Abstract
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A comparative genetics approach allowed to precisely determine the map position of the restorer gene Rfp3 in rye and revealed that Rfp3 and the restorer gene Rfm1 in barley reside at different positions in a syntenic 4RL/6HS segment.
Abstract
Cytoplasmic male sterility (CMS) is a reliable and striking genetic mechanism for hybrid seed production. Breeding of CMS-based hybrids in cereals requires the use of effective restorer genes as an indispensable pre-requisite. We report on the fine mapping of a restorer gene for the Pampa cytoplasm in winter rye that has been tapped from the Iranian primitive rye population Altevogt 14160. For this purpose, we have mapped 41 gene-derived markers to a 38.8 cM segment in the distal part of the long arm of chromosome 4R, which carries the restorer gene. Male fertility restoration was comprehensively analyzed in progenies of crosses between a male-sterile tester genotype and 21 recombinant as well as six non-recombinant BC4S2 lines. This approach allowed us to validate the position of this restorer gene, which we have designated Rfp3, on chromosome 4RL. Rfp3 was mapped within a 2.5 cM interval and cosegregated with the EST-derived marker c28385. The gene-derived conserved ortholog set (COS) markers enabled us to investigate the orthology of restorer genes originating from different genetic resources of rye as well as barley. The observed localization of Rfp3 and Rfm1 in a syntenic 4RL/6HS segment asks for further efforts towards cloning of both restorer genes as an option to study the mechanisms of male sterility and fertility restoration in cereals.
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References
Akagi H, Nakamura A, Yokozeki-Misono Y, Inagaki A, Takahashi H, Mori K, Fujimura T (2004) Positional cloning of the rice Rf-1 gene, a restorer of BT-type cytoplasmic male sterility that encodes a mitochondria-targeting PPR protein. Theor Appl Genet 108:1449–1457. doi:10.1007/s00122-004-1591-2
An D, Zheng Q, Zhou Y, Ma P, Lv Z, Li L, Li B, Luo Q, Xu H, Xu Y (2013) Molecular cytogenetic characterization of a new wheat-rye 4R chromosome translocation line resistant to powdery mildew. Chromosome Res 21:419–432. doi:10.1007/s10577-013-9366-8
Anonymous (2015) Besondere Ernte- und Qualitätsermittlung (BEE 2015) Bundesministerium für Ernährung und Landwirtschaft [ed.], Berlin, 2016. p. 73, ISSN 0178–899 X
Ariyadasa R, Mascher M, Nussbaumer T, Schulte D, Frenkel Z, Poursarebani N, Zhou R, Steuernagel B, Gundlach H, Taudien S, Felder M, Platzer M, Himmelbach A, Schmutzer T, Hedley PE, Muehlbauer GJ, Scholz U, Korol A, Mayer KF, Waugh R, Langridge P, Graner A, Stein N (2014) A sequence-ready physical map of barley anchored genetically by two million single-nucleotide polymorphisms. Plant Physiol 164:412–423. doi:10.1104/pp.113.228213
Bauer E, Schmutzer T, Barilar I, Mascher M, Gundlach H, Martis MM, Twardziok SO, Hackauf B, Gordillo A, Wilde P, Schmidt M, Korzun V, Mayer KF, Schmid K, Schön C-C, Scholz U (2017) Towards a whole-genome sequence for rye (Secale cereale L.). Plant J. 89:853–869. doi:10.1111/tpj.13436
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. doi:10.1007/s001220050871
Curtis CA, Lukaszewski A (1993) Localization of genes in rye that restore male fertility to hexaploid wheat with timopheevii cytoplasm. Plant Breed 111:106–112. doi:10.1111/j.1439-0523.1993.tb00615.x
Dohmen G, Hessberg H, Geiger HH, Tudzynski P (1994) CMS in rye: comparative RFLP and transcript analyses of mitochondria from fertile and male-sterile plants. Theor Appl Genet 89:1014–1048. doi:10.1007/BF00224532
Falke KC, Sušić Z, Hackauf B, Korzun V, Schondelmaier J, Wilde P, Wehling P, Wortmann H, Mank R, Rouppe Voort van der J, Maurer HP, Miedaner T, Geiger HH (2008) Establishment of introgression libraries in hybrid rye (Secale cereale L.) from an Iranian primitive accession as a new tool for rye breeding and genomics. Theor Appl Genet 117:641–652 doi:10.1007/s00122-008-0808-1
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. doi:10.1111/j.1439-0523.2008.01589.x
Frary A, Nesbitt TC, Grandillo S, van der Knaap E, Cong B, Liu JP, Meller J, Elber R, Alpert KB, Tanksley SD (2000) fw2.2: A quantitative trait locus key to the evolution of tomato fruit size. Science 289:85–88. doi:10.1126/science.289.5476.85
Fridman E, Pleban T, Zamir D (2000) A recombination hotspot delimits a wild-species quantitative trait locus for tomato sugar content to 484 bp within an invertase gene. Proc Natl Acad Sci USA 97:4718–4723. doi:10.1073/pnas.97.9.4718
Fu S, Ren Z, Chen X, Yan B, Tan F, Fu T, Tang Z (2014) New wheat-rye 5DS-4RS·4RL and 4RS-5DS·5DL translocation lines with powdery mildew resistance. J Plant Res 127:743–753. doi:10.1007/s10265-014-0659-6
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
Gaborieau L, Brown GG, Mireau H (2016) The propensity of pentatricopeptide repeat genes to evolve into restorers of cytoplasmic male sterility. Front Plant Sci 7:1816. doi:10.3389/fpls.2016.01816
Geiger HH, Miedaner T (1996) Genetic basis and phenotypic stability of male-fertility restoration in rye. Vortr Pflanzenzücht 35:7–38
Geiger HH, Miedaner T (2009) Rye Breeding. In: M. J. Carena (ed.), Cereals (Handbook of Plant Breeding), 157–181, 1st Ed. Springer, New York
Geiger HH, Morgenstern K (1975) Angewandt-genetische Studien zur cytoplasmatischen Pollensterilität bei Winterroggen. Theor Appl Genet 46:269–276. doi:10.1007/BF00281148
Geiger HH, Schnell FW (1970) Cytoplasmic male sterility in rye (Secale cereale L.). Crop Sci 10:590–593. doi:10.2135/cropsci1970.0011183X001000050043x
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. 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. doi:10.1007/s00122-004-1869-4
Hackauf B, Rudd S, van der Voort JR, Miedaner T, Wehling P (2009a) Comparative mapping of DNA sequences in rye (Secale cereale L.) in relation to the rice genome. Theor Appl Genet 118:371–384. doi:10.1007/s00122-008-0906-0
Hackauf B, Stojałowski S, Wortmann H, Wilde P, Fromme FJ, Menzel J, Korzun V, Wehling P (2009b) Minimierung des Mutterkornbefalls im Hybridroggen durch Ansätze der Präzisionszüchtung. J Kulturpfl 61:15–20
Hackauf B, Korzun V, Wortmann H, Wilde P, Wehling P (2012) Development of conserved ortholog set markers linked to the restorer gene Rfp1 in rye. Mol Breed 30:1507–1518. doi:10.1007/s11032-012-9736-5
Haseneyer G, Schmutzer T, Seidel M, Zhou R, Mascher M, Schön C-C, 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. doi:10.1186/1471-2229-11-131
Hedgcoth C, el-Shehawi AM, Wei P, Clarkson M, Tamalis D (2002) A chimeric open reading frame associated with cytoplasmic male sterility in alloplasmic wheat with Triticum timopheevi mitochondria is present in several Triticum and Aegilops species, barley, and rye. Curr Genet 41:357–365. doi:10.1007/s00294-002-0315-x
IBSC The International Barley Genome Sequencing Consortium (2012) A physical, genetic and functional sequence assembly of the barley genome. Nature 491:711–716. doi:10.1038/nature11543
Kleine T, Leister D (2015) Emerging functions of mammalian and plant mTERFs. Biochim Biophys Acta 1847:786–797. doi:10.1016/j.bbabio.2014.12.009
Lurin C, Andrés C, Aubourg S, Bellaoui M, Bitton F, Bruyère C, Caboche M, Debast C, Gualberto J, Hoffmann B, Lecharny A, Le Ret M, Martin-Magniette ML, Mireau H, Peeters N, Renou JP, Szurek B, Taconnat L, Small I (2004) Genome-wide analysis of Arabidopsis pentatricopeptide repeat proteins reveals their essential role in organelle biogenesis. Plant Cell. 2004 Aug;16(8):2089–2103. doi:10.1105/tpc.104.022236
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. doi:10.1007/BF00293203
Martis MM, Zhou R, Haseneyer G, Schmutzer T, Vrána J, Kubaláková M, König S, Kugler KG, Scholz U, Hackauf B, Korzun V, Schön C-C, Dolezel J, Bauer E, Mayer KF, Stein N (2013) Reticulate evolution of the rye genome. Plant Cell 25:3685–3698. doi:10.1105/tpc.113.114553
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. doi:10.1105/tpc.110.082537
McIntosh RA, Yamazaki Y, Dubcovsky J, Rogers J, Morris C, Appels R, Xia XC (2013) Catalogue of gene symbols for wheat. 12th International Wheat Genetics Symposium 8–13 September 2013 Yokohama, Japan
Melonek J, Stone JD, Small I (2016) Evolutionary plasticity of restorer-of-fertility-like proteins in rice. Sci Rep 6:35152. doi:10.1038/srep35152
Michalek W, Kunzel G, Graner A (1999) Sequence analysis and gene identification in a set of mapped RFLP markers in barley (Hordeum vulgare). Genome 42:849–853. doi:10.1139/g99-03
Miedaner T, Geiger HH (2015) Biology, genetics, and management of ergot (Claviceps spp.) in rye, sorghum, and pearl millet. Toxins 7:659–678. doi:10.3390/toxins7030659
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. doi:10.1007/s00122-002-1153-4
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. doi:10.1111/j.1439-0523.2004.01038.x
Miedaner T, Mirdita V, Rodemann B, Drobeck T, Rentel, D (2010) Genetic variation of winter rye cultivars for their ergot (Claviceps purpurea) reaction tested in a field design with minimized interplot interference. Plant Breed 129:58–62. doi:10.1111/j.1439-0523.2009.01646.x
Miedaner T, Herter CP, Goßlau H, Wilde P, Hackauf B (2017) Correlated effects of exotic pollen-fertility restorer genes on agronomic and quality traits of hybrid rye. Plant Breed. doi:10.1111/pbr.12456
Paterson AH, Bowers JE, Chapman BA (2004) Ancient polyploidization predating divergence of the cereals, and its consequences for comparative genomics. Proc Natl Acad Sci USA 101:9903–9908
Quesada V (2016) The roles of mitochondrial transcription termination factors (MTERFs) in plants. Physiol Plant 157:389–399. doi:10.1111/ppl.12416
Schmalenbach I, March TJ, Bringezu T, Waugh R, Pillen K (2011) High-resolution genotyping of wild barley introgression lines and fine-mapping of the threshability locus thresh-1 using the Illumina GoldenGate Assay. G3 (Bethesda). 1(3):187–196. doi:10.1534/g3.111.000182
Song J, Hedgcoth C (1994) Influence of nuclear background on transcription of a chimeric gene (orf256) and coxI in fertile and cytoplasmic male sterile wheats. Genome 37:203–209
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
Stojałowski S, Lapiński 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. doi:10.1007/s00122-005-0164-3
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. doi:10.1007/s00122-002-1153-4
Sykes T, Yates S, Nagy I, Asp T, Small I, Studer B (2016) In-silico identification of candidate genes for fertility restoration in cytoplasmic male sterile perennial ryegrass (Lolium perenne L.). Genome Biol Evol. doi:10.1093/gbe/evw047
Touzet P, Meyer EH (2014) Cytoplasmic male sterility and mitochondrial metabolism in plants. Mitochondrion 19:166–171. 10.1016/j.mito.2014.04.009
Ui H, Sameri M, Pourkheirandish M, Chang MC, Shimada H, Stein N, Komatsuda T, Handa H (2015) High-resolution genetic mapping and physical map construction for the fertility restorer Rfm1 locus in barley. Theor Appl Genet 128:283–290. doi:10.1007/s00122-014-2428-2
Van Ooijen JW (2006) JoinMap® 4, Software for the calculation of genetic linkage maps in experimental populations. Kyazma B.V. Wageningen
Wang J, Chapman SC, Bonnett DG, Rebetzke GJ, Crouch J (2007) Application of population genetic theory and simulation models to efficiently pyramid multiple genes via marker-assisted selection. Crop Sci 47:582–590. doi:10.2135/cropsci2006.05.0341
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. doi:10.1093/jxb/ert333
Wilkinson PA, Winfield MO, Barker GLA, Allen AM, Burridge A, Coghill JA, Edwards KJ (2012) CerealsDB 2.0: an integrated resource for plant breeders and scientists. BMC Bioinform 13:219. doi:10.1186/1471-2105-13-219
Acknowledgements
Financial support by the German Federal Ministry of Education and Research granted through the Projektträger Jülich within the RYE-SELECT consortium is gratefully acknowledged (grant no. 0315946 A, B, D, E). We are grateful to F. Joachim Fromme (HYBRO Saatzucht GmbH & Co. KG) for providing seeds of the inbred line L2053-N. Excellent technical assistance of Rita Friedrich, Bärbel Lieberherr, and Regina Voss is gratefully acknowledged.
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122_2017_2879_MOESM1_ESM.xls
ESM 1—PCR primers and conditions for the 4RL COS-markers.[aDesignated according to EST consensus identifiers deposited in the TIGR database]. Supplementary material 1 (XLS 39 KB)
122_2017_2879_MOESM2_ESM.xls
ESM 2—Summary of the COS-marker development for the Rfp3 region.[aNovel rye markers designated according to EST consensus identifiers of rye Sce_assembly02 (Haseneyer et al. 2001; http://www.gabipd.org/download/cgi-bin/Download.pl.cgi?Mode=DownloadNow&File=Rye/Sce_Assembly02.fasta) and Genbank entries of barley fl-cDNAs;bRFLP probe identifier, barley fl-cDNA clone ID, as well as NAS marker ID according to Ui et al. (2015);cThe TIGR identifier for rice genes;dThe identifier for Brachypodium distachyon (Bd) and Sorghum bicolor (Sb) genes orthologous to the corresponding rice gene;e EST marker mapped in barley according to Mayer et al. (2011).;%: no ortholog identified.Supplementary material 2 (XLS 53 KB)
122_2017_2879_MOESM3_ESM.jpg
ESM 3—Integration of EST-derived markers in the genetic map of introgression library B. SNP polymorphism between the recurrent parent genotype L2053-N and the IL2045-N were identified using the Illumina® iSelect Rye 5K-array and mapped as CAPS markers in the BC1 generation of the cross L2053-N x Altevogt 14160 (Falke et al. 2009). The distinct co-linearity between markers on chromosome 1R and 4R in the BC1 map (A, C) confirmed the previously reported map positions of these markers on chromosomes 1R and 4R in the high density transcript map (B, D) of rye (Martis et al. 2013).Supplementary material 3 (JPG 390 KB)
122_2017_2879_MOESM4_ESM.rtf
ESM4—Multiple sequence alignment of a PPR-like gene in wheat, rye, barley and Brachypodium. The primers used to amplify orthologs of Bradi3g00900 from rye genomic DNA of lines L2053-N and IL2045 are underlined. AK358852: barley full-length cDNA clone NIASHv1084E22, csc941965: Chinese Spring contig 941965. Supplementary material 4 (RTF 1018 KB)
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Hackauf, B., Bauer, E., Korzun, V. et al. Fine mapping of the restorer gene Rfp3 from an Iranian primitive rye (Secale cereale L.). Theor Appl Genet 130, 1179–1189 (2017). https://doi.org/10.1007/s00122-017-2879-3
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DOI: https://doi.org/10.1007/s00122-017-2879-3