Abstract
Nucleotide-binding site leucine-rich repeat (NB-LRR) genes play important roles in plant disease resistance. Due to its similarity to Rp1 in maize (Zea mays), a novel NB-LRR gene was isolated from rice and designated as OsRP1L1 (Oryza sativa Rp1-like 1). Analysis of expression of a super green fluorescent protein (sGFP) fusion gene revealed that the OsRP1L1 protein localizes to the nucleolus. Expression patterns suggested that OsRP1L1 was involved in responses to several plant growth regulators (PGRs) and environmental stresses. To explore its function in bacterial blight (BB) resistance, OsRP1L1 was cloned and overexpressed in a susceptible japonica rice cultivar. Overexpression of OsRP1L1 moderately elevated the resistance of plants to Xanthomonas oryzae pv. oryzae strains PXO86 and PXO341. Transcriptome analysis showed that plants overexpressing OsRP1L1 had small changes in their transcriptome, with 26 genes showing statistically significant changes of more than two-fold. The most up-regulated transcripts—a DIN1-like gene and a terpene synthase (TPS) gene—were up-regulated 7.9- and 7.6-fold, respectively. It was also noted that seven of the up-regulated genes have also reportedly been induced by overexpression of OsbZIP46, which has been identified recently as a player in ABA sensing. All these findings suggest that OsRP1L1 plays an important role in rice BB resistance, and may be useful as a genetic resource for engineering disease resistance in plants.
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References
Azumi Y, Watanabe A (1991) Evidence for a senescence-associated gene induced by darkness. Plant Physiol 95:577–583
Bernoux M, Ellis JG, Dodds PN (2011) New insights in plant immunity signaling activation. Curr Opin Plant Biol 14:512–518
Century KS, Lagman RA, Adkisson M, Morlan J, Tobias R, Schwartz K, Smith A, Love J, Ronald PC, Whalen MC (1999) Short communication: developmental control of Xa21-mediated disease resistance in rice. Plant J 20:231–236
Chen H, Wang S, Zhang Q (2002) New gene for bacterial blight resistance in rice located on chromosome 12 identified from minghui 63, an elite restorer line. Phytopathology 92:750–754
Chen F, Tholl D, Bohlmann J, Pichersky E (2011) The family of terpene synthases in plants: a mid-size family of genes for specialized metabolism that is highly diversified throughout the kingdom. Plant J 66:212–229
Chen LN, Yang Y, Yan CQ, Wang XM, Yu CL, Zhou J, Zhang WL, Cheng Y, Cheng XY, Chen JP (2012) Identification of quantitative trait loci for bacterial blight resistance derived from Oryza meyeriana and agronomic traits in recombinant inbred lines of Oryza sativa. J Phytopathol 160:461–468
Cheong YH, Chang HS, Gupta R, Wang X, Zhu T, Luan S (2002) Transcriptional profiling reveals novel interactions between wounding, pathogen, abiotic stress, and hormonal responses in Arabidopsis. Plant Physiol 129:661–677
Christensen AH, Quail PH (1996) Ubiquitin promoter-based vectors for high-level expression of selectable and/or screenable marker genes in monocotyledonous plants. Transgenic Res 5:213–218
Collins N, Drake J, Ayliffe M, Sun Q, Ellis J, Hulbert S, Pryor T (1999) Molecular characterization of the maize Rp1-D rust resistance haplotype and its mutants. Plant Cell 11:1365–1376
Coruzzi G, Broglie R, Edwards C, Chua NH (1984) Tissue-specific and light-regulated expression of a pea nuclear gene encoding the small subunit of ribulose-1,5-bisphosphate carboxylase. EMBO J 3:1671–1679
Dong R, Chen J, Wang X, Li J, Zhou J, Yang Y, Yu C, Cheng Y, Yan C, Chen J (2012) Agrobacterium-mediated transformation efficiency is altered in a novel rice bacterial blight resistance cultivar and is influenced by environmental temperature. Physiol Mol Plant Pathol 77:33–40
Foyer CH, Kerchev PI, Hancock RD (2012) The ABA-INSENSITIVE-4 (ABI4) transcription factor links redox, hormone and sugar signaling pathways. Plant Signal Behav 7:276–281
He X, Tian J, Yang L, Huang Y, Zhao B, Zhou C, Ge R, Shen Y, Huang Z (2012) Overexpressing a glycogen synthase kinase gene from wheat, TaGSK1, enhances salt tolerance in transgenic Arabidopsis. Plant Mol Biol Rep 30:807–816
Howe GA, Jander G (2008) Plant immunity to insect herbivores. Annu Rev Plant Biol 59:41–66
Hulbert SH, Webb CA, Smith SM, Sun Q (2001) Resistance gene complexes: evolution and utilization. Annu Rev Phytopathol 39:285–312
Khraiwesh B, Zhu JK, Zhu J (2012) Role of miRNAs and siRNAs in biotic and abiotic stress responses of plants. Biochim Biophys Acta 1819:137–148
Kottapalli KR, Kottapalli P, Agrawal GK, Kikuchi S, Rakwal R (2007) Recessive bacterial leaf blight resistance in rice: complexity, challenges and strategy. Biochem Biophys Res Commun 355:295–301
Mchale L, Tan X, Koehl P, Michelmore RW (2006) Plant NBS-LRR proteins: adaptable guards. Genome Biol 7:212
Mitsuhara I, Iwai T, Seo S, Yanagawa Y, Kawahigasi H, Hirose S, Ohkawa Y, Ohashi Y (2008) Characteristic expression of 12 rice PR1 family genes in response to pathogen infection, wounding, and defense-related signal compounds (121/180). Mol Genet Genomics 279:415–427
Monosi B, Wisser RJ, Pennill L, Hulbert SH (2004) Full-genome analysis of resistance gene homologues in rice. Theor Appl Genet 109:1434–1447
Narusaka Y, Narusaka M, Seki M, Umezawa T, Ishida J, Nakajima M, Enju A, Shinozaki K (2004) Crosstalk in the responses to abiotic and biotic stresses in Arabidopsis: analysis of gene expression in cytochrome P450 gene superfamily by cDNA microarray. Plant Mol Biol 55:327–342
Robert-Seilaniantz A, Grant M, Jones JD (2011) Hormone crosstalk in plant disease and defense: more than just jasmonate-salicylate antagonism. Annu Rev Phytopathol 49:317–343
Rodrigues C, Vandenberghe LP, De Oliveira J, Soccol CR (2012) New perspectives of gibberellic acid production: a review. Crit Rev Biotechnol 32:263–273
Shi HT, Li RJ, Cai W, Liu W, Fu ZW, Lu YT (2012) In vivo role of nitric oxide in plant response to abiotic and biotic stress. Plant Signal Behav 7:437–439
Singh S, Sidhu JS, Huang N, Vikal Y, Li Z, Brar DS, Dhaliwal HS, Khush GS (2001) Pyramiding three bacterial blight resistance genes (xa5, xa13 and Xa21) using marker-assisted selection into indica rice cultivar PR106. Theor Appl Genet 102:1011–1015
Singh K, Foley RC, Onate-Sanchez L (2002) Transcription factors in plant defense and stress responses. Curr Opin Plant Biol 5:430–436
Tang N, Zhang H, Li X, Xiao J, Xiong L (2012) Constitutive activation of transcription factor OsbZIP46 improves drought tolerance in rice. Plant Physiol 158:1755–1768
Tripathy M, Tyagi W, Goswami M, Kaul T, Singla-Pareek S, Deswal R, Reddy M, Sopory S (2012) Characterization and functional validation of tobacco PLC delta for abiotic stress tolerance. Plant Mol Biol Rep 30:488–497
Yan CQ, Qian KX, Xue GP, Wu ZC, Chen YL, Yan QS, Zhang XQ, Wu P (2004a) Production of bacterial blight resistant lines from somatic hybridization between Oryza sativa L. and Oryza meyeriana L. J Zhejiang Univ Sci 5:1199–1205
Yan CQ, Qian KX, Yan QS, Zhang XQ, Xue GP, Huangfu WG, Wu YF, Zhao YZ, Xue ZY, Huang J, Xu GZ, Wu P (2004b) Use of asymmetric somatic hybridization for transfer of the bacterial blight resistance trait from Oryza meyeriana L. to O. sativa L. ssp. japonica. Plant Cell Rep 22:569–575
Yang Y, Yu CL, Wang XM, Yan CQ, Cheng Y, Chen JP (2011) Inoculation with Xanthomonas oryzae pv. oryzae induces thylakoid membrane association of Rubisco activase in Oryza meyeriana. J Plant Physiol 168:1701–1704
Yang Y, Chen LN, Yan CQ, Cheng Y, Chen XY, Chen JP (2012) Construction of a genetic linkage map of a bacterial blight resistance rice line derived from Oryza meyeriana L. Acta Agic Zhejiangensis 24:846–852
Yue JX, Meyers BC, Chen JQ, Tian D, Yang S (2012) Tracing the origin and evolutionary history of plant nucleotide-binding site-leucine-rich repeat (NBS-LRR) genes. New Phytol 193:1049–1063
Zhou J, Jiao FC, Wu ZC, Li YY, Wang XM, He XW, Zhong WQ, Wu P (2008) OsPHR2 is involved in phosphate-starvation signaling and excessive phosphate accumulation in shoots of plants. Plant Physiol 146:1673–1686
Acknowledgments
This work was supported by Chinese New Genetically Modified Organism Varieties Programme (2011ZX08009-003-001), National Natural Science Foundation of China for young scholars (30900263, 30900098, 31101208, 31201482), Zhejiang Provincial Foundation for Natural Science (LY12C14011, Y3100591), Zhejiang Leading Team of Science and Technology Innovation and the Program for Leading Team of Agricultural Research and Innovation of Ministry of Agriculture, China. We thank Xutao Hong at Zhejiang-California International NanoSystems Institute for advice on microarray data analysis and Professor M. J. Adams, Rothamsted Research, UK for his correction of the English manuscript.
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Supplementary Table S1
Primers for identification of positive transgenic lines. (DOC 28 kb)
Supplementary Table S2
Primers used for expression analysis of OsRP1L1. (Expression analysis, semiquantitative RT-PCR and qRT-PCR were all performed with these primers, which were designed with Primer Premier 5 Software. The qRT-PCR analyses were performed with SsoFast EvaGreen Supermix). (DOC 28 kb)
Supplementary Table S3
Primers used for expression analysis of PR1 genes. (DOC 40 kb)
Supplementary Table S4
Primer sequences and UPL probes used in quantitative real-time PCR for verification of microarray analysis. (DOC 42 kb)
Supplementary Table S5
Genes (probe sets) showing more than 2-fold enhanced expression in plants overexpressing RP1L1 compared with wild type. (DOC 42 kb)
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Wang, X., Chen, J., Yang, Y. et al. Characterization of a Novel NBS-LRR Gene Involved in Bacterial Blight Resistance in Rice. Plant Mol Biol Rep 31, 649–656 (2013). https://doi.org/10.1007/s11105-012-0537-0
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DOI: https://doi.org/10.1007/s11105-012-0537-0