Advertisement

Molecular Genetics and Genomics

, Volume 293, Issue 2, pp 451–462 | Cite as

Exploring the genetics of fertility restoration controlled by Rf1 in common wheat (Triticum aestivum L.) using high-density linkage maps

  • Manuel Geyer
  • Theresa Albrecht
  • Lorenz Hartl
  • Volker Mohler
Original Article

Abstract

Hybrid wheat breeding has the potential to significantly increase wheat productivity compared to line breeding. The induction of male sterility by the cytoplasm of Triticum timopheevii Zhuk. is a widely discussed approach to ensure cross-pollination between parental inbred lines in hybrid wheat seed production. As fertility restoration in hybrids with this cytoplasm is often incomplete, understanding the underlying genetics is a prerequisite to apply this technology. A promising component for fertility restoration is the restorer locus Rf1, which was first detected on chromosome 1A of the restorer accession R3. In the present study, we performed quantitative trait locus (QTL) analyses to locate Rf1 and estimate its effect in populations involving the restorer lines R3, R113 and L19. Molecular markers linked to Rf1 in these populations were used to analyse the genomic target region in T. timopheevii accessions and common wheat breeding lines. The QTL analyses revealed that Rf1 interacted with a modifier locus on chromosome 1BS and the restorer locus Rf4 on chromosome 6B. The modifier locus significantly influenced both the penetrance and expressivity of Rf1. Whereas Rf1 exhibited expressivity higher than that of Rf4, the effects of these loci were not additive. Evaluating the marker haplotype for the Rf1 region, we propose that the restoring Rf1 allele may be derived exclusively from T. timopheevii. The present study demonstrates that interactions between restorer and modifier loci play a critical role in fertility restoration of common wheat with the cytoplasm of T. timopheevii.

Keywords

Cytoplasmic male sterility Hybrid wheat Triticum timopheevii 

Notes

Acknowledgements

We acknowledge the excellent technical assistance of Ruth Torrijos Polo, Andreas Klankermeier, Petra Greim, Sabine Schmidt and the working group Wheat and Oat Breeding Research of the Bavarian State Research Center for Agriculture. We thank Finn Borum for providing the analysed restorer germplasm. The valuable suggestions of Adalbert Bund, Annette Block, Bianca Büttner, and Günther Schweizer are highly appreciated. The authors thank the International Wheat Genome Sequencing Consortium (http://www.wheatgenome.org) for providing pre-publication access to IWGSC RefSeq v1.0. The present study was part of the project “CMS-Hybridweizen” (AZ-1066-13) supported by the Bavarian Research Foundation.

Compliance with ethical standards

Funding

This study was funded by the Bavarian Research Foundation (AZ-1066-13).

Conflict of interest

The authors declare that they have no conflicts of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Supplementary material

438_2017_1396_MOESM1_ESM.pdf (303 kb)
Supplementary figures (PDF 303 KB)
438_2017_1396_MOESM2_ESM.xlsx (34.9 mb)
Supplementary tables (XLSX 35722 KB)

References

  1. Bahl PN, Maan SS (1973) Chromosomal location of male fertility restoring genes in six lines of common wheat. Crop Sci 13:317–320CrossRefGoogle Scholar
  2. Barlow KK, Driscoll CJ (1981) Linkage studies involving two chromosomal male-sterility mutants in hexaploid wheat. Genetics 98:791–799PubMedPubMedCentralGoogle Scholar
  3. Bing-Hua L, Jing-Yang D (1986) A dominant gene for male sterility in wheat. Plant Breed 97:204–209CrossRefGoogle Scholar
  4. Broman KW (2003) Mapping quantitative trait loci in the case of a spike in the phenotype distribution. Genetics 163:1169–1175PubMedPubMedCentralGoogle Scholar
  5. Broman KW, Wu H, Sen S, Churchill GA (2003) R/qtl: QTL mapping in experimental crosses. Bioinformatics 19:889–890CrossRefPubMedGoogle Scholar
  6. 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 100:959–966CrossRefPubMedPubMedCentralGoogle Scholar
  7. Crow JF (1998) 90 years ago: the beginning of hybrid maize. Genetics 148:923–928PubMedPubMedCentralGoogle Scholar
  8. Curtis CA, Lukaszewski AJ (1993) Localization of genes in rye that restore male fertility to hexaploid wheat with timopheevi cytoplasm. Plant Breed 111:106–112CrossRefGoogle Scholar
  9. Dill CL, Wise RP, Schnable PS (1997) Rf8 and Rf* mediate unique T-urf13-transcript accumulation, revealing a conserved motif associated with RNA processing and restoration of pollen fertility in T-cytoplasm maize. Genetics 147:1367–1379PubMedPubMedCentralGoogle Scholar
  10. Du H, Maan SS, Hammond JJ (1991) Genetic analyses of male-fertility restoration in wheat: III. Effects of aneuploidy. Crop Sci 31:319–322CrossRefGoogle Scholar
  11. Endo TR (1982) Gametocidal chromosomes of three Aegilops species in common wheat. Can J Genet Cytol 24:201–206CrossRefGoogle Scholar
  12. FAOSTAT (2017) Food and Agriculture Organization Corporate Statistical Database. http://www.fao.org/faostat/en/#home. Accessed 11 Oct 2017
  13. Fukasawa H (1953) Studies on restoration and substitution of nucleus of Aegilotricum, I. Appearance of male-sterile durum in substitution crosses. Cytologia 18:167–175CrossRefGoogle Scholar
  14. Geyer M, Bund A, Albrecht T, Hartl L, Mohler V (2016) Distribution of the fertility-restoring gene Rf3 in common and spelt wheat determined by an informative SNP marker. Mol Breed 36:167CrossRefGoogle Scholar
  15. Hackauf B, Bauer E, Korzun V, Miedaner T (2017) Fine mapping of the restorer gene Rfp3 from an Iranian primitive rye (Secale cereale L.). Theor Appl Genet 130:1179–1189CrossRefPubMedGoogle Scholar
  16. Haley C, Knott S (1992) A simple regression method for mapping quantitative trait loci in line crosses using flanking markers. Heredity 69:315–324CrossRefPubMedGoogle Scholar
  17. Hayward CF (1975) The status and prospects for hybrid winter wheat. In: Proceedings of the 2nd International Winter Wheat Conference. Zagreb, YugoslaviaGoogle Scholar
  18. Johnson JW, Patterson FL (1977) Interaction of genetic factors for fertility restoration in hybrid wheat. Crop Sci 17:695–699CrossRefGoogle Scholar
  19. Johnson VA, Schmidt JW, Mattern PJ (1967) Hybrid wheat in the US. Plant Food Hum Nutr 14:193–211CrossRefGoogle Scholar
  20. Jošt M (1982) Results of the 4th international wheat restorer germplasm screening nursery 1981. University of Zagreb, Faculty of Agricultural Science, ZagrebGoogle Scholar
  21. Keydel F (1973) Die Restoration der Fertilität in Weizenhybriden. Bayer Landwirtsch Jahrb 50:424–430Google Scholar
  22. Kihara H (1951) Substitution of nucleus and its effects on genome manifestations. Cytologia 16:177–193CrossRefGoogle Scholar
  23. 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, Wisconsin, pp 403–418Google Scholar
  24. Koekemoer FP, Van Eeden E, Bonjean AP. In: Van Ginkel M (ed) (2011) An overview of hybrid wheat production in South Africa and review of current worldwide wheat hybrid developments. In: Bonjean AP, Angus WJ The world wheat book—a history of plant breeding, vol 2. Lavoisier, Paris, pp 907–950Google Scholar
  25. Kosambi DD (1944) The estimation of map distances from recombination values. Ann Eug 12:172–175CrossRefGoogle Scholar
  26. Kučera L (1982) Monosomic analysis of fertility restoration in common wheat “Prof. Marchal”. Euphytica 31:895–900CrossRefGoogle Scholar
  27. Langridge P (2017) Introduction. In: Langridge P (ed) Achieving sustainable cultivation of wheat. Volume 1: breeding, quality traits, pests and diseases. Burleigh Dodds Science Publishing, Cambridge, pp XVIII–XIXGoogle Scholar
  28. Li Z, Zhu W, Ma S, Zhang G, Zhao X, Zhang P, Niu N, Wang J (2014) SSR analysis and identification of fertility restorer genes Rf1 and Rf4 of Triticum timopheevii cytoplasmic male sterility (T-CMS) in wheat (Triticum aestivum L.). J Agric Biotechnol 22:1114–1122Google Scholar
  29. Livers RW (1964) Fertility restoration and its inheritance in cytoplasmic male-sterile wheat. Science 144:420CrossRefGoogle Scholar
  30. 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 126:2791–2801CrossRefPubMedGoogle Scholar
  31. Lu C, Shen L, Tan Z, Xu Y, He P, Chen Y, Zhu L (1996) Comparative mapping of QTLs for agronomic traits of rice across environments using a doubled haploid population. Theor Appl Genet 93:1211–1217CrossRefPubMedGoogle Scholar
  32. Ma ZQ, Sorrells ME (1995) Genetic analysis of fertility restoration in wheat using restriction fragment length polymorphisms. Crop Sci 35:1137–1143CrossRefGoogle Scholar
  33. 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 247:351–357CrossRefPubMedGoogle Scholar
  34. Maan SS (1985) Genetic analyses of male-fertility restoration in wheat. II. Isolation, penetrance, and expressivity of Rf genes. Crop Sci 25:743–748CrossRefGoogle Scholar
  35. Maan SS, Lucken KA, Bravo JM (1984) Genetic analyses of male-fertility restoration in wheat. I. Chromosomal location of Rf genes. Crop Sci 24:17–20CrossRefGoogle Scholar
  36. Mantle PG, Swan DJ (1995) Effect of male sterility on ergot disease spread in wheat. Plant Pathol 44:392–395CrossRefGoogle Scholar
  37. Matsui K, Mano Y, Taketa S, Kawada N, Komatsuda T (2001) Molecular mapping of a fertility restoration locus (Rfm1) for cytoplasmic male sterility in barley (Hordeum vulgare L.). Theor Appl Genet 102:477–482CrossRefGoogle Scholar
  38. Mehrajuddin, Salgotra RK, Gupta BB (2013) Interaction of restorer genes in ‘WA’-type cytoplasmic male sterility system in rice (Oryza sativa L.). Natl Acad Sci Lett 36:259–264CrossRefGoogle Scholar
  39. Melchinger AE, Utz HF, Schön CC (1998) Quantitative trait locus (QTL) mapping using different testers and independent population samples in maize reveals low power of QTL detection and large bias in estimates of QTL effects. Genetics 149:383–403PubMedPubMedCentralGoogle Scholar
  40. Mette MF, Gils M, Longin CFH, Reif JC (2015) Hybrid breeding in wheat. In: Ogihara Y, Takumi S, Handa H (eds) Advances in wheat genetics: from genome to field. Springer, Tokyo, pp 225–232CrossRefGoogle Scholar
  41. Miedaner T, Glass C, Dreyer F, Wilde P, Wortmann H, Geiger HH (2000) Mapping of genes for male-fertility restoration in ‘Pampa’ CMS winter rye (Secale cereale L.). Theor Appl Genet 101:1226–1233CrossRefGoogle Scholar
  42. Oehler E, Ingold M (1966) New cases of male-sterility and new restorer sources in T. aestivum. Wheat Inf Serv 22:1–3Google Scholar
  43. Paradis E, Claude J, Strimmer K (2004) APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20:289–290CrossRefPubMedGoogle Scholar
  44. Plaschke J, Ganal MW, Röder MS (1995) Detection of genetic diversity in closely related bread wheat using microsatellite markers. Theor Appl Genet 91:1001–1007PubMedGoogle Scholar
  45. Pugsley AT, Oram RN (1959) Genic male sterility in wheat. Aust Plant Breed Genet Newsl 14:10–11Google Scholar
  46. R Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  47. Robertson LD, Curtis BC (1967) Monosomic analysis of fertility-restoration in common wheat (Triticum aestivum L.). Crop Sci 7:493–495CrossRefGoogle Scholar
  48. Schmidt JW, Johnson VA, Maan SS (1962) Hybrid-wheat. Neb Exp Station Q 9:9Google Scholar
  49. Schön CC, Utz HF, Groh S, Truberg B, Openshaw S, Melchinger AE (2004) Quantitative trait locus mapping based on resampling in a vast maize testcross experiment and its relevance to quantitative genetics for complex traits. Genetics 167:485–498CrossRefPubMedPubMedCentralGoogle Scholar
  50. Shull GH (1952) Beginnings of the heterosis concept. In: Gowen JW (ed) Heterosis. Iowa State College Press, Ames, pp 14–48Google Scholar
  51. Sinha P, Tomar SMS, 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 141:431–441CrossRefPubMedGoogle Scholar
  52. Tahir CM, Tsunewaki K (1969) Monosomic analysis of Triticum spelta var. duhamelianum, a fertility-restorer for T. timopheevi cytoplasm. Jpn J Genet 44:1–9CrossRefGoogle Scholar
  53. Tang HV, Pedersen JF, Chase CD, Pring DR (2007) Fertility restoration of the sorghum A3 male-sterile cytoplasm through a sporophytic mechanism derived from sudangrass. Crop Sci 47:943–950CrossRefGoogle Scholar
  54. Tsujimoto H, Tsunewaki K (1984) Gametocidal genes in wheat and its relatives. I. Genetic analyses in common wheat of a gametocidal gene derived from Aegilops speltoides. Can J Genet Cytol 26:78–84CrossRefGoogle Scholar
  55. Virmani SS, Edwards IB (1983) Current status and future prospects for breeding hybrid rice and wheat. Adv Agron 36:145–214CrossRefGoogle Scholar
  56. 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 12:787–796CrossRefPubMedPubMedCentralGoogle Scholar
  57. 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 64:5411–5428CrossRefPubMedGoogle Scholar
  58. Wilson JA (1962) Material prepared through DeKalb Agricultural Assoc. Inc Wheat Newsl 9:28–29Google Scholar
  59. Wilson JA, Ross WM (1962) Male sterility interaction of the Triticum aestivum nucleus and Triticum timopheevi cytoplasm. Wheat Inf Serv 14:29–30Google Scholar
  60. Winfield MO, Allen AM, Burridge AJ, Barker GLA, Benbow HR, Wilkinson PA, Coghill J, Waterfall C, Davassi A, Scopes G, Pirani A, Webster T, Brew F, Bloor C, King J, West C, Griffiths S, King I, Bentley AR, Edwards KJ (2016) High-density SNP genotyping array for hexaploid wheat and its secondary and tertiary gene pool. Plant Biotechnol J 14:1195–1206CrossRefPubMedGoogle Scholar
  61. Wricke G, Wilde P, Wehling P, Gieselmann C (1993) An isozyme marker for pollen fertility restoration in the Pampa cms system of rye (Secale cereale L.). Plant Breed 111:290–294CrossRefGoogle Scholar
  62. Wright S (1978) Evolution and the genetics of populations, vol 4. The University of Chicago Press, ChicagoGoogle Scholar
  63. Würschum T, Leiser WL, Weissmann S, Maurer HP (2017) Genetic architecture of male fertility restoration of Triticum timopheevii cytoplasm and fine-mapping of the major restorer locus Rf3 on chromosome 1B. Theor Appl Genet 130:1253–1266CrossRefPubMedGoogle Scholar
  64. Yen FS, Evans LE, Larter EN (1969) Monosomic analysis of fertility restoration in three restorer lines of wheat. Can J Genet Cytol 11:531–546CrossRefGoogle Scholar
  65. Zeileis A (2004) Econometric computing with HC and HAC covariance matrix estimators. J Stat Softw 11:1–17CrossRefGoogle Scholar
  66. Zeileis A, Hothorn T (2002) Diagnostic checking in regression relationships. R News 2:7–10Google Scholar
  67. Zeven AC (1967) Transfer and inactivation of male sterility and sources of restorer genes in wheat. Euphytica 16:183–189CrossRefGoogle Scholar
  68. 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 30:459–464PubMedGoogle Scholar
  69. Zhou K, Wang S, Feng Y, Ji W, Wang G (2008) A new male sterile mutant LZ in wheat (Triticum aestivum L.). Euphytica 159:403–410CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2017

Authors and Affiliations

  1. 1.Institute for Crop Science and Plant BreedingBavarian State Research Center for AgricultureFreisingGermany

Personalised recommendations