Skip to main content
Log in

Genome-wide analysis of defense-responsive genes in bacterial blight resistance of rice mediated by the recessive R gene xa13

  • Original Paper
  • Published:
Molecular Genetics and Genomics Aims and scope Submit manuscript

Abstract

Defense responses triggered by dominant and recessive disease resistance ( R) genes are presumed to be regulated by different molecular mechanisms. In order to characterize the genes activated in defense responses against bacterial blight mediated by the recessive R gene xa13, two pathogen-induced subtraction cDNA libraries were constructed using the resistant rice line IRBB13—which carries xa13 —and its susceptible, near-isogenic, parental line IR24. Clustering analysis of expressed sequence tags (ESTs) identified 702 unique expressed sequences as being involved in the defense responses triggered by xa13; 16% of these are new rice ESTs. These sequences define 702 genes, putatively encoding a wide range of products, including defense-responsive genes commonly involved in different host-pathogen interactions, genes that have not previously been reported to be associated with pathogen-induced defense responses, and genes (38%) with no homology to previously described functional genes. In addition, R -like genes putatively encoding nucleotide-binding site/leucine rich repeat (NBS-LRR) and LRR receptor kinase proteins were observed to be induced in the disease resistance activated by xa13. A total of 568 defense-responsive ESTs were mapped to 588 loci on the rice molecular linkage map through bioinformatic analysis. About 48% of the mapped ESTs co-localized with quantitative trait loci (QTLs) for resistance to various rice diseases, including bacterial blight, rice blast, sheath blight and yellow mottle virus. Furthermore, some defense-responsive sequences were conserved at similar locations on different chromosomes. These results reveal the complexity of xa13 -mediated resistance. The information obtained in this study provides a large source of candidate genes for understanding the molecular bases of defense responses activated by recessive R genes and of quantitative disease resistance.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2a, b

Similar content being viewed by others

References

  • Albar L, Lorieux M, Ahmadi N, Rimbault I, Pinel A, Sy AA, Fargette D, Ghesquiere A (1998) Genetic basis and mapping of the resistance to rice yellow mottle virus. I. QTLs identification and relationship between resistance and plant morphology. Theor Appl Genet 97:1145–1154

    Google Scholar 

  • Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    PubMed  Google Scholar 

  • Austin MJ, Muskett P, Kahn K, Feys BJ, Jones JDG, Parker JE (2002) Regulatory role of SGT1 in early R gene-mediated plant defenses. Science 295:2077–2080

    CAS  PubMed  Google Scholar 

  • Azevedo C, Sadanandom A, Kitagawa K, Freialdenhoven A, Shirasu K, Schulze-Lefert P (2002) The RAR1 interactor SGT1, an essential component of R gene-triggered disease resistance. Science 295:2073–2076

    CAS  PubMed  Google Scholar 

  • Baker B, Zambryski P, Staskawicz B, Dinesh-Kumar SP (1997) Signaling in plant-microbe interactions. Science 276:726–733

    CAS  PubMed  Google Scholar 

  • Buschges R, Hollricher K, Panstruga R, Simons G, Wolter M, Frijters A, van Daelen R, van der Lee T, Diergaarde P, Groenendijk J, Topsch S, Vos P, Salamini F, Schulze-Lefert P (1997) The barley Mol gene: a novel control element of plant pathogen resistance. Cell 88:695–705

    PubMed  Google Scholar 

  • Causse MA, Fulton TM, Cho YG, Ahn SN, Chunwongse J, Wu K, Xiao J, Yu Z, Ronald PC, Harrington SE, Second G, McCouch SR, Tanksley SD (1994) Saturated molecular map of the rice genome based on an interspecific backcross population. Genetics 138:1251–1274

    CAS  PubMed  Google Scholar 

  • Chen H (2001) Population structure of Pyricularia grisea from Central and Southern China and comparative mapping of QTL for blast- and bacterial blight-resistance in rice and barley (in Chinese). PhD Thesis. Huazhong Agriculture University, Wuhan, China

  • Chen H, Wang S, Zhang Q (2002) A new gene for bacterial blight resistance in rice located on chromosome 12 identified from Minghui 63, an elite restorer line. Phytopathology 92:750–754

    CAS  Google Scholar 

  • Chen H, Wang S, Xing Y, Xu C, Hayes PM, Zhang Q (2003) Comparative analyses of genomic locations and race specificities of loci for quantitative resistance to Pyricularia grisea in rice and barley. Proc Natl Acad Sci USA 100:2544–2549

    Article  CAS  PubMed  Google Scholar 

  • Choi D, Kim HM, Yun HK, Park JA, Kim WT, Bok SH (1996) Molecular cloning of a metallothionein-like gene from Nicotiana glutinosa L. and its induction by wounding and tobacco mosaic virus infection. Plant Physiol 112:353–359

    Article  CAS  PubMed  Google Scholar 

  • Dangl JL, Jones JDG (2001) Plant pathogens and integrated defence responses to infection. Nature 411:826–833

    CAS  PubMed  Google Scholar 

  • Deslandes L, Olivier J, Theulieres F, Hirsch J, Feng DX, Bittner-Eddy P, Beynon J, Marco Y (2002) Resistance to Ralstonia solanacearum in Arabidopsis thaliana is conferred by the recessive RPS1-R gene, a member of a novel family of resistance genes. Proc Natl Acad Sci USA 99:2404–2409

    Article  CAS  PubMed  Google Scholar 

  • Etienne P, Petitot AS, Houot V, Blein JP, Suty L (2000) Induction of tcI 7, a gene encoding a beta-subunit of proteasome, in tobacco plants treated with elicitins, salicylic acid or hydrogen peroxide. FEBS Lett 466:213–218

    Article  CAS  PubMed  Google Scholar 

  • Faris JD, Li WL, Liu DJ, Chen PD, Gill BS (1999) Candidate gene analysis of quantitative disease resistance in wheat. Theor Appl Genet 98:219–225

    CAS  Google Scholar 

  • Feinberg AP, Vogelstein B (1983) A technique for radiolabelling DNA restriction fragment length polymorphisms to high specific activity. Anal Biochem 132:6–13

    PubMed  Google Scholar 

  • Frye CA, Innes RW (1998) An Arabidopsis mutant with enhanced resistance to powdery mildew. Plant Cell 10:947–956

    CAS  PubMed  Google Scholar 

  • Frye CA, Tang D, Innes RW (2001) Negative regulation of defense responses in plants by a conserved MAPKK kinase. Proc Natl Acad Sci USA 98:373–378

    CAS  PubMed  Google Scholar 

  • Geffroy V, Sevignac M, de Oliveira JCF, Fouilloux G, Skroch P, Thoquet P, Gepts P, Langin T, Dron M (2000) Inheritance of partial resistance against Colletotrichum lindemuthianum in Phaseolus vulgaris and co-localization of quantitative trait loci with genes involved in specific resistance. Mol Plant-Microbe Interact 13:287–296

  • Harushima Y, et al (1998) A high-density rice genetic linkage map with 2275 markers using a single F2 population. Genetics 148:479–494

    CAS  PubMed  Google Scholar 

  • Jia Y, McAdams SA, Bryan GT, Hershey HP, Valent B (2000) Direct interaction of resistance gene and avirulence gene products confers rice blast resistance. EMBO J 19:4004–1014

    PubMed  Google Scholar 

  • Kauffman HE, Reddy APK, Hsieh SPY, Merca SD (1973) An improved technique for evaluating resistance of rice varieties to Xanthomonas oryzae. Plant Dis Rep 57:537–541

    Google Scholar 

  • Khush GS, Angeles ER (1999) A new gene for resistance to race 6 of bacterial blight in rice, Oryza sativa L. Rice Genet Newslett 16:92–93

    Google Scholar 

  • Kim MC, Panstruga R, Elliott C, Muller J, Devoto A, Yoon HW, Park HC, Cho MJ, Schulze-Lefert P (2002) Calmodulin interacts with MLO protein to regulate defence against mildew in barley. Nature 416:447–451

    Article  CAS  PubMed  Google Scholar 

  • Lahaye T (2002) The Arabidopsis RPS1 -R disease resistance gene—uncovering the plant’s nucleus as the new battlefield of plant defense? Trends Plant Sci 7:425–427

    Article  CAS  PubMed  Google Scholar 

  • Lee KS, Rasabandith S, Angeles ER, Khush GS (2003) Inheritance of resistance to bacterial blight in 21 cultivars of rice. Phytopathology 93:147–152

    Google Scholar 

  • Li Z, 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

    CAS  Google Scholar 

  • Li ZK, Luo LJ, Mei HW, Paterson AH, Zhao XH, Zhong DB, Wang YP, Yu XQ, Zhu L, Tabien R, Stansel JW, Ying CS (1999) A “defeated” rice resistance gene acts as a QTL against a virulent strain of Xanthomonas oryzae pv. oryzae. Mol Gen Genet 261:58–63

    CAS  PubMed  Google Scholar 

  • Li ZK, Sanchez A, Angeles E, Singh S, Domingo J, Huang N, Khush GS (2001) Are the dominant and recessive plant disease resistance genes similar? A case study of rice R genes and Xanthomonas oryzae pv. oryzae races. Genetics 159:757–765

    Google Scholar 

  • Lin XH, Zhang DP, Xie YF, Gao HP, Zhang QF (1996) Identifying and mapping a new gene for bacterial blight resistance in rice based on RFLP markers. Phytopathology 86:1156–1159

    CAS  Google Scholar 

  • Maleck K, Levine A, Eulgem T, Morgan A, Schmid J, Lawton KA, Dangl JL, Dietrich RA (2000) The transcriptome of Arabidopsis thaliana during systemic acquired resistance. Nature Genet 26:403–410

    Article  CAS  PubMed  Google Scholar 

  • Nagato Y, Yoshimura A (1998) Report of the Committee on Gene Symbolization, Nomenclature and Linkage Groups. Rice Genet Newslett 15:13–74

    Google Scholar 

  • Nimchuk Z, Rohmer L, Chang JH, Dangl JL (2001) Knowing the dancer from the dance: R -gene products and their interactions with other proteins from host and pathogen. Curr Opin Plant Biol 4:288–294

    CAS  PubMed  Google Scholar 

  • Ogawa T, Lin L, Tabien RE, Khush GS (1987) A new recessive gene for resistance to bacterial blight of rice. Rice Genet Newsl 4:98–100

    Google Scholar 

  • Ramalingam J, Vera Cruz CM, Kukreja K, Chittoor JM, Wu J-L, 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

    Google Scholar 

  • Roumen EC (1994) A strategy for accumulating genes for partial resistance to blast disease in rice within a conventional breeding program. In: Zeigler RS, Leong SA, Teng PS (eds) Rice blast disease. CAB International, Wallingford, UK, pp 245–265

  • Sanchez AC, Ilag LL, Yang D, Brar DS, Ausubel F, Khush GS, Yano M, Sasaki T, Li Z, Huang N (1999) Genetic and physical mapping of xa13, a recessive gene bacterial blight resistance gene in rice. Theor Appl Genet 98:1022–1028

    Article  CAS  Google Scholar 

  • Seehaus K, Tenhaken R (1998) Cloning of genes by mRNA differential display induced during the hypersensitive reaction of soybean after inoculation with Pseudomonas syringae pv. glycinea. Plant Mol Biol 38:1225–1234

    CAS  PubMed  Google Scholar 

  • Song W-Y, Wang G-L, Chen L-L, Kim H-S, Pi L-Y, Holsten T, Gardner J, Wang B, Zhai W-X, Zhu L-H, Fauquet C, Ronald P (1995) A receptor kinase-like protein encoded by the rice disease resistance gene, Xa21. Science 270:1804–1806

    CAS  PubMed  Google Scholar 

  • Sun X, Cao Y, Yang Z, Xu C, Li X, Wang S, Zhang Q (2004) Xa26, a gene conferring resistance to Xanthomonas oryzae pv. oryzae in rice, encoding an LRR receptor kinase-like protein. Plant J, in press

  • Takemoto D, Hayashi M, Doke N, Nishimura M, Kawakita K (1999) Molecular cloning of a defense-response-related cytochrome P450 gene from tobacco. Plant Cell Physiol 40:1232–1242

    CAS  PubMed  Google Scholar 

  • Tang X, Frederick RD, Zhou J, Halterman DA, Jia Y, Martin GB (1996) Initiation of plant disease resistance by physical interaction of AvrPto and Pto kinase. Science 274:2060–2063

    Article  CAS  PubMed  Google Scholar 

  • Tenhaken R, Levine A, Brisson LF, Dixon RA, Lamb C (1995) Function of the oxidative burst in hypersensitive disease resistance. Proc Natal Acad Sci USA 92:4158–4163

    CAS  Google Scholar 

  • Trognitz F, Manosalva P, Gysin R, Nino-Liu D, Simon R, Herrera MR, Trognitz B, Ghislain M, Nelson R (2002) Plant defense genes associated with quantitative resistance to potato late blight in Solanum phureja × Dihaploid S. tuberosum hybrids. Mol Plant-Microbe Interact 15:587–597

  • Wang G-L, Mackill DJ, Bonman M, McCouch SR, Champoux MC, Nelson RJ (1994) RFLP mapping of genes conferring complete and partial resistance to blast in a durably resistant rice cultivar. Genetics 136:1421–1434

    CAS  PubMed  Google Scholar 

  • Wang S, Liu N, Peng K, Zhang Q (1999) The distribution and copy number of copia -like retrotransposons in rice ( Oryza sativa L.) and their implications in the organization and evolution of the rice genome. Proc Natl Acad Sci USA 96:6824–6828

    Article  CAS  PubMed  Google Scholar 

  • Wang S, Wang J, Jiang J, Zhang Q (2000a) Mapping of centromeric regions on the molecular linkage map of rice ( Oryza sativa L.) using centromere-associated sequences. Mol Gen Genet 263:165–172

    Article  CAS  PubMed  Google Scholar 

  • Wang S-P, Liu K-D, Zhang Q-F (2000b) Segmental duplications are common in rice genome. Acta Botanica Sinica 42:1150–1155

    Google Scholar 

  • Wang Z, Taramino G, Yang D, Liu G, Tingey SV, Miao G-H, Wang G-L (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

    CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Xing YZ, Tan YF, Hua JP, Sun XL, Xu CG, Zhang Q (2002) Characterization of the main effects, epistatic effects and their environmental interactions of QTLs in the genetic basis of yield traits in rice. Theor Appl Genet 105:248–257

    CAS  Google Scholar 

  • Xiong L-Z, Wang S-P, Liu K-D, Dai X-K, Saghai Maroof MA, Hu J-G, Zhang Q-F (1998) Distribution of simple sequence repeat and AFLP markers in molecular linkage map of rice. Acta Botanica Sinica 40:605–614

    CAS  Google Scholar 

  • Xiong M, Wang S, Zhang Q (2002) Coincidence in map positions between pathogen-induced defense-responsive genes and quantitative resistance loci in rice. Science China (Series C) 45:518–526

    Google Scholar 

  • Yamamoto T, Kubiki Y, Lin SY, Sasaki T, Yano M (1998) Fine mapping of quantitative trait loci Hd-1, Hd-2 and Hd-3, controlling heading date of rice, as single Mendelian factors. Theor Appl Genet 97:37–44

    CAS  Google Scholar 

  • Yan J, Wang J, Zhang H (2002) An ankyrin repeat-containing protein plays a role in both disease resistance and antioxidation metabolism. Plant J 29:193–202

    Article  CAS  PubMed  Google Scholar 

  • Yang P, Chen C, Wang Z, Fan B, Chen Z (1999) A pathogen- and salicylic acid-induced WRKY DNA-binding activity recognizes the elicitor response element of the tobacco class I chitinase gene promoter. Plant J 18:141–149

    Article  CAS  Google Scholar 

  • Yang Z, Sun X, Wang S, Zhang Q (2003) Genetic and physical mapping of a new gene for bacterial blight resistance in rice. Theor Appl Genet 106:1467–1472

    CAS  PubMed  Google Scholar 

  • Yano M, Sasaki T (1997) Genetic and molecular dissection of quantitative traits in rice. Plant Mol Biol 35:145–153

    CAS  PubMed  Google Scholar 

  • Yano M, Katayose Y, Ashikari M, Yamanouchi U, Monna L, Fuse T, Baba T, Yamamoto K, Umehara Y, Nagamura Y, Sasaki T (2000) Hd1, a major photoperiod sensitivity quantitative trait locus in rice, is closely related to the Arabidopsis flowering time gene CONSTANS. Plant Cell 12:2473–2484

    CAS  PubMed  Google Scholar 

  • Yoshimura S, Yamanouchi U, Katayose Y, Toki S, Wang ZX, Kono I, Kuruta N, Yano M, Iwata N, Sasaki T (1998) Expression of Xa1, a bacterial blight resistance gene in rice, is induced by bacterial inoculation. Proc Natl Acad Sci USA 95:1663–1668

    CAS  PubMed  Google Scholar 

  • Yu D, Xie Z, Chen C, Fan B, Chen Z (1999) Expression of tobacco class II catalase gene activates the endogenous homologous gene and is associated with disease resistance in transgenic potato plants. Plant Mol Biol 39:477–488

    Article  CAS  PubMed  Google Scholar 

  • Zhang G, Angeles ER, Abenes MLP, Khush GS, Huang N (1996) RAPD and RFLP mapping of the bacterial blight resistance gene xa13 in rice. Theor Appl Genet 93:65–70

    Article  CAS  Google Scholar 

  • Zhang L-D, Yuan D-J, Zhang J-W, Wang S-P, Zhang Q-F (2003) A new method for EST clustering. Acta Genetica Sinica 30:147–153

    Article  CAS  PubMed  Google Scholar 

  • 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.). Science China (Series C) 45:449–467

    Google Scholar 

Download references

Acknowledgements

We sincerely thank the International Rice Research Institute for providing the near-isogenic resistance lines of rice, and the Philippine strains of Xoo. This research was supported by grants from the National Natural Science Foundation of China (39970450) and the National Program of research and Development of Transgenic Plants of China (JY03A0502)

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to S. Wang.

Additional information

The first two authors contributed equally to this work

Communicated by R. Hagemann

Electronic Supplementary Material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Chu, Z., Ouyang, Y., Zhang, J. et al. Genome-wide analysis of defense-responsive genes in bacterial blight resistance of rice mediated by the recessive R gene xa13 . Mol Genet Genomics 271, 111–120 (2004). https://doi.org/10.1007/s00438-003-0964-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00438-003-0964-6

Keywords

Navigation