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Full-genome analysis of resistance gene homologues in rice

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Abstract

The availability of the rice genome sequence enabled the global characterization of nucleotide-binding site (NBS)–leucine-rich repeat (LRR) genes, the largest class of plant disease resistance genes. The rice genome carries approximately 500 NBS–LRR genes that are very similar to the non-Toll/interleukin-1 receptor homology region (TIR) class (class 2) genes of Arabidopsis but none that are homologous to the TIR class genes. Over 100 of these genes were predicted to be pseudogenes in the rice cultivar Nipponbare, but some of these are functional in other rice lines. Over 80 other NBS-encoding genes were identified that belonged to four different classes, only two of which are present in dicotyledonous plant sequences present in databases. Map positions of the identified genes show that these genes occur in clusters, many of which included members from distantly related groups. Members of phylogenetic subgroups of the class 2 NBS–LRR genes mapped to as many as ten different chromosomes. The patterns of duplication of the NBS–LRR genes indicate that they were duplicated by many independent genetic events that have occurred continuously through the expansion of the NBS–LRR superfamily and the evolution of the modern rice genome. Genetic events, such as inversions, that inhibit the ability of recently duplicated genes to recombine promote the divergence of their sequences by inhibiting concerted evolution.

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References

  • Aarts N, Metz M, Holub E, Staskawicz BJ, Daniels MJ, Parker JE (1998) Different requirements for EDS1 and NDR1 by disease resistance genes define at least two R gene-mediated signaling pathways in Arabidopsis. Proc Natl Acad Sci USA 95:10306–10311

    Article  CAS  PubMed  Google Scholar 

  • Arnheim N (1983) Concerted evolution of multigene families. In: Nei M, Koehn RK (eds) Evolution of genes and proteins. Sinauer, Sunderland, Mass., pp 38–61

    Google Scholar 

  • Axtell MJ, McNellis TW, Mudgett MB, Hsu CS, Staskawicz BJ (2001) Mutational analysis of the Arabidopsis RPS2 disease resistance gene and the corresponding Pseudomonas syringae avrRpt2 avirulence gene. Mol Plant Microbe Interact 14:181–188

    CAS  PubMed  Google Scholar 

  • Bai J, Pennill L, Ning J, Lee SW, Ramalingam J, Webb CA, Zhao B, Sun Q, Nelson JC, Leach JE, Hulbert SH (2002) Diversity of nucleotide binding site-leucine-rich repeat genes in cereals. Genome Res 12:1871–1884

    Article  CAS  PubMed  Google Scholar 

  • Baumgarten A, Cannon S, Spangler R, May G (2003) Genome-level evolution of resistance genes in Arabidopsis thaliana. Genetics 165:309–319

    CAS  PubMed  Google Scholar 

  • Bennetzen JL, Freeling M (1993) Grasses as a single genetic system: genome composition, colinearity and compatibility. Trends Genet 9:259–261

    Article  CAS  PubMed  Google Scholar 

  • Bennetzen JL, Ramakrishna W (2003) Numerous small rearrangements of gene content, order and orientation differentiate grass genomes. Plant Mol Biol 48:821–827

    Article  Google Scholar 

  • Berruyer R, Adreit H, Milazzo J, Gaillard S, Berger A (2003) Identification and fine mapping of Pi33, the rice resistance genes corresponding to the Magnaporthe grisea avirulence gene ACE1. Theor Appl Genet 107:1139–1147

    Article  CAS  PubMed  Google Scholar 

  • Bryan GT, Wu K-S, Farrall L, Jia Y, Hershey HP, McAdams SA, Donaldson GK, Tarchini R, Valent B (2000) A single amino acid difference distinguishes resistant and susceptible alleles of the rice blast resistance gene Pi-ta. Plant Cell 12:2033–2046

    Article  CAS  PubMed  Google Scholar 

  • Burge C, Karlin S (1997) Prediction of complete gene structures in human genomic DNA. J Mol Biol 268:78–94

    Article  CAS  PubMed  Google Scholar 

  • Cannon SB, Zhu H, Baumgarten AM, Spangler R, May G, Cook DR, Young ND (2002) Diversity, distribution, and ancient taxonomic relationships within the TIR and non-TIR NBS–LRR resistance gene subfamilies. J Mol Evol 54:548–562

    Article  CAS  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 M, Presting G, Barbazuk W, Goicoechea JL, Blackmon B, Fang G, Kim H (2002) An integrated physical and genetic map of the rice genome. Plant Cell 14:537–545

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Conaway-Bormans CA, Marchetti MA, Johnson CW, McClung AM, Park WD (2003) Molecular markers linked to the blast resistance gene Pi-z in rice for use in marker-assisted selection. Theor Appl Genet 107:1014–1020

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Dinesh-Kumar SP, Baker BJ (2000) Alternatively spliced N resistance gene transcripts: their possible role in tobacco mosaic virus resistance. Proc Natl Acad Sci USA 97:1908–1913

    Article  CAS  PubMed  Google Scholar 

  • Dooner HK, Martinez-Ferez IM (1997) Recombination occurs uniformly within the bronze gene, a meiotic recombination hotspot in the maize genome. Plant Cell 9:1633–1646

    Article  CAS  PubMed  Google Scholar 

  • Dover GA (1982) Molecular drive: a cohesive mode of species evolution. Nature 199:111–117

    Google Scholar 

  • Feng Q, Zhang Y, Hao P, Wang S, Fu G, Huang Y, Li Y, Zhu J, Liu Y, Hu X, Jia P, Zhang Y, Zhao Q, Ying K, Yu S, Tang Y, Weng Q, Zhang L, Lu Y, Mu J, Lu Y, Zhang LS, Yu Z, Fan D, Liu X, Lu T, Li C, Wu Y, Sun T, Lei H, Li T, Hu H, Guan J, Wu M, Zhang R, Zhou B, Chen Z, Chen L, Jin Z, Wang R, Yin H, Cai Z, Ren S, Lv G, Gu W, Zhu G, Tu Y, Jia J, Zhang Y, Chen J, Kang H, Chen X, Shao C, Sun Y, Hu Q, Zhang X, Zhang W, Wang L, Ding C, Sheng H, Gu J, Chen S, Ni L, Zhu F, Chen W, Lan L, Lai Y, Cheng Z, Gu M, Jiang J, Li J, Hong G, Xue Y, Han B (2002) Sequence and analysis of rice chromosome 4. Nature 420:316–320

    Article  CAS  PubMed  Google Scholar 

  • Goff SA, Ricke D, Lan TH, Presting G, Wang R, Dunn M, Glazebrook J, Sessions A, Oeller P, Varma H, Hadley D, Hutchison D, Martin C, Katagiri F, Lange BM, Moughamer T, Xia Y, Budworth P, Zhong J, Miguel T, Paszkowski U, Zhang S, Colbert M, Sun WL, Chen L, Cooper B, Park S, Wood TC, Mao L, Quail P, Wing R, Dean R, Yu Y, Zharkikh A, Shen R, Sahasrabudhe S, Thomas A, Cannings R, Gutin A, Pruss D, Reid J, Tavtigian S, Mitchell J, Eldredge G, Scholl T, Miller RM, Bhatnagar S, Adey N, Rubano T, Tusneem N, Robinson R, Feldhaus J, Macalma T, Oliphant A, Briggs S (2002) A draft seqeunce of the rice genomes (Oryza sativa L. ssp. japonica). Science 296:92–100

    Article  CAS  PubMed  Google Scholar 

  • Gu K,Tian D, Yang F, Wu L, Sreekala C, Wang D, Wang G-L, 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  CAS  PubMed  Google Scholar 

  • Harushima Y, Yano M, Shomura A, Sato M, Shimano T, Kuboki Y, Yamamoto T, Lin SY, Antonio BA, Parco A, Kajiya H, Huang N, Yamamoto K, Nagamura Y, Kurata N, Khush GS, Sasaki T (1998) A high-density rice genetic linkage map with 2,275 markers using a single F2 population. Genetics 148:479–494

    PubMed  Google Scholar 

  • Henikoff JG, Greene EA, Pietrokovski S, Henikoff S (2000) Increased coverage of protein families with the Blocks Database servers. Nucleic Acids Res 28:228–230

    Article  CAS  PubMed  Google Scholar 

  • Hulbert SH, Webb CA, Smith SM, and Sun Q (2001) Resistance gene complexes: evolution and utilization. Annu Rev Phytopathol 39:285–312

    Article  CAS  PubMed  Google Scholar 

  • Jeanmougin F, Thompson JD, Guoy M, Higgins DG, Gibson TJ (1988) Multiple sequence alignment with Clustal X. Trends Biochem Sci 10:403–405

    Google Scholar 

  • Jeon J-S, Chen D, Yi G-H, Wang GL, Ronald PC (2003) Genetic and physical mapping of Pi5(t), a locus associated with broad-spectrum resistance to rice blast. Mol Gen Genet 269:280–289

    CAS  Google Scholar 

  • Jiang J, Wang S (2002) Identification of a 118-kb DNA fragment containing the locus of blast resistance gene Pi-2(t) in rice. Mol Genet Genomics 268:249–252

    Article  CAS  PubMed  Google Scholar 

  • Kikuchi S, Satoh K, Nagata T, Kawagashira N, Doi K, Kishimoto N, Yazaki J, Ishikawa M, Yamada H, Ooka H, Hotta I, Kojima K, Namiki T, Ohneda E, Yahagi W, Suzuki K, Li CJ, Ohtsuki K, Shishiki T, Otomo Y, Murakami K, Iida Y, Sugano S, Fujimura T, Suzuki Y, Tsunoda Y, Kurosaki T, Kodama T, Masuda H, Kobayashi M, Xie Q, Lu M, Narikawa R, Sugiyama A, Mizuno K, Yokomizo S, Niikura J, Ikeda R, Ishibiki J, Kawamata M, Yoshimura A, Miura J, Kusumegi T, Oka M, Ryu R, Ueda M, Matsubara K, Kawai J, Carninci P, Adachi J, Aizawa K, Arakawa T, Fukuda S, Hara A, Hashizume W, Hayatsu N, Imotani K, Ishii Y, Itoh M, Kagawa I, Kondo S, Konno H, Miyazaki A, Osato N, Ota Y, Saito R, Sasaki D, Sato K, Shibata K, Shinagawa A, Shiraki T, Yoshino M, Hayashizaki Y, Yasunishi A (2003) Collection, mapping, and annotation of over 28,000 cDNA clones from japonica rice. Science 301:376–379

    Article  PubMed  Google Scholar 

  • Kilian HF, Chen JP, Kudrna D, Steffenson B, Yamamoto K, Matsumoto T, Sasaki T, Kleinhofs A (1999) Sequence analysis of a rice BAC covering the syntenous barley Rpg1 region. Genome 42:1071–1076

    Article  PubMed  Google Scholar 

  • Leister D, Kurth J, Laurie DA, Yano M, Sasaki T, Devos K, Graner A, Schulze-Lefert P (1998) Rapid reorganization of resistance gene homologues in cereal genomes. Proc Natl Acad Sci USA 95:370–375

    Article  CAS  PubMed  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 Genet Genomics 261:58–63

    Article  CAS  Google Scholar 

  • Liu G, Lu G, Zeng L, Wang G-L (2002) Two broad-spectrum blast resistance genes, Pi9(t) and Pi2(t), are physically linked on rice chromosome 6. Mol Genet Genomics 267:472–480

    Article  CAS  PubMed  Google Scholar 

  • Meyers BC, Morgante M, Michelmore RW (2002) TIR-X and TIR–NBS proteins: two new families related to disease resistance TIR–NBS–LRR proteins encoded in Arabidopsis and other plant genomes. Plant J 32:77–92

    Article  CAS  PubMed  Google Scholar 

  • Meyers BC, Kozik A, Griego A, Kuang H, Michelmore RW (2003) Genome-wide analysis of NBS–LRR-encoding genes in Arabidopsis. Plant Cell 15:809–834

    Article  CAS  PubMed  Google Scholar 

  • Michelmore RW, Meyers BC (1998) Clusters of resistance genes in plants evolve by divergent selection and a birth-and-death process. Genome Res 8:1113–1130

    CAS  PubMed  Google Scholar 

  • Mondragon-Palomino M, Meyers BC, Michelmore RW, Gaut BS (2003) Patterns of positive selection in the complete NBS–LRR gene family of Arabidopsis thaliana. Genome Res 12:1305–1325

    Article  Google Scholar 

  • Nicholas KB, Nicholas HB, Deerfield DW (1997) GeneDoc: analysis and visualization of genetic variation. Embnet News 4:1–4

    Google Scholar 

  • Pan Q, Liu Y-S, Budai-Hadrian O, Sela M, Carmel-Goren L, Zamir D, Fluhr R (2000a) Comparative genetics of nucleotide binding site-leucine rich repeat resistance gene homologues in the genomes of two dicotyledons: tomato and Arabidopsis. Genetics 155:309–322

    CAS  PubMed  Google Scholar 

  • Pan Q, Wendel J, Fluhr R (2000b) Divergent evolution of plant NBS–LRR resistance gene homologues in dicot and cereal genomes. J Mol Evol 50:203–213

    CAS  PubMed  Google Scholar 

  • Parniske M, Jones JDG (1999) Recombination between diverged clusters of the tomato Cf-9 plant disease resistance gene family. Proc Natl Acad Sci USA 96:5850–5855

    Article  CAS  PubMed  Google Scholar 

  • Porter BW, Chittoor JM, Yano M, Sasaki T, White FF (2003) Development of mapping markers linked to the rice bacterial blight resistance gene Xa7. Crop Sci 43:1484–1492

    CAS  Google Scholar 

  • Ramalingam J, Vera Cruz CM, Kukreja K, Chittoor JM, Wu JL, Lee SW, Baraoidan MR, George ML, Cohen M, Hulbert SH, Leach JE, Leung H (2003) Candidate resistance genes from rice, barley, and maize and their association with qualitative and quantitative resistance in rice. Mol Plant Microbe Interact 16:14–24

    CAS  PubMed  Google Scholar 

  • Richly E, Kurth J, Leister D (2002) Mode of amplification and reorganization of resistance genes during recent Arabidopsis thaliana evolution. Mol Biol Evol 19:76–84

    CAS  PubMed  Google Scholar 

  • Salamov A, Solovyev V (2001) Ab initio gene finding in Drosophila genomic DNA. Genome Res 10:516–522

    Article  Google Scholar 

  • Sallaud C, Lorieux M, Roumen E, Tharreau D, Berruyer R, Svestasrani P, Garsmeur O, Ghesquiere A, Notteghem JL (2003) Identification of five new blast resistance genes in the highly blast-resistant rice variety IR64 using a QTL mapping strategy. Theor Appl Genet 106:794–803

    CAS  PubMed  Google Scholar 

  • Salmeron JM, Oldroyd GED, Tommens CMT, Scofield SR, Kim H-S, Lavelle DT, Dahlbeck D, Staskawicz BJ (1996) Tomato Prf is a member of the leucine-rich repeat class of plant disease resistance genes and lies embedded within the Pto kinase gene cluster. Cell 86:123–133

    Article  CAS  PubMed  Google Scholar 

  • Sasaki T, Matsumoto T, Yamamoto K, Sakata K, Baba T, Katayose Y, Wu J, Niimura Y, Cheng Z, Nagamura Y, Antonio BA, Kanamori H, Hosokawa S, Masukawa M, Arikawa K, Chiden Y, Hayashi M, Okamoto M, Ando T, Aoki H, Arita K, Hamada M, Harada C, Hijishita S, Honda M, Ichikawa Y, Idonuma A, Iijima M, Ikeda M, Ikeno M, Ito S, Ito T, Ito Y, Ito Y, Iwabuchi A, Kamiya K, Karasawa W, Katagiri S, Kikuta A, Kobayashi N, Kono I, Machita K, Maehara T, Mizuno H, Mizubayashi T, Mukai Y, Nagasaki H, Nakashima M, Nakama Y, Nakamichi Y, Nakamura M, Namiki N, Negishi M, Ohta I, Ono N, Saji S, Sakai K, Shibata M, Shimokawa T, Shomura A, Song J, Takazaki Y, Terasawa K, Tsuji K, Waki K, Yamagata H, Yamane H, Yoshiki S, Yoshihara R, Yukawa K, Zhong H, Iwama H, Endo T, Ito H, Hahn JH, Kim HI, Eun MY, Yano M, Jiang J, Gojobori T (2002) The genome sequence and structure of rice chromosome 1. Nature 420:312–316

    Article  CAS  PubMed  Google Scholar 

  • Sun Q, Collins NC, Ayliffe M, Smith SM, Drake J, Pryor A, Hulbert SH (2001) Recombination between paralogues at the rp1 rust resistance locus in maize. Genetics 158:423–438

    CAS  PubMed  Google Scholar 

  • Tabien E, Li Z, Patterson AH, Marchetti A, Stansel W, Pinson M (2002) Mapping QTLs for field resistance to the rice blast pathogen and evaluating their individual and combined utility in improved varieties. Theor Appl Genet 105:313–324

    Article  CAS  PubMed  Google Scholar 

  • Tao Y, Yuan F, Leister RT, Ausubel FM, Katagiri F (2000) Mutational analysis of the Arabidopsis nucleotide binding site-leucine-rich repeat resistance gene RPS2. Plant Cell 12:2541–2554

    Article  CAS  PubMed  Google Scholar 

  • Tian D, Traw MB, Chen JQ, Kreitman M, Bergelson J (2003) Fitness costs of R-gene-mediated resistance in Arabidopsis thaliana. Nature 423:74–77

    Article  CAS  PubMed  Google Scholar 

  • Tornero P, Chao RA, Luthin WN, Goff SA, Dangl JL (2002) Large-scale structure-function analysis of the ArabidopsisRPM1 disease resistance protein. Plant Cell 14:435–450

    Article  CAS  PubMed  Google Scholar 

  • Vandepoele K, Simillion C, Van de Peer Y (2003) Evidence that rice and other cereals are ancient aneuploids. Plant Cell 15:2192–2202

    Article  CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • Wang ZX, Yano M, Yamanouchi U, Iwamoto M, Monna L, Hayasaka H, Katayose Y, Sasaki T (1999) The Pib gene for rice blast resistance belongs to the nucleotide binding and leucine-rich repeat class of plant disease resistance genes. Plant J 19:55–64

    Article  PubMed  Google Scholar 

  • Ware DH, Jaiswal P, Ni J, Yap IV, Pan X, Clark KY, Teytelman L, Schmidt SC, Zhao W, Chang K, Cartinhour S, Stein LD, McCouch SR (2002) Gramene: a resource for comparative grass genomics. Nucleic Acids Res 30:103–105

    Article  CAS  PubMed  Google Scholar 

  • Webb CA, Richter TE, Collins NC, Nicolas M, Trick HN, Pryor T, Hulbert SH (2002) Genetic and molecular characterization of the maize rp3 rust resistance locus. Genetics 162:381–394

    CAS  PubMed  Google Scholar 

  • Wolfe KH, Gouy M, Yang YW, Sharp PM, Li WH (1989) Date of the monocot-dicot divergence estimated from chloroplast DNA sequence data. Proc Natl Acad Sci USA 86:6201–6205

    CAS  PubMed  Google Scholar 

  • Yoshimura S, Yoshimura A, Iwata N, McCouch SR, Abenes ML, Baraoidan MR, Mew TW, Nelson RJ (1995) Tagging and combining bacterial blight resistance genes in rice using RAPD and RFLP markers. Mol Breed 1:375–387

    CAS  Google Scholar 

  • Yoshimura S, Yamanouchi U, Katayose Y, Toki S, Wang Z-X, Kono I, 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  CAS  PubMed  Google Scholar 

  • Young ND (2000) The genetic architecture of resistance. Curr Opin Plant Biol 3:285–290

    Article  CAS  PubMed  Google Scholar 

  • Yu J, Hu S, Wang J, Wong GK, Li S, Liu B, Deng Y, Dai L, Zhou Y, Zhang X, Cao M, Liu J, Sun J, Tang J, Chen Y, Huang X, Lin W, Ye C, Tong W, Cong L, Geng J, Han Y, Li L, Li W, Hu G, Huang X, Li W, Li J, Liu Z, Li L, Liu J, Qi Q, Liu J, Li L, Li T, Wang X, Lu H, Wu T, Zhu M, Ni P, Han H, Dong W, Ren X, Feng X, Cui P, Li X, Wang H, Xu X, Zhai W, Xu Z, Zhang J, He S, Zhang J, Xu J, Zhang K, Zheng X, Dong J, Zeng W, Tao L, Ye J, Tan J, Ren X, Chen X, He J, Liu D, Tian W, Tian C, Xia H, Bao Q, Li G, Gao H, Cao T, Wang J, Zhao W, Li P, Chen W, Wang X, Zhang Y, Hu J, Wang J, Liu S, Yang J, Zhang G, Xiong Y, Li Z, Mao L, Zhou C, Zhu Z, Chen R, Hao B, Zheng W, Chen S, Guo W, Li G, Liu S, Tao M, Wang J, Zhu L, Yuan L, Yang H (2002) A draft sequence of the rice genome (Oryza sativa L ssp. indica). Science 296:79–92

    Article  CAS  PubMed  Google Scholar 

  • Zhou F, Kurth J, Wei F, Elliot C, Vale G, Yahiaoui N, Keller B, Somerville S, Wise R, Shulze-Lefert P (2001) Cell-autonomous expression of barley Mla1 confers race-specific resistance to the powdery mildew fungus via a Rar1-independent signaling pathway. Plant Cell 13:337–350

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

The authors wish to thank James C. Nelson, Rebecca Nelson, and Jianfa Bai for valuable suggestions for the data analysis and manuscript preparation. This work was supported by National Science Foundation grants 9975971 and 0090883. This is contribution number 04-197-J from the Kansas Agricultural Experiment Station.

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  1. Department of Plant Pathology, Kansas State University, Manhattan, KS, 66506-5502, USA

    B. Monosi, L. Pennill & S. H. Hulbert

  2. Department of Plant Pathology, Cornell University, Ithaca, NY, 14853, USA

    R. J. Wisser

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  1. B. Monosi
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Correspondence to S. H. Hulbert.

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Monosi, B., Wisser, R.J., Pennill, L. et al. Full-genome analysis of resistance gene homologues in rice. Theor Appl Genet 109, 1434–1447 (2004). https://doi.org/10.1007/s00122-004-1758-x

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