Silencing of tomato RBOH1 and MPK2 abolishes brassinosteroid-induced H2O2 generation and stress tolerance

Plant, Cell and Environment

Volumn 36, Issue 4, 2013, Pages 789-803

  Nie, Wen Feng ^a   Wang, Meng Meng ^a   Xia, Xiao Jian ^a   Zhou, Yan Hong ^a   Shi, Kai ^a   Chen, Zhixiang ^a,c   Yu, Jing Quan ^a,b  

^a ZHEJIANG UNIVERSITY   (China)

^b AGRO ENVIRONMENTAL PROTECTION INSTITUTE   (China)

^c PURDUE UNIVERSITY   (United States)

Author keywords

Brassinosteroids; Defence response; Hydrogen peroxide; Mitogen activated protein kinase; Photooxidation; Reactive oxygen species; Signal transduction.

Indexed keywords

ANTIOXIDANT; BRASSINOLIDE; BRASSINOSTEROID; CARBON DIOXIDE; HETEROCYCLIC STEROID; HYDROGEN PEROXIDE; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; PLANT RNA; REACTIVE OXYGEN METABOLITE; VEGETABLE PROTEIN;

ENVIRONMENTAL STRESS; FRUIT; GENE EXPRESSION; GROWTH RATE; HYDROGEN PEROXIDE; PHOTOOXIDATION; PLANT DEFENSE; STEROID; TOLERANCE;

ADAPTATION; APOPTOSIS; ARTICLE; DRUG EFFECT; GENE EXPRESSION REGULATION; GENE SILENCING; GENETICS; HEAT; METABOLISM; OXIDATION REDUCTION REACTION; PHYSIOLOGY; PLANT LEAF; SEEDLING; SIGNAL TRANSDUCTION; TIME; TOMATO;

ADAPTATION, PHYSIOLOGICAL; ANTIOXIDANTS; APOPTOSIS; BRASSINOSTEROIDS; CARBON DIOXIDE; GENE EXPRESSION REGULATION, PLANT; GENE SILENCING; HOT TEMPERATURE; HYDROGEN PEROXIDE; LYCOPERSICON ESCULENTUM; MITOGEN-ACTIVATED PROTEIN KINASES; OXIDATION-REDUCTION; PLANT LEAVES; PLANT PROTEINS; REACTIVE OXYGEN SPECIES; RNA, MESSENGER; RNA, PLANT; SEEDLING; SIGNAL TRANSDUCTION; STEROIDS, HETEROCYCLIC; TIME FACTORS;

LYCOPERSICON ESCULENTUM;

EID: 84874738459     PISSN: 01407791     EISSN: 13653040     Source Type: Journal    
DOI: 10.1111/pce.12014     Document Type: Article

References (65)

1. Asai T., Tena G., Plotnikova J., Willmann M.R., Chiu W., Gomez L.G., Boller T., Ausubel F.M. & Sheen J. (2002) MAP kinase signalling cascade in Arabidopsis innate immunity. Nature 415, 977-983.
2. Asai S., Ohta K. & Yoshioka H. (2008) MAPK signaling regulates nitric oxide and NADPH oxidase-dependent oxidative bursts in Nicotiana benthamiana. The Plant Cell 20, 1390-1406.
3. Bajguz A. & Hayat S. (2009) Effects of brassinosteroids on the plant responses to environmental stresses. Plant Physiology and Biochemistry 47, 1-8.
4. Bhattarai K., Atamian H., Kaloshian I. & Eulgem T. (2010) WRKY72-type transcription factors contribute immunity in tomato and Arabidopsis as well as resistance mediated by the tomato R gene Mi-1. The Plant Journal 63, 229-240.
5. Bhattarai K.K., Li Q., Liu Y., Dinesh-Kumar S.P. & Kaloshian I. (2007) The Mi-1-mediated pest resistance requires Hsp90 and Sgt1. Plant Physiology 144, 312-323.
6. Brodersen P., Petersen M., Nielsen H.B., Zhu S., Newman M., Shokat K.M., Rietz S., Parker J. & Mundy J. (2006) Arabidopsis MAP kinase 4 regulates salicylic acid- and jasmonic acid/ethylene-dependent responses via EDS1 and PAD4. The Plant Journal 47, 532-546.
7. Cui J.X., Zhou Y.H., Ding J.G., Xia X.J., Shi K., Chen S.C., Asami T., Chen Z.X. & Yu J.Q. (2011) Role of nitric oxide in hydrogen peroxide-dependent induction of abiotic stress tolerance by brassinosteroids in cucumber. Plant, Cell & Environment 34, 347-358.
8. Divi U.K. & Krishna P. (2009) Brassinosteroid: a biotechnological target for enhancing crop yield and stress tolerance. New Biotechnology 26, 131-136.
9. Doulis A.G., Debian N., Kingston Smith A.H. & Foyer C.H. (1997) Differential localization of antioxidants in maize leaves. Plant Physiology 114, 1031-1037.
10. Ekengren S.K., Liu Y., Schiff M., Dinesh-Kumar S.P. & Martin G.B. (2003) Two MAPK cascades, NPR1, and TGA transcription factors play a role in Pto-mediated disease resistance in tomato. The Plant Journal 36, 905-917.
11. Foyer C.H. & Halliwell B. (1976) The presence of glutathione and glutathione reductase in chloroplasts: a proposed role in ascorbic acid metabolism. Planta 133, 21-25.
12. Foyer C.H. & Noctor G. (2009) Redox regulation in photosynthetic organisms: signaling, acclimation, and practical implications. Antioxidants & Redox Signaling 11, 861-905.
13. Gao M.H., Liu J.M., Bi D.L., Zhang Z.B., Cheng F., Chen S.F. & Zhang Y.L. (2008) MEKK1, MKK1/MKK2 and MPK4 function together in a mitogen-activated protein kinase cascade to regulate innate immunity in plants. Cell Research 18, 1190-1198.
14. Higgins R., Lockwood T., Holley S., Yalamanchili R. & Stratmann J. (2007) Changes in extracellular pH are neither required nor sufficient for activation of mitogen-activated protein kinases (MAPKs) in response to systemin and fusicoccin in tomato. Planta 225, 1535-1546.
15. Holley S.R., Yalamanchili R.D., Moura S.D., Ryan C.A. & Stratmann J.W. (2003) Convergence of signaling pathways induced by systemin, oligosaccharide elicitors, and ultraviolet-B radiation at the level of mitogen-activated protein kinases in Lycopersicon peruvianum suspension-cultured cells. Plant Physiology 132, 1728-1738.
16. 2 assimilation in Cucumis sativus. New Phytologist 194, 932-943.
17. Jonak C., Ökrész L., Bögre L. & Hirt H. (2002) Complexity, cross talk and integration of plant MAP kinase signaling. Current Opinion in Plant Biology 5, 415-424.
18. Kagale S., Divi U.K., Krochko J.E., Keller W.A. & Krishna P. (2007) Brassinosteroid confers tolerance in Arabidopsis thaliana and Brassica napus to a range of abiotic stresses. Planta 225, 353-364.
19. Kandoth P.Y., Ranf S., Pancholi S.S., Jayanty S., Walla M.D., Miller W., Howe G.A., Lincoln D.E. & Stratmann J.W. (2007) Tomato MAPKs LeMPK1, LeMPK2, and LeMPK3 function in the systemin-mediated defense response against herbivorous insects. Proceedings of the National Academy of Sciences of the United States of America 29, 12205-12210.
20. Kong X.P., Pan J.W., Zhang M.Y., Xing X., Zhou Y., Liu Y., Li D.P. & Li D.Q. (2011) ZmMKK4, a novel group C mitogen-activated protein kinase kinase in maize (Zea mays), confers salt and cold tolerance in transgenic Arabidopsis. Plant Cell & Environment 34, 1291-1303.
21. Krishna P. (2003) Brassinosteroid-mediated stress responses. Journal of Plant Growth Regulation 22, 289-297.
22. Kwak J., Mori I., Pei Z., Leonhardt N., Torres M., Dangl J., Bloom R., Bodde S., Jones J. & Schroeder J. (2003) NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in Arabidopsis. European Molecular Biology Organization 26, 2623-2633.
23. Kwak J.M., Nguyen V. & Schroeder J.I. (2006) The role of reactive oxygen species in hormonal responses. Plant Physiology 141, 323-329.
24. Li Q., Xie Q.-G., Smith-Becker J., Navarre D.A. & Kaloshian I. (2006) Mi-1-mediated aphid resistance involves salicylic acid and mitogen-activated protein kinase signaling cascades. Molecular Plant-Microbe Interactions 19, 655-664.
25. Lin F., Ding H.D., Wang J.X., Zhang H., Zhang A.Y., Zhang Y., Tan M.P., Dong W. & Jiang M.Y. (2009) Positive feedback regulation of maize NADPH oxidase by mitogen-activated protein kinase cascade in abscisic acid signaling. Journal of Experimental Botany 60, 3221-3238.
26. Liu J.Z., Horstman H.D., Braun E., etal. (2011) Soybean homologs of MPK4 negatively regulate defense responses and positively regulate growth and development. Plant Physiology 57, 1363-1378.
27. -ΔΔCT method. Methods 25, 402-408.
28. Lu C., Han M.H., Guevara-Garcia A. & Fedoroff N.V. (2002) Mitogen-activated protein kinase signaling in postgermination arrest of development by abscisic acid. Proceedings of the National Academy of Sciences of the United States of America 99, 15812-15817.
29. Mao G., Meng X., Liu Y., Zheng Z., Chen Z. & Zhang S. (2011) Phosphorylation of a WRKY transcription factor by two pathogen-responsive MAPKs drives phytoalexin biosynthesis in Arabidopsis. The Plant Cell 23, 1639-1653.
30. Marino D., Dunand C., Puppo A. & Pauly N. (2012) A burst of plant NADPH oxidases. Trends in Plant Science 17, 9-15.
31. Menke F.L., Pelt J.A., Pieterse C.M. & Klessig D.F. (2004) Silencing of the mitogen-activated protein kinase MPK6 compromises disease resistance in Arabidopsis. The Plant Cell 16, 897-907.
32. Miller G., Schlauch K., Tam R., Cortes D., Torres M.A., Shulaev V., Dangl J.L. & Mittler R. (2009) The plant NADPH oxidase RBOHD mediates rapid systemic signaling in response to diverse stimuli. Science Signaling 2, ra45.
33. Mittler R., Vanderauwera S., Gollery M. & Van Breusegem F. (2004) Reactive oxygen gene network of plants. Trends in Plant Science 9, 490-498.
34. Møllera I.M. & Gardestromb P. (2007) Plant mitochondria - more active than ever. Physiologia Plantarum 129, 1-5.
35. Moon H., Lee B., Choi G., etal. (2003) NDP kinase 2 interacts with two oxidative stress-activated MAPKs to regulate cellular redox state and enhances multiple stress tolerance in transgenic plants. Proceedings of the National Academy of Sciences of the United States of America 100, 358-363.
36. Nakagami H., Soukupova H., Schikora A., Zarsky V. & Hirt H. (2006) A mitogen-activated protein kinase kinase kinase mediates reactive oxygen species homeostasis in Arabidopsis. Journal of Biological Chemistry 281, 38697-38704.
37. Nakano Y. & Asada K. (1981) Hydrogen peroxide is scavenged by ascorbate specific peroxidase in spinach chloroplasts. Plant and Cell Physiology 22, 867-880.
38. Ning J., Li X.H., Hicks L.M. & Xiong L.Z. (2010) A Raf-like MAPKKK gene DSM1 mediates drought resistance through reactive oxygen species scavenging in rice. Plant Physiology 152, 876-890.
39. Patra H.K., Kar M. & Mishra D. (1978) Catalase activity in leaves and cotyledons during plant development and senescence. Biochemie Und Physiologie Der Pflanzen 172, 385-390.
40. Pedley K.F. & Martin G.B. (2004) Identification of MAPKs and their possible MAPK kinase activators involved in the Pto-mediated defense response of tomato. Journal of Biological Chemistry 279, 49229-49235.
41. Petersen M., Brodersen P., Naested H., etal. (2000) Arabidopsis MAP kinase 4 negatively regulates systemic acquired resistance. Cell 103, 1111-1120.
42. Pitzschke A., Schikora A. & Hirt H. (2009) MAPK cascade signalling networks in plant defense. Current Opinion in Plant Biology 12, 421-426.
43. Rodriguez M.C., Petersen M. & Mundy J. (2010) Mitogen-activated protein kinase signaling in plants. Annual Review of Plant Biology 61, 621-649.
44. Sagi M. & Fluhr R. (2001) Superoxide production by plant homologues of the gp91phox NADPH oxidase. Modulation of activity by calcium and by tobacco mosaic virus infection. Plant Physiology 126, 1281-1290.
45. Sagi M., Davydov O., Orazova S., Yesbergenova Z., Ophir R., Stratmann J.W. & Fluhrb R. (2004) Plant respiratory burst oxidase homologs impinge on wound responsiveness and development in Lycopersicon esculentum. The Plant Cell 16, 616-628.
46. Samuel M.A. & Ellis B.E. (2002) Double jeopardy: both overexpression and suppression of a redox-activated plant mitogen-activated protein kinase render tobacco plants ozone sensitive. The Plant Cell 14, 2059-2069.
47. Schikora A., Schenk S.T., Stein E., Molitor A., Zuccaro A. & Kogel K.H. (2011) N-acyl-homoserine lactone confers resistance toward biotrophic and hemibiotrophic pathogens via altered activation of AtMPK6. Plant Physiology 157, 1407-1418.
48. Stewart R.R.C. & Bewley J.D. (1980) Lipid peroxidation associated with accelerated aging of soybean axes. Plant Physiology 65, 245-248.
49. Teige M., Scheikl E., Eulgem T., Doczi R., Ichimura K., Shinozaki K., Dangl J.L. & Hirt H. (2004) The MKK2 pathway mediates cold and salt stress signaling in Arabidopsis. Molecular Cell 15, 141-152.
50. Tena G., Asai T., Chiu W.L. & Sheen J. (2001) Plant mitogen-activated protein kinase signaling cascades. Current Opinion in Plant Biology 4, 392-400.
51. 2 accumulation in papillae and hypersensitive response during the barley-powdery mildew interaction. The Plant Journal 11, 1187-1194.
52. Torres M.A. & Dangl J.L. (2005) Functions of the respiratory burst oxidase in biotic interactions, abiotic stress and development. Current Opinion in Plant Biology 8, 397-403.
53. Torres M.A., Dangl J.L. & Jones J.D.G. (2002) Arabidopsis gp91phox homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response. Proceedings of the National Academy of Sciences of the United States of America 99, 517-522.
54. Vriet C., Russinova E. & Reuzeau C. (2012) Boosting crop yields with plant steroids. The Plant Cell 24, 842-857.
55. 2 and is indispensable for stress defense in C3 plants. The EMBO Journal 16, 4806-4816.
56. Xia X.J., Huang L.F., Zhou Y.H., Mao W.H., Shi K., Wu J.X., Asami T., Chen Z.X. & Yu J.Q. (2009a) Brassinosteroids promote photosynthesis and growth by enhancing activation of Rubisco and expression of photosynthetic genes in Cucumis sativus. Planta 230, 1185-1196.
57. Xia X.J., Wang Y.J., Zhou Y.H., Tao Y., Mao W.H., Shi K., Asami T., Chen Z.X. & Yu J.Q. (2009b) Reactive oxygen species are involved in brassinosteroid-induced stress tolerance in cucumber. Plant Physiology 150, 801-814.
58. Xia X.J., Zhou Y.H., Ding J., Shi K., Asami T., Chen Z.X. & Yu J.Q. (2011) Induction of systemic stress tolerance by brassinosteroid in Cucumis sativus. New Phytologist 191, 706-720.
59. 2 accumulation and resistance to Phytophthora infestans. The Plant Cell 15, 706-718.
60. Zhang A.Y., Jiang M.Y., Zhang J.H., Tan M.P. & Hu X.L. (2006) Mitogen-activated protein kinase is involved in abscisic acid-induced antioxidant defense and acts downstream of reactive oxygen species production in leaves of maize plants. Plant Physiology 141, 475-487.
61. 2 in brassinosteroid-induced antioxidant defense in leaves of maize. Journal of Experimental Botany 61, 4399-4411.
62. Zhang S.Q. & Klessig D.F. (1997) Salicylic acid activates a 48-kD MAP kinase in tobacco. The Plant Cell 9, 809-824.
63. Zhang S.Q. & Klessig D.F. (2001) MAPK cascades in plant defense signaling. Trends in Plant Science 6, 520-527.
64. Zhang S.S., Cai Z.Y. & Wang X.L. (2009a) The primary signaling outputs of brassinosteroids are regulated by abscisic acid signaling. Proceedings of the National Academy of Sciences of the United States of America 11, 4543-4548.
65. 2 and NO production and antioxidant defences. Plant, Cell & Environment 32, 509-519.