Plant Systematics and Evolution

, Volume 298, Issue 1, pp 33–42 | Cite as

Identification of neutral alleles at pollen sterility gene loci of cultivated rice (Oryza sativa L.) from wild rice (O. rufipogon Griff.)

  • Jin Quan Li
  • Muhammud Qasim Shahid
  • Jiu Huan Feng
  • Xiang Dong Liu
  • Xing Juan Zhao
  • Yong Gen LuEmail author
Original Article


Oryza rufipogon Griff. is the ancestor of Asian cultivated rice (O. sativa L.) and possesses valuable genes for rice breeding. Pollen abortion is one of the major causes of indicajaponica hybrid sterility in rice and it happens due to allelic interaction at the pollen sterility gene loci. A total of six loci (Sa, Sb, Sc, Sd, Se, and Sf) have been found to be associated with F1 pollen sterility between indica and japonica rice, and five of them (all except Sf) have been mapped. Neutral alleles (S n ) at each locus have the potential to overcome the pollen sterility associated with the respective locus. Therefore, exploitation and utilization of neutral alleles have significant importance in overcoming indicajaponica hybrid sterility. In this study, an accession (IRW28) of O. rufipogon, native to China, was selected as paternal to cross with typical japonica (Taichung 65) and indica (Guanglu’ai 4) tester lines, and two F2 populations were developed. The simple sequence repeat markers tightly linked to five pollen sterility loci were applied for genotyping the F2 populations. Chi-squared tests were applied to examine the normal segregation/distortion at each locus. The expected and observed pollen sterility for each locus were estimated. As a result, the genotypes at five pollen sterility gene loci for IRW28 were identified as: Sa i−1/Sa i−1, Sb n /Sb n , Sc i−2/Sc i−2, Sd n /Sd n and Se n /Se n . Our results suggest that IRW28 (O. rufipogon) has the neutral alleles for pollen fertility at the Sb, Sd and Se loci, and these alleles have a good affinity with indica and japonica rice. These neutral alleles provide valuable gene resources to overcome the inter-subspecific hybrid pollen sterility in rice.


Rice Oryza sativa Hybrid sterility Neutral allele Pollen abortion 



The authors thank Professor Gui Quan Zhang and professor Xiao Hua Ding South China Agricultural University for their valuable suggestions throughout this work, and thank Miss Lisa Brown of North Dakota State University, Miss Anja Bus of the Max Planck Institute for Plant Breeding Research for revising the manuscript. This work was funded by the National Key Natural Science Foundation of China (U0631003), the Agricultural Commission of Guangdong Province of China (2003360), and the Natural Science Foundation of Guangdong Province of China (032244).


  1. Chang TT (1976) Origin, evolution, cultivation, dissemination, and diversification of Asian and African rice. Euphytica 25:425–441CrossRefGoogle Scholar
  2. Chen JJ, Ding JH, Ouyang YD, Du HY, Yang JY, Cheng K, Zhao J, Qiu SQ, Zhang XL, Yao JL, Liu K, Wang L, Xu CG, Li XG, Xue YB, Xia M, Ji Q, Lu JF, Xu ML, Zhang QF (2008) A triallelic system of S5 is a major regulator of the reproductive barrier and compatibility of indica–japonica hybrids in rice. Proc Natl Acad Sci U S A 105:11436–11441PubMedCrossRefGoogle Scholar
  3. Ding XH, Zhang ZM, Zeng RZ, Li WT, Zhang GQ (2003) Genotypic identification of Sb locus in the indica-compatible japonica lines of rice (Oryza sativa). Chin J Rice Sci 17:297–301Google Scholar
  4. Ding XH, Zhang ZM, Zeng RZ, Zhang GQ (2005) Genotypic identification of the Sc locus in the indica-compatible japonica lines of rice (Oryza sativa L.). In: Proceedings of the 2005 International Conference on Plant Molecular Breeding, 27–30 Oct, Sanya, China, 53:32–35Google Scholar
  5. Harushima Y, Nakagahra M, Yano M, Sasaki T, Kurata N (2002) Diverse variation of reproductive barriers in three intraspecific rice crosses. Genetics 160:313–322PubMedGoogle Scholar
  6. He GH, Zheng JK, Yin GD, Yang ZL (1994) Gamete fertility of the between indica and japonica. Chin J Rice Sci 8:177–180Google Scholar
  7. Ikehashi H (2009) Why are there indica type and japonica type in rice?—History of the studies and a view for origin of two types. Rice Sci 16:1–13Google Scholar
  8. Ikehashi H, Araki H (1984) Varietal screening for compatibility types revealed in F1 fertility of distant crosses in rice. Jpn J Breed 34:304–312Google Scholar
  9. Ikehashi H, Araki H (1986) Genetics of F1 sterility in remote crosses of rice. In: International Rice Research Institute (ed) Rice genetics. IRRI, Manila, pp 119–130Google Scholar
  10. Ji Q, Lu JF, Chao Q, Gu MH, Xu ML (2005) Delimiting a rice wide-compatibility gene S5n to a 50 kb region. Theor Appl Genet 111:1495–1503PubMedCrossRefGoogle Scholar
  11. Kato S (1930) On the affinity of the cultivated rice varieties of rice plants, Oryza sativa L. J Dept Agri Kyushu Imp Univ 2:241–275Google Scholar
  12. Li WT, Zeng RZ, Zhang ZM, Zhang GQ (2002) Mapping of S-b locus for F1 pollen sterility in cultivated rice using PCR based markers. Acta Bot Sin 44:463–467Google Scholar
  13. Li WT, Zeng RZ, Zhang ZM, Ding XH, Zhang GQ (2006) Fine mapping of locus S-b for F1 pollen sterility in rice (Oryza sativa L.). Chin Sci Bull 51:675–680CrossRefGoogle Scholar
  14. Li JQ, Lu YG, Feng JH, Zhao XJ, Liu XD (2007) The crossability and F1 hybrid fertility between Oryza sativa and other AA genome species. J Plant Genet Resour 8:1–6Google Scholar
  15. Li WT, Zeng RZ, Zhang ZM, Ding XH, Zhang GQ (2008) Identification and fine mapping of S-d, a new locus conferring the partial pollen sterility of intersubspecific F1 hybrids in rice (Oryza sativa L.). Theor Appl Genet 116:915–922PubMedCrossRefGoogle Scholar
  16. Liang YM, Lu G, Li KA, Li DT (1997) Evolutionary genetics of the F1 of O. sativa × O. rufipogon. Southwest China J Agr Sci 10:7–10Google Scholar
  17. Lin SY, Ikehashi H, Yanagihara S, Kawashima A (1992) Segregation distortion via male gametes in hybrids between indica and japonica or wide-compatibility varieties of rice (Oryza sativa L.). Theor Appl Genet 84:812–818CrossRefGoogle Scholar
  18. Liu KD, Zhou ZQ, Xu CG, Zhang QF, Maroof MAS (1996) An analysis of hybrid sterility in rice using a diallele cross of 21 parents involving indica, japonica and wide compatibility varieties. Euphytica 90:275–280CrossRefGoogle Scholar
  19. Liu YS, Zhu LH, Sun JS, He P, Wang YZ, Shen LS (1997) Mapping quantitative trait loci for reproductive barriers occurring in hybrid between indica and japonica rice. Acta Bot Sin 39:1099–1104Google Scholar
  20. Liu HY, Xu CG, Zhang Q (2004) Male and female gamete abortions, and reduced affinity between the uniting gametes as the causes for sterility in an indica/japonica hybrid in rice. Sex Plant Reprod 17:55–62CrossRefGoogle Scholar
  21. Londo JP, Chiang YC, Hung KH, Chiang TY, Schaal BA (2006) Phylogeography of Asian wild rice, Oryza rufipogon, reveals multiple independent domestications of cultivated rice, Oryza sativa. Proc Natl Acad Sci U S A 103:9578–9583PubMedCrossRefGoogle Scholar
  22. Long YM, Zhao LF, Niu BX, Su J, Wu H, Chen YL, Zhang QY, Guo JX, Zhuang CX, Mei MT, Xia JX, Wang L, Wu HB, Liu YG (2008) Hybrid male sterility in rice controlled by interaction between divergent alleles of two adjacent genes. Proc Natl Acad Sci U S A 105:18871–18876PubMedCrossRefGoogle Scholar
  23. Lu C, Pan XG (1993) (1993) Studies on the wide compatibility inheritance of wild rice Dong-Ye, three cultivars 02428, 8504 and CPSL017. Acta Agriculturae Jiangxi 15:61–67Google Scholar
  24. Lu CG, Takabatake K, Ikehashi H (2000) Identification of segregation-distortion-neutral alleles to improve pollen fertility of indica–japonica hybrids in rice (Oryza sativa L.). Euphytica 113:101–107CrossRefGoogle Scholar
  25. Maekawa M, Inukai T, Shinbashi N (1997) Genetic analysis of hybrid sterility caused by anther indehiscence between distantly related rice varieties. Euphytica 94:311–318CrossRefGoogle Scholar
  26. Negra S, Oliveira MM, Jena KK, Mackill D (2009) Integration of genomic tools to assist breeding in the japonica subspecies of rice. Mol Breeding 22:159–168CrossRefGoogle Scholar
  27. Ngangkham U, Parida SK, De S, Kumar KA, Singh AK, Singh NK, Mohapatra T (2010) Genic markers for wild abortive (WA) cytoplasm based male sterility and its fertility restoration in rice. Mol Breeding 26:275–292. doi: 10.1007/s11032-010-9397-1 CrossRefGoogle Scholar
  28. Oka HI (1974) Analysis of genes controlling F1 sterility in rice by the use of isogenic lines. Genetics 77:521–534PubMedGoogle Scholar
  29. Ouyang YD, Chen JJ, Ding JH, Zhang QF (2009) Advances in the understanding of inter-subspecific hybrid sterility and wide-compatibility in rice. Chin Sci Bull 54:2332–2341CrossRefGoogle Scholar
  30. Powell W, Morgante M, Andre C, Hanafey M, Vogel J, Tingey S, Rafalski A (1996) The comparison of RFLP, RAPD, AFLP and SSR (microsatellite) markers for germplasm analysis. Mol Breeding 3:225–238CrossRefGoogle Scholar
  31. Sano Y, Chu YE, Oka HI (1979) Genetic studies of speciation in cultivated rice, 1. Genic analysis for the F1 sterility between O. sativa L. and O. glaberrima. Steud Jpn J Genet 54(2):121–132CrossRefGoogle Scholar
  32. Schulman AH (2006) Molecular markers to assess genetic diversity. Euphytica 158:313–321CrossRefGoogle Scholar
  33. Shi LG, Liu XD, Liu B, Zhao XJ, Wang L, Li JQ, Lu YG (2009) Identifying neutral allele Sb at pollensterility loci in cultivated rice with Oryza rufipogon origin. Chin Sci Bull 54:3813–3821Google Scholar
  34. Wan JM, Ikehashi H (1997) Identification of two types of differentiation in cultivated rice (Oryza sativa L.) detected by polymorphism of isozymes and hybrid sterility. Euphytica 94:151–161CrossRefGoogle Scholar
  35. Wang MX, Zhang HL, Zhang DL, Pan DJ, Li DY, Fan ZL, Qi WY, Sun JL, Yang QW, Li C, Li ZC (2008) Geographical genetic diversity and divergence of common wild rice (O. rufipogon Griff.) in China. Chin Sci Bull 53:3559–3566CrossRefGoogle Scholar
  36. Wei CM, Wang L, Yang YX, Chen ZX, Shahid MQ, Li JQ, Liu XD, Lu YG (2010) Identification of a S5n allele in Oryza rufipogon Griff and its effect on embryo sac fertility. Chin Sci Bull 13:1255–1262CrossRefGoogle Scholar
  37. Yan CJ, Liang GH, Gu SL, Yi CD, Lu JF, Li X, Tang SZ, Gu MH (2003) Molecular marker analysis and genetic basis for sterility of typical indica/japonica hybrids. Acta Genet Sin 30:267–276PubMedGoogle Scholar
  38. Yang CY, Chen ZZ, Zhuang CX, Mei MT, Liu YG (2004) Genetic map and fine physical mapping of the gene S-c for F1 pollen sterility in cultivated rice (Oryza sativa L.). Chin Sci Bull 49:1273–1277Google Scholar
  39. Yi CD, Yan CJ, Liang GH, Zhu LH, Gu MH (2001) RFLP analysis of the effect of wide compatibility genes in Aus variety ‘Dular’. Acta Genet Sin 28:540–549PubMedGoogle Scholar
  40. Yokoo M (1984) Female sterility in an indica–japonica cross of rice. Jpn J Breed 34:219–227Google Scholar
  41. Yuan LP (1987) Strategic hypotheses of breeding for hybrid rice. Hybrid Rice 1:1–3Google Scholar
  42. Zhang GQ, Lu YG (1989) Genetic studies of the hybrid sterility in cultivated rice (Oryza sativa). I. Diallel analysis of the hybrid sterility among isogenic F1 sterile lines. Chin J Rice Sci 3:97–101Google Scholar
  43. Zhang GQ, Lu YG (1993) Genetic studies of the hybrid sterility in cultivated rice (Oryza sativa). II. A genic model for F1 pollen sterility. Acta Genet Sin 20:222–228Google Scholar
  44. Zhang GQ, Lu YG, Liu GF, Yang JC, Zhang H (1993) Genetic studies of the hybrid sterility in cultivated rice (Oryza sativa). III. Allele differentiation of F1 pollen sterility in different types of varieties. Acta Genet Sin 20:541–551Google Scholar
  45. Zhang GQ, Lu YG, Zhang H, Yang JC, Liu GF (1994) Genetic studies on the hybrid sterility in cultivated rice (Oryza sativa). IV. Genotypes for F1 pollen sterility. Acta Genet Sin 21:34–41Google Scholar
  46. Zhang ZS, Lu YG, Liu XD, Feng JH, Zhang GQ (2006) Cytological mechanism of pollen abortion resulting from allelic interaction of F1 pollen sterility locus in rice (Oryza sativa L.). Genetica 127:295–302PubMedCrossRefGoogle Scholar
  47. Zheng KL, Huang N, Bennett J, Khush GS (1995) PCR-based phylogenetic analysis of wide compatibility varieties in Oryza sativa L. Theor Appl Genet 88:65–69Google Scholar
  48. Zhu WY, Li WT, Ding XH, Zhang ZM, Zeng RZ, Zhu HT, Zhang GQ (2008) Preliminary identification of F1 pollen sterility gene S-e in Oryza sativa. J South China Agric University 1:1–5Google Scholar
  49. Zhuang CX, Fu Y, Zhang GQ, Mei MT, Lu YG (2002) Molecular mapping of S-c, an F1 pollen sterility gene in cultivated rice. Euphytica 127:133–138CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Jin Quan Li
    • 1
  • Muhammud Qasim Shahid
    • 1
  • Jiu Huan Feng
    • 1
  • Xiang Dong Liu
    • 1
  • Xing Juan Zhao
    • 1
  • Yong Gen Lu
    • 1
    Email author
  1. 1.State Key Laboratory for Conservation and Utilization of Subtropical Agro-bioresources, College of AgricultureSouth China Agricultural UniversityGuangzhouChina

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