Transcription factor WRKY46 modulates the development of Arabidopsis lateral roots in osmotic/salt stress conditions via regulation of ABA signaling and auxin homeostasis

Plant Journal

Volumn 84, Issue 1, 2015, Pages 56-69

  Ding, Zhong Jie ^a   Yan, Jing Ying ^a   Li, Chun Xiao ^a   Li, Gui Xin ^b   Wu, Yun Rong ^a   Zheng, Shao Jian ^a  

^a ZHEJIANG UNIVERSITY   (China)

^b ZHEJIANG UNIVERSITY   (China)

Author keywords

abscisic acid; Arabidopsis thaliana; auxin; lateral root; osmotic stress; WRKY46

Indexed keywords

GENE ENCODING; PLANTS (BOTANY); POLYMERASE CHAIN REACTION; ROAD CONSTRUCTION; TRANSCRIPTION; TRANSCRIPTION FACTORS;

ABSCISIC ACID; ARABIDOPSIS THALIANA; AUXIN; LATERAL ROOTS; OSMOTIC STRESS; WRKY46;

OSMOSIS;

ABSCISIC ACID; ARABIDOPSIS PROTEIN; INDOLEACETIC ACID DERIVATIVE; TRANSCRIPTION FACTOR; WRKY46 PROTEIN, ARABIDOPSIS;

ARABIDOPSIS; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; OSMOTIC PRESSURE; PLANT ROOT;

ABSCISIC ACID; ARABIDOPSIS; ARABIDOPSIS PROTEINS; GENE EXPRESSION REGULATION, PLANT; INDOLEACETIC ACIDS; OSMOTIC PRESSURE; PLANT ROOTS; TRANSCRIPTION FACTORS;

EID: 84942831639     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.12958     Document Type: Article

References (53)

1. Bartel, B., and, Fink, G.R., (1995) ILR1, an amidohydrolase that releases active indole-3-acetic acid from conjugates. Science, 268, 1745-1748.
2. Benkova, E., Michniewicz, M., Sauer, M., Teichmann, T., Seifertova, D., Jurgens, G., and, Friml, J., (2003) Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell, 115, 591-602.
3. Brady, S.M., Sarkar, S.F., Bonetta, D., and, McCourt, P., (2003) The ABSCISIC ACID INSENSITIVE 3 (ABI3) gene is modulated by farnesylation and is involved in auxin signaling and lateral root development in Arabidopsis. Plant J. 34, 67-75.
4. Casimiro, I., Marchant, A., Bhalerao, R.P., et al. (2001) Auxin transport promotes Arabidopsis lateral root initiation. Plant Cell, 13, 843-852.
5. Czechowski, T., Stitt, M., Altmann, T., Udvardi, M.K., and, Scheible, W.R., (2005) Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis. Plant Physiol. 139, 5-17.
6. De Smet, I., Signora, L., Beeckman, T., Inze, D., Foyer, C.H., and, Zhang, H., (2003) An abscisic acid-sensitive checkpoint in lateral root development of Arabidopsis. Plant J. 33, 543-555.
7. De Smet, I., Zhang, H., Inze, D., and, Beeckman, T., (2006) A novel role for abscisic acid emerges from underground. Trends Plant Sci. 11, 434-439.
8. De Smet, I., Tetsumura, T., De Rybel, B., et al. (2007) Auxin-dependent regulation of lateral root positioning in the basal meristem of Arabidopsis. Development, 134, 681-690.
9. De Smet, I., Vassileva, V., De Rybel, B., et al. (2008) Receptor-like kinase ACR4 restricts formative cell divisions in the Arabidopsis root. Science, 322, 594-597.
10. Deak, K.I., and, Malamy, J., (2005) Osmotic regulation of root system architecture. Plant J. 43, 17-28.
11. Devaiah, B.N., Karthikeyan, A.S., and, Raghothama, K.G., (2007) WRKY75 transcription factor is a modulator of phosphate acquisition and root development in Arabidopsis. Plant Physiol. 143, 1789-1801.
12. Ding, Z.J., Yan, J.Y., Xu, 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, 825-835.
13. Ding, Z.J., Yan, J.Y., Xu, X.Y., Yu, D.Q., Li, G.X., Zhang, S.Q., and, Zheng, S.J., (2014) Transcription factor WRKY46 regulates osmotic stress responses and stomatal movement independently in Arabidopsis. Plant J. 79, 13-27.
14. Duan, L., Dietrich, D., Ng, C.H., Chan, P.M.Y., Bhalerao, R., Bennett, M.J., and, Dinneny, J.R., (2013) Endodermal ABA signaling promotes lateral root quiescence during salt stress in Arabidopsis seedlings. Plant Cell, 25, 324-341.
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., Wang, M.L., Lynch, T.J., Rao, S., and, Goodman, H.M., (1998) The Arabidopsis abscisic acid response locus ABI4 encodes an APETALA2 domain protein. Plant Cell, 10, 1043-1054.
17. Fukaki, H., Tameda, S., Masuda, H., and, Tasaka, M., (2002) Lateral root formation is blocked by a gain-of-function mutation in the SOLITARY-ROOT/IAA14 gene of Arabidopsis. Plant J. 29, 153-168.
18. González-Guzmán, M., Apostolova, N., Bellés, J.M., Barrero, J.M., Piqueras, P., Ponce, M.R., Micol, J.L., Serrano, R., and, Rodríguez, P.L., (2002) The short-chain alcohol dehydrogenase ABA2 catalyzes the conversion of xanthoxin to abscisic aldehyde. Plant Cell, 14, 1833-1846.
19. Hu, Y.R., Dong, Q.Y., and, Yu, D.Q., (2012) Arabidopsis WRKY46 coordinates WRKY70 and WRKY53 in basal resistance against pathogen Pseudomonas syringae. Plant Sci., 185, 288-297.
20. Jackson, R.G., Lim, E.K., Li, Y., Kowalczyk, M., Sandberg, G., Hoggett, J., Ashford, D.A., and, Bowles, D.J., (2001) Identification and biochemical characterization of an Arabidopsis indole-3-acetic acid glucosyltransferase. J. Biol. Chem. 276, 4350-4356.
21. Jakubowska, A., and, Kowalczyk, S., (2005) A specific enzyme hydrolyzing 6-O(4-O)-indole-3-ylacetyl-β-d-glucose in immature kernels of Zea mays. J. Plant Physiol. 162, 207-213.
22. Jefferson, R.A., Kavanagh, T., and, Bevan, M.W., (1987) GUS fusions: β-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J. 6, 3901-3907.
23. Korasick, D.A., Enders, T.A., and, Strader, L.C., (2013) Auxin biosynthesis and storage forms. J. Exp. Bot. 64, 2541-2555.
24. Lavenus, J., Goh, T., Roberts, I., Guyomarc'h, S., Lucas, M., De Smet, I., Fukaki, H., Beeckman, T., Bennett, M., and, Laplaze, L., (2013) Lateral root development in Arabidopsis: fifty shades of auxin. Trends Plant Sci. 18, 450-458.
25. LeClere, S., Tellez, R., Rampey, R.A., Matsuda, S.P.T., and, Bartel, B., (2002) Characterization of a family of IAA-amino acid conjugate hydrolases from Arabidopsis. J. Biol. Chem. 277, 20446-20452.
26. Ljung, K., Hull, A.K., Celenza, J., Yamada, M., Estelle, M., Normanly, J., and, Sandberg, G., (2005) Sites and regulation of auxin biosynthesis in Arabidopsis roots. Plant Cell, 17, 1090-1104.
27. Lopez-Molina, L., Mongrand, S., and, Chua, N.H., (2001) A postgermination developmental arrest checkpoint is mediated by abscisic acid and requires the ABI5 transcription factor in Arabidopsis. Proc. Natl Acad. Sci. USA, 98, 4782-4787.
28. Ludwig-Müller, J., (2011) Auxin conjugates: their role for plant development and in the evolution of land plants. J. Exp. Bot. 62, 1757-1773.
29. Ludwig-Müller, J., Walz, A., Solvin, J.P., Epstein, E., Cohen, J.D., Dong, W., and, Town, C.D., (2005) Overexpression of Maize IAGLU in Arabidopsis thaliana alters plant growth and sensitivity to IAA but not IBA and 2, 4-D. J. Plant Growth Regul. 24, 127-141.
30. Malamy, J.E., and, Benfey, P.N., (1997) Organization and cell differentiation in lateral roots of Arabidopsis thaliana. Development, 124, 33-44.
31. Mallory, A.C., Bartel, D.P., and, Bartel, B., (2005) MicroRNA-directed regulation of Arabidopsis AUXIN RESPONSE FACTOR17 is essential for proper development and modulates expression of early auxin response genes. Plant Cell, 17, 1360-1375.
32. Moreno-Risueno, M.A., Van Norman, J.M., Moreno, A., Zhang, J., Ahnert, S.E., and, Benfey, P.N., (2010) Oscillating gene expression determines competence for periodic Arabidopsis root branching. Science, 329, 1306-1311.
33. Okushima, Y., Fukaki, H., Onoda, M., Theologis, A., and, Tasaka, M., (2007) ARF7 and ARF19 regulates lateral root formation via direct activation of LBD/ASL genes in Arabidopsis. Plant Cell, 19, 118-130.
34. Osakabe, Y., Arinaga, N., Umezawa, T., et al. (2013) Osmotic stress responses and plant growth controlled by potassium transporter in Arabidopsis. Plant Cell, 25, 609-624.
35. Östin, A., Kowalczyk, M., Bhalerao, R.P., and, Sandberg, G., (1998) Metabolism of indole-3-acetic acid in Arabidopsis. Plant Physiol. 118, 285-296.
36. Peret, B., De Rybel, B., Casimiro, I., Benkova, E., Swarup, R., Laplaze, L., Beeckman, T., and, Bennett, M.J., (2009) Arabidopsis lateral root development: an emerging story. Trends Plant Sci. 14, 399-408.
37. Peret, B., Li, G., Zhao, J., et al. (2012) Auxin regulates aquaporin function to facilitate lateral root emergence. Nat. Cell Biol. 14, 991-998.
38. Prinsen, E., Van Laer, S., and, Van Onckelen, H., (2000) Auxin analysis. In Methods in Molecular Biology, Vol. 141: Plant Hormone Protocols (, Tucker, G.A., and, Roberts, A., eds). Totowa, NJ, USA: Humana Press, pp. 49-65.
39. Rampey, R.A., LeClere, S., Kowalczyk, M., Ljung, K., Sandberg, G., and, Bartel, B., (2004) A family of auxin-conjugate hydrolases that contributes to free indole-3-acetic acid levels during Arabidopsis germination. Plant Physiol. 135, 978-988.
40. Rushton, P.J., Somssich, I.E., Ringler, P., and, Shen, Q.J., (2010) WRKY transcription factors. Trends Plant Sci. 15, 247-258.
41. Schmittgen, T.D., and, Livak, K.J., (2008) Analyzing real-time PCR data by the comparative C(T) method. Nat. Protoc. 3, 1101-1108.
42. Seo, P.J., Xiang, F., Qiao, M., Park, J., Lee, Y.N., Kim, S., Lee, Y., Park, W.J., and, Park, C., (2009) The MYB96 transcription factor mediates abscisic acid signaling during drought stress response in Arabidopsis. Plant Physiol. 151, 275-289.
43. Shkolnik-Inbar, D., and, Bar-Zvi, D., (2010) ABI4 mediates abscisic acid and cytokinin inhibition of lateral root formation by reducing polar auxin transport in Arabidopsis. Plant Cell, 22, 3560-3573.
44. Signora, L., De Smet, I., Foyer, C., and, Zhang, H., (2001) ABA plays a central role in mediating the regulatory effects of nitrate on root branching in Arabidopsis. Plant J. 28, 655-662.
45. Staswick, P.E., Serban, B., Rowe, M., Tiryaki, I., Maldonado, M.T., Maldonado, M.C., and, Suza, W., (2005) Characterization of an Arabidopsis enzyme family that conjugates amino acids to indole-3-acetic acid. Plant Cell, 17, 616-627.
46. Swarup, K., Benkova, E., Swarup, R., et al. (2008) The auxin influx carrier LAX3 promotes lateral root emergence. Nat. Cell Biol. 10, 946-954.
47. Szerszen, J.B., Szczyglowski, K., and, Bandurski, R.S., (1994) iaglu, a gene from Zea mays involved in conjugation of growth hormone indole-3-acetic acid. Science, 265, 1699-1701.
48. Tian, C., Muto, H., Higuchi, K., Matamura, T., Tatematsu, K., Koshiba, T., and, Yamamoto, K.T., (2004) Disruption and overexpression of auxin response factor 8 gene of Arabidopsis affect hypocotyl elongation and root growth habit, indicating its possible involvement in auxin homeostasis in light condition. Plant J. 40, 333-343.
49. Ulker, B., and, Somssich, I.E., (2004) WRKY transcription factors: from DNA binding towards biological function. Curr. Opin. Plant Biol. 7, 491-498.
50. Ulmasov, T., Murfett, J., Hagen, G., and, Guilfoyle, T.J., (1997) Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements. Plant Cell, 9, 1963-1971.
51. Vanneste, S., De Rybel, B., Beemster, G.T., et al. (2005) Cell cycle progression in the pericycle is not sufficient for SOLITARY ROOT/IAA14-mediated lateral root initiation in Arabidopsis thaliana. Plant Cell, 17, 3035-3050.
52. Vartanian, N., Marcotte, L., and, Giraudat, J., (1994) Drought rhizogenesis in Arabidopsis thaliana. Differential responses of hormonal mutants. Plant Physiol. 127, 899-909.
53. Westfall, C.S., Herrmann, J., Chen, Q., Wang, S., and, Jez, J.M., (2010) Modulation plant hormones by enzyme action: the GH3 family of acyl acid amido synthetases. Plant Signal. Behav. 5, 1607-1612.