Arabidopsis enhanced drought tolerance1/HOMEODOMAIN GLABROUS11 confers drought tolerance in transgenic rice without yield penalty

Plant Physiology

Volumn 162, Issue 3, 2013, Pages 1378-1391

  Yu, Linhui ^a   Chen, Xi ^a   Wang, Zhen ^a   Wang, Shimei ^b,d   Wang, Yuping ^c   Zhu, Qisheng ^b,d   Li, Shigui ^c   Xiang, Chengbin ^a  

^a UNIVERSITY OF SCIENCE AND TECHNOLOGY OF CHINA   (China)

^b ANHUI AGRICULTURAL UNIVERSITY   (China)

^c SICHUAN AGRICULTURAL UNIVERSITY   (China)

^d RICE RESEARCH INSTITUTE   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA; ORYZA SATIVA;

EID: 84879731194     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.113.217596     Document Type: Article

References (94)

1. Abebe T, Guenzi AC, Martin B, Cushman JC (2003) Tolerance of mannitolaccumulating transgenic wheat to water stress and salinity. Plant Physiol 131: 1748-1755.
2. Agrawal GK, Jwa NS, Shibato J, Han O, Iwahashi H, Rakwal R (2003) Diverse environmental cues transiently regulate OsOPR1 of the "octadecanoid pathway" revealing its importance in rice defense/stress and development. Biochem Biophys Res Commun 310: 1073-1082.
3. Bao JY, Lee SG, Chen C, Zhang XQ, Zhang Y, Liu SQ, Clark T, Wang J, Cao ML, Yang HM, et al (2005) Serial analysis of gene expression study of a hybrid rice strain (LYP9) and its parental cultivars. Plant Physiol 138: 1216-1231.
4. Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39: 205-207.
5. Boonburapong B, Buaboocha T (2007) Genome-wide identification and analyses of the rice calmodulin and related potential calcium sensor proteins. BMC Plant Biol 7: 4.
6. Boyer JS (1982) Plant productivity and environment. Science 218: 443-448.
7. Cattivelli L, Rizza F, Badeck FW, Mazzucotelli E, Mastrangelo AM, Francia E, Mare C, Tondelli A, Stanca AM (2008) Drought tolerance improvement in crop plants: an integrated view from breeding to genomics. Field Crops Res 105: 1-14.
8. Chen JQ, Meng XP, Zhang Y, Xia M, Wang XP (2008) Over-expression of OsDREB genes lead to enhanced drought tolerance in rice. Biotechnol Lett 30: 2191-2198.
9. Chen Y, Yuan LP, Wang XH, Zhang DY, Chen J, Deng QY, Zhao BR, Xu DQ (2007) Relationship between grain yield and leaf photosynthetic rate in super hybrid rice. Zhi Wu Sheng Li Yu Fen Zi Sheng Wu Xue Xue Bao 33: 235-243.
10. Comstock JP (2002) Hydraulic and chemical signalling in the control of stomatal conductance and transpiration. J Exp Bot 53: 195-200.
11. Cui M, Zhang W, Zhang Q, Xu Z, Zhu Z, Duan F, Wu R (2011) Induced over-expression of the transcription factor OsDREB2A improves drought tolerance in rice. Plant Physiol Biochem 49: 1384-1391.
12. Desikan R, Cheung MK, Bright J, Henson D, Hancock JT, Neill SJ (2004) ABA, hydrogen peroxide and nitric oxide signalling in stomatal guard cells. J Exp Bot 55: 205-212.
13. Diédhiou CJ, Popova OV, Dietz KJ, Golldack D (2008) The SNF1-type serine-threonine protein kinase SAPK4 regulates stress-responsive gene expression in rice. BMC Plant Biol 8: 49.
14. Doheny-Adams T, Hunt L, Franks PJ, Beerling DJ, Gray JE (2012) Genetic manipulation of stomatal density influences stomatal size, plant growth and tolerance to restricted water supply across a growth carbon dioxide gradient. Philos Trans R Soc Lond B Biol Sci 367: 547-555.
15. Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28: 350-356.
16. 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: 751-763.
17. Ehleringer JR, Hall AE, Farquhar GD (1993) Stable Isotope and Plant Water Relations, Ed 1. Academic Press, San Diego
18. Ekanayake IJ, Otoole JC, Garrity DP, Masajo TM (1985) Inheritance of root characters and their relations to drought resistance in rice. Crop Sci 25: 927-933.
19. Frattini M, Morello L, Breviario D (1999) Rice calcium-dependent protein kinase isoforms OsCDPK2 and OsCDPK11 show different responses to light and different expression patterns during seed development. Plant Mol Biol 41: 753-764.
20. Gao T, Wu Y, Zhang Y, Liu L, Ning Y, Wang D, Tong H, Chen S, Chu C, Xie Q (2011) OsSDIR1 overexpression greatly improves drought tolerance in transgenic rice. Plant Mol Biol 76: 145-156.
21. Giri J, Vij S, Dansana PK, Tyagi AK (2011) Rice A20/AN1 zinc-finger containing stress-associated proteins (SAP1/11) and a receptor-like cytoplasmic kinase (OsRLCK253) interact via A20 zinc-finger and confer abiotic stress tolerance in transgenic Arabidopsis plants. New Phytol 191: 721-732.
22. Hetherington AM, Woodward FI (2003) The role of stomata in sensing and driving environmental change. Nature 424: 901-908.
23. Hiei Y, Ohta S, Komari T, Kumashiro T (1994) Efficient transformation of rice (Oryza sativa L.) mediated by Agrobacterium and sequence analysis of the boundaries of the T-DNA. Plant J 6: 271-282.
24. Hien DT, Jacobs M, Angenon G, Hermans C, Thu TT, Van Son L, Roosens NH (2003) Proline accumulation and D1-pyrroline-5-carboxylate synthetase gene properties in three rice cultivars differing in salinity and drought tolerance. Plant Sci 165: 1059-1068.
25. Hodges DM, Forney CF (2000) The effects of ethylene, depressed oxygen and elevated carbon dioxide on antioxidant profiles of senescing spinach leaves. J Exp Bot 51: 645-655.
26. Holmstrom KO, Mantyla E, Welin B, Mandal A, Palva ET (1996) Drought tolerance in tobacco. Nature 379: 683-684.
27. HongBo S, ZongSuo L, MingAn S (2005) Changes of anti-oxidative enzymes and MDA content under soil water deficits among 10 wheat (Triticum aestivum L.) genotypes at maturation stage. Colloids Surf B Biointerfaces 45: 7-13.
28. 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: 6410-6415.
29. Hsieh TH, Lee JT, Charng YY, Chan MT (2002) Tomato plants ectopically expressing Arabidopsis CBF1 show enhanced resistance to water deficit stress. Plant Physiol 130: 618-626.
30. Hu HH, Dai MQ, Yao JL, Xiao BZ, Li XH, Zhang QF, Xiong LZ (2006) Overexpressing a NAM, ATAF, and CUC (NAC) transcription factor enhances drought resistance and salt tolerance in rice. Proc Natl Acad Sci USA 103: 12987-12992.
31. Hu HH, You J, Fang YJ, Zhu XY, Qi ZY, Xiong LZ (2008) Characterization of transcription factor gene SNAC2 conferring cold and salt tolerance in rice. Plant Mol Biol 67: 169-181.
32. Huang DW, Sherman BT, Lempicki RA (2008) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4: 44-57.
33. Huang W, Sherman BT, Lempicki RA (2009a) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4: 44-57.
34. Huang XY, Chao DY, Gao JP, Zhu MZ, Shi M, Lin HX (2009b) A previously unknown zinc finger protein, DST, regulates drought and salt tolerance in rice via stomatal aperture control. Genes Dev 23: 1805-1817.
35. Hwang SG, Chen HC, Huang WY, Chu YC, Shii CT, Cheng WH (2010) Ectopic expression of rice OsNCED3 in Arabidopsis increases ABA level and alters leaf morphology. Plant Sci 178: 12-22.
36. Jefferies CJ (1977) Sequential staining to assess viability and starch content in individual pollen grains. Stain Technol 52: 277-283.
37. Jeong JS, Kim YS, Baek KH, Jung H, Ha SH, Do Choi Y, Kim M, Reuzeau C, Kim JK (2010) Root-specific expression of OsNAC10 improves drought tolerance and grain yield in rice under field drought conditions. Plant Physiol 153: 185-197.
38. Kasuga M, Liu Q, Miura S, Yamaguchi-Shinozaki K, Shinozaki K (1999) Improving plant drought, salt, and freezing tolerance by gene transfer of a single stress-inducible transcription factor. Nat Biotechnol 17: 287-291.
39. Kavar T, Maras M, Kidric M, Sustar-Vozlic J, Meglic V (2008) Identification of genes involved in the response of leaves of Phaseolus vulgaris to drought stress. Mol Breed 21: 159-172.
40. Kim TH, Böhmer M, Hu HH, Nishimura N, Schroeder JI (2010) Guard cell signal transduction network: advances in understanding abscisic acid, CO2, and Ca2+ signaling. Annu Rev Plant Biol 61: 561-591.
41. Kliebenstein DJ, Monde RA, Last RL (1998) Superoxide dismutase in Arabidopsis: an eclectic enzyme family with disparate regulation and protein localization. Plant Physiol 118: 637-650.
42. Kreps JA, Wu YJ, Chang HS, Zhu T, Wang X, Harper JF (2002) Transcriptome changes for Arabidopsis in response to salt, osmotic, and cold stress. Plant Physiol 130: 2129-2141.
43. Lake JA, Woodward FI (2008) Response of stomatal numbers to CO2 and humidity: control by transpiration rate and abscisic acid. New Phytol 179: 397-404.
44. Lei ZY, Zhao P, Cao MJ, Cui R, Chen X, Xiong LZ, Zhang QF, Oliver DJ, Xiang CB (2007) High-throughput binary vectors for plant gene function analysis. Journal of Integrative Plant Biol 49: 556-567.
45. Li X, Qian Q, Fu Z, Wang Y, Xiong G, Zeng D, Wang X, Liu X, Teng S, Hiroshi F, et al (2003) Control of tillering in rice. Nature 422: 618-621.
46. López-Bucio J, Cruz-Ramírez A, Herrera-Estrella L (2003) The role of nutrient availability in regulating root architecture. Curr Opin Plant Biol 6: 280-287.
47. Lynch J (1995) Root architecture and plant productivity. Plant Physiol 109: 7-13.
48. Mahmood A, Alam K, Salam A, Iqbal S (1991) Effect of flag leaf removal on grain-yield, its components and quality of hexaploid wheat. Cereal Res Commun 19: 305-310.
49. Makino A (2011) Photosynthesis, grain yield, and nitrogen utilization in rice and wheat. Plant Physiol 155: 125-129.
50. Masle J, Farquhar GD (1988) Effects of soil strength on the relation of water-use efficiency and growth to carbon isotope discrimination in wheat seedlings. Plant Physiol 86: 32-38.
51. Masle J, Gilmore SR, Farquhar GD (2005) The ERECTA gene regulates plant transpiration efficiency in Arabidopsis. Nature 436: 866-870.
52. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5: 621-628.
53. Mundy J, Chua NH (1988) Abscisic acid and water-stress induce the expression of a novel rice gene. EMBO J 7: 2279-2286.
54. Nakamura M, Katsumata H, Abe M, Yabe N, Komeda Y, Yamamoto KT, Takahashi T (2006) Characterization of the class IV homeodomain- Leucine Zipper gene family in Arabidopsis. Plant Physiol 141: 1363-1375.
55. Nakashima K, Tran L-SP, Van Nguyen D, Fujita M, Maruyama K, Todaka D, Ito Y, Hayashi N, Shinozaki K, Yamaguchi-Shinozaki K (2007) Functional analysis of a NAC-type transcription factor OsNAC6 involved in abiotic and biotic stress-responsive gene expression in rice. Plant J 51: 617-630.
56. Nelson DE, Repetti PP, Adams TR, Creelman RA, Wu J, Warner DC, Anstrom DC, Bensen RJ, Castiglioni PP, Donnarummo MG, et al (2007) Plant nuclear factor Y (NF-Y) B subunits confer drought tolerance and lead to improved corn yields on water-limited acres. Proc Natl Acad Sci USA 104: 16450-16455.
57. Oh SJ, Kim YS, Kwon CW, Park HK, Jeong JS, Kim JK (2009) Overexpression of the transcription factor AP37 in rice improves grain yield under drought conditions. Plant Physiol 150: 1368-1379.
58. Ouyang S-Q, Liu Y-F, Liu P, Lei G, He S-J, Ma B, Zhang W-K, Zhang J-S, Chen S-Y (2010) Receptor-like kinase OsSIK1 improves drought and salt stress tolerance in rice (Oryza sativa) plants. Plant J 62: 316-329.
59. Park S, Li JS, Pittman JK, Berkowitz GA, Yang HB, Undurraga S, Morris J, Hirschi KD, Gaxiola RA (2005) Up-regulation of a H+-pyrophosphatase (H+-PPase) as a strategy to engineer drought-resistant crop plants. Proc Natl Acad Sci USA 102: 18830-18835.
60. Peña-Castro JM, van Zanten M, Lee SC, Patel MR, Voesenek LAJC, Fukao T, Bailey-Serres J (2011) Expression of rice SUB1A and SUB1C transcription factors in Arabidopsis uncovers flowering inhibition as a submergence tolerance mechanism. Plant J 67: 434-446.
61. Price AH, Tomos AD, Virk DS (1997) Genetic dissection of root growth in rice (Oryza sativa L). I. A hydrophonic screen. Theor Appl Genet 95: 132-142.
62. Price AH, Tomos AD (1997) Genetic dissection of root growth in rice (Oryza sativa L). II. Mapping quantitative trait loci using molecular markers. Theor Appl Genet 95: 143-152.
63. Priyanka B, Sekhar K, Reddy VD, Rao KV (2010) Expression of pigeonpea hybrid-proline-rich protein encoding gene (CcHyPRP) in yeast and Arabidopsis affords multiple abiotic stress tolerance. Plant Biotechnol J 8: 76-87.
64. Ray S, Mondal WA, Choudhuri MA (1983) Regulation of leaf senescence, grain-filling and yield of rice by kinetin and abscisic acid. Physiol Plant 59: 343-346.
65. Robinson D (1994) The responses of plants to non-uniform supplies of nutrients. New Phytologist 127: 635-674.
66. Rockstrom J, Falkenmark M (2000) Semiarid crop production from a hydrological perspective: gap between potential and actual yields. Crit Rev Plant Sci 19: 319-346.
67. Romualdi C, Bortoluzzi S, D'Alessi F, Danieli GA (2003) IDEG6: a web tool for detection of differentially expressed genes in multiple tag sampling experiments. Physiol Genomics 12: 159-162.
68. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular Cloning: A Laboratory Manual, Ed 2. Cold Spring Harbor, New York
69. Schachtman DP, Goodger JQD (2008) Chemical root to shoot signaling under drought. Trends Plant Sci 13: 281-287.
70. Schachtman DP, Shin R (2007) Nutrient sensing and signaling: NPKS. Annu Rev Plant Biol 58: 47-69.
71. Schroeder JI, Kwak JM, Allen GJ (2001) Guard cell abscisic acid signalling and engineering drought hardiness in plants. Nature 410: 327-330.
72. Seki M, Narusaka M, Ishida J, Nanjo T, Fujita M, Oono Y, Kamiya A, Nakajima M, Enju A, Sakurai T, et al (2002) Monitoring the expression profiles of 7000. Arabidopsis genes under drought, cold and high-salinity stresses using a full-length cDNA microarray. Plant J 31: 279-292.
73. Serraj R, Kumar A, McNally KL, Slamet-Loedin I, Bruskiewich R, Mauleon R, Cairns J, Hijmans RJ (2009) Improvement of drought resistance in rice. Adv Agron 103: 41-99.
74. Shimazaki K, Doi M, Assmann SM, Kinoshita T (2007) Light regulation of stomatal movement. Annu Rev Plant Biol 58: 219-247.
75. Song GS, Zhai HL, Peng YG, Zhang L, Wei G, Chen XY, Xiao YG, Wang LL, Chen YJ, Wu B, et al (2010) Comparative transcriptional profiling and preliminary study on heterosis mechanism of super-hybrid rice. Mol Plant 3: 1012-1025.
76. Taiz L, Zeiger E (2010) Plant Physiology, Ed 5. Sinauer Associates, Sunderland, MA
77. Takasaki H, Maruyama K, Kidokoro S, Ito Y, Fujita Y, Shinozaki K, Yamaguchi-Shinozaki K, Nakashima K (2010) The abiotic stressresponsive NAC-type transcription factor OsNAC5 regulates stressinducible genes and stress tolerance in rice. Mol Genet Genomics 284: 173-183.
78. Todaka D, Nakashima K, Shinozaki K, Yamaguchi-Shinozaki K (2012) Toward understanding transcriptional regulatory networks in abiotic stress responses and tolerance in rice. Rice 5: 6.
79. Umezawa T, Fujita M, Fujita Y, Yamaguchi-Shinozaki K, Shinozaki K (2006) Engineering drought tolerance in plants: discovering and tailoring genes to unlock the future. Curr Opin Biotechnol 17: 113-122.
80. Verslues PE, Agarwal M, Katiyar-Agarwal S, Zhu J, Zhu JK (2006) Methods and concepts in quantifying resistance to drought, salt and freezing, abiotic stresses that affect plant water status. Plant J 45: 523-539.
81. Wang C, Zhang Q, Shou HX (2009) Identification and expression analysis of OsHsfs in rice. J Zhejiang Univ Sci B 10: 291-300.
82. Wang Y, Chen X, Xiang CB (2007) Stomatal density and bio-water saving. J Integr Plant Biol 49: 1435-1444.
83. Wei G, Tao Y, Liu GZ, Chen C, Luo RY, Xia HA, Gan Q, Zeng HP, Lu ZK, Han YN, et al (2009) A transcriptomic analysis of superhybrid rice LYP9 and its parents. Proc Natl Acad Sci USA 106: 7695-7701.
84. Werner T, Nehnevajova E, Köllmer I, Novák O, Strnad M, Krämer U, Schmülling T (2010) Root-specific reduction of cytokinin causes enhanced root growth, drought tolerance, and leaf mineral enrichment in Arabidopsis and tobacco. Plant Cell 22: 3905-3920.
85. Xiang Y, Tang N, Du H, Ye H, Xiong L (2008) Characterization of Osb- ZIP23 as a key player of the basic leucine zipper transcription factor family for conferring abscisic acid sensitivity and salinity and drought tolerance in rice. Plant Physiol 148: 1938-1952.
86. Xiao BZ, Huang YM, Tang N, Xiong LZ (2007) Over-expression of a LEA gene in rice improves drought resistance under the field conditions. Theor Appl Genet 115: 35-46.
87. Xie Z, Zhang ZL, Zou XL, Yang GX, Komatsu S, Shen QJ (2006) Interactions of two abscisic-acid induced WRKY genes in repressing gibberellin signaling in aleurone cells. Plant J 46: 231-242.
88. Yamaguchi-Shinozaki K, Shinozaki K (2006) Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu Rev Plant Biol 57: 781-803.
89. Yang A, Dai XY, Zhang WH (2012) A R2R3-type MYB gene, OsMYB2, is involved in salt, cold, and dehydration tolerance in rice. J Exp Bot 63: 2541-2556.
90. Yang J, Zhang J, Wang Z, Zhu Q, Wang W (2001) Hormonal changes in the grains of rice subjected to water stress during grain filling. Plant Physiol 127: 315-323.
91. Yang SJ, Vanderbeld B, Wan JX, Huang YF (2010) Narrowing down the targets: towards successful genetic engineering of drought-tolerant crops. Mol Plant 3: 469-490.
92. Yoshida S, Forno DA, Lock JH, Gomez KA (1976) A Laboratory Manual for the Physiological Studies of Rice. International Rice Research Institute, Manila, Philippines, pp 69-72.
93. Yu H, Chen X, Hong YY, Wang Y, Xu P, Ke SD, Liu HY, Zhu JK, Oliver DJ, Xiang CB (2008) Activated expression of an Arabidopsis HD-START protein confers drought tolerance with improved root system and reduced stomatal density. Plant Cell 20: 1134-1151.
94. Zou J, Liu CF, Liu AL, Zou D, Chen XB (2012) Overexpression of OsHsp17.0 and OsHsp23.7 enhances drought and salt tolerance in rice. J Plant Physiol 169: 628-635