Skip to main content
Log in

High-resolution genetic mapping of rice bacterial blight resistance gene Xa23

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

Abstract

Bacterial blight (BB) caused by Xanthomonas oryzae pv. oryzae (Xoo) is the most devastating bacterial disease of rice (Oryza sativa L.), a staple food crop that feeds half of the world’s population. In management of this disease, the most economical and effective approach is cultivating resistant varieties. Due to rapid change of pathogenicity in the pathogen, it is necessary to identify and characterize more host resistance genes for breeding new resistant varieties. We have previously identified the BB resistance (R) gene Xa23 that confers the broadest resistance to Xoo strains isolated from different rice-growing regions and preliminarily mapped the gene within a 1.7 cm region on the long arm of rice chromosome 11. Here, we report fine genetic mapping and in silico analysis of putative candidate genes of Xa23. Based on F2 mapping populations derived from crosses between Xa23-containing rice line CBB23 and susceptible varieties JG30 or IR24, six new STS markers Lj36, Lj46, Lj138, Lj74, A83B4, and Lj13 were developed. Linkage analysis revealed that the new markers were co-segregated with or closely linked to the Xa23 locus. Consequently, the Xa23 gene was mapped within a 0.4 cm region between markers Lj138 and A83B4, in which the co-segregating marker Lj74 was identified. The corresponding physical distance between Lj138 and A83B4 on Nipponbare genome is 49.8 kb. Six Xa23 candidate genes have been annotated, including four candidate genes encoding hypothetical proteins and the other two encoding a putative ADP-ribosylation factor protein and a putative PPR protein. These results will facilitate marker-assisted selection of Xa23 in rice breeding and molecular cloning of this valuable R gene.

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

Access this article

Price includes VAT (France)

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

References

  • Anantharaman V, Aravind L (2010) Novel eukaryotic enzymes modifying cell-surface biopolymers. Biology Direct 5:1. doi:10.1186/1745-6150-5-1

    Article  PubMed  PubMed Central  Google Scholar 

  • Bhasin H, Bhatia D, Raghuvanshi S, Lore JS, Sahi GK, Kaur B, Vikal Y, Singh K (2012) New PCR-based sequence-tagged site marker for bacterial blight resistance gene Xa38 of rice. Mol Breed 30:607–611

    Article  CAS  Google Scholar 

  • Blair MW, Garris AJ, Iyer AS, Chapman B, Kresovich S, McCouch SR (2003) High resolution genetic mapping and candidate gene identification at the xa5 locus for bacterial blight resistance in rice (Oryza sativa L.). Theor Appl Genet 107:62–73

    Article  PubMed  CAS  Google Scholar 

  • Böhlenius H, Mørch SM, Godfrey D, Nielsen ME, Thordal-Christensen H (2010) The multivesicular body-localized GTPase ARFA1b/1c is important for callose deposition and ROR2 syntaxin-dependent preinvasive basal defense in barley. Plant Cell 22:3831–3844

    Article  PubMed  PubMed Central  Google Scholar 

  • Brar DS, Khush GS (1997) Alien introgression in rice. Plant Mol Biol 35:35–47

    Article  PubMed  CAS  Google Scholar 

  • Cevher-Keskin B (2013) ARF1 and SAR1 GTPases in endomembrane trafficking in plants. Int J Mol Sci 14:18181–18199

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Cheema KK, Grewal NK, Vikal Y, Sharma R, Lore JS, Das A, Bhatia D, Mahajan R, Gupta V, Bharaj TS, Singh K (2008) A novel bacterial blight resistance gene from Oryza nivara mapped to 38 kb region on chromosome 4 and transferred to Oryza sativa L. Genet Res 90:397–407

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Chen S, Liu X, Zeng L, Ouyang D, Yang J, Zhu X (2011) Genetic analysis and molecular mapping of a novel recessive gene xa34(t) for resistance against Xanthomonas oryzae pv. oryzae. Theor Appl Genet 122:1331–1338

    Article  PubMed  CAS  Google Scholar 

  • Chu Z, Yuan M, Yao J, Ge X, Yuan B, Xu C, Li X, Fu B, Li Z, Bennetzen JL, Zhang Q, Wang S (2006) Promoter mutations of an essential gene for pollen development result in disease resistance in rice. Genes Dev 20:1250–1255

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Fan YL, Chen XW, Wang CL, Zhu LH, Zhang Q, Zhao KJ (2006) Mapping the rice bacterial blight resistance gene Xa23 with RFLP markers and converting RFLP to STS Marker. Acta Agron Sin 32:931–935

    CAS  Google Scholar 

  • Gu K, Tian D, Yang F, Wu L, Sreekala C, Wang D, Wang GL, Yin Z (2004) High-resolution genetic mapping of Xa27(t), a new bacterial blight resistance gene in rice, Oryza sativa L. Theor Appl Genet 108:800–807

    Article  PubMed  CAS  Google Scholar 

  • Gu K, Yang B, Tian D, Wu L, Wang D, Sreekala C, Yang F, Chu Z, Wang GL, White FF, Yin Z (2005) R gene expression induced by a type-III effector triggers disease resistance in rice. Nature 435:1122–1125

    Article  PubMed  CAS  Google Scholar 

  • Guo SB, Zhang DP, Lin XH (2010) Identification and mapping of a novel bacterial blight resistance gene Xa35(t) originated from Oryza minuta. Sci Agric Sin 43:2611–2618

    CAS  Google Scholar 

  • Härtel B, Zehrmann A, Verbitskiy D, van der Merwe JA, Brennicke A, Takenaka M (2013) MEF10 is required for RNA editing at nad2-842 in mitochondria of Arabidopsis thaliana and interacts with MORF8. Plant Mol Biol 81:337–346

    Article  PubMed  Google Scholar 

  • Huang B, Xu JY, Hou MS, Ali J, Mou TM (2012) Introgression of bacterial blight resistance genes Xa7, Xa21, Xa22 and Xa23 into hybrid rice restorer lines by molecular marker-assisted selection. Euphytica 187:449–459

    Article  CAS  Google Scholar 

  • Hyodo K, Mine A, Taniguchi T, Kaido M, Mise K, Taniguchi H, Okuno T (2013) ADP ribosylation factor 1 plays an essential role in the replication of a plant RNA virus. J Virol 87:163–176

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Iyer AS, McCouch SR (2004) The rice bacterial blight resistance gene xa5 encodes a novel form of disease resistance. Mol Plant-Microbe Interact 17:1348–1354

    Article  PubMed  CAS  Google Scholar 

  • Jiang GH, Xia ZH, Zhou YL, Wan J, Li DY, Chen RS, Zhai WX, Zhu LH (2006) Testifying the rice bacterial blight resistance gene xa5 by genetic complementation and further analyzing xa5 (Xa5) in comparison with its homolog TFIIAg1. Mol Genet Genomics 275:354–366

    Article  PubMed  CAS  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 Report 57:537–541

    Google Scholar 

  • Kawahara Y, Bastide M, Hamilton JP, Kanamori H, McCombie WR, Ouyang S, Schwartz DC, Tanaka T, Wu J, Zhou S, Childs KL, Davidson RM, Lin H, Quesada-Ocampo L, Vaillancourt B, Sakai H, Lee SS, Kim J, Numa H, Itoh T, Buell CR, Matsumoto T (2013) Improvement of the Oryza sativa Nipponbare reference genome using next generation sequence and optical map data. Rice 6:4

    Article  PubMed  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 Newsl 16:92–93

    Google Scholar 

  • Korinsak S, Sriprakhon S, Sirithanya P, Jairin J, Korinsak S, Vanavichit A, Toojinda T (2009) Identification of microsatellite markers (SSR) linked to a new bacterial blight resistance gene xa33(t) in rice cultivar ‘Ba7’. Maejo Intern J Sci and Technol 3:235–247

    CAS  Google Scholar 

  • Kosambi DD (1944) The estimation of map distances from recombination values. Ann Eugen 12:172–175

    Article  Google Scholar 

  • Kumar PN, Sujatha K, Laha GS, Rao KS, Mishra B, Viraktamath BC, Hari Y, Reddy CS, Balachandran SM, Ram T, Madhav MS, Rani NS, Neeraja CN, Reddy GA, Shaik H, Sundaram RM (2012) Identification and fine-mapping of Xa33, a novel gene for resistance to Xanthomonas oryzae pv. oryzae. Phytopathology 102:222–228

    Article  PubMed  CAS  Google Scholar 

  • Lee MH, Sano H (2007) Attenuation of the hypersensitive response by an ATPase associated with various cellular activities (AAA) protein through suppression of a small GTPase, ADP ribosylation factor, in tobacco plants. Plant J 51:127–139

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Lee WY, Hong JK, Kim CY, Chun HJ, Park HC, Kim JC, Yun DJ, Chung WS, Lee SH, Lee SY, Cho MJ, Lim CO (2003b) Over-expressed rice ADP-ribosylation factor 1 (RARF1) induces pathogenesis-related genes and pathogen resistance in tobacco plants. Physiol Plant 119:573–581

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Lin H, Wang R, Qian Q, Yan M, Meng X, Fu Z, Yan C, Jiang B, Su Z, Li J, Wang Y (2009) DWARF27, an iron-containing protein required for the biosynthesis of strigolactones, regulates rice tiller bud outgrowth. Plant Cell 21:1512–1525

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Lincoln S, Daly M, Lander E (1993) Constructing genetic maps with Mapmaker/Exp 3.0, vol 3. Whitehead Institute Technical Report, Cambridge

    Google Scholar 

  • Liu Q, Yuan M, Zhou Y, Li X, Xiao J, Wang S (2011) A paralog of the MtN3/saliva family recessively confers race-specific resistance to Xanthomonas oryzae in rice. Plant Cell Environ 34:1958–1969

    Article  PubMed  CAS  Google Scholar 

  • Matheson LA, Hanton SL, Rossi M, Latijnhouwers M, Stefano G, Renna L, Brandizzi F (2007) Multiple roles of ADP-ribosylation factor 1 in plant cells include spatially regulated recruitment of coatomer and elements of the Golgi matrix. Plant Physiol 143:1615–1627

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • McCouch SR, Kochert Q, Yu ZH, Wang ZY, Khush GS, Coffman WR, Tanksley SD (1988) Molecular mapping of rice chromosome. Theor Appl Genet 26:815–829

    Article  Google Scholar 

  • Miao LL, Wang CL, Zheng CK, Che JY, Gao Y, Wen YC, Li GQ, Zhao KJ (2010) Molecular mapping of a new gene for resistance to rice bacterial blight. Sci Agric Sin 43:3051–3058

    CAS  Google Scholar 

  • Nakamura T, Yagi Y, Kobayashi K (2012) Mechanistic insight into pentatricopeptide repeat proteins as sequence-specific RNA-binding proteins for organellar RNAs in plants. Plant Cell Physiol 53:1171–1179

    Article  PubMed  CAS  Google Scholar 

  • Naramoto S, Kleine-Vehn J, Robert S, Fujimoto M, Dainobu T, Paciorek T, Ueda T, Nakano A, Van Montagu MC, Fukuda H, Friml J (2010) ADP-ribosylation factor machinery mediates endocytosis in plant cells. Proc Natl Acad Sci USA 107:21890–21895

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Nielsen ME, Feechan A, Böhlenius H, Ueda T, Thordal-Christensen H (2012) Arabidopsis ARF-GTP exchange factor, GNOM, mediates transport required for innate immunity and focal accumulation of syntaxin PEN1. Proc Natl Acad Sci USA 109:11443–11448

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Niño-Liu DO, Ronald PC, Bogdanove AJ (2006) Xanthomonas oryzae pathovars: model pathogens of a model crop. Mol Plant Pathol 7:303–324

    Article  PubMed  Google Scholar 

  • Sakai H, Lee SS, Tanaka T, Numa H, Kim J, Kawahara Y, Wakimoto H, Yang CC, Iwamoto M, Abe T, Yamada Y, Muto A, Inokuchi H, Ikemura T, Matsumoto T, Sasaki T, Itoh T (2013) Rice annotation project database (RAP-DB): an integrative and interactive database for rice genomics. Plant Cell Physiol 54:e6. doi:10.1093/pcp/pcs183

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Song WY, Wang GL, Chen LL, Kim HS, Pi LY, Holsten T, Gardner J, Wang B, Zhai WX, Zhu LH, Fauquet C, Ronald P (1995) A receptor kinase-like protein encoded by the rice disease resistance gene, Xa21. Science 270:1804–1806

    Article  PubMed  CAS  Google Scholar 

  • Sosso D, Canut M, Gendrot G, Dedieu A, Chambrier P, Barkan A, Consonni G, Rogowsky PM (2012) PPR8522 encodes a chloroplast-targeted pentatricopeptide repeat protein necessary for maize embryogenesis and vegetative development. J Exp Bot 63:5843–5857

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Suh JP, Jeung JU, Noh TH, Cho YC, Park SH, Park HS, Shin MS, Kim CK, Jena KK (2013) Development of breeding lines with three pyramided resistance genes that confer broad-spectrum bacterial blight resistance and their molecular analysis in rice. Rice 6:5. doi:10.1186/1939-8433-6-5

    Article  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, encodes an LRR receptor kinase-like protein. Plant J 37:517–527

    Article  PubMed  CAS  Google Scholar 

  • Tan GX, Ren X, Weng QM, Shi ZY, Zhu LL, He GC (2004) Mapping of a new resistance gene to bacterial blight in rice line introgressed from Oryza officinalis. Acta Genet Sin 31:724–729

    PubMed  CAS  Google Scholar 

  • Tian D, Wang J, Zeng X, Gu K, Qiu C, Yang X, Zhou Z, Goh M, Luo Y, Murata-Hori M, White FF, Yin Z (2014) The rice TAL effector-dependent resistance protein XA10 triggers cell death and calcium depletion in the endoplasmic reticulum. Plant Cell. http://www.plantcell.org/cgi/doi/10.1105/tpc.113.119255

  • Wang CL, Qi HX, Pan HJ, Li JB, Fan YL, Zhang Q, Zhao KJ (2005) EST-markers flanking the rice bacterial blight resistance gene Xa23 and their application in marker-assisted selection. Sci Agric Sin 38:1996–2001

    CAS  Google Scholar 

  • Wang CL, Chen LT, Zeng CZ, Zhang QY, Liu PQ, Liu YG, Fan YL, Zhang Q, Zhao KJ (2006) Chromosome walking for fine mapping of Xa23 gene locus by using genomic libraries. Chin J Rice Sci 20:355–360

    CAS  Google Scholar 

  • Wang CT, Wen GS, Lin XH, Liu XQ, Zhang DP (2009) Identification and fine mapping of the new bacterial blight resistance gene, Xa31(t), in rice. Eur J Plant Pathol 123:235–240

    Article  CAS  Google Scholar 

  • Wang CL, Qin TF, Yu H, Zhang XP, Che JY, Gao Y, Zheng CK, Yang B, Zhao KJ (2013) The broad bacterial blight resistance of rice line CBB23 is triggered by a novel TAL effector of Xanthomonas oryzae pv. oryzae. Mol Plant. doi:10.1111/mpp.12092

    Google Scholar 

  • Xiang Y, Cao Y, Xu C, Li X, Wang S (2006) Xa3, conferring resistance for rice bacterial blight and encoding a receptor kinase-like protein, is the same as Xa26. Theor Appl Genet 113:1347–1355

    Article  PubMed  CAS  Google Scholar 

  • Xin Z, Mandaokar A, Chen J, Last RL, Browse J (2007) Arabidopsis ESK1 encodes a novel regulator of freezing tolerance. Plant J 49:786–799

    Article  PubMed  CAS  Google Scholar 

  • Yoshimura S, Yamanouchi U, Katayose Y, Toki S, Wang ZX, Kono I, Kurata 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

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Zhang Q, Lin SC, Zhao BY, Wang CL, Yang WC, Zhou YL, Li DY, Chen CB, Zhu LH (1998) Identifying of a new gene for resistance to bacterial blight from O. rufipogon. Rice Genet Newsl 15:138–142

    Google Scholar 

  • Zhang Q, Wang CL, Zhao KJ, Yang WC, Qiao F, Zhou YL, Jiang QX, Liu GC (2002) Development of near- isogenic line CBB23 with a new resistance gene to bacterial blight in rice and its application. Chin J Rice Sci 16:206–210

    CAS  Google Scholar 

  • Zheng CK, Wang CL, Yu YJ, Liang YT, Zhao KJ (2009) Identification and molecular mapping of Xa32(t), a novel resistance gene for bacterial blight (Xanthomonas oryzae pv. oryzae) in rice. Acta Agron Sin 35:1173–1180

    CAS  Google Scholar 

  • Zhou YL, Xu JL, Zhou SC, Yu J, Xie XW, Xu MR, Sun Y, Zhu LH, Fu BY, Gao YM, Li ZK (2009) Pyramiding Xa23 and Rxo1 for resistance to two bacterial diseases into an elite indica rice variety using molecular approaches. Mol Breed 23:279–287

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by the National High-Technology Research Program (The “863” Program: Grant No. 2006AA10Z106) of Ministry of Science and Technology of China and National Natural Science Foundation of China (Grant No. 31171812).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Kaijun Zhao.

Additional information

Communicated by S. Hohmann.

C. Wang, Y. Fan and C. Zheng contributed equally to this work.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wang, C., Fan, Y., Zheng, C. et al. High-resolution genetic mapping of rice bacterial blight resistance gene Xa23 . Mol Genet Genomics 289, 745–753 (2014). https://doi.org/10.1007/s00438-014-0848-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00438-014-0848-y

Keywords

Navigation