An Arabidopsis homolog of importin β1 is required for ABA response and drought tolerance

Plant Journal

Volumn 75, Issue 3, 2013, Pages 377-389

  Luo, Yanjie ^a,b,c   Wang, Zhijuan ^a   Ji, Hongtao ^a   Fang, Hui ^c,d   Wang, Shuangfeng ^a   Tian, Lining ^c,d   Li, Xia ^a  

^a INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c AGRICULTURE AND AGRI FOOD CANADA   (Canada)

^d UNIVERSITY OF WESTERN ONTARIO   (Canada)

Author keywords

ABA response; Arabidopsis thaliana; drought resistance; Importin 1; nuclear importin; nuclear proteins

Indexed keywords

ABA RESPONSE; ARABIDOPSIS THALIANA; DROUGHT RESISTANCE; NUCLEAR IMPORTIN; NUCLEAR PROTEINS;

AGRONOMY; CYTOLOGY; DROUGHT; GENE EXPRESSION; SEED;

PROTEINS;

ARABIDOPSIS; ARABIDOPSIS THALIANA;

ABI1 PROTEIN, ARABIDOPSIS; ABI2 PROTEIN, ARABIDOPSIS; ABI5 PROTEIN, ARABIDOPSIS; ABSCISIC ACID; ARABIDOPSIS PROTEIN; BASIC LEUCINE ZIPPER TRANSCRIPTION FACTOR; CATION TRANSPORT PROTEIN; KARYOPHERIN BETA; KPNB1 PROTEIN, ARABIDOPSIS; KPNB1 PROTEIN, HUMAN; NUCLEAR PROTEIN; PHOSPHOPROTEIN PHOSPHATASE; RAN1 PROTEIN, ARABIDOPSIS;

ABA RESPONSE; ARABIDOPSIS; ARABIDOPSIS THALIANA; ARTICLE; CELL NUCLEUS; CYTOPLASM; DROUGHT; DROUGHT RESISTANCE; DRUG EFFECT; EPISTASIS; GENE EXPRESSION REGULATION; GENETICS; GERMINATION; GROWTH, DEVELOPMENT AND AGING; IMPORTIN Β1; METABOLISM; MUTATION; NUCLEAR IMPORTIN; OSMOTIC PRESSURE; PHYSIOLOGICAL STRESS; PHYSIOLOGY; PLANT SEED; PLANT STOMA; TRANSGENIC PLANT;

ABA RESPONSE; ARABIDOPSIS THALIANA; DROUGHT RESISTANCE; IMPORTIN Β1; NUCLEAR IMPORTIN; NUCLEAR PROTEINS;

ABSCISIC ACID; ARABIDOPSIS; ARABIDOPSIS PROTEINS; BASIC-LEUCINE ZIPPER TRANSCRIPTION FACTORS; BETA KARYOPHERINS; CATION TRANSPORT PROTEINS; CELL NUCLEUS; CYTOPLASM; DROUGHTS; EPISTASIS, GENETIC; GENE EXPRESSION REGULATION, PLANT; GERMINATION; MUTATION; OSMOTIC PRESSURE; PHOSPHOPROTEIN PHOSPHATASES; PLANT STOMATA; PLANTS, GENETICALLY MODIFIED; SEEDS; STRESS, PHYSIOLOGICAL;

EID: 84880781422     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.12207     Document Type: Article

References (50)

1. Antoni, R., Rodriguez, L., Gonzalez-Guzman, M., Pizzio, G.A., and, Rodriguez, P.L., (2011) News on ABA transport, protein degradation, and ABFs/WRKYs in ABA signaling. Curr. Opin. Plant Biol. 14, 547-553.
2. Bartels, S., Besteiro, M.A.G., Lang, D., and, Ulm, R., (2010) Emerging functions for plant MAP kinase phosphatases. Trends Plant Sci. 15, 322-329.
3. Bollman, K.M., Aukerman, M.J., Park, M.Y., Hunter, C., Berardini, T.Z., and, Poethig, R.S., (2003) HASTY, the Arabidopsis ortholog of exportin 5/MSN5, regulates phase change and morphogenesis. Development, 130, 1493-1504.
4. Conti, E., Muller, C.W., and, Stewart, M., (2006) Karyopherin flexibility in nucleocytoplasmic transport. Curr. Opin. Struct. Biol. 16, 237-244.
5. Cutler, S.R., Rodriguez, P.L., Finkelstein, R.R., and, Abrams, S.R., (2010) Abscisic acid: emergence of a core signaling network. Annu. Rev. Plant Biol. 61, 651-679.
6. Ek-Ramos, M.J., Avila, J., Cheng, C., Martin, G.B., and, Devarenne, T.P., (2010) The T-loop extension of the tomato protein kinase AvrPto-dependent Pto-interacting protein 3 (Adi3) directs nuclear localization for suppression of plant cell death. J. Biol. Chem. 285, 17584-17594.
7. Frey, S., and, Görlich, D., (2007) A saturated FG-repeat hydrogel can reproduce the permeability properties of nuclear pore complexes. Cell, 130, 512-523.
8. Frieman, M., Yount, B., Heise, M., Kopecky-Bromberg, S.A., Palese, P., and, Baric, R.S., (2007) Severe acute respiratory syndrome coronavirus ORF6 antagonizes STAT1 function by sequestering nuclear import factors on the rough endoplasmic reticulum/Golgi membrane. J. Virol. 81, 9812-9824.
9. 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.
10. Goldfarb, D.S., Corbett, A.H., Mason, D.A., Harreman, M.T., and, Adam, S.A., (2004) Importin α: a multipurpose nuclear-transport receptor. Trends Cell Biol. 14, 505-514.
11. Haasen, D., Kohler, C., Neuhaus, G., and, Merkle, T., (1999) Nuclear export of proteins in plants: AtXPO1 is the export receptor for leucine-rich nuclear export signals in Arabidopsis thaliana. Plant J. 20, 695-705.
12. Hill, C.S., (2009) Nucleocytoplasmic shuttling of Smad proteins. Cell Res. 19, 36-46.
13. Hirayama, T., and, Shinozaki, K., (2007) Perception and transduction of abscisic acid signals: keys to the function of the versatile plant hormone ABA. Trends Plant Sci. 12, 343-351.
14. Hubbard, K.E., Nishimura, N., Hitomi, K., Getzoff, E.D., and, Schroeder, J.I., (2010) Early abscisic acid signal transduction mechanisms: newly discovered components and newly emerging questions. Genes Dev. 24, 1695-1708.
15. Hugouvieux, V., Kwak, J.M., and, Schroeder, J.I., (2001) An mRNA cap binding protein, ABH1, modulates early abscisic acid signal transduction in Arabidopsis. Cell, 106, 477-487.
16. Jäkel, S., and, Görlich, D., (1998) Importin β, transportin, RanBP5 and RanBP7 mediate nuclear import of ribosomal proteins in mammalian cells. EMBO J. 17, 4491-4502.
17. Kaiserli, E., and, Jenkins, G.I., (2007) UV-B promotes rapid nuclear translocation of the Arabidopsis UV-B-specific signaling component UVR8 and activates its function in the nucleus. Plant Cell, 19, 2662-2673.
18. Karimi, M., Depicker, A., and, Hilson, P., (2007) Recombinational cloning with plant gateway vectors. Plant Physiol. 145, 1144-1154.
19. Kim, S.Y., (2006) The role of ABF family bZIP class transcription factors in stress response. Physiol. Plant. 126, 519-527.
20. Kinoshita, N., Berr, A., Belin, C., Chappuis, R., Nishizawa, N.K., and, Lopez-Molina, L., (2010) Identification of growth insensitive to ABA3 (gia3), a recessive mutation affecting ABA signaling for the control of early post-germination growth in Arabidopsis thaliana. Plant Cell Physiol. 51, 239-251.
21. Kuromori, T., Miyaji, T., Yabuuchi, H., Shimizu, H., Sugimoto, E., Kamiya, A., Moriyama, Y., and, Shinozaki, K., (2010) ABC transporter AtABCG25 is involved in abscisic acid transport and responses. Proc. Natl Acad. Sci. USA 107, 2361-2366.
22. Leng, Y., Cao, C., Ren, J., Huang, L., Chen, D., Ito, M., and, Kufe, D., (2007) Nuclear import of the MUC1-C oncoprotein is mediated by nucleoporin Nup62. J. Biol. Chem. 282, 19321-19330.
23. Li, J., and, Chen, X., (2003) PAUSED, a putative exportin-t, acts pleiotropically in Arabidopsis development but is dispensable for viability. Plant Physiol. 132, 1913-1924.
24. Liu, H., and, Stone, S.L., (2010) Abscisic acid increases Arabidopsis ABI5 transcription factor levels by promoting KEG E3 ligase self-ubiquitination and proteasomal degradation. Plant Cell, 22, 2630-2641.
25. Liu, X., Yu, C.W., Duan, J., Luo, M., Wang, K., Tian, G., Cui, Y., and, Wu, K., (2012) HDA6 directly interacts with DNA methyltransferase MET1 and maintains transposable element silencing in Arabidopsis. Plant Physiol. 158, 119-129.
26. Lo, H., and, Hung, M., (2006) Nuclear EGFR signalling network in cancers: linking EGFR pathway to cell cycle progression, nitric oxide pathway and patient survival. Br. J. Cancer 94, 184-188.
27. Lopez, M.L., Mongrand, S., McLachlin, D.T., Chait, B.T., and, Chua, N.H., (2002) ABI5 acts downstream of ABI3 to execute an ABA dependent growth arrest during germination. Plant J. 32, 317-328.
28. Lott, K., Bhardwaj, A., Mitrousis, G., Pante, N., and, Cingolani, G., (2010) The importin β binding domain modulates the avidity of importin β for the nuclear pore complex. J. Biol. Chem. 285, 13769-13780.
29. Lu, Q., Tang, X., Tian, G., et al. (2010) Arabidopsis homolog of the yeast TREX2 mRNA export complex: components and anchoring nucleoporin. Plant J. 61, 259-270.
30. Merkle, T., (2003) Nucleo-cytoplasmic partitioning of proteins in plants: implications for the regulation of environmental and developmental signalling. Curr. Genet. 44, 231-260.
31. Merkle, T., (2009) Nuclear export of proteins and RNA. In Functional Organization of the Plant Nucleus (, Meier, I., and, Robinson, D.G., eds). Berlin/Heidelberg: Springer, pp. 55-77.
32. Merlot, S., Gosti, F., Guerrier, D., Vavasseur, A., and, Giraudat, J., (2001) The ABI1 and ABI2 protein phosphatases 2C act in a negative feedback regulatory loop of the abscisic acid signalling pathway. Plant J. 25, 295-303.
33. Miura, K., Lee, J., Jin, J.B., Yoo, C.Y., Miura, T., and, Hasegawa, P.M., (2009) Sumoylation of ABI5 by the Arabidopsis SUMO E3 ligase SIZ1 negatively regulates abscisic acid signaling. Proc. Natl Acad. Sci. USA 106, 5418-5423.
34. Moes, D., Himmelbach, A., Korte, A., Haberer, G., and, Grill, E., (2008) Nuclear localization of the mutant protein phosphatase abi1 is required for insensitivity towards ABA responses in Arabidopsis. Plant J. 54, 806-819.
35. Ren, X., Chen, Z., Liu, Y., Zhang, H., Zhang, M., Liu, Q., Hong, X., Zhu, J.K., and, Gong, Z., (2010) ABO3, a WRKY transcription factor, mediates plant responses to abscisic acid and drought tolerance in Arabidopsis. Plant J. 63, 417-429.
36. Saez, A., Robert, N., Maktabi, M.H., Schroeder, J.I., Serrano, R., and, Rodriguez, P.L., (2006) Enhancement of abscisic acid sensitivity and reduction of water consumption in Arabidopsis by combined inactivation of the protein phosphatases type 2C ABI1 and HAB1. Plant Physiol. 141, 1389-1399.
37. Saez, A., Rodrigues, A., Santiago, J., Rubio, S., and, Rodriguez, P.L., (2008) HAB1-SWI3B interaction reveals a link between abscisic acid signaling and putative SWI/SNF chromatin-remodeling complexes in Arabidopsis. Plant Cell, 20, 2972-2988.
38. Sheffield, J., and, Wood, E.F., (2008) Projected changes in drought occurrence under future global warming from multi-model, multi-scenario, IPCC AR4 simulations. Clim. Dyn. 31, 79-105.
39. Sparkes, I.A., Runions, J., Kearns, A., and, Hawes, C., (2006) Rapid, transient expression of fluorescent fusion proteins in tobacco plants and generation of stably transformed plants. Nat. Protoc. 1, 2019-2025.
40. Ström, A.C., and, Weis, K., (2001) Importin-β-like nuclear transport receptors. Genome Biol. 2, 3008.1-3008.9.
41. Takizawa, C.G., Weis, K., and, Morgan, D.O., (1999) Ran-independent nuclear import of cyclin B1-Cdc2 by importin β. Proc. Natl Acad. Sci. USA 96, 7938-7943.
42. Umezawa, T., Nakashima, K., Miyakawa, T., Kuromori, T., Tanokura, M., Shinozaki, K., and, Yamaguchi-Shinozaki, K., (2010) Molecular basis of the core regulatory network in ABA responses: sensing, signaling and transport. Plant Cell Physiol. 51, 1821-1839.
43. Verslues, P.E., Guo, Y., Dong, C.H., Ma, W., and, Zhu, J.K., (2006) Mutation of SAD2, an importin β-domain protein in Arabidopsis, alters abscisic acid sensitivity. Plant J. 47, 776-787.
44. Wang, W., Ye, R., Xin, Y., Fang, X., Li, C., Shi, H., Zhou, X., and, Qi, Y., (2011) An importin β protein negatively regulates microRNA activity in Arabidopsis. Plant Cell, 23, 3565-3576.
45. Wu, F.H., Shen, S.C., Lee, L.Y., Lee, S.H., Chan, M.T., and, Lin, C.S., (2009) Tape-Arabidopsis sandwich-a simpler Arabidopsis protoplast isolation method. Plant Methods 5, 16.
46. Xu, S., Zhang, Z., Jing, B., Gannon, P., Ding, J., Xu, F., Li, X., and, Zhang, Y., (2011) Transportin-SR is required for proper splicing of Resistance genes and plant immunity. PLoS Genet. 7, e1002159.
47. Yang, W., and, Musser, S.M., (2006) Nuclear import time and transport efficiency depend on importin β concentration. J. Cell Biol. 174, 951-961.
48. Zhang, X., Henriques, R., Lin, S.S., Niu, Q.W., and, Chua, N.H., (2006) Agrobacterium-mediated transformation of Arabidopsis thaliana using the floral-dip method. Nat. Protoc. 1, 641-646.
49. Zhao, Y., Wang, T., Zhang, W., and, Li, X., (2011) SOS3 mediates lateral root development under low salt stress through regulation of auxin redistribution and maxima in Arabidopsis. New Phytol. 189, 112-1134.
50. Zheng, Y., Schumaker, K.S., and, Guo, Y., (2012) Sumoylation of transcription factor MYB30 by the small ubiquitin-like modifier E3 ligase SIZ1 mediates abscisic acid response in Arabidopsis thaliana. Proc. Natl Acad. Sci. USA 109, 12822-12827. Agriculture