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Undesired fertility restoration in msm1 barley associates with two mTERF genes

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Abstract

Key message

The novel Rfm3 locus causing undesired fertility restoration in the msm1 cytoplasm of winter barley is located on the short arm of chromosome 6H.

Abstract

Undesired fertility restoration of cytoplasmic male sterile (CMS) mother lines in absence of the functional Rfm1 restorer gene is a significant problem for hybrid breeding in winter barley. Here, we describe that a novel restorer locus on the short arm of chromosome 6H, designated Rfm3, is closely linked to two mitochondrial transcription termination factor family (mTERF) protein coding genes. Genome-wide association studies in a multiparental mapping population revealed that two of the most significantly associated markers are located very close to these genes, with one marker lying directly within one mTERF gene sequence. Sequences of the candidate genes in the parental lines, segregating individuals and an independent set of breeding lines clearly revealed haplotypes discriminating completely sterile, partially fertile and Rfm1-restorer lines. The haplotypes segregate for several single nucleotide polymorphisms, a 6 bp insertion–deletion (InDel) polymorphism and another 2 bp InDel. CMS-unstable genotypes carrying haplotypes associated with undesired fertility restoration showed significantly higher grain setting on bagged spikes when plants were subjected to elevated temperatures during anthesis, indicating a temperature influence on pollen fertility. SNPs associated with desirable Rfm3 haplotypes can be implemented in marker-assisted selection of stable CMS mother lines.

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Abbreviations

CMS:

Cytoplasmic male sterility

FT:

Fertility index

InDel:

Insertion–deletion

mTERF:

Mitochondrial transcription termination factor

PCA:

Principal component analysis

PPR:

Pentatricopeptide repeat

SD:

Standard deviation

WSS:

Within sum of squares

References

  • Abdel-Ghani AH, Frey FP, Parzies HK (2013) Effect of temperature on the expression of cytoplasmic male sterility in cultivated barley (Hordeum vulgare L.). Plant Breed 132(1):42–47

    Article  Google Scholar 

  • Ahokas H (1979) Cytoplasmic male sterility in barley. III. Maintenance of sterility and restoration of fertility in the msm1 cytoplasm. Euphytica 28:409–419

    Article  Google Scholar 

  • Ahokas H (1980) Cytoplasmic male sterility in barley. Part 7: nuclear genes for restoration. Theor Appl Genet 57:193–202

    Article  CAS  PubMed  Google Scholar 

  • Ahokas H (1982) Cytoplasmic male sterility in barley. XI. The msm2 cytoplasm. Genetics 102:285–295

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ahokas H (2018) Barley CMS detected in Finland in 1976 enabled growing of productive winter-barley F1 hybrids in the European winter-barley zone since 2002. Suomen Maataloustieteellisen Seuran Tiedote 35:1–7

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Aulchenko YS, Ripke S, Isaac A, van Duijn CM (2007) GenABEL: An R library for genome-wide association analysis. Bioinformatics 23:1294–1296

    Article  CAS  PubMed  Google Scholar 

  • Babiychuk E, Vandepoele K, Wissing J, Garcia-Diaz M, De Rycke R, Akbari H, Joubès J, Beeckman T, Jänsch L, Frentzen M, Van Montagu MCE, Kushnir S (2011) Plastid gene expression and plant development require a plastidic protein of the mitochondrial transcription termination factor family. Proc Natl Acad Sci USA 108:6674–6679

    Article  PubMed  Google Scholar 

  • Barkan A, Small I (2014) Pentatricopeptide repeat proteins in plants. Annu Rev Plant Biol 65:415–442

    Article  CAS  PubMed  Google Scholar 

  • Bayer MM, Rapazote-Flores P, Ganal M, Hedley PE, Macaulay M, Plieske J, Ramsay L, Russell J, Shaw PD, Thomas W, Waugh R (2017) Development and evaluation of a barley 50k iSelect SNP array. Front Plant Sci 8:1792

    Article  PubMed  PubMed Central  Google Scholar 

  • Beier S, Himmelbach A, Colmsee C, Zhang X-Q, Barrero RA, Zhang Q, Lin L, Bayer M, Bolser D, Taudien S, Groth M, Felder M, Hastie A, Šimková H, Staňková H, Vrána J, Chan S, Muñoz-Amatriaín M, Ounit R, Wanamaker S, Schmutzer T, Aliyeva-Schnorr L, Grasso S, Tanskanen J, Sampath D, Heavens D, Cao S, Chapman B, Dai F, Han Y, Li H, Li X, Lin C, McCooke JK, Tan C, Wang S, Yin S, Zhou G, Poland JA, Bellgard MI, Houben A, Doležel J, Ayling S, Lonardi S, Langridge P, Muehlbauer GJ, Kersey P, Clark MD, Caccamo M, Schulman AH, Platzer M, Close TJ, Hansson M, Zhang G, Braumann I, Li C, Waugh R, Scholz U, Stein N, Mascher M (2017) Construction of a map-based reference genome sequence for barley, Hordeum vulgare L. Sci. Data 4:170044

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bentolila S, Alfonso AA, Hanson MR (2002) A pentatricopeptide repeat-containing gene restores fertility to cytoplasmic male-sterile plants. Proc Natl Acad Sci USA 99:10887–10892

    Article  CAS  PubMed  Google Scholar 

  • Bernhard T, Friedt W, Voss-Fels KP, Frisch M, Snowdon RJ, Wittkop B (2017a) Heterosis for biomass and grain yield facilitates breeding of productive dual-purpose winter barley hybrids. Crop Sci 57:2405–2418

    Article  Google Scholar 

  • Bernhard T, Friedt W, Snowdon RJ, Wittkop B (2017b) New insights into genotypic thermodependency of cytoplasmic male sterility for hybrid barley breeding. Plant Breed 136:8–17

    Article  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 

  • Brown GG, Formanová N, Jin H, Wargachuk R, Dendy C, Patil P, Laforest M, Zhang J, Cheung WY, Landry BS (2003) The radish Rfo restorer gene of Ogura cytoplasmic male sterility encodes a protein with multiple pentatricopeptide repeats. Plant J 35:262–272

    Article  CAS  PubMed  Google Scholar 

  • Bundessortenamt (2018) Beschreibende Sortenliste Getreide, Mais, Öl- und Faserpflanzen, Leguminosen, Rüben, Zwischenfrüchte 2018. Bundessortenamt, Hannover

    Google Scholar 

  • Chateigner-Boutin A-L, Colas des Francs-Small C, Fujii S, Okuda K, Tanz SK, Small I (2013) The E domains of pentatricopeptide repeat proteins from different organelles are not functionally equivalent for RNS editing. Plant J 74:935–945

    Article  CAS  PubMed  Google Scholar 

  • Chen L, Liu YG (2014) Male sterility and fertility restoration in crops. Annu Rev Plant Biol 65:579–606

    Article  CAS  PubMed  Google Scholar 

  • Cui X, Wise RP, Schnable PS (1996) The rf2 nuclear restorer gene of male-sterile T-cytoplasm maize. Science 272:1334–1336

    Article  CAS  PubMed  Google Scholar 

  • 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 147:1367–1379

    CAS  PubMed  PubMed Central  Google Scholar 

  • Doyle JJ (1990) Isolation of plant DNA from fresh tissue. Focus 12:13–15

    Google Scholar 

  • Fujii S, Toriyama K (2009) Suppressed expression of RETROGRADE-REGULATED MALE STERILITY restores pollen fertility in cytoplasmic male sterile rice plants. PNAS 106(23):9513–9518

    Article  PubMed  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  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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 130:1179–1189

    Article  CAS  PubMed  Google Scholar 

  • Hartigan JA, Wong MA (1979) A k-means clustering algorithm. Ser C Appl Stat 28:100–108

    Article  Google Scholar 

  • Hatzig SV, Frisch M, Breuer F, Nesi N, Docournau S, Wagner M-H, Leckband G, Abbadi A, Snowdon RJ (2015) Genome-wide association mapping unravels the genetic control of seed germination and vigor in Brassica napus. Front Plant Sci 6:221

    Article  PubMed  PubMed Central  Google Scholar 

  • Hockett EA, Aastveit K, Gilbertson KM (1989) Selfing behavior of cytoplasmic male sterile barley in Norway and the United States. Hereditas 111:159–165

    Article  Google Scholar 

  • Hsu Y-W, Wang H-J, Hsieh M-H, Hsieh H-L, Jauh G-Y (2014) Arabidopsis mTERF15 is required for mitochondrial nad2 intron 3 splicing and functional complex I activity. PLoS ONE 9(11):e112360

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hu J, Wang K, Huang W, Liu G, Gao Y, Wang J, Huang Q, Ji Y, Qin X, Wan L, Zhu R, Li S, Yang D, Zhu Y (2012) The rice pentatricopeptide repeat protein Rf5 Restores Fertility in Hong-Lian cytoplasmic male-sterile lines via a complex with the glycine-rich protein GPR162. Plant Cell 24:109–122

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Itabashi E, Iwata N, Fujii S, Kazama T, Toriyama K (2011) The fertility restorer gene, Rf2, for Lead Rice-type cytoplasmic male sterility of rice encodes a mitochondrial glycine-rich protein. Plant J 65:359–367

    Article  CAS  PubMed  Google Scholar 

  • Jordan D, Mace ES, Henzell R, Klein P, Klein R (2010) Molecular mapping and candidate gene identification of the Rf2 gene for pollen fertility restoration in sorghum [Sorghum bicolor (L.) Moench]. Theor Appl Genet 120:1279–1287

    Article  CAS  PubMed  Google Scholar 

  • Jordan D, Klein R, Sakrewski K, Henzell R, Klein P, Mace E (2011) Mapping and characterization of Rf5: a new gene conditioning pollen fertility restoration in A1 and A2 cytoplasm in sorghum (Sorghum bicolor (L.) Moench). Theor Appl Genet 123:383–396

    Article  CAS  PubMed  Google Scholar 

  • Kleine T (2012) Arabidopsis thaliana mTERF proteins: evolution and functional classification. Front Plant Sci 3(233):1–15

    Google Scholar 

  • Kleine T, Leister D (2015) Emerging functions of mammalian and plant mTERFs. Biochem Biophys Acta 1847:786–797

    CAS  PubMed  Google Scholar 

  • Linder T, Park CB, Asin-Cayuela J, Pellegrini M, Larsson N-G, Falkenberg M, Samuelsson T, Gustafsson CM (2005) A family of putative transcription termination factors shared amongst metazoans and plants. Curr Genet 48:265–269

    Article  CAS  PubMed  Google Scholar 

  • Longin CFH, Mühleisen J, Maurer HP, Zhang H, Gowda M, Reif JC (2012) Hybrid breeding in autogamous cereals. Theor Appl Genet 125:1087–1096

    Article  PubMed  Google Scholar 

  • MacQueen J (1967) Some methods for classification and analysis of multivariate observations. In: Proceedings of the Fifth Berkeley Symposium on Mathematical Statistics and Probability, vol 1, pp 281–297

  • Mascher M, Gundlach H, Himmelbach A, Beier S, Twardziok SO, Wicker T, Radchuk V, Dockter C, Hedley PE, Russell J, Bayer M, Ramsay L, Liu H, Haberer G, Zhang XQ, Zhang Q, Barrero A, Li L, Taudien S, Groth M, Felder M, Hastie A, Šimková H, Staňková Vrána J, Chan S, Muñoz-Amatriaín M, Ounit R, Wanamaker S, Bolser D, Colmsee C, Schmutzer T, Aliyeva-Schnorr L, Grasso S, Tanskanen J, Chailyan A, Sampath D, Heavens D, Clissold L, Cao S, Chapman B, Dai F, Han Y, Li H, Li X, Lin C, McCooke JK, Tan C, Wang P, Wang S, Yin S, Zhou G, Poland JA, Bellgard MI, Borisjuk L, Houben A, Doležel J, Ayling S, Lonardi S, Kersey P, Langridge P, Muehlbauer GJ, Clark MD, Caccamo M, Schulman AH, Mayer KFX, Platzer M, Close TJ, Scholz U, Hansson M, Zhang G, Braumann I, Spannagl M, Li C, Waugh R, Stein N (2017) A chromosome conformation capture ordered sequence of the barley genome. Nature 544:427–433

    Article  CAS  Google Scholar 

  • Matsuhira H, Kagami H, Kurata M, Kitazaki K, Matsunaga M, Hamaguchi Y, Hagihara E, Ueda M, Harada M, Muramatsu A, Yui-Kurino R, Taguchi K, Tamagake H, Mikami T, Kubo T (2012) Unusual and typical features of a novel Restorer-of-fertility gene of sugar beet (Beta vulgaris L.). Genetics 192:1347–1358

    Article  CAS  PubMed  PubMed Central  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(4):477–482

    Article  CAS  Google Scholar 

  • Melonek J, Stone JD, Small I (2016) Evolutionary plasticity of restorer-of-fertility-like proteins in rice. Sci Rep 6:35152

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Meskauskiene R, Würsch M, Laloi C, Vidi P-A, Coll NS, Kessler F, Baruah A, Kim C, Apel K (2009) A mutation in the Arabidopsis mTERF-related plastid protein SOLDAT10 activates retrograde signaling and suppresses 1O2-induced cell death. Plant J 60:399–410

    Article  CAS  PubMed  Google Scholar 

  • Mühleisen J, Maurer HP, Stiewe G, Bury P, Reif JC (2013a) Hybrid breeding in barley. Crop Sci 53(3):819–824

    Article  Google Scholar 

  • Mühleisen J, Piepho H-P, Maurer HP, Longin CFH, Reif JC (2013b) Yield stability of hybrids versus lines in wheat, barley and triticale. Theor Appl Genet 127(2):309–316

    Article  PubMed  Google Scholar 

  • Mühleisen J, Piepho H-P, Maurer HP, Zhao Y, Reif JC (2014) Exploitation of yield stability in barley. Theor Appl Genet 127:1949–1962

    Article  PubMed  Google Scholar 

  • Okuda K, Myouga F, Motohashi R, Shinozaki K, Shikanai T (2007) Conserved domain structure of pentatricopeptide repeat proteins involved in chloroplast RNS editing. PNAS 104(19):8178–8183

    Article  CAS  PubMed  Google Scholar 

  • Okuda K, Chateigner-Boutin A-L, Nakamura T, Delannoy E, Sugita M, Myouga F, Motohashi R, Shinozaki K, Small I, Shikanai T (2009) Pentatricopeptide repeat proteins with the DYW motif have distinct molecular functions in RNA editing and RNA cleavage in Arabidopsis chloroplasts. Plant Cell 21:146–156

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Park CB, Asin-Cayuela J, Cámara Y, Shi Y, Pellegrini M, Gaspari M, Wibom R, Hultenby K, Erdjument-Bromage H, Tempst P, Falkenberg M, Gustafsson CM, Larsson N-G (2007) MTERF3 is a negative regulator of mammalian mtDNA transcription. Cell 130:273–285

    Article  CAS  PubMed  Google Scholar 

  • Price AL, Zaitlen NA, Reich D, Patterson N (2010) New approaches to population stratification in genome-wide association studies. Nat Rev Genet 11:459–463

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Quesada V (2016) The roles of mitochondrial transcription termination factors (MTERFs) in plants. Physiol Plant 157:389–399

    Article  CAS  PubMed  Google Scholar 

  • Quesada V, Sarmiento-Mañús R, González-Bayón R, Hricová A, Pérez-Marcos R, Graciá-Martínez E, Medina-Ruiz L, Leyva-Díaz E, Ponce MR, Micol JL (2011) Arabidopsis RUGOSA2 encodes an mTERF family member required for mitochondrion, chloroplast and leaf development. Plant J 68(4):738–753

    Article  CAS  PubMed  Google Scholar 

  • R Development Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org

  • Rizzolatti C, Bury P, Tatara E, Pin PA, Rodde N, Bergès H, Budar F, Mireau H, Gielen JJL (2017) Map-based cloning of the fertility restoration locus Rfm1 in cultivated barley (Hordeum vulgare). Euphytica 213:276

    Article  CAS  Google Scholar 

  • Robles P, Micol JL, Quesada V (2012) Arabidopsis MDA1, a nuclear-encoded protein, functions in chloroplast development and abiotic stress responses. PLoS ONE 7(8):e42924

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Robles P, Micol JL, Quesada V (2015) Mutations in the plant-conserved MTERF9 alter chloroplast gene expression, development and tolerance to abiotic stress in Arabidopsis thaliana. Physiol Plant 154:297–313

    Article  CAS  PubMed  Google Scholar 

  • Saha D, Prasad AM, Srinivasan R (2007) Pentatricopeptide repeat proteins and their emerging roles in plants. Plant Physiol Biochem 45:521–534

    Article  CAS  PubMed  Google Scholar 

  • Shin J-H, Blay S, McNeney B, Graham J (2006) LDheatmap: an R function for graphical display of pairwise linkage disequilibria between single nucleotide polymorphisms. J Stat Softw 16:1–10

    Article  Google Scholar 

  • Shull GH (1908) The composition of a field of maize. J Hered 1:296–301

    Article  Google Scholar 

  • Svishcheva GS, Axenovich TI, Belonogova NM, van Duijn CM, Aulchenko YS (2012) Rapid variance components-based method for whole-genome association analysis. Nat Genet 44:1166–1170

    Article  CAS  PubMed  Google Scholar 

  • Ui H, Sameri M, Pourkheirandish M, Chang M-C, Shimada H, Stein N, Komatsuda T, Handa H (2015) High-resolution genetic mapping and physical map construction for fertility restorer Rfm1 locus in barley. Theor Appl Genet 128(2):283–290

    Article  CAS  PubMed  Google Scholar 

  • Wang Z, Zou Y, Li X, Zhang Q, Chen L, Wu H, Su D, Chen Y, Guo J, Luo D, Long Y, Zhong Y, Liu Y-G (2006) Cytoplasmic male sterility of rice with Boro II cytoplasm is caused by a cytotoxic peptide and is restored by two related PPR motif genes via distinct modes of mRNA silencing. Plant Cell 18:676–687

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Weider C, Stamp P, Christov N, Hüsken A, Foueillassar X, Camp K-H, Munsch M (2009) Stability of cytoplasmic male sterility in maize under different environmental conditions. Crop Sci 49:77–84

    Article  Google Scholar 

  • Wright S (1978) Evolution and genetics of populations. Vol. 4: variability within and among natural populations. The University of Chicago Press, Chicago

    Google Scholar 

  • You FM, Huo N, Gu YQ, M-c Luo, Ma Y, Hane D, Lazo GR, Dvorak J, Anderson OD (2008) BatchPrimer3: a high throughput web application for PCR and sequencing primer design. BMC Bioinform 9:253

    Article  CAS  Google Scholar 

  • Zadoks JC, Chang TT, Konzak CF (1974) A decimal code for the growth stages of cereals. Weed Res 14:415–421

    Article  Google Scholar 

  • Zhao Y, Cai M, Zhang X, Li Y, Zhang J, Zhao H, Kong F, Zheng Y, Qiu F (2014) Genome-wide identification, evolution and expression analysis of mTERF gene family in maize. PLoS ONE 9(4):e94126

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This project was part of the collaborative projects “HybGPS” and “SpeedBarley” coordinated by the Federal Agency of Renewable Resources (FNR) and the Federal Office for Agriculture and Food, respectively, and funded by the Federal Ministry of Food and Agriculture. Thanks are due to the collaborative companies German Seed Alliance GmbH, Ackermann Saatzucht GmbH & Co. KG, Deutsche Saatveredelung AG (DSV), Nordsaat Saatzuchtgesellschaft mbH, Saaten-Union Recherche s.a.s. (SUR), W. von Borries-Eckendorf GmbH & Co. KG (WvB) and Saaten-Union Biotech GmbH (SUB) for their support and cooperation. We are particularly grateful to Dr. Jutta Ahlemeyer, Dr. Jens Vaupel and Astrid Hoffmann (DSV), Dr. Laszlo Cselenyi and Ulrike Avenhaus (WvB), Dr. Charles Snijders (SUR), Dr. Eberhard Laubach (Nordsaat) and Jutta Förster (SUB) for actively supporting this study and for valuable discussions. We also thank Annette Plank, Birgit Keiner, Stavros Tzigos, Lisa Unterberg, Petra Kretschmer and Nadine Biermann (DSV) for their valuable experimental assistance.

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Authors and Affiliations

  1. Department of Plant Breeding, IFZ Research Centre for Biosystems, Land Use and Nutrition, Justus Liebig University, Heinrich-Buff-Ring 26-32, 35392, Giessen, Germany

    Timm Bernhard, Rod J. Snowdon, Wolfgang Friedt & Benjamin Wittkop

  2. Deutsche Saatveredelung AG, Thueler Str. 30, 33154, Salzkotten, Germany

    Michael Koch

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  1. Timm Bernhard
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Author contribution statement

TB conducted the greenhouse and climate chamber trials, did the statistical analyses and the genome-wide association study, prepared the figures and tables and wrote the manuscript. MK and TB developed the sequencing primers and guided the reprocessing of the sequencing data for the candidate gene. TB, BW, WF and RJS conceived the research. BW, WF and RJS provided advice on trial conductance and on genome analysis and data interpretation. MK, BW, WF and RJS edited the manuscript.

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Correspondence to Timm Bernhard.

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Bernhard, T., Koch, M., Snowdon, R.J. et al. Undesired fertility restoration in msm1 barley associates with two mTERF genes. Theor Appl Genet 132, 1335–1350 (2019). https://doi.org/10.1007/s00122-019-03281-9

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