A maize phytochrome-interacting factor 3 improves drought and salt stress tolerance in rice

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• 作者：Yong Gao (1) (2)
  Wei Jiang (1) (2)
  Yi Dai (1) (2)
  Ning Xiao (1) (2)
  Changquan Zhang (2)
  Hua Li (1) (2)
  Yi Lu (1) (2)
  Meiqin Wu (1) (2)
  Xiaoyi Tao (1) (2)
  Dexiang Deng (2)
  Jianmin Chen (1) (2)
  
  1. College of Bioscience and Biotechnology ; Yangzhou University ; 88 South University Ave ; Yangzhou ; 225009 ; Jiangsu ; People鈥檚 Republic of China
  2. Jiangsu Key Laboratories of Crop Genetics and Physiology and Plant Functional Genomics of the Ministry of Education ; Yangzhou University ; Yangzhou ; 225009 ; Jiangsu ; People鈥檚 Republic of China
  
• 关键词：Abiotic stress tolerance ; Expression pattern ; Morphological character ; Physiological trait ; Transcription factor ; Zea mays
• 刊名：Plant Molecular Biology
• 出版年：2015
• 出版时间：March 2015
• 年：2015
• 卷：87
• 期：4-5
• 页码：413-428
• 全文大小：10,090 KB
• 参考文献：1. Achard, P, Genschik, P (2009) Releasing the brakes of plant growth: how GAs shutdown DELLA proteins. J Exp Bot 60: pp. 1085-1092 CrossRef
  2. Achard, P, Cheng, H, Grauwe, L, Decat, J, Schoutteten, H, Moritz, T, Straeten, D, Peng, JR, Harberd, NP (2006) Integration of plant responses to environmentally activated phytohormonal signals. Science 311: pp. 91-94 CrossRef
  3. Achard, P, Gong, F, Cheminant, S, Alioua, M, Hedden, P, Genschik, P (2008) The cold-inducible CBF1 factor-dependent signaling pathway modulates the accumulation of the growth-repressing DELLA proteins via its effect on gibberellin metabolism. Plant Cell 20: pp. 2117-2129 CrossRef
  4. Al-Sady, B, Ni, WM, Kircher, S, Schafer, E, Quail, PH (2006) Photoactivated phytochrome induces rapid PIF3 phosphorylation prior to proteasome-mediated degradation. Mol Cell 23: pp. 439-446 CrossRef
  5. Al-Sady, B, Kikis, EA, Monte, E, Quail, PH (2008) Mechanistic duality of transcription factor function in phytochrome signaling. Proc Natl Acad Sci USA 105: pp. 2232-2237 CrossRef
  6. Ashraf, M, Ahmad, S (2000) Influence of sodium chloride on ion accumulation, yield components and fibre characteristics in salt-tolerant and salt-sensitive lines of cotton (Gossypium hirsutum L.). Field Crop Res 66: pp. 115-127 CrossRef
  7. Bai, MY, Shang, JX, Oh, E, Fan, M, Bai, Y, Zentella, R, Sun, TP, Wang, ZY (2012) Brassinosteroid, gibberellin and phytochrome impinge on a common transcription module in Arabidopsis. Nat Cell Biol 14: pp. 810-817 CrossRef
  8. Bartels, D, Sunkar, R (2005) Drought and salt tolerance in plants. Crit Rev Plant Sci 24: pp. 23-58 CrossRef
  9. Buchanan, CD, Klein, PE, Mullet, JE (2004) Phylogenetic analysis of 5鈥?noncoding regions from the ABA-responsive rab16/17 gene family of sorghum, maize and rice provides insight into the composition, organization and function of cis-regulatory modules. Genetics 168: pp. 1639-1654 CrossRef
  10. Campo, S, Peris-Peris, C, Montesinos, L, Penas, G, Messeguer, J, Segundo, BS (2012) Expression of the maize ZmGF14-6 gene in rice confers tolerance to drought stress while enhancing susceptibility to pathogen infection. J Exp Bot 63: pp. 983-999 CrossRef
  11. Chen, DQ, Xu, G, Tang, WJ, Jing, YJ, Ji, Q, Fei, ZJ, Lin, RC (2013) Antagonistic basic helix-loop-helix/bZIP transcription factors form transcriptional modules that integrate light and reactive oxygen species signaling in Arabidopsis. Plant Cell 25: pp. 1657-1673 CrossRef
  12. Lucas, M, Prat, S (2014) PIFs get BRright: phytochrome interacting factors as integrators of light and hormonal signals. New Phytol 202: pp. 1126-1141 CrossRef
  13. Lucas, M, Daviere, JM, Rodriguez-Falcon, M, Pontin, M, Iglesias-Pedraz, JM, Lorrain, S, Fankhauser, C, Blazquez, MA, Titarenko, E, Prat, S (2008) A molecular framework for light and gibberellin control of cell elongation. Nature 451: pp. 480-484 CrossRef
  14. Dhanda, SS, Sethi, GS (1998) Inheritance of excised-leaf water loss and relative water content in bread wheat (Triticum aestivum). Euphytica 104: pp. 39-47 CrossRef
  15. Dubouzet, JG, Sakuma, Y, Ito, Y, Kasuga, M, Dubouzet, EG, Miura, S, Seki, M, Shinozaki, K, Yamaguchi-Shinozaki, K (2003) OsDREB genes in rice, Oryza sativa L., encode transcription activators that function in drought-, high-salt- and cold-responsive gene expression. Plant J 33: pp. 751-763 CrossRef
  16. Fairchild, CD, Schumaker, MA, Quail, PH (2000) HFR1 encodes an atypical bHLH protein that acts in phytochrome A signal transduction. Genes Dev 14: pp. 2377-2391
  17. Feng, SH, Martinez, C, Gusmaroli, G (2008) Coordinated regulation of Arabidopsis thaliana development by light and gibberellins. Nature 451: pp. 475-479 CrossRef
  18. Flowers, TJ, Colmer, TD (2008) Salinity tolerance in halophytes. New Phytol 179: pp. 945-963 CrossRef
  19. Franca, MGC, Thi, ATP, Pimentel, C, Rossiello, ROP, Zuily, FY, Laffray, D (2000) Differences in growth and water relations among Phaseolus vulgaris cultivars in response to induced drought stress. Environ Exp Bot 43: pp. 227-237 CrossRef
  20. Franklin, KA, Lee, SH, Patel, D (2011) Phytochrome-interacting factor 4 (PIF4) regulates auxin biosynthesis at high temperature. Proc Natl Acad Sci USA 108: pp. 20231-20235 CrossRef
  21. Hornitschek, P, Kohnen, MV, Lorrain, S (2012) Phytochrome interacting factors 4 and 5 control seedling growth in changing light conditions by directly controlling auxin signaling. Plant J 71: pp. 699-711 CrossRef
  22. Hou, X, Xie, K, Yao, J, Qi, Z, Xiong, L (2009) A homolog of human skiinteracting protein in rice positively regulates cell viability and stress tolerance. Proc Natl Acad Sci USA 106: pp. 6410-6415 CrossRef
  23. Jaedicke, K, Lichtenthaler, AL, Meyberg, R, Zeidler, M, Hughes, J (2012) A phytochrome鈥損hototropin light signaling complex at the plasma membrane. Proc Natl Acad Sci USA 109: pp. 12231-12236 CrossRef
  24. Keller, MM, Jaillais, Y, Pedmale, UV, Moreno, JE, Chory, J, Ballare, CL (2011) Cryptochrome 1 and phytochrome B control shade-avoidance responses in Arabidopsis via partially independent hormonal cascades. Plant J 67: pp. 195-207 CrossRef
  25. Khanna, R, Huq, E, Kikis, EA, Al-Sady, B, Lanzatella, C, Quail, PH (2004) A novel molecular recognition motif necessary for targeting photoactivated phytochrome signaling to specific basic helix-loop-helix transcription factors. Plant Cell 16: pp. 3033-3044 CrossRef
  26. Kim, JY, Yi, HK, Choi, G, Shin, B, Song, PS, Choi, GS (2003) Functional characterization of phytochrome-interacting factor 3 in phytochrome-mediated light signal transduction. Plant Cell 15: pp. 2399-2407 CrossRef
  27. Kim, DH, Yamaguchi, S, Lim, S, Oh, E, Park, J, Hanada, A, Kamiya, Y, Choi, G (2008) SOMNUS, a CCCH-type zinc finger protein in Arabidopsis, negatively regulates light-dependent seed germination downstream of PIL5. Plant Cell 20: pp. 1260-1277 CrossRef
  28. Koini, MA, Alvey, L, Allen, T, Tilley, CA, Harberd, NP, Whitelam, GC, Franklin, KA (2009) High temperature-mediated adaptations in plant architecture require the bHLH transcription factor PIF4. Curr Biol 19: pp. 408-413 CrossRef
  29. Krause, G, Weis, E (1991) Chlorophyll fluorescence and photosynthesis: the basics. Annu Rev Plant Biol 42: pp. 313-349 CrossRef
  30. Leivar, P, Quail, PH (2011) PIFs: pivotal components in a cellular signaling hub. Trends Plant Sci 16: pp. 19-28 CrossRef
  31. Leivar, P, Monte, E, Al-Sady, B, Carle, C, Storer, A, Alonso, JM, Ecker, JR, Quail, PH (2008) The Arabidopsis phytochrome-interacting factor PIF7, together with PIF3 and PIF4, regulates responses to prolonged red light by modulating phyB levels. Plant Cell 20: pp. 337-352 CrossRef
  32. Leivar, P, Tepperman, JM, Monte, E, Calderon, RH, Liu, TL, Quail, PH (2009) Definition of early transcriptional circuitry involved in light-induced reversal of PIF-imposed repression of photomorphogenesis in young Arabidopsis seedlings. Plant Cell 21: pp. 3535-3553 CrossRef
  33. Li, H, Gao, Y, Xu, H, Dai, Y, Deng, DQ, Chen, JM (2013) ZmWRKY33, a WRKY maize transcription factor conferring enhanced salt stress tolerances in Arabidopsis. Plant Growth Regul 70: pp. 207-216 CrossRef
  34. Livak, KJ, Schmittgen, TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2鈭捨斘擟T method. Methods 25: pp. 402-408 CrossRef
  35. Lorrain, S, Allen, T, Duek, PD, Whitelam, GC, Fankhauser, C (2008) Phytochrome-mediated inhibition of shade avoidance involves degradation of growth-promoting bHLH transcription factors. Plant J 53: pp. 312-323 CrossRef
  36. Lorrain, S, Trevisan, M, Pradervand, S, Fankhauser, C (2009) Phytochrome interacting factors 4 and 5 redundantly limit seedling de-etiolation in continuous far-red light. Plant J 60: pp. 449-461 CrossRef
  37. Ludwig, AA, Romeis, T, Jones, JDG (2004) CDPK-mediated signalling pathways: specificity and cross-talk. J Exp Bot 55: pp. 181-188 CrossRef
  38. Monte, E, Tepperman, JM, Al-Sady, B, Kaczorowski, KA, Alonso, JM, Ecker, JR, Li, X, Zhang, YL, Quail, PH (2004) The phytochrome-interacting transcription factor, PIF3, acts early, selectively, and positively and light-induced chloroplast development. Proc Natl Acad Sci USA 101: pp. 16091-16098 CrossRef
  39. Mukherjee, K, Choudhury, AR, Gupta, B, Gupta, S, Sengupta, DN (2006) An ABRE-binding factor, OsBZ8, is highly expressed in salt tolerant cultivars than in salt sensitive cultivars of indica rice. BMC Plant Biol 6: pp. 18 CrossRef
  40. Munns, R (2002) Comparative physiology of salt and water stress. Plant, Cell Environ 25: pp. 239-250 CrossRef
  41. Munns, R, Tester, M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59: pp. 651-681 CrossRef
  42. Nakagawa, H, Ohmiya, K, Hattori, T (1996) A rice bZIP protein, designated OSBZ8, is rapidly induced by abscisic acid. Plant J 9: pp. 217-227 CrossRef
  43. Navarro, L, Bari, R, Achard, P, Lison, P, Nemri, A, Harberd, NP, Jones, JDG (2008) DELLAs control plant immune responses by modulating the balance of jasmonic acid and salicylic acid signaling. Curr Biol 18: pp. 650-655 CrossRef
  44. Ni, M, Tepperman, JM, Quail, PH (1999) Binding of phytochrome B to its nuclear signaling partner PIF3 is reversibly induced by light. Nature 400: pp. 781-784 CrossRef
  45. Nozue, K, Maloof, JN (2006) Diurnal regulation of plant growth. Plant, Cell Environ 29: pp. 396-408 CrossRef
  46. Nylander, M, Svensson, J, Palva, ET, Welin, BV (2001) Stress induced accumulation and tissue-specific localization of dehydrins in Arabidopsis thaliana. Plant Mol Biol 45: pp. 263-279 CrossRef
  47. Oh, E, Yamaguchi, S, Hu, JH, Yusuke, J, Jung, B, Paik, I, Lee, HS, Sun, TP, Kamiya, Y, Choi, G (2007) PIL5, a phytochrome-interacting bHLH protein, regulates gibberellin responsiveness by binding directly to the GAI and RGA promoters in Arabidopsis seeds. Plant Cell 19: pp. 1192-1208 CrossRef
  48. Oh, E, Kang, H, Yamaguchi, S, Park, J, Lee, D, Kamiya, Y, Choi, G (2009) Genome-wide analysis of genes targeted by phytochrome interacting factor 3-like5 during seed germination in Arabidopsis. Plant Cell 21: pp. 403-419 CrossRef
  49. Park, E, Kim, J, Lee, Y, Shin, J, Oh, E, Chung, WI, Liu, JR, Choi, G (2004) Degradation of phytochrome interacting factor 3 in phytochrome-mediated light signaling. Plant Cell Physiol 45: pp. 968-975 CrossRef
  50. Qin, F, Kakimoto, M, Sakuma, Y, Maruyama, K, Osakabe, Y, Tran, LS, Shinozaki, K, Yamaguchi-Shinozaki, K (2007) Regulation and functional analysis of ZmDREB2A in response to drought and heat stresses in Zea mays L. Plant J 50: pp. 54-69 CrossRef
  51. Rabbani, MA, Maruyama, K, Abe, H, Khan, MA, Katsura, K, Ito, Y, Yoshiwara, K, Seki, M, Shinozaki, K, Yamaguchi-Shinozaki, K (2003) Monitoring expression profiles of rice genes under cold, drought, and high-salinity stresses and abscisic acid application using cDNA microarray and RNA gel-blot analyses. Plant Physiol 133: pp. 1755-1767 CrossRef
  52. Sakuma, Y, Maruyama, K, Osakabe, Y, Qin, F, Seki, M, Shinozaki, K, Yamaguchi-Shinozaki, K (2006) Functional analysis of an Arabidopsis transcription factor, DREB2A, involved in droughtresponsive gene expression. Plant Cell 18: pp. 1292-1309 CrossRef
  53. Schafer, E, Nagy, F (2006) Photomorphogenesis in plants and bacteria: function and signal transduction mechanisms. Springer, Dordrecht CrossRef
  54. Schonfeld, MA, Johnson, RC, Carver, BF (1988) Water relations in winter wheat as drought resistance indicator. Crop Sci 28: pp. 526-531 CrossRef
  55. Shen, H, Zhu, L, Castillon, A, Majee, M, Downie, B, Huq, E (2008) Light-induced phosphorylation and degradation of the negative regulator phytochrome-interacting factor1 from Arabidopsis depend upon its direct physical interactions with photoactivated phytochromes. Plant Cell 20: pp. 1586-1602 CrossRef
  56. Shimizu-Sato, S, Huq, E, Tepperman, JM, Quail, PH (2002) A light-switchable gene promoter system. Nat Biotechnol 20: pp. 1041-1044 CrossRef
  57. Song, S, Chen, Y, Zhao, M, Zhang, WH (2012) A novel Medicago truncatula HD-Zip gene, MtHB2, is involved in abiotic stress responses. Environ Exp Bot 80: pp. 1-9 CrossRef
  58. Spartz, AK, Gray, WM (2008) Plant hormone receptors: new perceptions. Genes Dev 22: pp. 2139-2148 CrossRef
  59. Stavang, JA, Gallego-Bartolome, J, Gomez, MD, Yoshida, S, Asami, T, Olsen, JE, Garcia-Martinez, JL, Alabadi, D, Blazquez, MA (2009) Hormonal regulation of temperature-induced growth in Arabidopsis. Plant J 60: pp. 589-601 CrossRef
  60. Strasser, RJ, Srivastava, A, Tsimilli-Michae, MI The fluorescence transient as a tool to characterize and screen photosynthetic samples. In: Mohanty, P, Yunus, U, Pathre, M eds. (2002) Probing photosynthesis: mechanism, regulation and adaptation. Taylor and Francis, London, pp. 443-480
  61. Su, J, Wu, R (2004) Stress-inducible synthesis of proline in transgenic rice confers faster growth under stress conditions than that with constitutive synthesis. Plant Sci 166: pp. 941-948 CrossRef
  62. Sun, JQ, Qi, LL, Li, YN, Chu, JF, Li, CY (2012) PIF4-mediated activation of YUCCA8 expression integrates temperature into the auxin pathway in regulating Arabidopsis hypocotyl growth. PLoS Genet 8: pp. e1002594 CrossRef
  63. Tian, SJ, Mao, XG, Zhang, HY, Chen, SS, Zhai, CC, Yang, SM, Jing, RL (2013) Cloning and characterization of TaSnRK2.3, a novel SnRK2 gene in common wheat. J Exp Bot 64: pp. 2063-2080 CrossRef
  64. Toledo-Ortiz, G, Huq, E, Quail, PH (2003) The Arabidopsis basic/helix-loop-helix transcription factor family. Plant Cell 15: pp. 1749-1770 CrossRef
  65. Xu, ML, Jiang, JF, Ge, L, Xu, YY, Chen, H, Zhao, Y, Bi, YR, Wen, JQ, Chong, K (2005) FPF1 transgene leads to altered flowering time and root development in rice. Plant Cell Rep 24: pp. 79-85 CrossRef
  66. Xue, T, Wang, D, Zhang, S, Ehlting, J (2008) Genome-wide and expression analysis of protein phosphatase 2C in rice and Arabidopsis. BMC Genom 9: pp. 1-21 CrossRef
  67. Yi, N, Kim, Y, Jeong, MH, Oh, SJ, Jeong, J, Park, SH, Jung, H, Choi, Y, Kim, JK (2010) Functional analysis of six drought-inducible promoters in transgenic rice plants throughout all stages of plant growth. Planta 232: pp. 743-754 CrossRef
  68. Zhang, HY, Mao, XG, Jing, RL, Chang, XP, Xie, HM (2011) Characterization of a common wheat (Triticum aestivum L.) TaSnRK2.7 gene involved in abiotic stress responses. J Exp Bot 62: pp. 975-988 CrossRef
  69. Zorb, C, Schmitt, S, Neeb, A, Karl, S, Linder, M, Schubert, S (2004) The biochemical reaction of maize (Zea mays L.) to salt stress is characterized by a mitigation of symptoms and not by a specific adaptation. Plant Sci 167: pp. 91-100 CrossRef
  
• 刊物类别：Biomedical and Life Sciences
• 刊物主题：Life Sciences
  Plant Sciences
  Biochemistry
  Plant Pathology
  
• 出版者：Springer Netherlands
• ISSN：1573-5028

文摘

Phytochrome-interacting factor 3 (PIF3) activates light-responsive transcriptional network genes in coordination with the circadian clock and plant hormones to modulate plant growth and development. However, little is known of the roles PIF3 plays in the responses to abiotic stresses. In this study, the cloning and functional characterization of the ZmPIF3 gene encoding a maize PIF3 protein is reported. Subcellular localization revealed the presence of ZmPIF3 in the cell nucleus. Expression patterns revealed that ZmPIF3 is expressed strongly in leaves. This expression responds to polyethylene glycol, NaCl stress, and abscisic acid application, but not to cold stress. ZmPIF3 under the control of the ubiquitin promoter was introduced into rice. No difference in growth and development between ZmPIF3 transgenic and wild-type plants was observed under normal growth conditions. However, ZmPIF3 transgenic plants were more tolerant to dehydration and salt stresses. ZmPIF3 transgenic plants had increased relative water content, chlorophyll content, and chlorophyll fluorescence, as well as significantly enhanced cell membrane stability under stress conditions. The over-expression of ZmPIF3 increased the expression of stress-responsive genes, such as Rab16D, DREB2A, OSE2, PP2C, Rab21, BZ8 and P5CS, as detected by real-time PCR analysis. Taken together, these results improve our understanding of the role ZmPIF3 plays in abiotic stresses signaling pathways; our findings also indicate that ZmPIF3 regulates the plant response to drought and salt stresses.