Abstract
Os2H16, a rice gene of unknown function, has been previously reported to be upregulated in response to infection by Xanthomonas oryzae pv. oryzae. In this study, expression patterns of Os2H16 were analyzed, demonstrating that expression of Os2H16 was dramatically induced by both bacterial and fungal infection as well as by drought stress, but repressed by salt treatment. To further investigate the role of Os2H16 in plant defense responses to abiotic and biotic stresses, transgenic lines of rice were developed. In comparison with wild-type rice, transgenic lines overexpressing Os2H16 show enhanced tolerance to bacterial blight and sheath blight disease, respectively caused by Xanthomonas oryzae pv. oryzae and Rhizoctonia solani. On the contrary, Os2H16 knockdown lines were more susceptible to both pathogens. Consistent with their individual phenotypes, upon inoculation, the expression of defense-related marker genes were elevated in Os2H16 overexpression individuals than in wild-type, while they were significantly reduced in Os2H16 knockdown lines. We also show that Os2H16 overexpression lines display enhanced tolerance to drought stress and elevated induction of drought-related genes, compared to wild-type rice. Os2H16 knockdown lines were more sensitive to drought stress and exhibited reduced induction of drought-related genes. Our study provides the first functional characterization of the rice Os2H16 gene, and suggests that Os2H16 positively modulate plant defense to abiotic and biotic stress.
Similar content being viewed by others
References
Anderson JP, Badruzsaufari E, Schenk PM, Manners JM, Desmond OJ, Ehlert C, Maclean DJ, Ebert PR, Kazan K (2004) Antagonistic interaction between abscisic acid and jasmonate-ethylene signaling pathways modulates defense gene expression and disease resistance in Arabidopsis. Plant Cell 16:3460–3479
Banniza S, Holderness M (2001) Major fungal diseases of rice: recent advances. Kluwer, Norwell
Campo S, Peris CP, 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 63:983–999
Chandler PM, Robertson M (1994) Gene expression regulated by abscisic acid and its relation to stress tolerance. Annu Rev Plant Physiol Plant Mol Biol 45:113–141
Channamallikarjuna V, Sonah H, Prasad M, Rao G, Chand S, Upreti H, Singh N, Sharma T (2010) Identification of major quantitative trait loci qSBR11-1 for sheath blight resistance in rice. Mol Breed 25:155–166
Chern M, Fitzgerald HA, Canlas PE, Navarre DA, Ronald P (2005) Overexpression of a rice NPR1 homolog leads to constitutive activation of defense response and hypersensitivity to light. Mol Plant-Microbe Interact 18:511–520
Cheung MY, Zeng NY, Tong SW, Li WY, Xue Y, Zhao KJ, Wang CL, Zhang Q, Fu Y, Sun Z, Sun SSM, Lam HM (2008) Constitutive expression of a rice GTPase-activating protein induces defense responses. New Phytol 179:530–545
Chini A, Grant JJ, Seki M, Shinozaki K, Loake GJ (2004) Drought tolerance established by enhanced expression of the CC-NB-LRR genes, ADR1, requires salicylic acid, EDS1 and ABI1. Plant J 38:810–822
Chu Z, Ouyang Y, Zhang J, Yang H, Wang S (2004) Genome-wide analysis of defense-responsive genes in bacterial blight resistance of rice mediated by the recessive R gene xa13. Mol Gen Genomics 271:111–120
Datta K, Velazhahan R, Oliva N, Ona I, Mew T, Khush GS, Muthukrishnan S, Datta SK (1999) Over-expression of the cloned rice thaumatin-like protein (PR-5) gene in transgenic rice plants enhances environmental friendly resistance to Rhizoctonia solani causing sheath blight disease. Theor Appl Genet 98:1138–1145
Datta K, Tu JM, Oliva N, Ona I, Velazhahan R, Mew TW, Muthukrishnan S, Datta SK (2001) Enhanced resistance to sheath blight by constitutive expression of infection-related rice chitinase in transgenic elite indica rice cultivar. Plant Sci 160:405–414
Deng HQ, Liu HB, Li XH, Xiao JH, Wang SP (2012) A CCCH-type zinc finger nucleic acid-binding protein quantitatively confers resistance against rice bacterial blight disease. Plant Physiol 158:876–889
Ding XH, Cao YL, Huang LL, Zhao J, Xu CG, Li XH, Wang SP (2008) Activation of the indole-3-acetic acid-amido synthetase GH3-8 suppresses expansin expression and promotes salicylate- and jasmonate-independent basal immunity in rice. Plant Cell 20:228–240
Du H, Wu N, Fu J, Wang SP, Li XH, Xiao JH, Xiong LZ (2012) A GH3 family member, OsGH3-2, modulates auxin and abscisic acid levels and differentially affects drought and cold tolerance in rice. J Exp Bot 18:6467–6480
Fu J, Liu HB, Li Y, Yu HH, Li XH, Xiao JH, Wang SP (2010) Manipulating broad-spectrum disease resistance by suppressing pathogen-induced auxin accumulation in rice. Plant Physiol 155:589–602
Gust AA, Brunner F, Nürnberger T (2010) Biotechnological concepts for improving plant innate immunity. Curr Opin Biotechnol 21:204–210
Hammond-Kosack KE, Parker JE (2003) Deciphering plant-pathogen communication: fresh perspectives for molecular resistance breeding. Curr Opin Biotechnol 14:177–193
Helliwell EE, Wang Q, Yang YN (2013) Transgenic rice with inducible ethylene production exhibits broad-spectrum disease resistance to the fungal pathogens Magnaporthe oryzae and Rhizoctonia solani. Plant Biotechnol J 11:33–42
Jha S, Chattoo B (2010) Expression of a plant defensing in rice confers resistance to fungal phytopathogens. Transgenic Res 19:373–384
Jha S, Tank H, Prasad B, Chattoo B (2009) Expression of Dm-AMP1 in rice confers resistance to Magnaporthe oryzae and Rhizoctonia solani. Transgenic Res 18:59–69
Kou YJ, Wang SP (2010) Broad-spectrum and durability: understanding of quantitative disease resistance. Curr Opin Plant Biol 13:181–185
Leung J, Giraudat J (1998) Abscisic acid signal transduction. Annu Rev Plant Physiol Plant Mol Biol 49:199–222
Li ZK, Pinson SRM, Marchetti MA, Stansel JW, Park WD (1995) Characterization of quantitative trait loci (QTLs) in cultivated rice contributing to field resistance to sheath blight (Rhizoctonia solani). Theor Appl Genet 91:382–388
Li Q, Chen F, Sun L, Zhang Z, Yang Y, He Z (2006) Expression profiling of rice genes in early defense responses to blast and bacterial blight pathogens using cDNA microarray. Physiol Mol Plant Pathol 68:51–60
Lin YJ, Zhang QF (2005) Optimising the tissue culture conditions for high efficiency transformation of indica rice. Plant Cell Rep 23:540–547
Liu Q, Kasuga M, Sakuma Y, Abe H, Miura S, Yamaguchi-Shinozaki K, Shinozaki K (1998) Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA binding domain separate two cellular signal transduction pathways in drought- and low-temperature-responsive gene expression, respectively, in Arabidopsis. Plant Cell 10:1391–1406
Liu X, Bai X, Wang X, Chu C (2007) OsWRKY71, a rice transcription factor, is involved in rice defense response. J Plant Physiol 164:969–979
Liu G, Jia Y, Correa-Victoria FJ, Prado A, Yeater KM, McClung A, Correll JC (2009) Mapping quantitative trait loci responsible for resistance to sheath blight in rice. Phytopathology 99:1078–1084
Lyu JI, Min SR, Lee JH, Lim YH, Kim JK, Bae CH, Liu JR (2013) Overexpression of a trehalose-6-phosphate synthase/phosphatase fusion gene enhances tolerance and photosynthesis during drought and salt stress without growth aberrations in tomato. Plant Cell Tissue Org Cult 112:257–262
Mani-Mauch B, Mauch F (2005) The role of abscisic acid in plant-pathogen interactions. Curr Opin Plant Biol 8:409–414
Melotto M, Underwood W, Koczan J, Nomura K, He SY (2006) Plant stomata function in innate immunity against bacterial invasion. Cell 126:969–980
Mohr PG, Cahill DM (2003) Abscisic acid influences the susceptibility of Arabidopsis thaliana to Pseudomonas syringae pv. tomato and Peronospora parasitica. Funct Plant Biol 30:461–469
Ou SH (1985) Rice disease. Kew, Surrey
Qiu DY, Xiao J, Ding XH, Xiong M, Cai M, Cao YL, Li XH, Xu CG, Wang SP (2007) OsWRKY13 mediates rice disease resistance by regulating defense-related genes in salicylate- and jasmonate-dependent signaling. Mol Plant Microbe Interact 20:492–499
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 133:1755–1767
Ramalingam J, Vera Cruz CM, Kukreja K, Chittoor JM, Wu JL, Lee SW, Baraoidan M, George ML, Cohen MB, Hulbert SH, Leach JE, Leung H (2003) Candidate defense genes from rice, barley, and maize and their association with qualitative and quantitative resistance in rice. Mol Plant Microbe Interact 16:14–24
Schroeder JI, Kwak JM, Allen GJ (2001) Guard cell abscisic acid signaling and engineering drought hardiness in plants. Nature 410:327–330
Schulze-Lefert P, Robatzek S (2006) Plant pathogens trick guard cells into opening the gates. Cell 126:831–834
Shen XL, Yuan B, Liu HB, Li XH, Xu CG, Wang SP (2010) Opposite functions of a rice mitogen-activated protein kinase during the process of resistance against Xanthomonas oryzae. Plant J 64:86–99
Shen XL, Liu HB, Yuan B, Li XH, Xu CG, Wang SP (2011) OsEDR1 negatively regulates rice bacterial resistance via activation of ethylene biosynthesis. Plant, Cell Environ 34:179–191
Shinozaki K, 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
Shinozaki K, Yamaguchi-Shinozaki K, Seki M (2003) Regulatory network of gene expression in the drought and cold stress responses. Curr Opin Plant Biol 6:410–417
Skriver K, Mundy J (1990) Gene expression in response to abscisic acid and osmotic stress. Plant Cell 2:503–512
Stockinger EJ, Gilmour SJ, Thomashow MF (1997) Arabidopsis thaliana CBF1 encodes an AP2 domain-containing transcriptional activator that binds to the C-repeat/DRE, a cis-acting DNA regulatory element that stimulates transcription in response to low temperature and water deficit. Proc Natl Acad Sci USA 94:1035–1040
Tao Z, Liu HB, Qiu DY, Zhou Y, Li XH, Xu CG, Wang SP (2009) A pair of allelic WRKY genes play opposite roles in rice-bacteria interactions. Plant Physiol 151:936–948
Wang Z, Taramino G, Yang D, Liu G, Tingey SV, Miao GH, Wang GL (2001) Rice ESTs with disease-resistance gene- or defense-response gene-like sequences mapped to regions containing major resistance genes or QTLs. Mol Genet Genomics 265:302–310
Wang GN, Ding XH, Yuan M, Qiu DY, Li XH, Xu CG, Wang SP (2006) Dual function of rice OsDR8 gene in disease resistance and thiamine accumulation. Plant Mol Biol 60:437–449
Wang Y, Pinson SRM, Fjellstrom RG, Tabien RE (2012) Phenotypic gain from introgression of two QTL, qSB9-2 and qSB12-1, for rice sheath blight resistance. Mol Breed 30:293–303
Wei Q, Hu P, Kuai BK (2012) Ectopic expression of an Ammopiptanthus mongolicus H+-pyrophosphatase gene enhances drought and salt tolerance in Arabidopsis. Plant Cell Tissue Org Cult 110:359–369
Wen N, Chu Z, Wang S (2003) Three types of defense-responsive genes are involved in resistance to bacterial blight and fungal blast diseases in rice. Mol Genet Genomics 269:331–339
Whenham RJ, Fraser RSS, Brown LP, Payne JA (1986) Tobacco mosaic virus-induced increase in abscisic acid concentration in tobacco leaves: intracellular location in light and dark green areas, and relationship to symptom development. Planta 168:592–598
Xiang Y, Tang N, Du H, Ye HY, Xiong LZ (2008) Characterization of OsbZIP23 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
Xiong L, Zhu JK (2002) Molecular and genetic aspects of plant responses to osmotic stress. Plant, Cell Environ 25:131–139
Xiong L, Schumaker KS, Zhu JK (2002a) Cell signaling during cold, drought, and salt stress. Plant Cell 14(Suppl):S165–S183
Xiong M, Wang S, Zhang Q (2002b) Coincidence in map positions between pathogen-induced defense-responsive genes and quantitative resistance loci in rice. Sci China (Series C) 45:518–526
Yi RH, Zhu XR, Zhou EX (2003) On the evaluation of different methods by artificially inoculating with rice sheath blight fungus (Rhizoctonia solani). J Guangzhou Univ 2:224–227
Yi N, Kim Y, Jeong MH, Oh SJ, Jeong J, Park SH, Jung H, Choi Y, Kim J (2010) Functional analysis of six drought-inducible promoters in transgenic rice plants throughout all stages of plant growth. Planta 232:743–754
Zhou B, Peng K, Chu Z, Wang S, Zhang Q (2002) The defense-responsive genes showing enhanced and repressed expression after pathogen infection in rice (Oryza sativa L.). Sci China (Series C) 45:450–467
Acknowledgments
This study was supported by the National Program of Transgenic Variety Development of China (2011ZX08009-004, 2011ZX08001-002), National Natural Science Foundation of China (Grant No. 31071381) and the Taishan Scholar Programme of Shandong Province. We thank L. Xiong for providing Osbzip23 mutant line, G. Chen for providing RS105 strains as well as J. Yu for providing R. solani strain. We also thank F. Yao for management of rice in the field.
Author information
Authors and Affiliations
Corresponding authors
Additional information
Ning Li and Lingguang Kong contributed equally to this work.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Li, N., Kong, L., Zhou, W. et al. Overexpression of Os2H16 enhances resistance to phytopathogens and tolerance to drought stress in rice. Plant Cell Tiss Organ Cult 115, 429–441 (2013). https://doi.org/10.1007/s11240-013-0374-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11240-013-0374-3