Copy number variations of CBF genes at the Fr-A2 locus are essential components of winter hardiness in wheat

Plant Journal

Volumn 89, Issue 4, 2017, Pages 764-773

  Würschum, Tobias ^a   Longin, C Friedrich H ^a   Hahn, Volker ^a   Tucker, Matthew R ^b   Leiser, Willmar L ^a  

^a UNIVERSITY OF HOHENHEIM   (Germany)

^b UNIVERSITY OF ADELAIDE   (Australia)

Author keywords

association mapping; copy number variation; Fr A2; Vrn A1; wheat; winter hardiness

Indexed keywords

GENES; MAPPING;

ASSOCIATION MAPPING; COPY NUMBER VARIATIONS; VRN-A1; WHEAT; WINTER HARDINESS;

PLANTS (BOTANY);

GENETIC ENGINEERING; MAPPING; WHEAT;

PLANT PROTEIN;

COPY NUMBER VARIATION; GENE EXPRESSION REGULATION; GENETICS; GENOME-WIDE ASSOCIATION STUDY; GENOTYPE; PHYSIOLOGY; PLANT CHROMOSOME; QUANTITATIVE TRAIT LOCUS; SEASON; WHEAT;

CHROMOSOMES, PLANT; DNA COPY NUMBER VARIATIONS; GENE EXPRESSION REGULATION, PLANT; GENOME-WIDE ASSOCIATION STUDY; GENOTYPE; PLANT PROTEINS; QUANTITATIVE TRAIT LOCI; SEASONS; TRITICUM;

EID: 85012927492     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.13424     Document Type: Article

References (44)

1. Beales, J., Turner, A., Griffiths, S., Snape, J.W. and Laurie, D.A. (2007) A pseudo-response regulator is misexpressed in the photoperiod insensitive Ppd-D1a mutant of wheat (Triticum aestivum L.). Theor. Appl. Genet. 115, 721–733.
2. Benjamini, Y. and Hochberg, Y. (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. 57, 289–300.
3. Bentley, A.R., Scutari, M., Gosman, N. et al. (2014) Applying association mapping and genomic selection to the dissection of key traits in elite European wheat. Theor. Appl. Genet. 127, 2619–2633.
4. Bernardo, R. (2014) Genomewide selection when major genes are known. Crop Sci. 54, 68–75.
5. Boeven, P.H.G., Longin, C.F.H. and Würschum, T. (2016a) A unified framework for hybrid breeding and the establishment of heterotic groups in wheat. Theor. Appl. Genet., 129, 1231–1245.
6. Boeven, P.H.G., Longin, C.F.H., Leiser, W.L., Kollers, S., Ebmeyer, E. and Würschum, T. (2016b) Genetic architecture of male floral traits required for hybrid wheat breeding. Theor. Appl. Genet. 129, 2343–2357.
7. Chu, C., Tan, C.T., Yu, G., Zhong, S., Xu, S.S. and Yan, L. (2011) A novel retrotransposon inserted in the dominant Vrn-B1 allele confers spring growth habit in tetraploid wheat (Triticum turgidum L.). G3, 1, 637–645.
8. Díaz, A., Zikhali, M., Turner, A.S., Isaac, P. and Laurie, D.A. (2012) Copy number variation affecting the Photoperiod-B1 and Vernalization-A1 genes is associated with altered flowering time in wheat (Triticum aestivum). PLoS ONE, 7, e33234.
9. Eagles, H.A., Cane, K. and Trevaskis, B. (2011) Veery wheats carry an allele of Vrn-A1 that has implications for freezing tolerance in winter wheats. Plant Breeding, 130, 413–418.
10. Ellis, M., Spielmeyer, W., Gale, K., Rebetzke, G. and Richards, R. (2002) “Perfect” markers for the Rht-B1b and Rht-D1b dwarfing genes in wheat. Theor. Appl. Genet. 105, 1038–1042.
11. Endelman, J.B. (2011) Ridge regression and other kernels for genomic selection with R package rrBLUP. Plant Genome, 4, 250–255.
12. Endelman, J.B. and Jannink, J.-L. (2012) Shrinkage estimation of the realized relationship matrix. G3, 2, 1405–1413.
13. Fu, D., Szűcs, P., Yan, L., Helguera, M., Skinner, J., Zitzewitz, J.V., Hayes, P.M. and Dubcovsky, J. (2005) Large deletions within the first intron in VRN-1 are associated with spring growth habit in barley and wheat. Mol. Gen. Genomics, 273, 54–65.
14. Galiba, G., Vágújfalvi, A., Li, C., Solté, A. and Dubcovsky, J. (2009) Regulatory genes involved in the determination of frost tolerance in temperate cereals. Plant Sci. 176, 12–19.
15. Gilmour, A.R., Gogel, B.J., Cullis, B.R. and Thompson, R. (2009) ASReml User Guide Release 3.0. Hemel Hempstead: International Ltd.
16. Heffner, E.L., Sorrells, M.E. and Jannink, J.-L. (2009) Genomic selection for crop improvement. Crop Sci. 49, 1–12.
17. Holland, J.B., Portyanko, V.A., Hoffman, D.L. and Lee, M. (2002) Genomic regions controlling vernalization and photoperiod responses in oat. Theor. Appl. Genet. 105, 113–126.
18. Knox, A.K., Li, C., Vágújfalvi, A., Galiba, G., Stockinger, E.J. and Dubcovsky, J. (2008) Identification of candidate CBF genes for the frost tolerance locus Fr-Am 2 in Triticum monococcum. Plant Mol. Biol. 67, 257–270.
19. Kraakman, A.T., Niks, R.E., Van den Berg, P.M., Stam, P. and Van Eeuwijk, F.A. (2004) Linkage disequilibrium mapping of yield and yield stability in modern spring barley cultivars. Genetics, 168, 435–446.
20. Krzywinski, M., Schein, J., Birol, I., Connors, J., Gascoyne, R., Horsman, D., Jones, S.J. and Marra, M.A. (2009) Circos: an information aesthetic for comparative genomics. Genome Res. 19, 1639–1645.
21. Langer, S.M., Longin, C.F.H. and Würschum, T. (2014) Flowering time control in European winter wheat. Front. Plant Sci. 5, 537.
22. Li, H., Vikram, P., Singh, R.P. et al. (2015) A high density GBS map of bread wheat and its application for dissecting complex disease resistance traits. BMC Genomics, 16, 216.
23. Miller, A.K., Galiba, G. and Dubcovsky, J. (2006) A cluster of 11 CBF transcription factors is located at the frost tolerance locus Fr-Am 2 in Triticum monococcum. Mol. Genet. Genomics, 275, 193–203.
24. Money, D., Gardner, K.M., Migicovsky, Z., Schwaninger, H., Zhong, G.Y. and Myles, S. (2015) LinkImpute–fast and accurate genotype imputation for non-model organisms. G3, 5, 2383–2390.
25. Pearce, S., Zhu, J., Boldizsár, Á., Vágújfalvi, A., Burke, A., Garland-Campbell, K., Galiba, G. and Dubcovsky, J. (2013) Large deletions in the CBF gene cluster at the Fr-B2 locus are associated with reduced frost tolerance in wheat. Theor. Appl. Genet. 126, 2683–2697.
26. Piepho, H.P. and Möhring, J. (2007) Computing heritability and selection response from unbalanced plant breeding trials. Genetics, 177, 1881–1888.
27. Sieber, A.-N., Longin, C.F.H., Leiser, W.L. and Würschum, T. (2016) Copy number variation of CBF-A14 at the Fr-A2 locus determines frost tolerance in winter durum wheat. Theor. Appl. Genet. 129, 1087–1097.
28. Spindel, J.E., Begum, H., Akdemir, D., Collard, B., Redoña, E., Jannink, J.-L. and McCouch, S. (2016) Genome-wide prediction models that incorporate de novo GWAS are a powerful new tool for tropical rice improvement. Heredity, 116, 395–408.
29. Utz, H.F., Melchinger, A.E. and Schön, C.C. (2000) Bias and sampling error of the estimated proportion of genotypic variance explained by quantitative trait loci determined from experimental data in maize using cross validation and validation with independent samples. Genetics, 154, 1839–1849.
30. Vágújfalvi, A., Aprile, A., Miller, A., Dubcovsky, J., Delugu, G., Galiba, G. and Cattivelli, L. (2005) The expression of several Cbf genes at the Fr-A2 locus is linked to frost resistance in wheat. Mol. Genet. Genomics, 274, 506–514.
31. Williams, E., Piepho, H.-P. and Whitaker, D. (2011) Augmented p-rep designs. Biom. J. 53, 19–27.
32. Würschum, T. (2012) Mapping QTL for agronomic traits in breeding populations. Theor. Appl. Genet. 125, 201–210.
33. Würschum, T. and Kraft, T. (2014) Cross-validation in association mapping and its relevance for the estimation of QTL parameters of complex traits. Heredity, 112, 463–468.
34. Würschum, T., Maurer, H.P., Dreyer, F. and Reif, J.C. (2013) Effect of inter- and intragenic epistasis on the heritability of oil content in rapeseed (Brassica napus L.). Theor. Appl. Genet. 126, 435–441.
35. Würschum, T., Boeven, P.H., Langer, S.M., Longin, C.F.H. and Leiser, W.L. (2015a) Multiply to conquer: copy number variations at Ppd-B1 and Vrn-A1 facilitate global adaptation in wheat. BMC Genet. 16, 96.
36. Würschum, T., Langer, S.M. and Longin, C.F.H. (2015b) Genetic control of plant height in European winter wheat cultivars. Theor. Appl. Genet. 128, 865–874.
37. Würschum, T., Leiser, W.L., Kazman, E. and Longin, C.F.H. (2016) Genetic control of protein content and sedimentation volume in European winter wheat cultivars. Theor. Appl. Genet. 129, 1685–1696.
38. Yan, L., Helguera, M., Kato, K., Fukuyama, S., Sherman, J. and Dubcovsky, J. (2004) Allelic variation at the VRN-1 promoter region in polyploid wheat. Theor. Appl. Genet. 109, 1677–1686.
39. Yan, L., Fu, D., Li, C., Blechl, A., Tranquilli, G., Bonafede, M., Sanchez, A., Valarik, M., Yasuda, S. and Dubcovsky, J. (2006) The wheat and barley vernalization gene VRN3 is an orthologue of FT. Proc. Natl Acad. Sci. USA, 103, 19581–19586.
40. Yu, J., Pressoir, G., Briggs, W.H. et al. (2006) A unified mixed-model method for association mapping that accounts for multiple levels of relatedness. Nat. Genet. 38, 203–208.
41. Zhao, Y., Gowda, M., Würschum, T. et al. (2013) Dissecting the genetic architecture of frost tolerance in Central European winter wheat. J. Exp. Bot. 64, 4453–4460.
42. Zhao, Y., Mette, M.F., Gowda, M., Longin, C.F.H. and Reif, J.C. (2014) Bridging the gap between marker-assisted and genomic selection of heading time and plant height in hybrid wheat. Heredity, 112, 638–645.
43. Zhu, J., Pearce, S., Burke, A., See, D.R., Skinner, D.Z., Dubcovsky, J. and 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.
44. Żmieńko, A., Samelak, A., Kozłowski, P. and Figlerowicz, M. (2014) Copy number polymorphism in plant genomes. Theor. Appl. Genet. 127, 1–18.