Phosphorylation of a WRKY Transcription Factor by MAPKs Is Required for Pollen Development and Function in Arabidopsis

PLoS Genetics

Volumn 10, Issue 5, 2014, Pages

  Guan, Yuefeng ^a,b   Meng, Xiangzong ^a   Khanna, Reshma ^a   LaMontagne, Erica ^a   Liu, Yidong ^a   Zhang, Shuqun ^a  

^a University of Missouri   (United States)

^b INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

Author keywords

[No Author keywords available]

Indexed keywords

HYBRID PROTEIN; LAT52 PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE 6; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; VEGETABLE PROTEIN; WRKY2 PROTEIN; WRKY34 PROTEIN; ARABIDOPSIS PROTEIN; MPK6 PROTEIN, ARABIDOPSIS; WRKY34 PROTEIN, ARABIDOPSIS;

ARABIDOPSIS THALIANA; ARTICLE; CONTROLLED STUDY; ENZYME REGULATION; EPISTASIS; GENETIC ASSOCIATION; GERMINATION; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; PHASE TRANSITION; PLANT GAMETOGENESIS; POLLEN DEVELOPMENT; POLLEN TUBE GROWTH; PROTEIN DEGRADATION; PROTEIN DEPHOSPHORYLATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; SIGNAL TRANSDUCTION; TRANSGENE; UPREGULATION; ARABIDOPSIS; CELL DIFFERENTIATION; GAMETOGENESIS; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PHOSPHORYLATION; POLLEN; PROMOTER REGION; TRANSGENIC PLANT;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CELL DIFFERENTIATION; GAMETOGENESIS; GENE EXPRESSION REGULATION, PLANT; GERMINATION; MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; PLANTS, GENETICALLY MODIFIED; POLLEN; PROMOTER REGIONS, GENETIC; TRANSCRIPTION FACTORS;

EID: 84901595753     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1004384     Document Type: Article

References (50)

1. McCormick S, (2004) Control of male gametophyte development. Plant Cell 16Suppl: 53.
2. Honys D, Twell D, (2004) Transcriptome analysis of haploid male gametophyte development in Arabidopsis. Genome Biol 5: R85.
3. Mascarenhas JP, (1990) Gene activity during pollen development. Annu Rev Plant Biol 41: 317-655.
4. Wang J, Qiu X, Li Y, Deng Y, Shi T, (2011) A transcriptional dynamic network during Arabidopsis thaliana pollen development. BMC Systems Bio 5: S8.
5. Verelst W, Twell D, de Folter S, Immink R, Saedler H, et al. (2007) MADS-complexes regulate transcriptome dynamics during pollen maturation. Genome Biol 8: R249.
6. Kobayashi A, Sakamoto A, Kubo K, Rybka Z, Kanno Y, et al. (1998) Seven zinc-finger transcription factors are expressed sequentially during the development of anthers in petunia. Plant J 13: 571-577.
7. Seger R, Krebs EG, (1995) The MAPK signaling cascade. FASEB J 9: 726-735.
8. Jacobs D, Glossip D, Xing H, Muslin AJ, Kornfeld K, (1999) Multiple docking sites on substrate proteins form a modular system that mediates recognition by ERK MAP kinase. Genes Dev 13: 163-175.
9. Mao G, Meng X, Liu Y, Zheng Z, Chen Z, et al. (2011) Phosphorylation of a WRKY transcription factor by two pathogen-responsive MAPKs drives phytoalexin biosynthesis in Arabidopsis. Plant Cell 23: 1639-1653.
10. Lampard GR, Macalister CA, Bergmann DC, (2008) Arabidopsis stomatal initiation is controlled by MAPK-mediated regulation of the bHLH SPEECHLESS. Science 322: 1113-1116.
11. Bethke G, Unthan T, Uhrig JF, Poschl Y, Gust AA, et al. (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.
12. 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: 3386-3485.
13. Wang H, Ngwenyama N, Liu Y, Walker J, Zhang S, (2007) Stomatal development and patterning are regulated by environmentally responsive mitogen-activated protein kinases in Arabidopsis. Plant Cell 19: 63-73.
14. Meng X, Xu J, He Y, Yang KY, Mordorski B, et al. (2013) Phosphorylation of an ERF transcription factor by Arabidopsis MPK3/MPK6 regulates plant defense gene induction and fungal resistance. Plant Cell 25: 1126-1142.
15. Zheng Z, Qamar S, Chen Z, Mengiste T, (2006) Arabidopsis WRKY33 transcription factor is required for resistance to necrotrophic fungal pathogens. Plant J 48: 592-1197.
16. Li G, Meng X, Wang R, Mao G, Han L, et al. (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.
17. Eulgem T, Rushton P, Robatzek S, Somssich I, (2000) The WRKY superfamily of plant transcription factors. Trends Plant Sci 5: 199-206.
18. Zou C, Jiang W, Yu D, (2010) Male gametophyte-specific WRKY34 transcription factor mediates cold sensitivity of mature pollen in Arabidopsis. J Exp Bot 61: 3901-3914.
19. Honys D, Oh SA, Renak D, Donders M, Solcova B, et al. (2006) Identification of microspore-active promoters that allow targeted manipulation of gene expression at early stages of microgametogenesis in Arabidopsis. BMC Plant Biol 6: 31.
20. Twell D, Yamaguchi J, McCormick S, (1990) Pollen-specific gene expression in transgenic plants: coordinate regulation of two different tomato gene promoters during microsporogenesis. Development 109: 705-713.
21. Smyth DR, Bowman JL, Meyerowitz EM, (1990) Early flower development in Arabidopsis. Plant Cell 2: 755-767.
22. Twell D, Yamaguchi J, Wing RA, Ushiba J, McCormick S, (1991) Promoter analysis of genes that are coordinately expressed during pollen development reveals pollen-specific enhancer sequences and shared regulatory elements. Genes Dev 5: 496-507.
23. Kinoshita E, Takahashi M, Takeda H, Shiro M, Koike T, (2004) Recognition of phosphate monoester dianion by an alkoxide-bridged dinuclear zinc(II) complex. Dalton Trans 2004: 1189-1193.
24. Ueda M, Zhang Z, Laux T, (2011) Transcriptional activation of Arabidopsis axis patterning genes WOX8/9 links zygote polarity to embryo development. Dev Cell 20: 264-334.
25. Alexander M, (1969) Differential staining of aborted and nonaborted pollen. Stain Technol 44: 117-122.
26. Wang H, Liu Y, Bruffett K, Lee J, Hause G, et al. (2008) Haplo-insufficiency of MPK3 in MPK6 mutant background uncovers a novel function of these two MAPKs in Arabidopsis ovule development. Plant Cell 20: 602-613.
27. Morrison DK, Davis RJ, (2003) Regulation of MAP kinase signaling modules by scaffold proteins in mammals. Annu Rev Cell Dev Biol 19: 91-118.
28. Dard N, Peter M, (2006) Scaffold proteins in MAP kinase signaling: more than simple passive activating platforms. Bioessays 28: 146-156.
29. Kolch W, (2005) Coordinating ERK/MAPK signalling through scaffolds and inhibitors. Nat Rev Mol Cell Biol 6: 827-837.
30. Remenyi A, Good MC, Bhattacharyya RP, Lim WA, (2005) The role of docking interactions in mediating signaling input, output, and discrimination in the yeast MAPK network. Mol Cell 20: 951-962.
31. Widmann C, Gibson S, Jarpe MB, Johnson GL, (1999) Mitogen-activated protein kinase: conservation of a three-kinase module from yeast to human. Physiol Rev 79: 143-180.
32. Mor A, Philips MR, (2006) Compartmentalized Ras/MAPK signaling. Annu Rev Immunol 24: 771-800.
33. Schwartz MA, Madhani HD, (2004) Principles of MAP kinase signaling specificity in Saccharomyces cerevisiae. Annu Rev Genet 38: 725-748.
34. Zhang S, Klessig D, (2001) MAPK cascades in plant defense signaling. Trends Plant Sci 6: 520-527.
35. Zhang S (2008) Mitogen-activated protein kinase cascades in plant intracellular signaling. In: Yang Z, editor. Annual Plant Reviews Volume 33: Intracellular Signaling in Plants: Oxford: Wiley-Blackwell. pp. 100-136.
36. Ren D, Liu Y, Yang K, Han L, Mao G, et al. (2008) A fungal-responsive MAPK cascade regulates phytoalexin biosynthesis in Arabidopsis. Proc Natl Acad Sci USA 105: 5638-5643.
37. Rushton P, Somssich I, Ringler P, Shen Q, (2010) WRKY transcription factors. Trends Plant Sci 15: 247-305.
38. Miao Y, Laun T, Zimmermann P, Zentgraf U, (2004) Targets of the WRKY53 transcription factor and its role during leaf senescence in Arabidopsis. Plant Mol Biol 55: 853-867.
39. Kang X, Li W, Zhou Y, Ni M, (2013) A WRKY transcription factor recruits the SYG1-like protein SHB1 to activate gene expression and seed cavity enlargement. PLoS Genet 9: e1003347.
40. Grunewald W, De Smet I, Lewis DR, Lofke C, Jansen L, et al. (2012) Transcription factor WRKY23 assists auxin distribution patterns during Arabidopsis root development through local control on flavonol biosynthesis. Proc Natl Acad Sci USA 109: 1554-1559.
41. Teige M, Scheikl E, Eulgem T, Doczi R, Ichimura K, et al. (2004) The MKK2 pathway mediates cold and salt stress signaling in Arabidopsis. Mol Cell 15: 141-152.
42. Jiang W, Yu D, (2009) Arabidopsis WRKY2 transcription factor mediates seed germination and postgermination arrest of development by abscisic acid. BMC Plant Biol 9: 96.
43. Fisher C, Pei G, (1997) Modification of a PCR-based site-directed mutagenesis method. Biotechniques 23: 570.
44. Zheng L, Baumann U, Reymond J-L, (2004) An efficient one-step site-directed and site-saturation mutagenesis protocol. Nucleic Acids Res 32: e115.
45. Hellens RP, Edwards EA, Leyland NR, Bean S, Mullineaux PM, (2000) pGreen: a versatile and flexible binary Ti vector for Agrobacterium-mediated plant transformation. Plant Mol Biol 42: 819-832.
46. Clough S, Bent A, (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16: 735-778.
47. Heslop-Harrison J, Heslop-Harrison Y, (1970) Evaluation of pollen viability by enzymatically induced fluorescence; intracellular hydrolysis of fluorescein diacetate. Stain Technol 45: 115-120.
48. Boavida LC, McCormick S, (2007) Temperature as a determinant factor for increased and reproducible in vitro pollen germination in Arabidopsis thaliana. Plant J 52: 570-582.
49. Abràmoff MD, Magalhães PJ, Ram SJ, (2004) Image processing with ImageJ. Biophotonics Int 11: 36-78.
50. Kumar S, Nei M, Dudley J, Tamura K, (2008) MEGA: a biologist-centric software for evolutionary analysis of DNA and protein sequences. Brief Bioinform 9: 299-306.