Skip to main content
Log in

Exploring new alleles for frost tolerance in winter rye

  • Original Article
  • Published:
Theoretical and Applied Genetics Aims and scope Submit manuscript

Abstract

Key message

Rye genetic resources provide a valuable source of new alleles for the improvement of frost tolerance in rye breeding programs.

Abstract

Frost tolerance is a must-have trait for winter cereal production in northern and continental cropping areas. Genetic resources should harbor promising alleles for the improvement of frost tolerance of winter rye elite lines. For frost tolerance breeding, the identification of quantitative trait loci (QTL) and the choice of optimum genome-based selection methods are essential. We identified genomic regions involved in frost tolerance of winter rye by QTL mapping in a biparental population derived from a highly frost tolerant selection from the Canadian cultivar Puma and the European elite line Lo157. Lines per se and their testcrosses were phenotyped in a controlled freeze test and in multi-location field trials in Russia and Canada. Three QTL on chromosomes 4R, 5R, and 7R were consistently detected across environments. The QTL on 5R is congruent with the genomic region harboring the Frost resistance locus 2 (Fr2) in Triticeae. The Puma allele at the FrR2 locus was found to significantly increase frost tolerance. A comparison of predictive ability obtained from the QTL-based model with different whole-genome prediction models revealed that besides a few large, also small QTL effects contribute to the genomic variance of frost tolerance in rye. Genomic prediction models assigning a high weight to the FrR2 locus allow increasing the selection intensity for frost tolerance by genome-based pre-selection of promising candidates.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Akar T, Francia E, Tondelli A, Rizza F, Stanca AM, Pecchioni N (2009) Marker-assisted characterization of frost tolerance in barley (Hordeum vulgare L.). Plant Breed 128:381–386

    Article  Google Scholar 

  • Båga M, Chodaparambil SV, Limin AE, Pecar M, Fowler DB, Chibbar RN (2007) Identification of quantitative trait loci and associated candidate genes for low-temperature tolerance in cold-hardy winter wheat. Funct Integr Genom 7:53–68

    Article  Google Scholar 

  • 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 KFX, Schmid K, Schön C-C, Scholz U (2017) Towards a whole-genome sequence for rye (Secale cereale L.). Plant J 89:853–869

    Article  CAS  PubMed  Google Scholar 

  • Browning SR, Browning BL (2007) Rapid and accurate haplotype phasing and missing-data inference for whole-genome association studies by use of localized haplotype clustering. Am J Hum Genet 81:1084–1097

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Browning BL, Browning SR (2009) A unified approach to genotype imputation and haplotype-phase inference for large data sets of trios and unrelated individuals. Am J Hum Genet 84:210–223

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Butler D, Cullis B, Gilmour A, Gogel B (2009) ASReml-R reference manual. Queensland Department of Primary Industries and Fisheries, Toowoomba

    Google Scholar 

  • Campoli C, Matus-Cadiz MA, Pozniak CJ, Cattivelli L, Fowler DB (2009) Comparative expression of Cbf genes in the Triticeae under different acclimation induction temperatures. Mol Genet Genom 282:141–152

    Article  CAS  Google Scholar 

  • Case AJ, Skinner DZ, Garland-Campbell KA, Carter AH (2014) Freezing tolerance-associated quantitative trait loci in the Brundage × Coda wheat recombinant inbred line population. Crop Sci 54:982–992

    Article  Google Scholar 

  • Churchill G, Doerge R (1994) Empirical threshold values for quantitative trait mapping. Genetics 138:963–971

    CAS  PubMed  PubMed Central  Google Scholar 

  • Collard BCY, Mackill DJ (2008) Marker-assisted selection: an approach for precision plant breeding in the twenty-first century. Philos Trans R Soc B 363:557–572

    Article  CAS  Google Scholar 

  • Deng W, Nickle DC, Learn GH, Maust B, Mullins JI (2007) ViroBLAST: a stand-alone BLAST web server for flexible queries of multiple databases and user’s datasets. Bioinformatics 23:2334–2336

    Article  CAS  PubMed  Google Scholar 

  • Doležel J, Greilhuber J, Lucretti S, Meister A, Lysák MA, Nardi L, Obermayer R (1998) Plant genome size estimation by flow cytometry: inter-laboratory comparison. Ann Bot 82:17–26

    Google Scholar 

  • Dubcovsky J, Lijavetzky D, Appendino L, Tranquilli G (1998) Comparative RFLP mapping of Triticum monococcum genes controlling vernalization requirement. Theor Appl Genet 97:968–975

    Article  CAS  Google Scholar 

  • Erath W, Bauer E, Kastirr U, Schmidt M, Korzun V, Schmiedchen B, Wilde P, Schön C-C (2016) Oligogenic control of resistance to soil-borne viruses SBCMV and WSSMV in rye (Secale cereale L.). Plant Breed 135:552–559

    Article  CAS  Google Scholar 

  • Fowler DB (2008) Cold acclimation threshold induction temperatures in cereals. Crop Sci 48:1147–1154

    Article  Google Scholar 

  • Fowler DB, Limin AE (1987) Exploitable genetic-variability for cold tolerance in commercially grown cereals. Can J Plant Sci 67:278

    Google Scholar 

  • Fowler DB, Limin AE (2004) Interactions among factors regulating phenological development and acclimation rate determine low-temperature tolerance in wheat. Ann Bot 94:717–724

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fowler DB, Siminovitch D, Pomeroy MK (1973) Evaluation of an artificial test for frost hardiness in wheat. Can J Plant Sci 53:53–59

    Article  Google Scholar 

  • Francia E, Rizza F, Cattivelli L, Stanca AM, Galiba G, Tóth B, Hayes PM, Skinner JS, Pecchioni N (2004) Two loci on chromosome 5H determine low-temperature tolerance in a ‘Nure’ (winter) × ‘Tremois’ (spring) barley map. Theor Appl Genet 108:670–680

    Article  CAS  PubMed  Google Scholar 

  • Friedman J, Hastie T, Tibshirani R (2010) Regularization paths for generalized linear models via coordinate descent. J Stat Softw 33:1–22

    Article  PubMed  PubMed Central  Google Scholar 

  • Galiba G, Vágújfalvi A, Li C, Soltész A, Dubcovsky J (2009) Regulatory genes involved in the determination of frost tolerance in temperate cereals. Plant Sci 176:12–19

    Article  CAS  Google Scholar 

  • Geiger H, Miedaner T (2009) Rye breeding. In: Carena MJ (ed) Cereals. Springer, US, pp 157–181

    Chapter  Google Scholar 

  • Gray GR, Chauvin LP, Sarhan F, Huner N (1997) Cold acclimation and freezing tolerance (A complex interaction of light and temperature). Plant Physiol 114:467–474

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gusta LV, O’Connor BJ, MacHutcheon MG (1997) The selection of superior winter-hardy genotypes using a prolonged freeze test. Can J Plant Sci 77:15–21

    Article  Google Scholar 

  • Gusta LV, O’Connor BJ, Gao YP, Jana S (2001) A re-evaluation of controlled freeze-tests and controlled environment hardening conditions to estimate the winter survival potential of hardy winter wheats. Can J Plant Sci 81:241–246

    Article  Google Scholar 

  • Habier D, Fernando RL, Dekkers JCM (2007) The impact of genetic relationship information on genome-assisted breeding values. Genetics 177:2389–2397

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hackauf B, Rudd S, Van der Voort J, 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  CAS  PubMed  Google Scholar 

  • Haldane J (1919) The combination of linkage values and the calculation of distances between the loci of linked factors. J Genet 8:299–309

    Article  Google Scholar 

  • Haseneyer G, Schmutzer T, Seidel M, Zhou RN, 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Haussmann B, Parzies H, Presterl T, Susic Z, Miedaner T (2004) Plant genetic resources in crop improvement. Plant Genet Resour 2:3–21

    Article  Google Scholar 

  • Holland J, Nyquist W, Cervantes-Martínez C (2003) Estimating and interpreting heritability for plant breeding: an update. Plant Breed Rev 22:9–112

    Google Scholar 

  • Knox AK, Li CX, Vágújfalvi A, Galilba G, Stockinger EJ, Dubcovsky J (2008) Identification of candidate Cbf genes for the frost tolerance locus Fr-A m 2 in Triticum monococcum. Plant Mol Biol 67:257–270

    Article  CAS  PubMed  Google Scholar 

  • Knox AK, Dhillon T, Cheng HM, Tondelli A, Pecchioni N, Stockinger EJ (2010) Cbf gene copy number variation at Frost Resistance-2 is associated with levels of freezing tolerance in temperate-climate cereals. Theor Appl Genet 121:21–35

    Article  PubMed  Google Scholar 

  • Korzun V, Malyshev S, Kartel N, Westermann T, Weber WE, Börner A (1998) A genetic linkage map of rye (Secale cereale L.). Theor Appl Genet 96:203–208

    Article  CAS  Google Scholar 

  • Li Y, Böck A, Haseneyer G, Korzun V, Wilde P, Schön C-C, Ankerst D, Bauer E (2011a) Association analysis of frost tolerance in rye using candidate genes and phenotypic data from controlled, semi-controlled, and field phenotyping platforms. BMC Plant Biol 11:146

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li Y, Haseneyer G, Schön C-C, Ankerst D, Korzun V, Wilde P, Bauer E (2011b) High levels of nucleotide diversity and fast decline of linkage disequilibrium in rye (Secale cereale L.) genes involved in frost response. BMC Plant Biol 11:6

    Article  PubMed  PubMed Central  Google Scholar 

  • Lu C-A, Ho TD, Ho S-L, Yu S-M (2002) Three novel MYB proteins with one DNA binding repeat mediate sugar and hormone regulation of α-amylase gene expression. Plant Cell 14:1963–1980

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Matsubara K, Yamanouchi U, Nonoue Y, Sugimoto K, Wang Z-X, Minobe Y, Yano M (2011) Ehd3, encoding a plant homeodomain finger-containing protein, is a critical promoter of rice flowering. Plant J 66:603–612

    Article  CAS  PubMed  Google Scholar 

  • McCouch S, Baute GJ, Bradeen J, Bramel P, Bretting PK, Buckler E, Burke JM, Charest D, Cloutier S, Cole G, Dempewolf H, Dingkuhn M, Feuillet C, Gepts P, Grattapaglia D, Guarino L, Jackson S, Knapp S, Langridge P, Lawton-Rauh A, Lijua Q, Lusty C, Michael T, Myles S, Naito K, Nelson RL, Pontarollo R, Richards CM, Rieseberg L, Ross-Ibarra J, Rounsley S, Hamilton RS, Schurr U, Stein N, Tomooka N, van der Knaap E, van Tassel D, Toll J, Valls J, Varshney RK, Ward J, Waugh R, Wenzl P, Zamir D (2013) Agriculture: feeding the future. Nature 499:23–24

    Article  CAS  PubMed  Google Scholar 

  • McIntosh R, Yamazaki Y, Dubcovsky J, Rogers W, Morris C, Appels R, Xia X (2013) Catalogue of Gene Symbols for Wheat. 12th International Wheat Genetic Symposium. Yokohama, Japan, September, 8–13, 2013

  • Meyer RS, Choi JY, Sanches M, Plessis A, Flowers JM, Amas J, Dorph K, Barretto A, Gross B, Fuller DQ, Bimpong IK, Ndjiondjop M-N, Hazzouri KM, Gregorio GB, Purugganan MD (2016) Domestication history and geographical adaptation inferred from a SNP map of African rice. Nat Genet 48:1083–1088

    Article  CAS  PubMed  Google Scholar 

  • Miedaner T (2013) Roggenanbau: Eine erfolgreiche Alternative. DLG-Verlag GmbH, AgrarPraxis kompakt

    Google Scholar 

  • Mihaljevic R, Schön C-C, Utz HF, Melchinger AE (2005) Correlations and QTL correspondence between line per se and testcross performance for agronomic traits in four populations of European maize. Crop Sci 45:114–122

    Article  Google Scholar 

  • Millet EJ, Welcker C, Kruijer W, Negro S, Coupel-Ledru A, Nicolas SD, Laborde J, Bauland C, Praud S, Ranc N, Presterl T, Tuberosa R, Bedő Z, Draye X, Usadel B, Charcosset A, Van Eeuwijk F, Tardieu F (2016) Genome-wide analysis of yield in Europe: allelic effects vary with drought and heat scenarios. Plant Physiol 172:749–764

    CAS  PubMed  PubMed Central  Google Scholar 

  • Möhring J, Piepho H-P (2009) Comparison of weighting in two-stage analysis of plant breeding trials. Crop Sci 49:1977–1988

    Article  Google Scholar 

  • Paradis E, Claude J, Strimmer K (2004) APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20:289–290

    Article  CAS  PubMed  Google Scholar 

  • Pasquariello M, Barabaschi D, Himmelbach A, Steuernagel B, Ariyadasa R, Stein N, Gandolfi F, Tenedini E, Bernardis I, Tagliafico E, Pecchioni N, Francia E (2014) The barley Frost resistance-H2 locus. Funct Integr Genom 14:85–100

    Article  CAS  Google Scholar 

  • Petoukhov V, Semenov VA (2010) A link between reduced Barents-Kara sea ice and cold winter extremes over northern continents. J Geophys Res (Atmos) 115:D21111

    Article  Google Scholar 

  • Plaschke J, Börner A, Xie DX, Koebner RMD, Schlegel R, Gale MD (1993) RFLP mapping of genes affecting plant height and growth habit in rye. Theor Appl Genet 85:1049–1054

    Article  CAS  PubMed  Google Scholar 

  • Pomeroy M, Fowler DB (1973) Use of lethal dose temperature estimates as indices of frost tolerance for wheat cold acclimated under natural and controlled environments. Can J Plant Sci 53:489–494

    Article  Google Scholar 

  • Schön C-C, Dhillon BS, Utz HF, Melchinger AE (2010) High congruency of QTL positions for heterosis of grain yield in three crosses of maize. Theor Appl Genet 120:321–332

    Article  PubMed  Google Scholar 

  • Schwegler DD, Gowda M, Schulz B, Miedaner T, Liu W, Reif JC (2014) Genotypic correlations and QTL correspondence between line per se and testcross performance in sugar beet (Beta vulgaris L.) for the three agronomic traits beet yield, potassium content, and sodium content. Mol Breed 34:205–215

    Article  CAS  Google Scholar 

  • Shebeski L, McGinnis R, Evans L, Zuzens D (1973) Puma, a new cultivar of winter rye. Can J Plant Sci 53:67

    Article  Google Scholar 

  • Skinner DZ, Mackey B (2009) Freezing tolerance of winter wheat plants frozen in saturated soil. Field Crops Res 113:335–341

    Article  Google Scholar 

  • Skinner J, Zitzewitz J, Szűcs P, Marquez-Cedillo L, Filichkin T, Amundsen K, Stockinger E, Thomashow M, Chen TH, Hayes P (2005) Structural, functional, and phylogenetic characterization of a large Cbf gene family in barley. Plant Mol Biol 59:533–551

    Article  CAS  PubMed  Google Scholar 

  • Snape JW, Sarma R, Quarrie SA, Fish L, Galiba G, Sutka J (2001) Mapping genes for flowering time and frost tolerance in cereals using precise genetic stocks. Euphytica 120:309–315

    Article  CAS  Google Scholar 

  • Sorokina SA, Li C, Wettstein JJ, Kvamstø NG (2016) Observed atmospheric coupling between Barents Sea ice and the warm-Arctic cold-Siberian anomaly pattern. J Clim 29:495–511

    Article  Google Scholar 

  • Thomashow MF (1999) Plant cold acclimation: freezing tolerance genes and regulatory mechanisms. Annu Rev Plant Physiol Plant Mol Biol 50:571–599

    Article  CAS  PubMed  Google Scholar 

  • Tibshirani R (1996) Regression shrinkage and selection via the LASSO. J R Stat Soc Ser B (Methodol) 58:267–288

    Google Scholar 

  • Tóth B, Francia E, Rizza F, Stanca AM, Galiba G, Pecchioni N (2004) Development of PCR-based markers on chromosome 5H for assisted selection of frost-tolerant genotypes in barley. Mol Breed 14:265–273

    Article  Google Scholar 

  • Utz HF (2011) PlabMQTL-Software for meta-QTL analysis with composite interval mapping. Version 0.9. Institute of Plant Breeding, Seed Science, and Population Genetics, University of Hohenheim

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

    Google Scholar 

  • Wimmer V, Albrecht T, Auinger H-J, Schön C-C (2012) synbreed: a framework for the analysis of genomic prediction data using R. Bioinformatics 28:2086–2087

    Article  CAS  PubMed  Google Scholar 

  • Wimmer V, Lehermeier C, Albrecht T, Auinger H-J, Wang Y, Schön C-C (2013) Genome-wide prediction of traits with different genetic architecture through efficient variable selection. Genetics 195:573–587

    Article  PubMed  PubMed Central  Google Scholar 

  • Wooten DR, Livingston DP, Holland JB, Marshall DS, Murphy JP (2008) Quantitative trait loci and epistasis for crown freezing tolerance in the ‘Kanota’ × ‘Ogle’ hexaploid oat mapping population. Crop Sci 48:149–157

    Article  Google Scholar 

  • Würschum T, Longin CFH, Hahn V, Tucker MR, Leiser WL (2017) Copy number variations of Cbf genes at the Fr-A2 locus are essential components of winter hardiness in wheat. Plant J 89:764–773

    Article  PubMed  Google Scholar 

  • Yan L, Loukoianov A, Tranquilli G, Helguera M, Fahima T, Dubcovsky J (2003) Positional cloning of the wheat vernalization gene VRN1. Proc Natl Acad Sci USA 100:6263–6268

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yan L, Loukoianov A, Blechl A, Tranquilli G, Ramakrishna W, SanMiguel P, Bennetzen JL, Echenique V, Dubcovsky J (2004) The wheat VRN2 gene is a flowering repressor down-regulated by vernalization. Science 303:1640–1644

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yan L, Fu D, Li C, Blechl A, Tranquilli G, Bonafede M, Sanchez A, Valarik M, Yasuda S, Dubcovsky J (2006) The wheat and barley vernalization gene VRN3 is an orthologue of FT. Proc Natl Acad Sci USA 103:19581–19586

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao Y, Gowda M, Würschum T, Longin CFH, Korzun V, Kollers S, Schachschneider R, Zeng J, Fernando R, Dubcovsky J, Reif JC (2013) Dissecting the genetic architecture of frost tolerance in Central European winter wheat. J Exp Bot 64:4453–4460

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu J, Pearce S, Burke A, See D, Skinner D, Dubcovsky J, Garland-Campbell K (2014) Copy number and haplotype variation at the VRN-A1 and central FR-A2 loci are associated with frost tolerance in hexaploid wheat. Theor Appl Genet 127:1183–1197

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This research was funded by the Federal Ministry of Education and Research (BMBF, Germany) within the project RYE SELECT (Grant ID 0315946). The authors are grateful to the field and lab team of KWS Lochow GmbH and to Stefan Schwertfirm and Amalie Fiedler from TUM for the technical assistance. The technical assistance of G. Schellhorn, Plant Sciences Department, University of Saskatchewan is also gratefully acknowledged. The authors thank Prof. Dr. H. Friedrich Utz (University of Hohenheim) for providing an extension of PlabMQTL which enabled the comparison of QTL and GP models.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Eva Bauer or Chris-Carolin Schön.

Ethics declarations

Conflict of interest

On behalf of all authors, the corresponding author states that there is no conflict of interest.

Ethical standards

The authors declare that this study complies with the current laws of the countries in which the experiments were performed.

Additional information

Communicated by Diane E. Mather.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Erath, W., Bauer, E., Fowler, D.B. et al. Exploring new alleles for frost tolerance in winter rye. Theor Appl Genet 130, 2151–2164 (2017). https://doi.org/10.1007/s00122-017-2948-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00122-017-2948-7

Navigation