Skip to main content
SpringerLink
Log in

Copy number variation at the HvCBF4–HvCBF2 genomic segment is a major component of frost resistance in barley

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

A family of CBF transcription factors plays a major role in reconfiguring the plant transcriptome in response to low-freezing temperature in temperate cereals. In barley, more than 13 HvCBF genes map coincident with the major QTL FR-H2 suggesting them as candidates to explain the function of the locus. Variation in copy number (CNV) of specific HvCBFs was assayed in a panel of 41 barley genotypes using RT-qPCR. Taking advantage of an accurate phenotyping that combined Fv/Fm and field survival, resistance-associated variants within FR-H2 were identified. Genotypes with an increased copy number of HvCBF4 and HvCBF2 (at least ten and eight copies, respectively) showed greater frost resistance. A CAPS marker able to distinguish the CBF2A, CBF2B and CBF2A/B forms was developed and showed that all the higher-ranking genotypes in term of resistance harbour only CBF2A, while other resistant winter genotypes harbour also CBF2B, although at a lower CNV. In addition to the major involvement of the HvCBF4-HvCBF2 genomic segment in the proximal cluster of CBF elements, a negative role of HvCBF3 in the distal cluster was identified. Multiple linear regression models taking into account allelic variation at FR-H1/VRN-H1 explained 0.434 and 0.550 (both at p < 0.001) of the phenotypic variation for Fv/Fm and field survival respectively, while no interaction effect between CNV at the HvCBFs and FR-H1/VRN-H1 was found. Altogether our data suggest a major involvement of the CBF genes located in the proximal cluster, with no apparent involvement of the central cluster contrary to what was reported for wheat.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Abbreviations

FR :

Frost resistance loci

CBF/DREB:

C-Repeat binding factor/dehydration responsive element binding factor proteins

CRT/DRE:

C-RepeaT/dehydration responsive elements

VRN :

Vernalization requirement genes and loci

CNV:

Copy number variation

CNVs:

Copy number variants

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. doi:10.1111/j.1439-0523.2008.01553.x

    Article  Google Scholar 

  • Alkan C, Coe BP, Eichler EE (2011) Genome structural variation discovery and genotyping. Nat Rev Genet 12:363–376. doi:10.1038/nrg2958

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Badawi M, Danyluk J, Boucho B, Houde M, Sarhan F (2007) The CBF gene family in hexaploid wheat and its relationship to the phylogenetic complexity of cereal CBFs. Mol Genet Genomics 277:533–554. doi:10.1007/s00438-006-0206-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Campoli C, Matus-Cádiz MA, Pozniak CJ, Cattivelli L, Fowler DB (2009) Comparative expression of Cbf genes in the Triticeae under different acclimation induction temperatures. Mol Genet Genomics 282:141–152. doi:10.1007/s00438-009-0451-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cook DE, Lee TG, Guo X, Melito S, Wang K, Bayless AM, Wang J, Hughes TJ, Willis DK, Clemente TE, Diers BW, Jiang J, Hudson ME, Bent AF (2012) Copy number variation of multiple genes at Rhg1 mediates nematode resistance in soybean. Science 338:1206–1209. doi:10.1126/science.1228746

    Article  CAS  PubMed  Google Scholar 

  • D’haene B, Vandesompele J, Hellemans J (2010) Accurate and objective copy number profiling using real-time quantitative PCR. Methods 50:262–270. doi:10.1016/j.ymeth.2009.12.007

    Article  PubMed  Google Scholar 

  • Deng W, Casao MC, Wang P, Sato K, Hayes PM, Finnegan EJ, Trevaskis B (2015) Direct links between the vernalization response and other key traits of cereal crops. Nat Commun 6:5882. doi:10.1038/ncomms6882

    Article  PubMed  Google Scholar 

  • Dhillon T, Stockinger EJ (2013) Cbf14 copy number variation in the A, B, and D genomes of diploid and polyploid wheat. Theor Appl Genet 126:2777–2789. doi:10.1007/s00122-013-2171-0

    Article  CAS  PubMed  Google Scholar 

  • Dhillon T, Pearce SP, Stockinger EJ, Distelfeld A, Li C, Knox AK, Vashegyi I, Galiba G, Vágú A, Galiba G, Dubcovsky J (2010) Regulation of freezing tolerance and flowering in temperate cereals: The VRN-1 connection. Plant Physiol 153:1846–1858. doi:10.1104/pp.110.159079

    Article  CAS  PubMed  PubMed Central  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 5 H determine low-temperature tolerance in a “Nure” (winter) × “Tremois” (spring) barley map. Theor Appl Genet 108:670–680. doi:10.1007/s00122-003-1468-9

    Article  CAS  PubMed  Google Scholar 

  • Francia E, Barabaschi D, Tondelli A, Laidò G, Rizza F, Stanca AM, Busconi M, Fogher C, Stockinger EJ, Pecchioni N (2007) Fine mapping of a HvCBF gene cluster at the frost resistance locus Fr-H2 in barley. Theor Appl Genet 115:1083–1091. doi:10.1007/s00122-007-0634-x

    Article  CAS  PubMed  Google Scholar 

  • Francia E, Pecchioni N, Policriti A, Scalabrin S (2015) CNV and sStructural variation in plants: prospects of NGS approaches. In: Sablok G, Kumar S, Ueno S, Kuo J, Varotto C (eds) Advances in the understanding of biological sciences using next generation sequencing (NGS) approaches. Springer Cham, pp 211–232. doi:10.1007/978-3-319-17157-9

    Chapter  Google Scholar 

  • Galiba G, Stockinger EJ, Francia E, Milc J, Kocsy G, Pecchioni N (2013) Freezing tolerance in the Triticeae. In: Varshney RK, Tuberosa R (eds) Translational genomics for crop breeding. Wiley, New york, pp 99–124. doi:10.1002/9781118728475

    Google Scholar 

  • International Barley Genome Sequencing Consortium, Mayer KFX, Waugh R, Brown JWS, Schulman A, Langridge P, Platzer M, Fincher GB, Muehlbauer GJ, Sato K, Close TJ, Wise RP, Stein N (2012) A physical, genetic and functional sequence assembly of the barley genome. Nature 491:711–716. doi:10.1038/nature11543

    CAS  PubMed  Google Scholar 

  • Jeknić Z, Pillman KA, Dhillon T, Skinner JS, Veisz O, Cuesta-Marcos A, Hayes PM, Jacobs AK, Chen THH, Stockinger EJ (2014) Hv-CBF2A overexpression in barley accelerates COR gene transcript accumulation and acquisition of freezing tolerance during cold acclimation. Plant Mol Biol 84:67–82. doi:10.1007/s11103-013-0119-z

    Article  PubMed  Google Scholar 

  • Jiao Y, Zhao H, Ren L, Song W, Zeng B, Guo J, Wang B, Liu Z, Chen J, Li W, Zhang M, Xie S, Lai J (2012) Genome-wide genetic changes during modern breeding of maize. Nat Genet 44:812–815. doi:10.1038/ng.2312

    Article  CAS  PubMed  Google Scholar 

  • Knox AK, Li C, Vágújfalvi A, Galiba 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. doi:10.1007/s11103-008-9316-6

    Article  CAS  PubMed  Google Scholar 

  • Knox AK, Dhillon T, Cheng H, 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. doi:10.1007/s00122-010-1288-7

    Article  PubMed  Google Scholar 

  • Kosová K, Prášil IT, Vítámvás P (2008) The relationship between vernalization- and photoperiodically-regulated genes and the development of frost tolerance in wheat and barley. Biol Plant 52:601–615. doi:10.1007/s10535-008-0120-6

    Article  Google Scholar 

  • Levitt J (1980) Chilling, freezing, and high temperature stresses. In: Levitt J (ed) In: response of plants to environmental stresses, 2nd edn. vol 1. Academic Press Inc., New York, NY

    Google Scholar 

  • Li W, Olivier M (2013) Current analysis platforms and methods for detecting copy number variation. Physiol Genomics 45:1–16. doi:10.1152/physiolgenomics.00082.2012

    Article  PubMed  Google Scholar 

  • Limin AE, Fowler DB (2006) Low-temperature tolerance and genetic potential in wheat (Triticum aestivum L.): response to photoperiod, vernalization, and plant development. Planta 224:360–366. doi:10.1007/s00425-006-0219-y

    Article  CAS  PubMed  Google Scholar 

  • Ma L, Chung WK (2014) Quantitative analysis of copy number variants based on real-time LightCycler PCR. Curr Protoc Hum Genet 80:7.21.1–7.21.8. doi:10.1002/0471142905.hg0721s80

    Article  Google Scholar 

  • Manolio TA, Collins FS, Cox NJ, Goldstein DB, Hindorff LA, Hunter DJ, McCarthy MI, Ramos EM, Cardon LR, Chakravarti A, Cho JH, Guttmacher AE, Kong A, Kruglyak L, Mardis E, Rotimi CN, Slatkin M, Valle D, Whittemore AS, Boehnke M, Clark AG, Eichler EE, Gibson G, Haines JL, Mackay TFC, McCarroll SA, Visscher PM (2009) Finding the missing heritability of complex diseases. Nature 461:747–753. doi:10.1038/nature08494

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maron LG, Guimarães CT, Kirst M, Albert PS, Birchler JA, Bradbury PJ, Buckler ES, Coluccio AE, Danilova TV, Kudrna D, Magalhaes JV, Piñeros MA, Schatz MC, Wing RA, Kochian LV (2013) Aluminum tolerance in maize is associated with higher MATE1 gene copy number. Proc Natl Acad Sci USA 110:5241–5246. doi:10.1073/pnas.1220766110

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marozsán-Tóth Z, Vashegyi I, Galiba G, Tóth B (2015) The cold response of CBF genes in barley is regulated by distinct signaling mechanisms. J Plant Physiol 181:42–49. doi:10.1016/j.jplph.2015.04.002

    Article  PubMed  Google Scholar 

  • McHale LK, Haun WJ, Xu WW, Bhaskar PB, Anderson JE, Hyten DL, Gerhardt DJ, Jeddeloh JA, Stupar RM (2012) Structural variants in the soybean genome localize to clusters of biotic stress-response genes. Plant Physiol 159:1295–1308. doi:10.1104/pp.112.194605

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mickelbart MV, Hasegawa PM, Bailey-Serres J (2015) Genetic mechanisms of abiotic stress tolerance that translate to crop yield stability. Nat Rev Genet 16:237–251. doi:10.1038/nrg3901

    Article  CAS  PubMed  Google Scholar 

  • Miller AK, Galiba G, Dubcovsky J (2006) A cluster of 11 CBF transcription factors is located at the frost tolerance locus Fr-A m 2 in Triticum monococcum. Mol Genet Genomics 275:193–203. doi:10.1007/s00438-005-0076-6

    Article  CAS  PubMed  Google Scholar 

  • Mohseni S, Che H, Djillali Z, Dumont E, Nankeu J, Danyluk J (2012) Wheat CBF gene family: identification of polymorphisms in the CBF coding sequence. Genome 55:865–881. doi:10.1139/gen-2012-0112

    Article  CAS  PubMed  Google Scholar 

  • Morran S, Eini O, Pyvovarenko T, Parent B, Singh R, Ismagul A, Eliby S, Shirley N, Langridge P, Lopato S (2011) Improvement of stress tolerance of wheat and barley by modulation of expression of DREB/CBF factors. Plant Biotechnol J 9:230–249. doi:10.1111/j.1467-7652.2010.00547.x

    Article  CAS  PubMed  Google Scholar 

  • Muñoz-Amatriaín M, Eichten SR, Wicker T, Richmond TA, Mascher M, Steuernagel B, Scholz U, Ariyadasa R, Spannagl M, Nussbaumer T, Mayer KF, Taudien S, Platzer M, Jeddeloh JA, Springer NM, Muehlbauer GJ, Stein N (2013) Distribution, functional impact, and origin mechanisms of copy number variation in the barley genome. Genome Biol 14:R58. doi:10.1186/gb-2013-14-6-r58

    Article  PubMed  PubMed Central  Google Scholar 

  • Nitcher R, Distelfeld A, Tan C, Yan L, Dubcovsky J (2013) Increased copy number at the HvFT1 locus is associated with accelerated flowering time in barley. Mol Genet Genomics 288:261–275. doi:10.1007/s00438-013-0746-8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Novillo F, Medina J, Rodríguez-Franco M, Neuhaus G, Salinas J (2011) Genetic analysis reveals a complex regulatory network modulating CBF gene expression and Arabidopsis response to abiotic stress. J Exp Bot 63(1):293–304. doi:10.1093/jxb/err279

    Article  PubMed  PubMed Central  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 Genomics 14(1):85–100. doi:10.1007/s10142-014-0360-9

    Article  CAS  PubMed  Google Scholar 

  • Payne R (2014) A guide to regression, nonlinear and generalized linear models in GenStat, 17th edn. VSN International, Hemel Hempstead

    Google Scholar 

  • Pearce S, Zhu J, Boldizsár Á, Vágújfalvi A, Burke A, Garland-Campbell K, Galiba G, 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. doi:10.1007/s00122-013-2165-y

    Article  PubMed  PubMed Central  Google Scholar 

  • Pecchioni N, Kosová K, Vítámvás P, Prášil IT, Milc JA, Francia E, Gulyás Z, Kocsy G, Galiba G (2012) Genomics of low-temperature tolerance for an increased sustainability of wheat and barley production. In: Tuberosa R, Graner A, Frison E (eds) Genomics of plant genetic resources to improve crop production, food security and nutritional quality. Springer, Berlin, pp 149–183. doi:10.1007/978-94-007-7575-6

    Google Scholar 

  • Poland JA, Brown PJ, Sorrells ME, Jannink J-L (2012) Development of high-density genetic maps for barley and wheat using a novel two-enzyme genotyping-by-sequencing approach. PLoS One 7(2):e32253. doi:10.1371/journal.pone.0032253

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rizza F, Pagani D, Gut M, Prášil IT, Lago C, Tondelli A, Orrù L, Mazzucotelli E, Francia E, Badeck F-W, Crosatti C, Terzi V, Cattivelli L, Stanca AM (2011) Diversity in the response to low temperature in representative barley genotypes cultivated in Europe. Crop Sci 51:2759–2779. doi:10.2135/cropsci2011.01.0005

    Article  CAS  Google Scholar 

  • Skinner JS, von Zitzewitz J, Szucs P, Marquez-Cedillo L, Filichkin T, Amundsen K, Stockinger EJ, Thomashow MF, Chen THH, Hayes PM (2005) Structural, functional, and phylogenetic characterization of a large CBF gene family in barley. Plant Mol Biol 59:533–551. doi:10.1007/s11103-005-2498-2

    Article  CAS  PubMed  Google Scholar 

  • Skinner JS, Szucs P, von Zitzewitz J, Marquez-Cedillo L, Filichkin T, Stockinger EJ, Thomashow MF, Chen THH, Hayes PM (2006) Mapping of barley homologs to genes that regulate low temperature tolerance in Arabidopsis. Theor Appl Genet 112:832–842. doi:10.1007/s00122-005-0185-y

    Article  CAS  PubMed  Google Scholar 

  • Soltész A, Smedley M, Vashegyi I, Galiba G, Harwood W, Vagu jfalvi A (2013) Transgenic barley lines prove the involvement of TaCBF14 and TaCBF15 in the cold acclimation process and in frost tolerance. J Exp Bot 64:1849–1862. doi:10.1093/jxb/ert050

    Article  PubMed  PubMed Central  Google Scholar 

  • Stockinger EJ, Skinner JS, Gardner KG, Francia E, Pecchioni N (2007) Expression levels of barley Cbf genes at the Frost resistance-H2 locus are dependent upon alleles at Fr-H1 and Fr-H2. Plant J 51:308–321. doi:10.1111/j.1365-313X.2007.0141.x

    Article  CAS  PubMed  Google Scholar 

  • Sutton T, Baumann U, Hayes J, Collins NC, Shi B-J, Schnurbusch T, Hay A, Mayo G, Pallotta M, Tester M, Langridge P (2007) Boron-toxicity tolerance in barley arising from efflux transporter amplification. Science 318:1446–1449. doi:10.1126/science.1146853

    Article  CAS  PubMed  Google Scholar 

  • Swanson-Wagner RA, Eichten SR, Kumari S, Tiffin P, Stein JC, Ware D, Springer NM (2010) Pervasive gene content variation and copy number variation in maize and its undomesticated progenitor. Genome Res 20:1689–1699. doi:10.1101/gr.109165.110

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thomashow MF (2010) Molecular basis of plant cold acclimation: insights gained from studying the CBF cold response pathway. Plant Physiol 154:571–577. doi:10.1104/pp.110.161794

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tondelli A, Francia E, Barabaschi D, Pasquariello M, Pecchioni N (2011) Inside the CBF locus in Poaceae. Plant Sci 180:39–45

    Article  CAS  PubMed  Google Scholar 

  • Tondelli A, Pagani D, Ghafoori IN, Rahimi M, Ataei R, Rizza F, Flavell AJ, Cattivelli L (2014) Allelic variation at Fr-H1/Vrn-H1 and Fr-H2 loci is the main determinant of frost tolerance in spring barley. Environ Exp Bot 106:148–155. doi:10.1016/j.envexpbot.2014.02.014

    Article  CAS  Google Scholar 

  • Tranquilli G, Dubcovsky J (2000) Epistatic interaction between vernalization genes Vrn-A m 1 and Vrn-A m 2 in diploid wheat. J Hered 91:304–306

    Article  CAS  PubMed  Google Scholar 

  • Visioni A, Tondelli A, Francia E, Pswarayi A, Malosetti M, Russell J, Thomas W, Waugh R, Pecchioni N, Romagosa I, Comadran J (2013) Genome-wide association mapping of frost tolerance in barley (Hordeum vulgare L.) BMC Genomics 14:424. doi:10.1186/1471-2164-14-424

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • von Zitzewitz J, Szucs P, Dubcovsky J, Yan L, Francia E, Pecchioni N, Casas A, Chen THH, Hayes PM, Skinner JS (2005) Molecular and structural characterization of barley vernalization genes. Plant Mol Biol 59:449–467. doi:10.1007/s11103-005-0351-2

    Article  CAS  Google Scholar 

  • von Zitzewitz J, Cuesta-Marcos A, Condon F, Castro AJ, Chao S, Corey A, Filichkin T, Fisk SP, Gutierrez L, Haggard K, Karsai I, Muehlbauer GJ, Smith KP, Veisz O, Hayes PM (2011) The genetics of winterhardiness in barley: perspectives from genome-wide association mapping. Plant Genome J 4:76. doi:10.3835/plantgenome2010.12.0030

    Article  Google Scholar 

  • Weaver S, Dube S, Mir A, Qin J, Sun G, Ramakrishnan R, Jones RC, Livak KJ (2010) Taking qPCR to a higher level: analysis of CNV reveals the power of high throughput qPCR to enhance quantitative resolution. Methods 50:271–276. doi:10.1016/j.ymeth.2010.01.003

    Article  CAS  PubMed  Google Scholar 

  • Zhu J, Pearce S, Burke A, See DR, Skinner DZ, 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. doi:10.1007/s00122-014-2290-2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zmieńko A, Samelak A, Kozłowski P, Figlerowicz M (2013) Copy number polymorphism in plant genomes. Theor Appl Genet 127:1–18. doi:10.1007/s00122-013-2177-7

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

This work was partially supported by Fondazione Cassa di Risparmio di Modena, Progetto di Ricerca Internazionale “FROSTMAP—Physical mapping of the barley Frost resistance-H2 (Fr-H2) locus”. Funding from “GENOMORE” project of the Fondazione Cassa di Risparmio di Carpi is also acknowledged. The authors are grateful to Dr. Franz W. Badeck (PIK—Potsdam, Germany) for his critical suggestions during statistical analysis and to Mrs. Donata Pagani (CRA-GPG, Fiorenzuola, Italy) for the excellent technical assistance during phenotypic analysis, and to Dr. Ilja Tom Prášil (Crop Research Institute, Prague, Czech Republic) for providing some barley varieties.

Author contributions

All the authors have participated in the work and none of them have any conflict of interest. In particular, Enrico Francia and Nicola Pecchioni conceived the study. Enrico Francia and Caterina Morcia designed sequence-specific amplicons on the tested genes, carried out RT-qPCR and copy number calculation. Marianna Pasquariello and Valentina Mazzamurro developed a novel CAPS marker and together with Justyna Milc performed CBF2A/B screening. Fulvia Rizza and Valeria Terzi performed the phenotypic characterization for frost resistance of the plant material. Nicola Pecchioni contributed to analysis and interpretation of data and participated in the discussion of results. The manuscript was written Enrico Francia and Justyna Milc.

Author information

Author notes

  1. Marianna Pasquariello

    Present address: Department of Crop Genetics, John Innes Centre (JIC), Norwich Research Park, Norwich, NR4 7UH, UK

  2. Nicola Pecchioni

    Present address: Cereal Research Centre, Council for Agricultural Research and Economics, 71122, Foggia, Italy

Authors and Affiliations

  1. Department of Life Sciences, University of Modena and Reggio Emilia, Via Amendola 2, Pad.Besta, 42122, Reggio Emilia, Italy

    Enrico Francia, Marianna Pasquariello, Valentina Mazzamurro, Justyna Anna Milc & Nicola Pecchioni

  2. Center for Genome Research (CGR), University of Modena and Reggio Emilia, Via Campi 287, 41125, Modena, Italy

    Enrico Francia, Justyna Anna Milc & Nicola Pecchioni

  3. Genomics Research Centre (GPG), Council for Agricultural Research and Economics, Via San Protaso 302, 29017, Fiorenzuola d’Arda, Italy

    Caterina Morcia, Fulvia Rizza & Valeria Terzi

Authors
  1. Enrico Francia
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Caterina Morcia
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Marianna Pasquariello
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Valentina Mazzamurro
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Justyna Anna Milc
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Fulvia Rizza
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Valeria Terzi
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Nicola Pecchioni
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Enrico Francia.

Additional information

E. Francia and C. Morcia have equally contributed to this work.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 39 KB)

11103_2016_505_MOESM2_ESM.tif

Supplementary Fig. 1 Graphical genotyping and frost resistance of ‘Nure’ x ‘Tremois’ F5:6 recombinants in the HvCBF cluster at Fr-H2. a Graphical representation of chromosome 5H region of the phenotyped F5:6 plants. Markers name and order derive from Francia et al. (2007) and Pasquariello et al. (2014). Chromosomal segments with ‘Nure’ and ‘Tremois’ marker alleles are in dark and light gray, respectively. NT-42 and NT-64 are DH lines of the ‘NxT’ population developed by Francia et al. (2004). The number of genotypes considered for each recombinant class is in parenthesis. b Bar graph for Fv/Fm representing the mean ± s.e. for n = 5 independent experiments in controlled conditions (freezing stress ranged from −11°C to −13°C). c Bar graph for winter survival representing the mean ± s.e. for a field trial in 2012/13 (min temp. −7°C). Lowercase letters in (b) and (c) represent least significant differences (LSD0.05) (TIF 1956 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Francia, E., Morcia, C., Pasquariello, M. et al. Copy number variation at the HvCBF4–HvCBF2 genomic segment is a major component of frost resistance in barley. Plant Mol Biol 92, 161–175 (2016). https://doi.org/10.1007/s11103-016-0505-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11103-016-0505-4

Keywords

Search

Navigation