOSTEROIDS; DISEASE RESISTANCE; ENZYME ACTIVATION; FLAGELLIN; HYPOCOTYL; MITOGEN-ACTIVATED PROTEIN KINASES; NUCLEAR PROTEINS; PHOSPHORYLATION; PHOSPHOSERINE; PLANT DISEASES; PLANT IMMUNITY; PLANT ROOTS; PROTEIN BINDING; PSEUDOMONAS SYRINGAE; SUBSTRATE SPECIFICITY;

EID: 84923667144     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.114.250985     Document Type: Article

References (61)

1. Albrecht C, Boutrot F, Segonzac C, Schwessinger B, Gimenez-Ibanez S, Chinchilla D, Rathjen JP, de Vries SC, Zipfel C (2012) Brassinosteroids inhibit pathogen-associated molecular pattern-triggered immune signaling independent of the receptor kinase BAK1. Proc Natl Acad Sci USA 109: 303-308.
2. Alvarez-Venegas R, Abdallat AA, Guo M, Alfano JR, Avramova Z (2007) Epigenetic control of a transcription factor at the cross section of two antagonistic pathways. Epigenetics 2: 106-113.
3. Andreasson E, Jenkins T, Brodersen P, Thorgrimsen S, Petersen NH, Zhu S, Qiu JL, Micheelsen P, Rocher A, Petersen M, et al (2005) The MAP kinase substrate MKS1 is a regulator of plant defense responses. EMBO J 24: 2579-2589.
4. Asai T, Tena G, Plotnikova J, Willmann MR, Chiu WL, Gomez-Gomez L, Boller T, Ausubel FM, Sheen J (2002) MAP kinase signalling cascade in Arabidopsis innate immunity. Nature 415: 977-983.
5. Belkhadir Y, Jaillais Y, Epple P, Balsemão-Pires E, Dangl JL, Chory J (2012) Brassinosteroids modulate the efficiency of plant immune responses to microbe-associated molecular patterns. Proc Natl Acad Sci USA 109: 297-302.
6. Berr A, McCallum EJ, Alioua A, Heintz D, Heitz T, Shen WH (2010) Arabidopsis histone methyltransferase SET DOMAIN GROUP8 mediates induction of the jasmonate/ethylene pathway genes in plant defense response to necrotrophic fungi. Plant Physiol 154: 1403-1414.
7. Bethke G, Unthan T, Uhrig JF, Pöschl Y, Gust AA, Scheel D, Lee J (2009) Flg22 regulates the release of an ethylene response factor substrate from MAP kinase 6 in Arabidopsis thaliana via ethylene signaling. Proc Natl Acad Sci USA 106: 8067-8072.
8. 2+ sensor protein kinases. Nature 464: 418-422.
9. Chen H, Xue L, Chintamanani S, Germain H, Lin H, Cui H, Cai R, Zuo J, Tang X, Li X, et al (2009) ETHYLENE INSENSITIVE3 and ETHYLENE INSENSITIVE3-LIKE1 repress SALICYLIC ACID INDUCTION DEFICIENT2 expression to negatively regulate plant innate immunity in Arabidopsis. Plant Cell 21: 2527-2540.
10. Chen H, Zou Y, Shang Y, Lin H, Wang Y, Cai R, Tang X, Zhou JM (2008) Firefly luciferase complementation imaging assay for protein-protein interactions in plants. Plant Physiol 146: 368-376.
11. Chinchilla D, Bauer Z, Regenass M, Boller T, Felix G (2006) The Arabidopsis receptor kinase FLS2 binds flg22 and determines the specificity of flagellin perception. Plant Cell 18: 465-476.
12. Chinchilla D, Zipfel C, Robatzek S, Kemmerling B, Nürnberger T, Jones JD, Felix G, Boller T (2007) A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence. Nature 448: 497-500.
13. Djamei A, Pitzschke A, Nakagami H, Rajh I, Hirt H (2007) Trojan horse strategy in Agrobacterium transformation: abusing MAPK defense signaling. Science 318: 453-456.
14. Fan M, Bai MY, Kim JG, Wang T, Oh E, Chen L, Park CH, Son SH, Kim SK, Mudgett MB, et al (2014) The bHLH transcription factor HBI1 mediates the trade-off between growth and pathogen-associated molecular pattern-triggered immunity in Arabidopsis. Plant Cell 26: 828-841.
15. Feng F, Yang F, RongW, Wu X, Zhang J, Chen S, He C, Zhou JM(2012) A Xanthomonas uridine 5′-monophosphate transferase inhibits plant immune kinases. Nature 485: 114-118.
16. Gómez-Gómez L, Boller T (2000) FLS2: an LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis. Mol Cell 5: 1003-1011.
17. Gómez-Gómez L, Felix G, Boller T (1999) A single locus determines sensitivity to bacterial flagellin in Arabidopsis thaliana. Plant J 18: 277-284.
18. Han L, Li GJ, Yang KY, Mao G, Wang R, Liu Y, Zhang S (2010) Mitogenactivated protein kinase 3 and 6 regulate Botrytis cinerea-induced ethylene production in Arabidopsis. Plant J 64: 114-127.
19. He JX, Gendron JM, Sun Y, Gampala SS, Gendron N, Sun CQ, Wang ZY (2005) BZR1 is a transcriptional repressor with dual roles in brassinosteroid homeostasis and growth responses. Science 307: 1634-1638.
20. Heese A, Hann DR, Gimenez-Ibanez S, Jones AM, He K, Li J, Schroeder JI, Peck SC, Rathjen JP (2007) The receptor-like kinase SERK3/BAK1 is a central regulator of innate immunity in plants. Proc Natl Acad Sci USA 104: 12217-12222.
21. Hoehenwarter W, Thomas M, Nukarinen E, Egelhofer V, Röhrig H, Weckwerth W, Conrath U, Beckers GJ (2013) Identification of novel in vivo MAP kinase substrates in Arabidopsis thaliana through use of tandem metal oxide affinity chromatography. Mol Cell Proteomics 12: 369-380.
22. Kadota Y, Sklenar J, Derbyshire P, Stransfeld L, Asai S, Ntoukakis V, Jones JD, Shirasu K, Menke F, Jones A, et al (2014) Direct regulation of the NADPH oxidase RBOHD by the PRR-associated kinase BIK1 during plant immunity. Mol Cell 54: 43-55.
23. Kyriakis JM, Avruch J (2001) Mammalian mitogen-activated protein kinase signal transduction pathways activated by stress and inflammation. Physiol Rev 81: 807-869.
24. Li G, Meng X, Wang R, Mao G, Han L, Liu Y, Zhang S (2012) Dual-level regulation of ACC synthase activity by MPK3/MPK6 cascade and its downstream WRKY transcription factor during ethylene induction in Arabidopsis. PLoS Genet 8: e1002767.
25. Li J, Wen J, Lease KA, Doke JT, Tax FE, Walker JC (2002) BAK1, an Arabidopsis LRR receptor-like protein kinase, interacts with BRI1 and modulates brassinosteroid signaling. Cell 110: 213-222.
26. Li L, Li M, Yu L, Zhou Z, Liang X, Liu Z, Cai G, Gao L, Zhang X, Wang Y, et al (2014) The FLS2-associated kinase BIK1 directly phosphorylates the NADPH oxidase RbohD to control plant immunity. Cell Host Microbe 15: 329-338.
27. Li X, Lin H, Zhang W, Zou Y, Zhang J, Tang X, Zhou JM (2005) Flagellin induces innate immunity in nonhost interactions that is suppressed by Pseudomonas syringae effectors. Proc Natl Acad Sci USA 102: 12990-12995.
28. Lin W, Lu D, Gao X, Jiang S, Ma X, Wang Z, Mengiste T, He P, Shan L (2013) Inverse modulation of plant immune and brassinosteroid signaling pathways by the receptor-like cytoplasmic kinase BIK1. Proc Natl Acad Sci USA 110: 12114-12119.
29. Liu Y, Zhang S (2004) Phosphorylation of 1-aminocyclopropane-1-carboxylic acid synthase by MPK6, a stress-responsive mitogen-activated protein kinase, induces ethylene biosynthesis in Arabidopsis. Plant Cell 16: 3386-3399.
30. Lozano-Durán R, Macho AP, Boutrot F, Segonzac C, Somssich IE, Zipfel C (2013) The transcriptional regulator BZR1 mediates trade-off between plant innate immunity and growth. eLife 2: e00983.
31. Lu D, Lin W, Gao X, Wu S, Cheng C, Avila J, Heese A, Devarenne TP, He P, Shan L (2011) Direct ubiquitination of pattern recognition receptor FLS2 attenuates plant innate immunity. Science 332: 1439-1442.
32. Lu D, Wu S, Gao X, Zhang Y, Shan L, He P (2010) A receptor-like cytoplasmic kinase, BIK1, associates with a flagellin receptor complex to initiate plant innate immunity. Proc Natl Acad Sci USA 107: 496-501.
33. Malinovsky FG, Batoux M, Schwessinger B, Youn JH, Stransfeld L, Win J, Kim SK, Zipfel C (2014) Antagonistic regulation of growth and immunity by the Arabidopsis basic helix-loop-helix transcription factor HOMOLOG OF BRASSINOSTEROID ENHANCED EXPRESSION2 INTERACTING WITH INCREASED LEAF INCLINATION1 BINDING bHLH1. Plant Physiol 164: 1443-1455.
34. Meng X, Xu J, He Y, Yang KY, Mordorski B, Liu Y, Zhang S (2013) Phosphorylation of an ERF transcription factor by Arabidopsis MPK3/ MPK6 regulates plant defense gene induction and fungal resistance. Plant Cell 25: 1126-1142.
35. Merkouropoulos G, Andreasson E, Hess D, Boller T, Peck SC (2008) An Arabidopsis protein phosphorylated in response tomicrobial elicitation, AtPHOS32, is a substrate of MAP kinases 3 and 6. J Biol Chem 283: 10493-10499.
36. Moffat CS, Ingle RA, Wathugala DL, Saunders NJ, Knight H, Knight MR (2012) ERF5 and ERF6 play redundant roles as positive regulators of JA/Etmediated defense against Botrytis cinerea in Arabidopsis. PLoS ONE 7: e35995.
37. Peck SC, Nühse TS, Hess D, Iglesias A, Meins F, Boller T (2001) Directed proteomics identifies a plant-specific protein rapidly phosphorylated in response to bacterial and fungal elicitors. Plant Cell 13: 1467-1475.
38. Petersen M, Brodersen P, Naested H, Andreasson E, Lindhart U, Johansen B, Nielsen HB, Lacy M, Austin MJ, Parker JE, et al (2000) Arabidopsis map kinase 4 negatively regulates systemic acquired resistance. Cell 103: 1111-1120.
39. Pitzschke A, Schikora A, Hirt H (2009) MAPK cascade signalling networks in plant defence. Curr Opin Plant Biol 12: 421-426.
40. Ryu H, Cho H, Kim K, Hwang I (2010) Phosphorylation dependent nucleocytoplasmic shuttling of BES1 is a key regulatory event in brassinosteroid signaling. Mol Cells 29: 283-290.
41. Ryu H, KimK, Cho H, Park J, Choe S, Hwang I (2007) Nucleocytoplasmic shuttling of BZR1 mediated by phosphorylation is essential in Arabidopsis brassinosteroid signaling. Plant Cell 19: 2749-2762.
42. Schwessinger B, Zipfel C (2008) News from the frontline: recent insights into PAMP-triggered immunity in plants. Curr Opin Plant Biol 11: 389- 395.
43. Shi H, Shen Q, Qi Y, Yan H, Nie H, Chen Y, Zhao T, Katagiri F, Tang D (2013) BR-SIGNALING KINASE1 physically associates with FLAGELLIN SENSING2 and regulates plant innate immunity in Arabidopsis. Plant Cell 25: 1143-1157.
44. Shimada TL, Shimada T, Hara-Nishimura I (2010) A rapid and nondestructive screenable marker, FAST, for identifying transformed seeds of Arabidopsis thaliana. Plant J 61: 519-528.
45. Son GH, Wan J, Kim HJ, Nguyen XC, Chung WS, Hong JC, Stacey G (2012) Ethylene-responsive element-binding factor 5, ERF5, is involved in chitin-induced innate immunity response. Mol Plant Microbe Interact 25: 48-60.
46. Sun Y, Li L, Macho AP, Han Z, Hu Z, Zipfel C, Zhou JM, Chai J (2013) Structural basis for flg22-induced activation of the Arabidopsis FLS2- BAK1 immune complex. Science 342: 624-628.
47. Tang W, Kim TW, Oses-Prieto JA, Sun Y, Deng Z, Zhu S, Wang R, Burlingame AL, Wang ZY (2008) BSKsmediate signal transduction from the receptor kinase BRI1 in Arabidopsis. Science 321: 557-560.
48. Veronese P, Nakagami H, Bluhm B, Abuqamar S, Chen X, Salmeron J, Dietrich RA, Hirt H, Mengiste T (2006) The membrane-anchored BOTRYTIS-INDUCED KINASE1 plays distinct roles in Arabidopsis resistance to necrotrophic and biotrophic pathogens. Plant Cell 18: 257- 273.
49. Wang X, Chory J (2006) Brassinosteroids regulate dissociation of BKI1, a negative regulator of BRI1 signaling, from the plasma membrane. Science 313: 1118-1122.
50. Wang X, Kota U, He K, Blackburn K, Li J, Goshe MB, Huber SC, Clouse SD (2008) Sequential transphosphorylation of the BRI1/BAK1 receptor kinase complex impacts early events in brassinosteroid signaling. Dev Cell 15: 220-235.
51. Wang Y, Sun S, Zhu W, Jia K, Yang H, Wang X (2013) Strigolactone/ MAX2-induced degradation of brassinosteroid transcriptional effector BES1 regulates shoot branching. Dev Cell 27: 681-688.
52. Wang ZY, Nakano T, Gendron J, He J, Chen M, Vafeados D, Yang Y, Fujioka S, Yoshida S, Asami T, et al (2002) Nuclear-localized BZR1 mediates brassinosteroid-induced growth and feedback suppression of brassinosteroid biosynthesis. Dev Cell 2: 505-513.
53. Yin Y, Vafeados D, Tao Y, Yoshida S, Asami T, Chory J (2005) A new class of transcription factors mediates brassinosteroid-regulated gene expression in Arabidopsis. Cell 120: 249-259.
54. Yin Y, Wang ZY, Mora-Garcia S, Li J, Yoshida S, Asami T, Chory J (2002) BES1 accumulates in the nucleus in response to brassinosteroids to regulate gene expression and promote stem elongation. Cell 109: 181- 191.
55. Yu X, Li L, Li L, Guo M, Chory J, Yin Y (2008) Modulation of brassinosteroidregulated gene expression by Jumonji domain-containing proteins ELF6 and REF6 in Arabidopsis. Proc Natl Acad Sci USA 105: 7618-7623.
56. Yu X, Li L, Zola J, Aluru M, Ye H, Foudree A, Guo H, Anderson S, Aluru S, Liu P, et al (2011) A brassinosteroid transcriptional network revealed by genome-wide identification of BESI target genes in Arabidopsis thaliana. Plant J 65: 634-646.
57. Zhang J, Li W, Xiang T, Liu Z, Laluk K, Ding X, Zou Y, Gao M, Zhang X, Chen S, et al (2010) Receptor-like cytoplasmic kinases integrate signaling from multiple plant immune receptors and are targeted by a Pseudomonas syringae effector. Cell Host Microbe 7: 290-301.
58. Zhang J, Shao F, Li Y, Cui H, Chen L, Li H, Zou Y, Long C, Lan L, Chai J, et al (2007) A Pseudomonas syringae effector inactivates MAPKs to suppress PAMP-induced immunity in plants. Cell Host Microbe 1: 175-185.
59. Zhang J, Zhou JM (2010) Plant immunity triggered by microbial molecular signatures. Mol Plant 3: 783-793.
60. Zhang Z, Wu Y, Gao M, Zhang J, Kong Q, Liu Y, Ba H, Zhou J, Zhang Y (2012) Disruption of PAMP-induced MAP kinase cascade by a Pseudomonas syringae effector activates plant immunity mediated by the NBLRR protein SUMM2. Cell Host Microbe 11: 253-263.
61. Zipfel C, Kunze G, Chinchilla D, Caniard A, Jones JD, Boller T, Felix G (2006) Perception of the bacterial PAMP EF-Tu by the receptor EFR restricts Agrobacterium-mediated transformation. Cell 125: 749-760.