Plant Cell Reports

, Volume 34, Issue 11, pp 1885–1897 | Cite as

Fine mapping of S37, a locus responsible for pollen and embryo sac sterility in hybrids between Oryza sativa L. and O. glaberrima Steud

  • Yumin Shen
  • Zhigang Zhao
  • Hongyang Ma
  • Xiaofeng Bian
  • Yang Yu
  • Xiaowen Yu
  • Haiyuan Chen
  • Linglong Liu
  • Wenwei Zhang
  • Ling Jiang
  • Jiawu Zhou
  • Dayun Tao
  • Jianmin Wan
Original Article


Key message

Hybrid sterility locus S37 between Oryza glaberrima and Oryza sativa results in both pollen and embryo sac sterility.


Interspecific crossing between African cultivated rice Oryza glaberrima and Oryza sativa cultivars is hindered by hybrid sterility. To dissect the mechanism of interspecific hybrid sterility, we developed a near-isogenic line (NIL)-S37 using Dianjingyou1 (DJY1) as the recipient parent and an African cultivated rice variety as the donor parent. Empty pollen and embryo sac sterility were observed in F1 hybrids between DJY1 and NIL-S37. Cytological analyses showed that pollen abortion in the F1 hybrids occurred at the late binucleate stage due to a failure of starch accumulation in pollen grains. In addition, partial abortion of the embryo sac in the F1 hybrid was observed during function megaspore developing into mature embryo sac. Molecular analysis revealed that the semi-sterility was largely caused by the abortion of male and female gametophytes carrying the S37 allele from DJY1. A population of 25,600 plants derived from the hybrid DJY1/NIL-S37 was developed to fine map S37. Based on the physical location of molecular markers, S37 locus was finally delimited to a region of 205 kb on the short arm of chromosome 1 in terms of reference sequences of cv. Nipponbare. Interestingly, an about 97-kb DNA segment was deleted in the NIL-S37 based on BAC clone information of O. glaberrima. Fifty-four open reading frames (ORF) were predicted in this 205-kb region of DJY1, whereas only 31 ORFs were in that of NIL-S37. These results are valuable for cloning of S37 gene and further breaking reproductive isolation between Oryza glaberrima and Oryza sativa cultivars, as well as marker-assisted transferring of the corresponding neutral allele in rice breeding programs.


Hybrid sterility Female gamete abortion Pollen abortion Cytological mechanism Fine mapping 



4′, 6-Diamidino-2-phenylindole






Marker-assisted selection


Microspore mother cell


Near-isogenic line


Open reading frame


Simple sequence repeat


Transmission ratio distortion


Whole-mount stain-clearing laser scanning confocal microscopy



This research was supported by the grants from the Ministry of Agriculture Key Laboratory of the middle and lower reaches of the Yangtze River japonica rice biology and genetic breeding, National Transform Science and Technology Program (2013ZX08001004-002), the Chinese National High Technology Research and Development Program (“863” Program, Nos. 2014AA10A604).

Compliance with ethical standards

Conflict of interest

The authors declare no competing financial interests.

Supplementary material

299_2015_1835_MOESM1_ESM.docx (47 kb)
Supplementary material 1 (DOCX 46 kb)
299_2015_1835_MOESM2_ESM.docx (506 kb)
Supplementary material 2 (DOCX 506 kb)
299_2015_1835_MOESM3_ESM.docx (22 kb)
Supplementary material 3 (DOCX 21 kb)
299_2015_1835_MOESM4_ESM.docx (18 kb)
Supplementary material 4 (DOCX 18 kb)
299_2015_1835_MOESM5_ESM.docx (18 kb)
Supplementary material 5 (DOCX 17 kb)
299_2015_1835_MOESM6_ESM.docx (20 kb)
Supplementary material 6 (DOCX 19 kb)
299_2015_1835_MOESM7_ESM.docx (33 kb)
Supplementary material 7 (DOCX 32 kb)


  1. Attere A, Fatokun C (1983) Reaction of Oryza glaberrima accessions to rice yellow mottle virus. Plant Dis 67:420–421CrossRefGoogle Scholar
  2. Bomblies K (2010) Doomed lovers: mechanism of isolation and incompatibility in plants. Annu Rev Plant Biol 61:109–124CrossRefPubMedGoogle Scholar
  3. Chen LT, Liu YG (2014) Male sterility and fertility restoration in crops. Annu Rev Plant Biol 65:579–606CrossRefPubMedGoogle Scholar
  4. Chen X, Temnykh S, Xu Y, Cho YG, McCouch SR (1997) Development of a microsatellite framework map providing genome-wide coverage in rice (Oryza sativa L.). Theor Appl Genet 95:553–567CrossRefGoogle Scholar
  5. Chen JJ, Ding JH, Ouyang YD, Du HY, Yang JY, Cheng K, Zhao J, Qiu SQ, Zhang XL, Yao JL, Liu KD, Wang L, Xu CG, Li XH, 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. Pro Natl Acad Sci USA 105:11436–11441CrossRefGoogle Scholar
  6. Dellaporta SL, Wood J, Hicks JB (1983) A plant DNA mini preparation: versionII. Plant Mol Biol Rep 1:19–21CrossRefGoogle Scholar
  7. Doi K, Taguchi K, Yoshimura A (1998) A new locus affecting high F1 pollen sterility found in backcross progenies of japonica rice and African rice. Rice Genet Newsl 15:146–148Google Scholar
  8. Doi K, Taguchi K, Yoshimura A (1999) RFLP mapping of S20 and S21 for F1 pollen semi-sterility found in backcross progeny of Oryza sativa and O.glaberrima. Rice Genet Newsl 16:65–68Google Scholar
  9. Garavito A, Guyot R, Lozano J, Gavory F, Samain S, Panaud O, Tohme J, Ghesquiere A, Lorieux M (2010) A genetic model for the female sterility barrier between Asian and African cultivated rice species. Genetics 185:1425–1440PubMedCentralCrossRefPubMedGoogle Scholar
  10. Gutierrez A, Carabali S, Giraldo O, Martinez C, Correa F, Prado G, Tohme J, Lorieux M (2010) Identification of a rice stripe necrosis virus resistance locus and yield component QTLs using Oryza satia × O. glaberrima introgression lines. BMC Plant Biol 10:6PubMedCentralCrossRefPubMedGoogle Scholar
  11. Hu FY, Xu P, Deng XN, Zhou JW, Li J, Tao DY (2006) Molecular mapping of a pollen killer gene S29(t) in Oryza glaberrima and co-linear analysis with S22 in O.glumaepatula. Euphytica 151:273–278CrossRefGoogle Scholar
  12. Ikeda R, Sokei Y, Akintayo I (2009) Seed fertility of F1 hybrids between upland rice NERICA cultivars and Oryza sativa L. or O. glaberrima Steud. Breeding Sci 59:27–35CrossRefGoogle Scholar
  13. Johan D, Jeroen RV (2003) Breeding by design. Trend Plant Sci 8:330–334CrossRefGoogle Scholar
  14. Jones M, Mande S, Aluko K (1997) Diversity and potential of Oryza glaberrima Steud. in upland rice breeding. Breeding Sci 47:395–398Google Scholar
  15. Koide Y, Onishi K, Nishimoto D, Baruah AR, Kanazawa A, Sano Y (2008) Sex-independent transmission ratio distortion system responsible for reproductive barriers between Asian and African rice species. New Phytol 179:888–900CrossRefPubMedGoogle Scholar
  16. Lander ES, Green P, Abrahamson J, Barlow A, Daly MJ, Lincoln SE, Newburg L (1987) MAPMAKER: an interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. Genomics 1:174–181CrossRefPubMedGoogle Scholar
  17. Li H, Lin Y, Heath RM, Zhu MX, Yang Z (1999) Control of pollen tube tip growth by a Rop GTPase-dependent pathway that leads to tip-localized calcium influx. Plant Cell 11:1731–1742PubMedCentralPubMedGoogle Scholar
  18. Li J, Xu P, Deng XN, Zhou JW, Hu FY, Wan JM, Tao DY (2008) Identification of four genes for stable hybrid sterility and an epistatic QTL from a cross between Oryza sativa and Oryza glaberrima. Euphytica 164:699–708CrossRefGoogle Scholar
  19. 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. Pro Natl Acad Sci USA 105:18871–18876CrossRefGoogle Scholar
  20. Lorieux M, Reversat C, Garcia D, Denance C, Jouvenet N, Orieux Y, Bourger N, Pando-Bahuon A, Ghesquière A (2003) Linkage mapping of Has-1 0g, a resistance gene of African rice to the cyst nematode, Heterodera sacchari. Theor Appl Genet 107:691–696CrossRefPubMedGoogle Scholar
  21. Maheshwari S, Barbash (2011) The genetics of hybrid incompatibilities. Annu Rev Genet 45:331–355CrossRefPubMedGoogle Scholar
  22. Majerus V, Bertin P, Lutts S (2007) Effects of iron toxicity on osmotic potential, osmolytes and polyamines concentrations in Africa rice (Oryza glaberrima Steud.). Plant Sci 173:96–105CrossRefGoogle Scholar
  23. Mizuta Y, Harushima Y, Kurata N (2010) Rice pollen hybrid incompatibility caused by reciprocal gene loss of duplicated genes. Proc Natl Acad Sci 107:17–22CrossRefGoogle Scholar
  24. Park SK, Howden R, Twell D (1998) The Arabidopsis thaliana gametophytic mutation Gemini pollen 1 disrupts microspore polarity, division asymmetry and pollen cell fate. Development 125:3789–3799PubMedGoogle Scholar
  25. Sanguinetti CJ, Dias NE, Simpson AJG (1994) Rapid silver staining and recover of PCR products separated on polyacrylamide gels. Biotechniques 17:915–919Google Scholar
  26. Sano Y (1990) The genic nature of gamete eliminator in rice. Genetics 125:183–191PubMedCentralPubMedGoogle Scholar
  27. Sarla N, Swamy B (2005) Oryza glaberrima: a source for the improvement of Oryza sativa. Curr Sci 89:955–963Google Scholar
  28. Spielmeyer W, Ellis M, Chandler P (2002) Semi-dwarf (sd-1), “green revolution” rice, contains a defective gibberellin 20-oxidase gene. Proc Natl Acad Sci USA 99:9043–9048PubMedCentralCrossRefPubMedGoogle Scholar
  29. Taguchi K, Doi K, Yoshimura A (1999) RFLP mapping of S19, a gene for F1 pollen semi-sterility found in backcross progeny of Oryza sativa and O. glaberrima. Rice Genet Newsl 16:70–71Google Scholar
  30. Wan J, Yamaguchi Y, Kato H, Ikehashi H (1996) Two new loci for hybrid sterility in cultivated rice (Oryza sativa L.). Theor Appl Genet 92:183–190CrossRefPubMedGoogle Scholar
  31. Wang Y, Xue Y, Li J (2005) Towards molecular breeding and improvement of rice in China. Trends Plant Sci 10:610–614CrossRefPubMedGoogle Scholar
  32. Wang M, Yu Y, Haberer G, Marri P, Fan C, Goicoechea et al (2014) The genome sequence of African rice (Oryza glaberrima) and evidence for independent domestication. Nat Genet 46:982–988CrossRefPubMedGoogle Scholar
  33. WARDA (West Africa Rice Development Association) (2006) Providing what’s needed. In: WARDA annual report 2005–2006, pp 8–11Google Scholar
  34. Xu P, Zhou JW, Li J, Hu FY, Deng XN, Feng SF, Ren GY, Zhang Z, Deng W, Tao DY (2014) Mapping three new interspecific hybrid sterile loci between Oryza sativa and O. glaberrima. Breeding Sci 63:1–7CrossRefGoogle Scholar
  35. Yamagata Y, Yamamoto E, Aya K, Win KT, Doi K, Sobrizal Ito T, Kanamori H, Wu JZ, Matsumoto T, Matsuoka M, Ashikari M, Yoshimura A (2010) Mitochondrial gene in the nuclear genome induces reproductive barrier in rice. Pro Natl Acad Sci USA 107:1494–1499CrossRefGoogle Scholar
  36. Yang JY, Zhao XB, Cheng K, Du HY, Ouyang YD, Chen JJ, Qiu SQ, Huang JY, Jiang YH, Jiang LW, Ding JH, Wang J, Xu CG, Li XH, Zhang QF (2012) A killer-protector system regulates both hybrid sterility and segregation distortion in rice. Science 337:1336–1340CrossRefPubMedGoogle Scholar
  37. Yogesh V, Aparna D, Patra B, Goel RK, Sidhu JS, Kuldeep S (2007) Identification of new sources of bacterial blight (Xanthomonas oryzae pv. oryzae) resistance in wild Oryza species and O. glaberrima. Plant Genet Res Charact Util 5:108–112CrossRefGoogle Scholar
  38. Zhang DB, Wilson ZA (2009) Stamen specification and anther development in rice. Chin Sci Bull 54:2342–2353CrossRefGoogle Scholar
  39. Zhang YH, Zhao ZG, Zhou JW, Jiang L, Bian XF, Wang Y, Wang CL, Zhong ZZ, Wang JK, Tao DY, Wan JM (2011) Fine mapping of a gene responsible for pollen semi-sterility in hybrids between Oryza sativa L. and O. glaberrima Steud. Mol Breeding 28:323–334CrossRefGoogle Scholar
  40. Zhao ZG, Jiang L, Zhang WW, Yu CY, Zhu SS, Xie K, Tian H, Liu LL, Ikehashi H, Wan JM (2007) Fine mapping of S31, a gene responsible for hybrid embryo-sac abortion in rice (Oryza sativa L.). Planta 226:1087–1096CrossRefPubMedGoogle Scholar
  41. Zhou JW, Xu P, Deng XN, Li J, Hu FY, Ren GY, Zhang Z, Luan YH, Deng W, Zhao ZG, Jiang L, Wan JM, Tao DY (2010) Genetic dissection of a chromosomal region conferring hybrid sterility using multi-donors from Oryza glaberrima. Euphytica 175:395–407CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Yumin Shen
    • 1
  • Zhigang Zhao
    • 1
  • Hongyang Ma
    • 1
  • Xiaofeng Bian
    • 1
  • Yang Yu
    • 1
  • Xiaowen Yu
    • 1
  • Haiyuan Chen
    • 1
  • Linglong Liu
    • 1
  • Wenwei Zhang
    • 1
  • Ling Jiang
    • 1
  • Jiawu Zhou
    • 3
  • Dayun Tao
    • 3
  • Jianmin Wan
    • 1
    • 2
  1. 1.National Key Laboratory for Crop Genetics and Germplasm Enhancement, Jiangsu Plant Gene Engineering Research CenterNanjing Agricultural UniversityNanjingChina
  2. 2.Institute of Crop ScienceChinese Academy of Agricultural SciencesBeijingChina
  3. 3.Food Crops Research InstituteYunnan Academy of Agricultural SciencesKunmingChina

Personalised recommendations