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Undesired fertility restoration in msm1 barley associates with two mTERF genes

  • Timm BernhardEmail author
  • Michael Koch
  • Rod J. Snowdon
  • Wolfgang Friedt
  • Benjamin Wittkop
Original Article
  • 90 Downloads

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.

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

Notes

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.

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.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

The authors declare that the experiments comply with the current laws of Germany.

Supplementary material

122_2019_3281_MOESM1_ESM.docx (26 kb)
Supplementary material 1 (DOCX 25 kb)

References

  1. 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):42–47CrossRefGoogle Scholar
  2. Ahokas H (1979) Cytoplasmic male sterility in barley. III. Maintenance of sterility and restoration of fertility in the msm1 cytoplasm. Euphytica 28:409–419CrossRefGoogle Scholar
  3. Ahokas H (1980) Cytoplasmic male sterility in barley. Part 7: nuclear genes for restoration. Theor Appl Genet 57:193–202CrossRefGoogle Scholar
  4. Ahokas H (1982) Cytoplasmic male sterility in barley. XI. The msm2 cytoplasm. Genetics 102:285–295Google Scholar
  5. 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 35:1–7Google Scholar
  6. 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 108:1449–1457CrossRefGoogle Scholar
  7. Aulchenko YS, Ripke S, Isaac A, van Duijn CM (2007) GenABEL: An R library for genome-wide association analysis. Bioinformatics 23:1294–1296CrossRefGoogle Scholar
  8. 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 108:6674–6679CrossRefGoogle Scholar
  9. Barkan A, Small I (2014) Pentatricopeptide repeat proteins in plants. Annu Rev Plant Biol 65:415–442CrossRefGoogle Scholar
  10. 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 8:1792CrossRefGoogle Scholar
  11. 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 4:170044CrossRefGoogle Scholar
  12. Bentolila S, Alfonso AA, Hanson MR (2002) A pentatricopeptide repeat-containing gene restores fertility to cytoplasmic male-sterile plants. Proc Natl Acad Sci USA 99:10887–10892CrossRefGoogle Scholar
  13. 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 57:2405–2418CrossRefGoogle Scholar
  14. Bernhard T, Friedt W, Snowdon RJ, Wittkop B (2017b) New insights into genotypic thermodependency of cytoplasmic male sterility for hybrid barley breeding. Plant Breed 136:8–17CrossRefGoogle Scholar
  15. 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 97:99–102CrossRefGoogle Scholar
  16. 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 35:262–272CrossRefGoogle Scholar
  17. Bundessortenamt (2018) Beschreibende Sortenliste Getreide, Mais, Öl- und Faserpflanzen, Leguminosen, Rüben, Zwischenfrüchte 2018. Bundessortenamt, HannoverGoogle Scholar
  18. 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 74:935–945CrossRefGoogle Scholar
  19. Chen L, Liu YG (2014) Male sterility and fertility restoration in crops. Annu Rev Plant Biol 65:579–606CrossRefGoogle Scholar
  20. Cui X, Wise RP, Schnable PS (1996) The rf2 nuclear restorer gene of male-sterile T-cytoplasm maize. Science 272:1334–1336CrossRefGoogle Scholar
  21. 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 147:1367–1379Google Scholar
  22. Doyle JJ (1990) Isolation of plant DNA from fresh tissue. Focus 12:13–15Google Scholar
  23. Fujii S, Toriyama K (2009) Suppressed expression of RETROGRADE-REGULATED MALE STERILITY restores pollen fertility in cytoplasmic male sterile rice plants. PNAS 106(23):9513–9518CrossRefGoogle Scholar
  24. 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 108:1723–1728CrossRefGoogle Scholar
  25. Gaborieau L, Brown GG, Mireau H (2016) The propensity of pentatricopeptide repeat genes to evolve into restorers of cytoplasmic male sterility. Front Plant Sci 7:1816CrossRefGoogle Scholar
  26. 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 30:1507–1518CrossRefGoogle Scholar
  27. 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 130:1179–1189CrossRefGoogle Scholar
  28. Hartigan JA, Wong MA (1979) A k-means clustering algorithm. Ser C Appl Stat 28:100–108CrossRefGoogle Scholar
  29. 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 6:221CrossRefGoogle Scholar
  30. Hockett EA, Aastveit K, Gilbertson KM (1989) Selfing behavior of cytoplasmic male sterile barley in Norway and the United States. Hereditas 111:159–165CrossRefGoogle Scholar
  31. 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):e112360CrossRefGoogle Scholar
  32. 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 24:109–122CrossRefGoogle Scholar
  33. 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 65:359–367CrossRefGoogle Scholar
  34. 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 120:1279–1287CrossRefGoogle Scholar
  35. 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 123:383–396CrossRefGoogle Scholar
  36. Kleine T (2012) Arabidopsis thaliana mTERF proteins: evolution and functional classification. Front Plant Sci 3(233):1–15Google Scholar
  37. Kleine T, Leister D (2015) Emerging functions of mammalian and plant mTERFs. Biochem Biophys Acta 1847:786–797Google Scholar
  38. 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 48:265–269CrossRefGoogle Scholar
  39. Longin CFH, Mühleisen J, Maurer HP, Zhang H, Gowda M, Reif JC (2012) Hybrid breeding in autogamous cereals. Theor Appl Genet 125:1087–1096CrossRefGoogle Scholar
  40. 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 281–297Google Scholar
  41. 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 544:427–433CrossRefGoogle Scholar
  42. 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 192:1347–1358CrossRefGoogle Scholar
  43. 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):477–482CrossRefGoogle Scholar
  44. Melonek J, Stone JD, Small I (2016) Evolutionary plasticity of restorer-of-fertility-like proteins in rice. Sci Rep 6:35152CrossRefGoogle Scholar
  45. 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 60:399–410CrossRefGoogle Scholar
  46. Mühleisen J, Maurer HP, Stiewe G, Bury P, Reif JC (2013a) Hybrid breeding in barley. Crop Sci 53(3):819–824CrossRefGoogle Scholar
  47. 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):309–316CrossRefGoogle Scholar
  48. Mühleisen J, Piepho H-P, Maurer HP, Zhao Y, Reif JC (2014) Exploitation of yield stability in barley. Theor Appl Genet 127:1949–1962CrossRefGoogle Scholar
  49. 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):8178–8183CrossRefGoogle Scholar
  50. 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 21:146–156CrossRefGoogle Scholar
  51. 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 130:273–285CrossRefGoogle Scholar
  52. Price AL, Zaitlen NA, Reich D, Patterson N (2010) New approaches to population stratification in genome-wide association studies. Nat Rev Genet 11:459–463CrossRefGoogle Scholar
  53. Quesada V (2016) The roles of mitochondrial transcription termination factors (MTERFs) in plants. Physiol Plant 157:389–399CrossRefGoogle Scholar
  54. 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):738–753CrossRefGoogle Scholar
  55. 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
  56. 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 213:276CrossRefGoogle Scholar
  57. 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):e42924CrossRefGoogle Scholar
  58. 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 154:297–313CrossRefGoogle Scholar
  59. Saha D, Prasad AM, Srinivasan R (2007) Pentatricopeptide repeat proteins and their emerging roles in plants. Plant Physiol Biochem 45:521–534CrossRefGoogle Scholar
  60. 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 16:1–10CrossRefGoogle Scholar
  61. Shull GH (1908) The composition of a field of maize. J Hered 1:296–301CrossRefGoogle Scholar
  62. Svishcheva GS, Axenovich TI, Belonogova NM, van Duijn CM, Aulchenko YS (2012) Rapid variance components-based method for whole-genome association analysis. Nat Genet 44:1166–1170CrossRefGoogle Scholar
  63. 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):283–290CrossRefGoogle Scholar
  64. 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 18:676–687CrossRefGoogle Scholar
  65. 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 49:77–84CrossRefGoogle Scholar
  66. Wright S (1978) Evolution and genetics of populations. Vol. 4: variability within and among natural populations. The University of Chicago Press, ChicagoGoogle Scholar
  67. 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 9:253CrossRefGoogle Scholar
  68. Zadoks JC, Chang TT, Konzak CF (1974) A decimal code for the growth stages of cereals. Weed Res 14:415–421CrossRefGoogle Scholar
  69. 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):e94126CrossRefGoogle Scholar

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© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Plant Breeding, IFZ Research Centre for Biosystems, Land Use and NutritionJustus Liebig UniversityGiessenGermany
  2. 2.Deutsche Saatveredelung AGSalzkottenGermany

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