Molecular Breeding

, Volume 33, Issue 3, pp 555–567 | Cite as

Positional cloning of the rice male sterility gene ms-IR36, widely used in the inter-crossing phase of recurrent selection schemes

  • Julien Frouin
  • Denis Filloux
  • James Taillebois
  • Cécile Grenier
  • Fabienne Montes
  • Frédéric de Lamotte
  • Jean-Luc Verdeil
  • Brigitte Courtois
  • Nourollah Ahmadi
Article

Abstract

The monogenetic recessive male-sterile gene ms-IR36 is widely used to facilitate the inter-crossing phase of recurrent selection in rice (Oryza sativa), but its segregation within the progeny disturbs other breeding phases. Marker-assisted early identification of msms and Msms seedlings would help overcome this drawback. Using successively bulked segregant analysis and large F2 populations, we mapped the ms-IR36 gene to a 33-kb region on the short arm of chromosome 2 that includes 10 candidate genes. Sequencing of these candidates together with checking rice genome annotations and expression databases allowed the target to be narrowed down to one candidate gene already isolated and characterized as the tapetum degeneration retardation (TDR) gene and reported to be involved in tapetal programmed cell death. Comparison of the sequence of the TDR gene between male-sterile (MS) and male-fertile (MF) IR36 plants detected one non-synonymous nucleotide substitution affecting the active domain of the encoded protein. Perfect co-segregation was observed between polymorphism at this nucleotide (SNP) and the MS/MF phenotype of 946 F2 plants. Spatial modelling of the active domain of the candidate protein reinforced the candidate status of the only SNP identified. Histological characterization of anther development in MS IR36 revealed defects identical to the ones observed in mutants used for the isolation and characterization of the TDR gene: delayed/non-degradation of tapetum tissue and collapse of the haploid microspores. We concluded that ms-IR36 corresponded to the TDR gene with a different mutation from the earlier one described in the same gene. No significant linkage drag was associated with ms-IR36. A SNP-based marker that enables simple early identification of MS plants and MF plants with the Msms genotype was designed.

Keywords

Rice Male-sterility ms-IR36 Anther development Recurrent selection 

Supplementary material

11032_2013_9972_MOESM1_ESM.xls (100 kb)
Supplementary material 1 (XLS 99 kb)
11032_2013_9972_MOESM2_ESM.pdf (444 kb)
Supplementary figure SF1: Pattern of expression of the seven candidate genes selected based on map data. Expression data were retrieved from RiceXPro database (http://ricexpro.dna.affrc.go.jp/GGEP/index.html) (PDF 443 kb)

References

  1. Buffard-Morel J, Verdeil JL, Pannetier C (1992) Embryogenèse somatique du cocotier (Cocos nucifera L.) à partir d’explant foliaire: étude histologique. Can J Bot 70:735–741CrossRefGoogle Scholar
  2. Chatel M, Guimaraes EP (1997) Recurrent selection in rice using male-sterility gene. CIAT publication no. 276. ISBN 958-9439-90-X. Cali, Colombia, p 77Google Scholar
  3. Comstock RE, Robinson HF, Harvey PH (1949) A breeding procedure designed to make maximum use of both general and specific combining ability. Agron J 41:360–367CrossRefGoogle Scholar
  4. Courtois B, Filloux D, Ahmadi N, Noyer JL, Billot C, Guimaraes EP (2005) Using molecular markers in rice population improvement through recurrent selection. In: Guimaraes EP (ed) Population improvement: a way of exploiting the rice genetic resources of Latin America. FAO, Rome, pp 56–94Google Scholar
  5. da Cunha KS, Pereira MG, Gonçalves LSA, Berilli APCG, de Oliveira ED, Ramos HCC, do Amaral Júnior AD (2012) Full-sib reciprocal recurrent selection in the maize populations Cimmyt and Piranão. Genet Mol Res 11(3):3398–3408CrossRefPubMedGoogle Scholar
  6. Fisher DB (1968) Protein staining of ribboned epon sections for light microscopy. Histochemie 16:92–96CrossRefPubMedGoogle Scholar
  7. Fujimaki H (1979) Recurrent selection by using genetic male sterility for rice improvement. JARQ (Tsukuba) 13(3):153–156Google Scholar
  8. Gallais A (1977) Amélioration des populations, méthodes de sélection et création de variétés. I. Synthèse critique sur les problèmes généraux et sur les bases théoriques pour la sélection récurrente intrapopulation. Ann Amélior Plant 27:281–330Google Scholar
  9. Gallais A (1978) Amélioration des populations, méthodes de sélection et de création de variétés. II. Le concept de valeur variétale et ses conséquences pour la sélection récurrente. Ann Amélior Plant 28:269–287Google Scholar
  10. Gallais A (2009) Full-sib reciprocal recurrent selection with the use of doubled haploids. Crop Sci 49:150–152CrossRefGoogle Scholar
  11. Gaudet M, Fara A-G, Sabatti M, Kuzminsky E, Mugnozza GS (2007) Single-reaction for SNP Genotyping on Agarose Gelby Allele-specific PCR in Black Poplar (Populus nigra L.) Plant Mol Biol Rep 25(1–2):1–9. doi: 10.1007/s11105-007-0003-6
  12. Guimaraes EP (2005) Population improvement: a way of exploiting the rice genetic resources of Latin America. FAO, Rome, pp 56–94Google Scholar
  13. Guo JX, Liu YG (2012) Molecular control of male reproductive development and pollen fertility in rice. J Integr Plant Biol 54(12):967–978CrossRefPubMedGoogle Scholar
  14. Hallauer AR (1985) Compendium of recurrent selection methods and their application. Crit Rev Plant Sci 3:1–33Google Scholar
  15. Hallauer AR, Carena MJ, Miranda Filho JB (2009) Quantitative genetics in maize breeding. Springer, New YorkGoogle Scholar
  16. Hara S (1946) Linkage between factors for sterility and anthocyanin pigmentation in rice plant. Jpn J Genet 21(2):32 (in Japanese)CrossRefGoogle Scholar
  17. Hull F (1945) Recurrent selection for specific combining ability in corn. J Am Soc Agron 37:134–145CrossRefGoogle Scholar
  18. Khera P, Priyadarshi R, Singh A, Mohan R, Gangashetti MG, Singh BN, Kole C, Shenoy V (2012) Molecular characterization of different cytoplasmic male sterile lines using mitochondrial DNA specific markers in rice. J Biol Sci 12:154–160CrossRefGoogle Scholar
  19. Kinoshita T (1995) Report of committee on gene symbolization, nomenclature and linkage groups. Rice Genet Newsl 12:9–153Google Scholar
  20. Ko T, Yamagata H (1987) Gene analysis of male-sterility induced in rice. Studies on the utility of artificial mutations in plant breeding. XVI. Jpn J Breed 37:192–198 (in Japanese with English summary)CrossRefGoogle Scholar
  21. Ko T, Yamagata H (1989) Studies on the induction of male-sterile strains in rice. Linkage groups of few male-sterility genes. Jpn J Breed 39(Suppl. 1):234–235. (in Japanese)Google Scholar
  22. Lee S, Jung KH, An GH, Chung YY (2004) Isolation and characterization of a rice cysteine protease gene, OSCP1, using T-DNA gene-trap system. Plant Mol Biol 54:755–765CrossRefPubMedGoogle Scholar
  23. Li N, Zhang D, Liu HS, Yin CS, Li XX, Liang W, Yuan Z, Xu B, Chu HW, Wang J, Wen TQ, Huang H, Luo D, Ma H, Zhang DB (2006a) The rice tapetum degeneration retardation gene is required for tapetum degradation and anther development. Plant Cell 18:2999–3014CrossRefPubMedCentralPubMedGoogle Scholar
  24. Li X, Duan X, Jiang H, Sun Y, Tang Y, Yuan Z, Guo J, Liang W, Chen L, Wang J, Ma H, Yin J, Zhang D (2006b) Genome-wide analysis of basic/helix-loop-helix transcription factor family in rice and Arabidopsis. Plant Physiol 141:1167–1184CrossRefPubMedCentralPubMedGoogle Scholar
  25. Li S, Yang D, Zhu Y (2007) Characterization and use of male sterility in hybrid rice breeding. J Integr Plant Biol 49(6):791–804CrossRefGoogle Scholar
  26. Liu HS, Chu H, Li H, Wang H, Wei J, Li N, Ding S, Huang H, Ma H, Huang C, Luo D, Yuang Z, Liu J, Zhang D (2005) Genetic analysis and mapping of rice (Oryza sativa L.) male-sterile (OsMS-L) mutant. Chin Sci Bull 50:38–41Google Scholar
  27. Long Y, Zhao L, Niu B, Su J, Wu H, Chen Y, Zhang Q, Guo J, Zhuang C, Mei M, Xia J, Wang L, Wu H, Liu YG (2009) Hybrid male sterility in rice controlled by interaction between divergent alleles of two adjacent genes. Proc Natl Acad Sci USA 105(48):18871–18876CrossRefGoogle Scholar
  28. Ma H (2005) Molecular genetic analyses of microsporogenesis and microgametogenesis in flowering plants. Annu Rev Plant Biol 56:393–434CrossRefPubMedGoogle Scholar
  29. Michelmore RW, Paran I, Kesseli RV (1991) Identification of markers linked to disease-resistance genes by bulked segregant analysis: a rapid method to detect markers in specific genomic regions by using segregating populations. Proc Natl Acad Sci USA 88:9828–9832CrossRefPubMedGoogle Scholar
  30. Oka HI (1983) The indica-japonica differentiation of rice cultivars. A review. In: Proceedings of the 4th international SABRAO congress. 4–8 May 1981, Kuala Lumpur, pp 117–128Google Scholar
  31. Pons JL, Labesse G (2009) @TOME-2: a new pipeline for comparative modeling of protein–ligand complexes. Nucleic Acids Res: 1–7. doi: 10.1093/nar/gkp368
  32. Risterucci AM, Grivet L, N’Goran JAK, Pieretti I, Flament MH, Lanaud C (2000) A high-density linkage map of Theobroma cacao L. Theor Appl Genet 101:948–955CrossRefGoogle Scholar
  33. Rutger JN, Shinio (1980) Male sterility in rice and its potential use in breeding. In: Proceedings of the international rice research conference. Innovative approach to rice breeding. IRRI. Los Banos, The Philippines, pp 53–66Google Scholar
  34. Schwendiman J, Pannetier C, Michaux-Ferriere N (1988) Histology of somatic embryogenesis from leaf explants of the oil palm Elaeis guineensis. Ann Bot 62:43–52Google Scholar
  35. Singh RJ, Ikehashi H (1981) Monogenic male-sterility in rice: introduction, identification and inheritance. Crop Sci 21:286–289CrossRefGoogle Scholar
  36. Suneson CA (1956) An evolutionary plant breeding method. Agron J 48:188–191CrossRefGoogle Scholar
  37. Taillebois JE (2006) CIRAD hybrid rice program: lower breeding costs and sustainability. In: 2nd international rice research congress, 9–13 October 2006, New Delhi, India. CIRAD, Montpellier, FranceGoogle Scholar
  38. Tan HX, Liang WQ, Hu JP, Zhang DB (2012) MICROSPORE AND TAPETUM REGULATOR 1 encodes a secretory fasciclin glycoprotein required for male reproductive development in rice. Dev Cell 22:1127–1137CrossRefPubMedGoogle Scholar
  39. Van Ooijen JW (2006) JoinMap ® 4, Software for the calculation of genetic linkage maps in experimental population. Kyazma B.V, WagningenGoogle Scholar
  40. Zhang H, Liang WQ, Yang XJ, Luo X, Jiang N, Ma H, Zhang DB (2010) Carbon starved anther encodes a MYB domain protein that regulates sugar partitioning required for rice pollen development. Plant Cell 22:672–689CrossRefPubMedCentralPubMedGoogle Scholar
  41. Zhang D, Luo X, Zhu L (2011) Cytological analysis and genetic control of rice anther development. J Genet Genomics 38:379–390CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • Julien Frouin
    • 1
  • Denis Filloux
    • 2
  • James Taillebois
    • 1
  • Cécile Grenier
    • 1
  • Fabienne Montes
    • 1
  • Frédéric de Lamotte
    • 3
  • Jean-Luc Verdeil
    • 1
  • Brigitte Courtois
    • 1
  • Nourollah Ahmadi
    • 1
  1. 1.Cirad, UMR AGAPMontpellier Cedex 5France
  2. 2.Cirad, UMR BGPIMontpellier Cedex 5France
  3. 3.INRA, UMR AGAPMontpellier Cedex 5France

Personalised recommendations