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Distribution of the fertility-restoring gene Rf3 in common and spelt wheat determined by an informative SNP marker

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Abstract

Male sterility induced by the cytoplasm of Triticum timopheevii Zhuk. has shown potential for hybrid seed production in common wheat (Triticum aestivum L.). As hybrids produced by this method are often partially sterile, fertility restoration is crucial for implementing this technology in breeding practice. Several restorer genes were identified, of which Rf3 is one of the most effective genes for achieving restoration. Previous studies located Rf3 on chromosome 1B in common and spelt wheat. However, the distribution of Rf3 in these taxa remained unclear. In the present study, we genetically mapped Rf3 using a BC1 population derived from CMS-Sperber and the restorer line Primepi (N = 193). After marker validation in four independent BC1 populations and a diversity panel, we evaluated the distribution of Rf3 in 524 common wheat and 30 European spelt genotypes. In the mapping population, the SNP marker IWB72107 cosegregated with Rf3, whereas IWB14060 was mapped 2.0 cM distal on chromosome 1BS. Surveying the linkage between IWB72107 and Rf3 in the four validation populations revealed map distances that ranged from 0.4 to 2.3 cM. Validation of IWB72107 in the diversity panel showed that it is suitable for marker-assisted selection and related applications. Using this marker, we estimated that 8.8% of the common wheat lines and 66.7% of the spelt cultivars carried the restoring Rf3 allele. We propose that Rf3 explains the restoration capacity of a large proportion of European common wheat lines.

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References

  • Ahmed TA, Tsujimoto H, Sasakuma T (2001) QTL analysis of fertility-restoration against cytoplasmic male sterility in wheat. Genes Genet Syst 76:33–38

    Article  CAS  PubMed  Google Scholar 

  • Bahl PN, Maan SS (1973) Chromosomal location of male fertility restoring genes in six lines of common wheat. Crop Sci 13:317–320

    Article  Google Scholar 

  • Brown-Guedira GL, Singh S, Fritz AK (2003) Performance and mapping of leaf rust resistance transferred to wheat from Triticum timopheevii subsp. armeniacum. Phytopathology 93:784–789

    Article  CAS  PubMed  Google Scholar 

  • Cheng SH, Zhuang JY, Fan YY, Du JH, Cao LY (2007) Progress in research and development on hybrid rice: a super-domesticate in China. Ann Bot 100:959–966

    Article  PubMed  PubMed Central  Google Scholar 

  • Crow JF (1998) 90 years ago: the beginning of hybrid maize. Genetics 148:923–928

    CAS  PubMed  PubMed Central  Google Scholar 

  • Curtis CA, Lukaszewski AJ (1993) Localization of genes in rye that restore male fertility to hexaploid wheat with timopheevi cytoplasm. Plant Breed 111:106–112

    Article  Google Scholar 

  • Fukasawa H (1953) Studies on restoration and substitution of nucleus of Aegilotricum, I. Appearance of male-sterile durum in substitution crosses. Cytologia 18:167–175

    Article  Google Scholar 

  • Geiger HH, Miedaner T (2009) Rye breeding. In: Carena MJ (ed) Cereals (handbook of plant breeding), 1st edn. Springer, New York, pp. 157–181

    Google Scholar 

  • Gowda M, Longin CFH, Lein V, Reif JC (2012) Relevance of specific versus general combining ability in winter wheat. Crop Sci 52:2494–2500

    Article  Google Scholar 

  • Hayward CF (1975) The status and prospects for hybrid winter wheat. In: Proceedings of the 2nd International Winter Wheat Conference. Zagreb, Yugoslavia

  • Hohn CE, Lukaszewski AJ (2016) Engineering the 1BS chromosome arm in wheat to remove the Rf multi locus restoring male fertility in cytoplasms of Aegilops kotschyi, Ae. uniaristata and Ae. mutica. Theor Appl Genet. doi:10.1007/s00122-016-2738-7

    PubMed  Google Scholar 

  • Ingold M (1968) Male sterility and restorer systems in wheat. Euphytica 17:69–74

    Google Scholar 

  • Johnson JW, Patterson FL (1977) Interaction of genetic factors for fertility restoration in hybrid wheat. Crop Sci 17:695–699

    Article  Google Scholar 

  • Johnson VA, Schmidt JW, Mattern PJ (1967) Hybrid wheat in the United States. Plant Food Hum Nutr 14:193–211

    Article  Google Scholar 

  • Keydel F (1973) Die Restoration der Fertilität in Weizenhybriden. Bayer Landwirtsch Jahrb 50:424–430

    Google Scholar 

  • Kihara H (1951) Substitution of nucleus and its effects on genome manifestations. Cytologia 16:177–193

    Article  Google Scholar 

  • Kihara H, Tsunewaki K (1967) Genetic principles applied to the breeding of crop plants. In: Brink RA (ed) Heritage from Mendel. University of Wisconsin Press, Madison, pp. 403–418

    Google Scholar 

  • Koekemoer FP, Van Eeden E, Bonjean AP (2011) An overview of hybrid wheat production in South Africa and review of current worldwide wheat hybrid developments. In: Bonjean AP, Angus WJ, Van Ginkel M (eds) The world wheat book: a history of plant breeding. Lavoisier, Paris, pp 907–950

  • Kojima T, Tsujimoto H, Ogihara Y (1997) High-resolution RFLP mapping of the fertility restoration Rf3 gene against Triticum timopheevi cytoplasm located on chromosome 1BS of common wheat. Genes Genet Syst 72:353–359

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Kučera L (1982) Monosomic analysis of fertility restoration in common wheat “Prof. Marchal”. Euphytica 31:895–900

    Article  Google Scholar 

  • Landjeva S, Korzun V, Ganeva G (2006) Evaluation of genetic diversity among Bulgarian winter wheat (Triticum aestivum L.) varieties during the period 1925–2003 using microsatellites. Genet Resour Crop Evol 53:1605–1614

    Article  CAS  Google Scholar 

  • Livers RW (1964) Fertility restoration and its inheritance in cytoplasmic male-sterile wheat. Science 144:420

    Article  Google Scholar 

  • Longin CFH, Gowda M, Mühleisen J, Ebmeyer E, Kazman E, Schachschneider R, Schacht J, Kirchhoff M, Zhao Y, Reif JC (2013) Hybrid wheat: quantitative genetic parameters and consequences for the design of breeding programs. Theor Appl Genet 126:2791–2801

    Article  PubMed  Google Scholar 

  • Ma ZQ, Sorrells ME (1995) Genetic analysis of fertility restoration in wheat using restriction fragment length polymorphisms. Crop Sci 35:1137–1143

    Article  CAS  Google Scholar 

  • Ma ZQ, Zhao YH, Sorrells ME (1995) Inheritance and chromosomal locations of male fertility restoring gene transferred from Aegilops umbellulata Zhuk. to Triticum aestivum L. Mol Gen Genet 247:351–357

    Article  CAS  PubMed  Google Scholar 

  • Maan SS, Lucken KA, Bravo JM (1984) Genetic analyses of male-fertility restoration in wheat. I. Chromosomal location of Rf genes. Crop Sci 24:17–20

    Article  Google Scholar 

  • Maan SS (1985) Genetic analyses of male-fertility restoration in wheat. II. Isolation, penetrance, and expressivity of Rf genes. Crop Sci 25:743–748

    Article  Google Scholar 

  • Maccaferri M, Ricci A, Salvi S, Milner SG, Noli E, Martelli PL, Casadio R, Akhunov E, Scalabrin S, Vendramin V, Ammar K, Blanco A, Desiderio F, Distelfeld A, Dubcovsky J, Fahima T, Faris J, Korol A, Massi A, Mastrangelo AM, Morgante M, Pozniak C, N’Diaye A, Xu S, Tuberosa R (2015) A high-density, SNP-based consensus map of tetraploid wheat as a bridge to integrate durum and bread wheat genomics and breeding. Plant Biotechnol J 13:648–663

    Article  CAS  PubMed  Google Scholar 

  • Miller JF, Schmidt JW, Johnson VA (1974) Inheritance of genes controlling male-fertility restoration in the wheat cultivar Primépi. Crop Sci 14:437–438

    Article  Google Scholar 

  • Oehler E, Ingold M (1966) New cases of male-sterility and new restorer sources in T. aestivum. Wheat Inf Serv 22:1–3

    Google Scholar 

  • Paradis E, Claude J, Strimmer K (2004) APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20:289–290

    Article  CAS  PubMed  Google Scholar 

  • Patterson FL, Ohm HW, Johnson JW, Wickersham DS (1996) Registration of five wheat pollen fertility restorer germplasm lines: PR143, PR189, PR267, PR270, PR302. Crop Sci 36:1424

    Article  Google Scholar 

  • Plaschke J, Ganal MW, Röder MS (1995) Detection of genetic diversity in closely related bread wheat using microsatellite markers. Theor Appl Genet 91:1001–1007

    CAS  PubMed  Google Scholar 

  • R Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria

  • Schmidt JW, Johnson VA, Maan SS (1962) Hybrid-wheat. Neb Exp Sta Quar 9:9

    Google Scholar 

  • Sinha P, Tomar SMS, Vinod, Singh VK, Balyan HS (2013) Genetic analysis and molecular mapping of a new fertility restorer gene Rf8 for Triticum timopheevi cytoplasm in wheat (Triticum aestivum L.) using SSR markers. Genetica 141:431–441

    Article  CAS  PubMed  Google Scholar 

  • Somers DJ, Isaac P, Edwards K (2004) A high-density microsatellite consensus map for bread wheat (Triticum aestivum L.). Theor Appl Genet 109:1105–1114

    Article  CAS  PubMed  Google Scholar 

  • Tahir CM, Tsunewaki K (1969) Monosomic analysis of Triticum spelta var. duhamelianum, a fertility-restorer for T. timopheevi cytoplasm. Jpn J Genetics 44:1–9

    Article  Google Scholar 

  • Tsunewaki K (2015) Fine mapping of the first multi-fertility-restoring gene, Rf multi, of wheat for three Aegilops plasmons, using 1BS-1RS recombinant lines. Theor Appl Genet 128:723–732

    Article  CAS  PubMed  Google Scholar 

  • Wang S, Wong D, Forrest K, Allen A, Chao S, Huang BE, Maccaferri M, Salvi S, Milner SG, Cattivelli L, Mastrangelo AM, Whan A, Stephen S, Barker G, Wieseke R, Plieske J, International Wheat Genome Sequencing Consortium, Lillemo M, Mather D, Appels R, Dolferus R, Brown-Guedira G, Korol A, Akhunova AR, Feuillet C, Salse J, Morgante M, Pozniak C, Luo M-C, Dvorak J, Morell M, Dubcovsky J, Ganal M, Tuberosa R, Lawley C, Mikoulitch I, Cavanagh C, Edwards KJ, Hayden M, Akhunov E (2014) Characterization of polyploid wheat genomic diversity using a high-density 90,000 single nucleotide polymorphism array. Plant Biotechnol J 12:787–796

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Whitford R, Fleury D, Reif JC, Garcia M, Okada T, Korzun V, Langridge P (2013) Hybrid breeding in wheat: technologies to improve hybrid wheat seed production. J Exp Bot 64:5411–5428

    Article  CAS  PubMed  Google Scholar 

  • Wilson JA (1962) Material prepared through DeKalb Agricultural Assoc. Inc. Wheat Newsl 9:28–29

    Google Scholar 

  • Wilson JA, Ross WM (1962) Male sterility interaction of the Triticum aestivum nucleus and Triticum timopheevi cytoplasm. Wheat Inf Serv 14:29–30

    Google Scholar 

  • Wright S (1978) Evolution and the genetics of populations, volume 4. The University of Chicago Press, Chicago

    Google Scholar 

  • Yen FS, Evans LE, Larter EN (1969) Monosomic analysis of fertility restoration in three restorer lines of wheat. Can J Genet Cytol 11:531–546

    Article  Google Scholar 

  • Zanke CD, Ling J, Plieske J, Kollers S, Ebmeyer E, Korzun V, Argillier O, Stiewe G, Hinze M, Neumann K, Ganal MW, Röder MS (2014) Whole genome association mapping of plant height in winter wheat (Triticum aestivum L.). PLoS One 9:e113287

    Article  PubMed  PubMed Central  Google Scholar 

  • Zeven AC (1967) Transfer and inactivation of male sterility and sources of restorer genes in wheat. Euphytica 16:183–189

    Article  Google Scholar 

  • Zhang C, Wang HY, Shen YZ, Zhao BC, Zhu ZG, Huang ZJ (2003) Location of the fertility restorer gene for T-type CMS wheat by microsatellite marker. Acta Genet Sin 30:459–464

    CAS  PubMed  Google Scholar 

  • Zhou W, Kolb FL, Domier LL, Wang S (2005) SSR markers associated with fertility restoration genes against Triticum timopheevii cytoplasm in Triticum aestivum. Euphytica 141:33–40

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank Ruth Torrijos, Petra Greim, Sabine Schmidt and the working group Wheat and Oat Breeding Research of the Bavarian State Research Center for Agriculture for their excellent technical assistance. The valuable suggestions of Günther Schweizer and Bianca Büttner are highly appreciated. We also thank the breeding companies for providing their breeding material. The present study was part of the project “CMS-Hybridweizen” (AZ-1066-13) supported by the Bavarian Research Foundation.

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Correspondence to Manuel Geyer.

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Geyer, M., Bund, A., Albrecht, T. et al. Distribution of the fertility-restoring gene Rf3 in common and spelt wheat determined by an informative SNP marker. Mol Breeding 36, 167 (2016). https://doi.org/10.1007/s11032-016-0592-6

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