CaPUB1, a hot pepper U-box E3 ubiquitin ligase, confers enhanced cold stress tolerance and decreased drought stress tolerance in transgenic rice (Oryza sativa L.)

Molecules and Cells

Volumn 39, Issue 3, 2016, Pages 250-257

  Min, Hye Jo ^a   Jung, Ye Jin ^a   Kang, Bin Goo ^b   Kim, Woo Taek ^a  

^a Yonsei University   (South Korea)

^b Korea Institute of Science and Technology Information (KISTI)   (South Korea)

Author keywords

Cold stress; Cross talk in stress response; Drought stress; Transgenic rice (Oryza sativa) plants; U box E3 Ub ligase

Indexed keywords

CAPSICUM ANNUUM PUTATIVE U BOX PROTEIN 1; CHLOROPHYLL A; CHLOROPHYLL B; CYTOCHROME P450; DREB1A PROTEIN; DREB1B PROTEIN; DREB1C PROTEIN; ELECTROLYTE; HYGROMYCIN; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; VEGETABLE PROTEIN; PLANT PROTEIN; UBIQUITIN PROTEIN LIGASE;

ARABIDOPSIS; ARTICLE; CALLUS (PLANT); CAPSICUM ANNUUM; CHLOROPHYLL CONTENT; COLD STRESS; COLD TOLERANCE; COLD TREATMENT; CONDUCTANCE; CONTROLLED STUDY; DEHYDRATION; DROUGHT STRESS; DROUGHT TOLERANCE; ENVIRONMENTAL STRESS; GENE OVEREXPRESSION; MONOCOT; NONHUMAN; PHENOTYPE; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; RICE; SOUTHERN BLOTTING; SURVIVAL RATE; TRANSGENIC CROP; UPREGULATION; COLD; DROUGHT; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; ORYZA; PEPPER; PHYSIOLOGICAL STRESS; TRANSGENIC PLANT;

CAPSICUM; COLD TEMPERATURE; DROUGHTS; GENE EXPRESSION REGULATION, PLANT; ORYZA; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED; STRESS, PHYSIOLOGICAL; UBIQUITIN-PROTEIN LIGASE COMPLEXES;

EID: 84964977657     PISSN: 10168478     EISSN: 02191032     Source Type: Journal    
DOI: 10.14348/molcells.2016.2290     Document Type: Article

References (39)

1. Agarwal, P.K., Agarwal, P., Reddy, M., and Sopory, S.K. (2006). Role of DREB transcription factors in abiotic and biotic stress tolerance in plants. Plant Cell Rep. 25, 1263-1274
2. Benjamin, J.G., and Nielsen, D.C. (2006). Water deficit effects on root distribution of soybean, field pea and chickpea. Field Crops Res. 97, 248-253
3. Bergler, J., and Hoth, S. (2011). Plant U-box armadillo repeat proteins AtPUB18 and AtPUB19 are involved in salt inhibition of germination in Arabidopsis. Plant Biol. (Stuttg) 13, 725-730
4. Byun, M.Y., Lee, J., Cui, L.H., Kang, Y., Oh, T.K., P, H., Lee, H., and Kim, W.T. (2015). Constitutive expression of DaCBF7, an Antarctic vascular plant, Deschampsia antarctica CBF homolog, resulted in improved cold tolerance in transgenic rice plants. Plant Science 236, 61-74
5. Cho, S.K., Chung, H.S., Ryu, M.Y., Park, M.J., Lee, M.M., Bahk, Y.Y., Kim, J., Pai, H.S., and Kim, W.T. (2006). Heterologous expression and molecular and cellular characterization of CaPUB1 encoding a hot pepper U-Box E3 ubiquitin ligase homolog. Plant Physiol. 142, 1664-1682
6. Cho, S.K., Ryu, M.Y., Song, C., Kwak, J.M., and Kim, W.T. (2008). Arabidopsis PUB22 and PUB23 are homologous U-Box E3 ubiquitin ligases that play combinatory roles in response to drought stress. Plant Cell 20, 1899-1914
7. Cho, S.K., Ryu, M.Y., Seo, D.H., Kang, B.G., and Kim, W.T. (2011). The Arabidopsis RING E3 ubiquitin ligase AtAIRP2 plays combinatory roles with AtAIRP1 in abscisic acid-mediated drought stress responses. Plant physiol. 157, 2240-2257
8. Dubouzet, J.G., Sakuma, Y., Ito, Y., Kasuga, M., Dubouzet, E.G., Miura, S., Seki, M., Shinozaki, K., and Yamaguchi-Shinozaki, K. (2003). OsDREB genes in rice, Oryza sativa L., encode transcription activators that function in drought-, high-salt-and coldresponsive gene expression. Plant J. 33, 751-763
9. Gilmour, S.J., Sebolt, A.M., Salazar, M.P., Everard, J.D., and Thomashow, M.F. (2000). Over-expression of the Arabidopsis CBF3 transcriptional activator mimics multiple biochemical changes associated with cold acclimation. Plant Physiol. 124, 1854-1865
10. Han, M., Kim, C.-Y., Lee, J., Lee, S.-K., and Jeon, J.-S. (2014). OsWRKY42 represses OsMT1d and induces reactive oxygen species and leaf senescence in rice. Mol. Cells 37, 532-539
11. Ito, Y., Katsura, K., Maruyama, K., Taji, T., Kobayashi, M., Seki, M., Shinozaki, K., and Yamaguchi-Shinozaki, K. (2006). Functional analysis of rice DREB1/CBF-type transcription factors involved in cold-responsive gene expression in transgenic rice. Plant Cell Physiol. 47, 141-153
12. Kim, S.I., and Tai, T.H. (2011). Evaluation of seedling cold tolerance in rice cultivars: a comparison of visual ratings and quantitative indicators of physiological changes. Euphytica 178, 437-447
13. Kim, S.J., and Kim, W.T. (2013). Suppression of Arabidopsis RING E3 ubiquitin ligase AtATL78 increases tolerance to cold stress and decreases tolerance to drought stress. FEBS Lett. 587, 2584-2590
14. Lee, J-H., and Kim, W.T. (2011). Regulation of abiotic stress signal transduction by E3 ubiquitin ligases in Arabidopsis. Mol. Cells 31, 201-208
15. Lichtenthaler, H.K. (1987). Chlorophylls and carotenoids: Pigments of photosynthetic biomembranes. Methods Enzymol. 148, 350-382
16. Liu, F., Xu, W., Wei, Q., Zhang, Z., Xing, Z., Tan, L., Di, C., Yao, D., Wang, C., Tan, Y., et al. (2010). Gene expression profiles deciphering rice phenotypic variation between Nipponbare (Japonica) and 93-11 (Indica) during oxidative stress. PLoS One 5, e8632
17. Liu, Y.C., Wu, Y.R., Huang, X.H., Sun, J., and Xie, Q. (2011). AtPUB19, a U-box E3 ubiquitin ligase, negatively regulates abscisic acid and drought responses in Arabidopsis thaliana. Mol. Plant 4, 938-946
18. Lyzenga, W.J., and Stone, S.L. (2012). Abiotic stress tolerance mediated by protein ubiquitination. J. Exp. Bot. 63, 599-616
19. Mackill, D.J., and Lei, X. (1997). Genetic variation for traits related to temperature adaptation of rice cultivars. Crop Sci. 37, 1340-1346
20. Park, J.J., Yi, J., Yoon, J., Cho, L.H., Ping, J., Jeong, H.J., Cho, S.K., Kim, W.T., and An, G. (2011). OsPUB15, an E3 ubiquitin ligase, functions to reduce cellular oxidative stress during seedling es tablishment. Plant J. 65, 194-205
21. Praba, M.L., Cairns, J.E., Babu, R.C., and Lafitte, H.R. (2009). Identification of physiological traits underlying cultivar differences in drought tolerance in rice and wheat. J. Agron. Crop Sci. 195, 30-46
22. Seo, D.H., Ryu, M.Y., Jammes, F., Hwang, J.H., Turek, M., Kang, B.G., Kwak, J.M., and Kim, W.T. (2012). Roles of four Arabidopsis U-box E3 ubiquitin ligases in negative regulation of abscisic acid-mediated drought stress responses. Plant Physiol. 160, 556-568
23. Shaw, C.H. (1995). Introduction of cloning plasmids into Agrobacterium tumefaciens. In Plant gene transfer and expression protocols, Springer New York, 49, 33-37
24. Shen, C., Li, D., He, R., Fang, Z., Xia, Y., Gao, J., Shen, H., and Cao, M. (2014). Comparative transcriptome analysis of RNAseq data for cold-tolerant and cold-sensitive rice genotypes under cold stress. J. Plant Biol. 56, 337-348
25. Shinozaki, K., and Yamaguchi-Shinozaki, K. (2000). Molecular responses to dehydration and low temperature: differences and cross-talk between two stress signaling pathways. Curr. Opin. Plant Biol. 3, 217-223
26. Stegmann, M., Anderson, R.G., Ichimura, K., Pecenkova, T., Reuter, P., Žárský, V., McDowell, J.M., Shirasu, K., and Trujillo, M. (2012). The ubiquitin ligase PUB22 targets a subunit of the exocyst complex required for PAMP-triggered responses in Arabidopsis. Plant Cell 24, 4703-4716
27. Su, C.F., Wang, Y.C., Hsieh, T.H., Tseng, T.H., Lu, C.A., Tseng, T.H., and Yu, S.M. (2010). A novel MYBS3-dependent pathway confers cold tolerance in rice. Plant Physiol. 153, 145-158
28. Thomashow, M.F. (2010). Molecular basis of plant cold acclimation: insights gained from studying the CBF cold response pathway. Plant Physiol. 154, 571-577
29. Tripathi, R.D., Tripathi, P., Dwivedi, S., Dubey, S., Chatterjee, S., Chakrabarty, D., and Trivedi, P.K. (2012). Arsenomics: omics of arsenic metabolism in plants. Front. Physiol. 3, 275
30. Trujillo, M., Ichimura, K., Casais, C., and Shirasu, K. (2008). Negative regulation of PAMP-triggered immunity by an E3 ubiquitin ligase triplet in Arabidopsis. Curr. Biol. 18, 1396-1401
31. Vierstra, R.D. (2009). The ubiquitin-26S proteasome system at the nexus of plant biology. Nat. Rev. Mol. Cell. Biol. 110, 385-397
32. Wang, Q., Guan, Y., Wu, Y., Chen, H., Chen, F., and Chu, C. (2008). Overexpression of a rice OsDREB1F gene increases salt, drought, and low temperature tolerance in both Arabidopsis and rice. Plant Mol. Biol. 67, 589-602
33. Wang, C., Wei, Q., Zhang, K., Wang, L., Liu, F., Zhao, L., Tan, Y., Di, C., Yan, H., Yu, J., et al. (2013). Down-regulation of OsSPX1 causes high sensitivity to cold and oxidative stresses in rice seedlings. PLoS One 8, e81849
34. Xu, M., Li, L., Fan, Y., Wan, J., and Wang, L. (2011). ZmCBF3 overexpression improves tolerance to abiotic stress in transgenic rice (Oryza sativa) without yield penalty. Plant Cell Rep. 30, 1949-1957
35. Yang, C.W., González-Lamothe, R., Ewan, R.A., Rowland, O., Yoshioka, H., Shenton, M., Ye, H., O'Donnell, E., Jones, J.D., and Sadanandom, A. (2006). The E3 ubiquitin ligase activity of Arabidopsis PLANT U-BOX17 and its functional tobacco homolog ACRE276 are required for cell death and defense. Plant Cell 18, 1084-1098
36. Yee, D., and Goring, D.R. (2009). The diversity of plant U-box E3 ubiquitin ligases: from upstream activators to downstream target substrates. J. Exp. Bot. 60, 1109-1121
37. Zeng, L.R., Qu, S., Bordeos, A., Yang, C., Baraoidan, M., Yan, H., Xie, Q., Nahm, B.H., Leung, H., and Wang, G.L. (2004). Spotted leaf11, a negative regulator of plant cell death and defense, encodes a U-box/armadillo repeat protein endowed with E3 ubiquitin ligase activity. Plant Cell 16, 2795-2808
38. Zeng, D-E., Hou, P., Xiao, F., and Liu, Y. (2014). Overexpressing a novel RING-H2 finger protein gene, OsRHP1, enhances drought and salt tolerance in rice (Oryza sativa L.). J. Plant Biol. 57, 357-365
39. Zhang, Q., Jiang, N., Wang, G.L., Hong, Y., and Wang, Z. (2013). Advances in understanding cold sensing and the coldresponsive network in rice. Adv. Crop Sci. Tech. 1, 104