Skip to main content
SpringerLink
Log in

Development of conserved ortholog set markers linked to the restorer gene Rfp1 in rye

  • Published:
Molecular Breeding Aims and scope Submit manuscript

Abstract

Restoration of male fertility is a prerequisite for hybrid rye breeding and currently the most straightforward approach to minimize ergot infection in hybrid rye varieties. Molecular markers are important tools for the efficient introgression and management of restorer genes like Rfp1 originating from unadapted genetic resources. Furthermore, closely linked markers flanking Rfp1 are indispensible for identifying and selecting individuals with haplotypes showing recombination between Rfp1 and other gene(s) that reside in close proximity and have a negative influence on yield. We identified orthologous gene sets in rice, Brachypodium, and Sorghum and used these gene models as templates to establish conserved ortholog set (COS) markers for the restorer gene Rfp1 on the long arm of rye chromosome 4R. The novel co-dominant markers delimit Rfp1 within a 0.7-cM interval and allow prediction of Rfp1 genotypes with a precision not feasible before. The COS markers enabled an alignment of the improved genetic map of rye chromosome 4R with wheat and barley maps and allowed identification of regions orthologous to Rfp1 in wheat and barley on the short arms of chromosomes 6D and 6H, respectively. Results obtained in this study revealed that micro-collinearity around the Rfp1 locus in rye is affected by rearrangements relative to other grass genomes. The impact of the novel COS markers for practical hybrid rye breeding is discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Akhunov ED, Akhunova AR, Anderson OD, Anderson JA, Blake N, Clegg MT, Coleman-Derr D, Conley EJ, Crossman CC, Deal KR, Dubcovsky J, Gill BS, Gu YQ, Hadam J, Heo H, Huo N, Lazo GR, Luo MC, Ma YQ, Matthews DE, McGuire PE, Morrell PL, Qualset CO, Renfro J, Tabanao D, Talbert LE, Tian C, Toleno DM, Warburton ML, You FM, Zhang W, Dvorak J (2010) Nucleotide diversity maps reveal variation in diversity among wheat genomes and chromosomes. BMC Genomics 11:702–723

    Article  PubMed  CAS  Google Scholar 

  • Bolot S, Abrouk M, Masood-Quraishi U, Stein N, Messing J, Feuillet C, Salse J (2009) The ‘inner circle’ of the cereal genomes. Curr Opin Plant Biol 12:119–125

    Article  PubMed  CAS  Google Scholar 

  • Börner A, Korzun V, Polley A, Malyshev S, Melz G (1998) Genetics and molecular mapping of a male fertility restoration locus (Rfg1) in rye (Secale cereale L.). Theor Appl Genet 97:99–102

    Article  Google Scholar 

  • Bundessortenamt (2011) Database of descriptive variety lists. http://www.bundessortenamt.de

  • Chase CD (2007) Cytoplasmic male sterility: a window to the world of plant mitochondrial–nuclear interactions. Trends Genet 23:81–90

    Article  PubMed  CAS  Google Scholar 

  • Collins NC, Shirley NJ, Saeed M, Pallotta M, Gustafson JP (2008) An ALMT1 gene cluster controlling aluminum tolerance at the Alt4 locus of rye (Secale cereale L.). Genetics 179:669–682

    Article  PubMed  CAS  Google Scholar 

  • Curtis GA, 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 

  • Desloire S, Gherbi H, Laloui W, Marhadour S, Clouet V, Cattolico L, Falentin C, Giancola S, Renard M, Budar F, Small I, Caboche M, Delourme R, Bendahmane A (2003) Identification of the fertility restoration locus, Rfo, in radish, as a member of the pentatricopeptide-repeat protein family. EMBO Rep 4:588–594

    Article  PubMed  CAS  Google Scholar 

  • Devos KM, Atkinson MD, Chinoy CN, Francis HA, Harcourt RL, Koebner RMD, Liu CJ, Masojć P, Xie DX, Gale MD (1993) Chromosomal rearrangements in the rye genome relative to that of wheat. Theor Appl Genet 85:673–680

    Article  CAS  Google Scholar 

  • Endo TR, Gill BS (1996) The deletion stocks of common wheat. J Hered 87:295–307

    Article  CAS  Google Scholar 

  • Erayman M, Sandhu D, Sidhu D, Dilbirligi M, Baenziger PS, Gill KS (2004) Demarcating the gene-rich regions of the wheat genome. Nucleic Acids Res 32:3546–3565

    Article  PubMed  CAS  Google Scholar 

  • Falke KC, Wilde P, Miedaner T (2009) Rye introgression lines as source of alleles for pollen-fertility restoration in Pampa CMS. Plant Breed 128:528–531

    Article  Google Scholar 

  • Fujii S, Bond CS, Small ID (2011) Selection patterns on restorer-like genes reveal a conflict between nuclear and mitochondrial genomes throughout angiosperm evolution. Proc Natl Acad Sci USA 108:1723–1728

    Article  PubMed  CAS  Google Scholar 

  • Fulton T, van der Hoeven R, Eannetta N, Tanksley S (2002) Identification, analysis and utilization of a conserved ortholog set (COS) markers for comparative genomics in higher plants. Plant Cell 14:1457–1467

    Article  PubMed  CAS  Google Scholar 

  • Geiger HH, Morgenstern KK (1975) Angewandt-genetische Studien zur cytoplasmatischen Pollensterilität bei Winterroggen. Theor Appl Genet 46:269–276

    Google Scholar 

  • Geiger HH, Schnell FW (1970) Cytoplasmic male sterility in rye (Secale cereale L.). Crop Sci 10:590–593

    Article  Google Scholar 

  • Geiger HH, Yuan Y, Miedaner T, Wilde P (1995) Environmental sensitivity of cytoplasmic male sterility (CMS) in Secale cereale L. In: Kück U, Wricke G (eds) Genetic mechanisms for hybrid breeding. Adv Plant Breed 18:7–18, Blackwell Wissenschaftsverlag, Berlin

  • Hackauf B, Wehling P (2005) Approaching the self-incompatibility locus Z in rye (Secale cereale L.) via comparative genetics. Theor Appl Genet 110:832–845

    Article  PubMed  CAS  Google Scholar 

  • Hackauf B, Rudd S, van der Voort JR, Miedaner T, Wehling P (2009) Comparative mapping of DNA sequences in rye (Secale cereale L.) in relation to the rice genome. Theor Appl Genet 118:371–384

    Article  PubMed  CAS  Google Scholar 

  • Haseneyer G, Schmutzer T, Seidel M, Zhou R, Mascher M, Schön CC, Taudien S, Scholz U, Stein N, Mayer KFX, Bauer E (2011) From RNA-seq to large-scale genotyping—genomics resources for rye (Secale cereale L.). BMC Plant Biol 11:131

    Article  PubMed  CAS  Google Scholar 

  • International Brachypodium Initiative (2010) Genome sequencing and analysis of the model grass Brachypodium distachyon. Nature 463:763–768

    Article  Google Scholar 

  • International Rice Genome Sequencing Project (2005) The mapbased sequence of the rice genome. Nature 436:793–800

    Article  Google Scholar 

  • Itebashi E, Iwata N, Fujii S, Kazama T, Toriyama K (2010) The fertlity restorer gene, Rf2, for lead rice-type cytoplasmic male sterility of rice encodes a mitochondrial gylcine-rich protein. Plant J 65:359–367

    Article  Google Scholar 

  • Komori T, Ohta S, Murai N, Takakura Y, Kuraya Y, Suzuki S, Hiei Y, Imaseki H, Nitta N (2004) Map-based cloning of a fertility restorer gene, Rf-1, in rice (Oryza sativa L.). Plant J 37:315–325

    Article  PubMed  CAS  Google Scholar 

  • Künzel G, Korzun L, Meister A (2000) Cytologically integrated physical restriction fragment length polymorphism maps for the barley genome based on translocation breakpoints. Genetics 154:397–412

    PubMed  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  PubMed  CAS  Google Scholar 

  • Mago R, Miah H, Lawrence GJ, Wellings CR, Spielmeyer W, Bariana HS, McIntosh RA, Pryor AJ, Ellis JG (2005) High-resolution mapping and mutation analysis separate the rust resistance genes Sr31, Lr26 and Yr9 on the short arm of rye chromosome 1. Theor Appl Genet 112:41–50

    Article  PubMed  CAS  Google Scholar 

  • Mason-Gamer RJ, Weil CF, Kellogg EA (1998) Granule-bound starch synthase: structure, function, and phylogenetic utility. Mol Biol Evol 15:1658–1673

    Article  PubMed  CAS  Google Scholar 

  • 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 102:477–482

    Article  CAS  Google Scholar 

  • Mayer KF, Martis M, Hedley PE, Simková H, Liu H, Morris JA, Steuernagel B, Taudien S, Roessner S, Gundlach H, Kubaláková M, Suchánková P, Murat F, Felder M, Nussbaumer T, Graner A, Salse J, Endo T, Sakai H, Tanaka T, Itoh T, Sato K, Platzer M, Matsumoto T, Scholz U, Dolezel J, Waugh R, Stein N (2011) Unlocking the barley genome by chromosomal and comparative genomics. Plant Cell 23:1249–1263

    Article  PubMed  CAS  Google Scholar 

  • 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 101:1226–1233

    Article  CAS  Google Scholar 

  • Miedaner T, Wilde P, Wortmann H (2005) Combining ability of non-adapted sources for male-fertility restoration in Pampa CMS of hybrid rye. Plant Breed 124:39–43

    Article  Google Scholar 

  • Miftahudin, Scoles GJ, Gustafson JP (2004) Development of PCR-based codominant markers flanking the Alt3 gene in rye. Genome 47:231–238

    Article  PubMed  CAS  Google Scholar 

  • Paterson AH, Bowers JE, Bruggmann R, Dubchak I, Grimwood J, Gundlach H, Haberer G, Hellsten U, Mitros T, Poliakov A, Schmutz J, Spannagl M, Tang H, Wang X, Wicker T, Bharti AK, Chapman J, Feltus FA, Gowik U, Grigoriev IV, Lyons E, Maher CA, Martis M, Narechania A, Otillar RP, Penning BW, Salamov AA, Wang Y, Zhang L, Carpita NC, Freeling M, Gingle AR, Hash CT, Keller B, Klein P, Kresovich S, McCann MC, Ming R, Peterson DG, Ware D, Mehboob-ur-Rahman, Westhoff P, Mayer KF, Messing J, Rokhsar DS (2009) The Sorghum bicolor genome and the diversification of grasses. Nature 457:551–556

    Article  PubMed  CAS  Google Scholar 

  • Proost S, Van Bel M, Sterck L, Billiau K, Van Parys T, Van de Peer Y, Vandepoele K (2009) PLAZA: a comparative genomics resource to study gene and genome evolution in plants. Plant Cell 21:3718–3731

    Article  PubMed  CAS  Google Scholar 

  • Randhawa HS, Dilbirligi M, Sidhu D, Erayman M, Sandhu D, Bondareva S, Chao S, Lazo GR, Anderson OD, Miftahudin, Gustafson JP, Echalier B, Qi LL, Gill BS, Akhunov ED, Dvorák J, Linkiewicz AM, Ratnasiri A, Dubcovsky J, Bermudez-Kandianis CE, Greene RA, Sorrells ME, Conley EJ, Anderson JA, Peng JH, Lapitan NL, Hossain KG, Kalavacharla V, Kianian SF, Pathan MS, Nguyen HT, Endo TR, Close TJ, McGuire PE, Qualset CO, Gill KS (2004) Deletion mapping of homoeologous group 6-specific wheat expressed sequence tags. Genetics 168:677–686

    Article  PubMed  CAS  Google Scholar 

  • Rieseberg LH, Blackman BK (2010) Speciation genes in plants. Ann Bot 106:439–455

    Article  PubMed  CAS  Google Scholar 

  • Roberti M, Polosa PL, Bruni F, Manzari C, Deceglie S, Gadaleta MN, Cantatore P (2009) The MTERF family proteins: mitochondrial transcription regulators and beyond. Biochim Biophys Acta 1787:303–311

    Article  PubMed  CAS  Google Scholar 

  • Scoles GJ, Evans LE (1979) The genetics of fertility restoration in cytoplasmic male-sterile rye. Can J Genet Cytol 21:417–422

    Google Scholar 

  • Stojałowski S, Jaciubek M, Masojć P (2005) Rye SCAR markers for male fertility restoration in the P cytoplasm are also applicable to marker-assisted selection in the C cytoplasm. J Appl Genet 46:371–373

    PubMed  Google Scholar 

  • Stojałowski S, Łapinski M, Szklarczyk M (2006) Identification of sterility-inducing cytoplasms in rye using the plasmotype–genotype interaction test and newly developed SCAR markers. Theor Appl Genet 112:627–633

    Article  PubMed  Google Scholar 

  • Stracke S, Schilling AG, Förster J, Weiss C, Glass C, Miedaner T, Geiger HH (2003) Development of PCR-based markers linked to dominant genes for male-fertility restoration in Pampa CMS of rye (Secale cereale L.). Theor Appl Genet 106:1184–1190

    PubMed  CAS  Google Scholar 

  • Van Ooijen JW (2006) JoinMap© 4, Software for the calculation of genetic linkage maps in experimental populations. Kyazma B.V, Wageningen

    Google Scholar 

  • Weber WE, Wricke G (1994) Genetic markers in plant breeding. Adv. Plant Breeding 16, 105 p., Paul Parey, Berlin and Hamburg

  • Weng Y, Lazar MD (2002) Comparison of homoeologous group-6 short arm physical maps of wheat and barley reveals a similar distribution of recombinogenic and gene-rich regions. Theor Appl Genet 104:1078–1085

    Article  PubMed  CAS  Google Scholar 

  • 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 111:290–294

    Article  CAS  Google Scholar 

  • Youens-Clark K, Buckler E, Casstevens T, Chen C, Declerck G, Derwent P, Dharmawardhana P, Jaiswal P, Kersey P, Karthikeyan AS, Lu J, McCouch SR, Ren L, Spooner W, Stein JC, Thomason J, Wei S, Ware D (2011) Gramene database in 2010: updates and extensions. Nucleic Acids Res 39(Database issue):D1085–D1094

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

We gratefully acknowledge excellent technical assistance by Marion Hos, Maria T. Goldfisch and Regina Voss.

Author information

Authors and Affiliations

  1. Julius Kühn-Institut, Institute for Breeding Research on Agricultural Crops, Rudolf-Schick-Platz 3a, 18190, Sanitz, Germany

    Bernd Hackauf & Peter Wehling

  2. KWS LOCHOW GmbH, Ferdinand-von-Lochow-Straße 5, 29303, Bergen, Germany

    Viktor Korzun & Peer Wilde

  3. HYBRO Saatzucht GmbH & Co. KG, Kleptow Nr. 53, 17291, Schenkenberg, Germany

    Heinrich Wortmann

Authors
  1. Bernd Hackauf
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Viktor Korzun
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Heinrich Wortmann
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Peer Wilde
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Peter Wehling
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Bernd Hackauf.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hackauf, B., Korzun, V., Wortmann, H. et al. Development of conserved ortholog set markers linked to the restorer gene Rfp1 in rye. Mol Breeding 30, 1507–1518 (2012). https://doi.org/10.1007/s11032-012-9736-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11032-012-9736-5

Keywords

Search

Navigation