Transcription factor WRKY46 regulates osmotic stress responses and stomatal movement independently in Arabidopsis

Plant Journal

Volumn 79, Issue 1, 2014, Pages 13-27

  Ding, Zhong Jie ^a   Yan, Jing Ying ^a   Xu, Xiao Yan ^a   Yu, Di Qiu ^b   Li, Gui Xin ^c   Zhang, Shu Qun ^a   Zheng, Shao Jian ^a  

^a ZHEJIANG UNIVERSITY   (China)

^b CHINESE ACADEMY OF SCIENCES   (China)

^c ZHEJIANG UNIVERSITY   (China)

Author keywords

Arabidopsis; drought; salt stress; stomatal movement; transcription factor; WRKY46

Indexed keywords

CELLS; CYTOLOGY; DEHYDRATION; PLANT SHUTDOWNS; STARCH; TRANSCRIPTION FACTORS;

ARABIDOPSIS; MICROARRAY ANALYSIS; REACTIVE OXYGEN SPECIES; REGULATORY MECHANISM; SALT STRESSS; STARCH METABOLISM; STOMATAL MOVEMENTS; WRKY46;

DROUGHT;

ARABIDOPSIS;

ARABIDOPSIS PROTEIN; INORGANIC SALT; MALONALDEHYDE; REACTIVE OXYGEN METABOLITE; STARCH; TRANSCRIPTION FACTOR; WRKY46 PROTEIN, ARABIDOPSIS;

ARABIDOPSIS; CYTOLOGY; DNA MICROARRAY; DROUGHT; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; HOMEOSTASIS; LIGHT; METABOLISM; OSMOTIC PRESSURE; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; PHENOTYPE; PHYSIOLOGICAL STRESS; PHYSIOLOGY; PLANT STOMA; RADIATION RESPONSE; SEEDLING; TRANSGENIC PLANT;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; DROUGHTS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; HOMEOSTASIS; LIGHT; MALONDIALDEHYDE; MUTAGENESIS, INSERTIONAL; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; OSMOTIC PRESSURE; OXIDATION-REDUCTION; OXIDATIVE STRESS; PHENOTYPE; PLANT STOMATA; PLANTS, GENETICALLY MODIFIED; REACTIVE OXYGEN SPECIES; SALTS; SEEDLING; STARCH; STRESS, PHYSIOLOGICAL; TRANSCRIPTION FACTORS;

EID: 84903275384     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.12538     Document Type: Article

References (71)

1. Abe, H., Urao, T., Ito, T., Seki, M., Shinozaki, K., and, Yamaguchi-Shinozaki, K., (2003) Arabidopsis AtMYC2 (bHLH) and AtMYB2 (MYB) function as transcriptional activators in abscisic acid signaling. Plant Cell, 15, 63-78.
2. Anderson, J.P., Badruzsaufari, E., Schenk, P.M., Manners, J.M., Desmond, O.J., Ehlert, C., Maclean, D.J., Ebert, P.R., and, Kazan, K., (2004) Antagonistic interaction between abscisic acid and jasmonate-ethylene signaling pathways modulates defense gene expression and disease resistance in Arabidopsis. Plant Cell, 16, 3460-3479.
3. Asselbergh, B., De Vieesschauwer, D., and, Hofte, M., (2008) Global switches and fine-tuning-ABA modulates plant pathogen defense. Mol. Plant Microbe Interact. 21, 709-719.
4. Atkinson, N.J., and, Urwin, P.E., (2012) The interaction of plant biotic and abiotic stresses: from genes to the field. J. Exp. Bot. 63, 3523-3543.
5. Boyer, J.S., (1982) Plant productivity and environment. Science, 218, 443-448.
6. Briggs, W.R., and, Christie, J.M., (2002) Phototropins 1 and 2: versatile plant blue-light receptors. Trends Plant Sci. 7, 204-210.
7. Choi, H.I., Hong, J.H., Ha, J.O., Kang, J.Y., and, Kim, S.Y., (2000) ABFs, a family of ABA-responsive element binding factors. J. Biol. Chem. 275, 1723-1730.
8. Cutler, S., Rodriguez, P., Finkelstein, R., and, Abrams, S., (2010) Abscisic acid: emergence of a core signaling network. Annu. Rev. Plant Biol. 61, 651-679.
9. Czechowski, T., Stitt, M., Altmann, T., Udvardi, M.K., and, Scheible, W.R., (2005) Genome-wide identi?cation and testing of superior reference genes for transcript normalization in Arabidopsis. Plant Physiol. 139, 5-17.
10. Davletova, S., Schlauch, K., Coutu, J., and, Mittler, R., (2005) The zinc-finger protein Zat12 plays a central role in reactive oxygen and abiotic stress signaling in Arabidopsis. Plant Physiol. 139, 847-856.
11. Delhaize, E., Craig, S., and, Beaton, C.D., (1993) Aluminum tolerance in wheat (Triticum aestivum L.) uptake and distribution of aluminum in root apices. Plant Physiol. 103, 685-693.
12. Ding, Z.J., Yan, J.Y., Xv, X.Y., Li, G.X., and, Zheng, S.J., (2013) WRKY46 functions as a transcriptional repressor of ALMT1, regulating aluminum-induced malate secretion in Arabidopsis. Plant J. 76, 823-835.
13. Eltayeb, A.E., Kawano, N., Badawi, G.H., Kaminaka, H., Sanekata, T., Shibahara, T., Inanaga, S., and, Tanaka, K., (2007) Overexpression of monodehydroascorbate reductase in transgenic tobacco confers enhanced tolerance to ozone, salt and polyethylene glycol stresses. Planta, 225, 1255-1264.
14. Epstein, E., Norlyn, J.D., Rush, D.W., Kingsbury, R.W., Kelly, D.B., Cunningham, G.A., and, Wrona, A.F., (1980) Saline culture of crops: a genetic approach. Science, 210, 399-404.
15. Eulgem, T., Rushton, P.J., Robatzek, S., and, Somssich, I.E., (2000) The WRKY superfamily of plant transcription factors. Trends Plant Sci. 5, 199-206.
16. Finkelstein, R.R., Gampala, S.S.L., and, Rock, C.D., (2002) Abscisic acid signaling in seeds and seedlings. Plant Cell, 14, S15-S45.
17. Fujii, H., and, Zhu, J.K., (2009) Arabidopsis mutant deficient in 3 abscisic acid-activated protein kinases reveals critical roles in growth, reproduction, and stress. Proc. Natl Acad. Sci. USA, 106, 8380-8385.
18. Fujii, H., Chinnusamy, V., Rodrigues, A., Rubio, S., Antoni, R., Park, S., Cutler, S., Sheen, J., Rodriguez, P., and, Zhu, J., (2009) In vitro reconstitution of an abscisic acid signaling pathway. Nature, 462, 660-664.
19. Fujita, M., Fujita, Y., Noutoshi, Y., Takahashi, F., Narusaka, Y., Yamaguchi-Shinozaki, K., and, Shinozaki, K., (2006) Crosstalk between abiotic and biotic stress responses: a current view from the points of convergence in the stress signaling networks. Curr. Opin. Plant Biol. 9, 436-442.
20. Fujita, Y., Fujita, M., Shinozaki, K., and, Yamaguchi-Shinozaki, K., (2011) ABA mediated transcriptional regulation in response to osmotic stress in plants. J. Plant. Res. 124, 509-525.
21. Guo, F.Q., Young, J., and, Crawford, N.M., (2003) The nitrate transporter AtNRT1.1 (CHL1) functions in stomatal opening and contributes to drought susceptibility in Arabidopsis. Plant Cell, 15, 107-117.
22. Himmelbach, A., Yang, Y., and, Grill, E., (2003) Relay and control of abscisic acid signaling. Curr. Opin. Plant Biol. 6, 470-479.
23. Hoekenga, O.A., Maron, L.G., Pineros, M.A., et al. (2006) AtALMT1, which encodes a malate transporter, is identified as one of several genes critical for aluminum tolerance in Arabidopsis. Proc. Natl Acad. Sci. USA, 103, 9738-9743.
24. Hu, Y.R., Dong, Q.Y., and, Yu, D.Q., (2012) Arabidopsis WRKY46 coordinates with WRKY70 and WRKY53 in basal resistance against pathogen Pseudomonas syringae. Plant Sci. 185, 288-297.
25. Ingram, J., and, Bartels, D., (1996) The molecular basis of dehydration tolerance in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47, 377-403.
26. Jakoby, M., Weisshaar, B., Dröge-Laser, W., Vicente-Carbajosa, J., Tiedemann, J., Kroi, T., and, Parcey, F., (2002) bZIP transcription factors in Arabidopsis. Trends Plant Sci. 7, 106-112.
27. Jiang, Y.J., Liang, G., and, Yu, D.Q., (2012) Activated expression of WRKY57 confers drought tolerance in Arabidopsis. Mol. Plant, 5, 1375-1388.
28. Kaye, Y., Golani, Y., Singer, Y., Leshem, Y., Cohen, G., Ercetin, M., Gillaspy, G., and, Levine, A., (2011) Inositol polyphosphate 5-phosphatase7 regulates the production of reactive oxygen species and salt tolerance in Arabidopsis. Plant Physiol. 157, 229-241.
29. 2+ signaling. Annu. Rev. Plant Biol. 61, 561-591.
30. +-ATPase by phosphorylation of the C-terminus in stomatal guard cells. EMBO J. 18, 5548-58.
31. Kobayashi, Y., Hoekenga, O.A., Itoh, H., Nakashima, M., Saito, S., Shaff, J.E., Maron, L.G., Pineros, M.A., Kochian, L.V., and, Koyama, H., (2007) Characterization of AtALMT1 expression in aluminum-inducible malate release and its role for rhizotoxic stress tolerance in Arabidopsis. Plant Physiol. 145, 843-852.
32. Kopka, J., Provart, N.J., and, Muller-Rober, B., (1997) Potato guard cells respond to drying soil by a complex change in the expression of genes related to carbon metabolism and turgor regulation. Plant J. 11, 871-882.
33. Laloi, C., Mestres-Ortega, D., Marco, Y., Meyer, Y., and, Reichheld, J.P., (2004) The Arabidopsis cytosolic thioredoxin h5 gene induction by oxidative stress and its W-Box-mediated response to pathogen elicitor. Plant Physiol. 134, 1006-1016.
34. Lasceve, G., Leymarie, J., and, Vavasseur, A., (1997) Alterations in light-induced stomatal opening in a starch-deficient mutant of Arabidopsis thaliana L. deficient in chloroplast phosphoglucomutase activity. Plant, Cell Environ. 20, 350-358.
35. Lata, C., and, Prasad, M., (2011) Role of DREBs in regulation of abiotic stress responses in plants. J. Exp. Bot. 62, 4731-4748.
36. Laurie-Berry, N., Joardar, V., Street, I.H., and, Kunkel, B.N., (2006) The Arabidopsis thaliana JASMONATE INSENSITIVE 1 gene is required for suppression of salicylic acid-dependent defenses during infection by Pseudomonas syringae. Mol. Plant Microbe Interact. 19, 789-800.
37. Leung, J., and, Giraudat, J., (1998) Abscisic acid signal transduction. Annu. Rev. Plant Physiol. Plant Mol. Biol. 49, 199-222.
38. Li, L., Foster, C.M., Gan, Q., Nettleton, D., James, M.G., Myers, A.M., and, Wurtele, E.S., (2009) Identification of the novel protein QQS as a component of the starch metabolic network in Arabidopsis leaves. Plant J. 58, 485-498.
39. Lu, Z., Liu, D., and, Liu, S., (2007) Two rice cytosolic ascorbate peroxidases differentially improve salt tolerance in transgenic Arabidopsis. Plant Cell Rep. 26, 1909-1917.
40. Miller, G., Suzuki, N., Ciftci-Yilmaz, S., and, Mittler, R., (2010) Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant, Cell Environ. 33, 453-467.
41. Mittler, R., Vanderauwera, S., Gollery, M., and, Van Breusegem, F., (2004) Reactive oxygen gene network of plants. Trends Plant Sci. 9, 490-498.
42. Noctor, G., and, Foyer, C., (1998) Ascorbate and glutathione: keeping active oxygen under control. Annu. Rev. Plant Physiol. Plant Mol. Biol. 49, 249-279.
43. Outlaw, W.H., and, Manchester, J., (1979) Guard cell starch concentration quantitatively related to stomatal aperture. Plant Physiol. 64, 79-82.
44. Pandey, S., Wang, X.Q., Coursol, S.A., and, Assmann, S.M., (2002) Preparation and application of Arabidopsis thaliana guard cell protoplasts. New Phytol. 153, 517-526.
45. Passardi, F., Cosio, C., Penel, C., and, Dunand, C., (2005) Peroxidases have more functions than a Swiss army knife. Plant Cell Rep. 24, 255-265.
46. Pei, Z.M., Kuchitsu, K., Ward, J.M., Schwarz, M., and, Schroeder, J.I., (1997) Differential abscisic acid regulation of guard cell slow anion channels in Arabidopsis wild-type and abi1 and abi2 mutants. Plant Cell, 9, 409-423.
47. Pei, Z.M., Murata, Y., Benning, G., Thomine, S., Klusener, B., Allen, G.J., Grill, E., and, Schroeder, J.I., (2000) Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cells. Nature, 406, 731-734.
48. Reddy, A.R., and, Das, V.S.R., (1986) Stomatal movement and sucrose uptake by guard cell protoplasts of Commelina benghalensis L. Plant Cell Physiol. 27, 1565-1570.
49. Ren, X.Z., Chen, Z.Z., Liu, Y., Zhang, H.R., Zhang, M., Liu, Q., Hong, X.H., Zhu, J.K., and, Gong, Z.Z., (2010) ABO3, a WRKY transcription factor, mediates plant responses to abscisic acid and drought tolerance in Arabidopsis. Plant J. 63, 417-429.
50. Rushton, P.J., Somssich, I.E., Ringler, P., and, Shen, Q.J., (2010) WRKY transcription factors. Trends Plant Sci. 15, 247-258.
51. Schmittgen, T.D., and, Livak, K.J., (2008) Analyzing real-time PCR data by the comparative C(T) method. Nat. Protoc. 3, 1101-1108.
52. Schroeder, J.I., Allen, G.J., Hugouvieux, V., Kwak, J.M., and, Waner, D., (2001) Guard cell signal transduction. Annu. Rev. Plant Physiol. Plant Mol. Biol. 52, 627-658.
53. Schurmann, P., and, Jacquot, J.P., (2000) Plant thioredoxin systems revisited. Annu. Rev. Plant Physiol. Plant Mol. Biol. 51, 371-400.
54. Shimazaki, K., Doi, M., Assmann, S., and, Kinoshita, T., (2007) Light regulation of stomatal movement. Annu. Rev. Plant Biol. 58, 219-247.
55. Soon, F., Ng, L., Zhou, X., et al. (2012) Molecular mimicry regulates ABA signaling by SnRK2 kinases and PP2C phosphatases. Science, 335, 85-88.
56. Tallman, G., and, Zeiger, E., (1988) Light quality and osmoregulation in Vicia guard cells. Evidence for involvement of three metabolic pathways. Plant Physiol. 88, 887-895.
57. Tao, Z., Kou, Y.J., Liu, H.B., Li, X.H., Xiao, J.H., and, Wang, S.P., (2011) OsWRKY45 alleles play different roles in abscisic acid signalling and salt stress tolerance but similar roles in drought and cold tolerance in rice. J. Exp. Bot. 62, 4863-4874.
58. Teige, M., Scheikl, E., Eulgem, T., Doczi, R., Ichimura, K., Shinozaki, K., Dangl, J.L., and, Hirt, H., (2004) The MKK2 pathway mediates cold and salt stress signaling in Arabidopsis. Mol. Cell, 15, 141-152.
59. Toufighi, K., Brady, S.M., Austin, R., Ly, E., and, Provart, N.J., (2005) The botany array resource: e-Northerns, expression angling, and promoter analyses. Plant J. 43, 153-163.
60. Tseng, M.J., Liu, C.W., and, Yiu, J.C., (2007) Enhanced tolerance to sulfur dioxide and salt stress of transgenic Chinese cabbage plants expressing both superoxide dismutase and catalase in chloroplasts. Plant Physiol. Biochem. 45, 822-833.
61. Ulker, B., and, Somssich, I.E., (2004) WRKY transcription factors: from DNA binding towards biological function. Curr. Opin. Plant Biol. 7, 491-498.
62. Umezawa, T., Sugiyama, N., Takahashi, F., Anderson, J., Ishihama, Y., Peck, S., and, Shinozaki, K., (2013) Genetics and phosphoproteomics reveal a protein phosphorylation network in the abscisic acid signaling pathway in Arabidopsis thaliana. Sci. Signal. 6, rs8.
63. Uno, Y., Furihata, T., Abe, H., Yoshida, R., Shinozaki, K., and, Yamaguchi-Shinozaki, K., (2000) Arabidopsis basic leucine zipper transcription factors involved in an abscisic acid-dependent signal transduction pathway under drought and high-salinity conditions. Proc. Natl Acad. Sci. USA, 97, 11632-11637.
64. Vanderauwera, S., Vandenbroucke, K., Inze, A., Cotte, B., Muhlenbock, P., Rycke, R., Naouar, N., Gaever, T., Montagu, M., and, Breusegem, F., (2012) AtWRKY15 perturbation abolishes the mitochondrial stress response that steers osmotic stress tolerance in Arabidopsis. Proc. Natl Acad. Sci. USA, 109, 20113-20118.
65. Vavasseur, A., and, Raghavendra, A.S., (2005) Guard cell metabolism and CO2 sensing. New Phytol. 165, 665-682.
66. Verslues, P.E., Agarwal, M., Katiyar-Agarwal, S., Zhu, J.H., and, Zhu, J.K., (2006) Methods and concepts in quantifying resistance to drought, salt and freezing, abiotic stresses that affect plant water status. Plant J. 45, 523-539.
67. Yamaguchi-Shinozaki, K., and, Shinozaki, K., (2006) Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stress. Annu. Rev. Plant Biol. 57, 781-803.
68. Yoo, S.D., Cho, Y.H., and, Sheen, J., (2007) Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nat. Protoc. 2, 1565-1672.
69. Zhang, X., Zhang, L., Dong, F., Gao, J., Galbraith, D.W., and, Song, C.P., (2001) Hydrogen peroxide is involved in abscisic acid-induced stomatal closure in Vicia faba. Plant Physiol. 126, 1438-1448.
70. Zhang, Z.J., Wang, J., Zhang, R.X., and, Huang, R.F., (2012) The ethylene response factor AtERF98 enhances tolerance to salt through the transcriptional activation of ascorbic acid synthesis in Arabidopsis. Plant J. 71, 273-287.
71. Zhu, J.K., (2002) Salt and drought stress signal transduction in plants. Annu. Rev. Plant Biol. 53, 247-273.