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Two loci on chromosome 5H determine low-temperature tolerance in a ‘Nure’ (winter) × ‘Tremois’ (spring) barley map

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Abstract

Barley (Hordeum vulgare subsp. vulgare) is an economically important diploid model for the Triticeae; and a better understanding of low-temperature tolerance mechanisms could significantly improve the yield of fall-sown cereals. We developed a new resource for genetic analysis of winter hardiness-related traits, the ‘Nure’ × ‘Tremois’ linkage map, based on a doubled-haploid population that is segregating for low-temperature tolerance and vernalization requirement. Three measures of low-temperature tolerance and one measure of vernalization requirement were used and, for all traits, QTLs were mapped on chromosome 5H. The vernalization response QTL coincides with previous reports at the Vrn-1/Fr1 region of the Triticeae. We also found coincident QTLs at this position for all measures of low-temperature tolerance. Using Composite Interval Mapping, a second proximal set, of coincident QTLs for low-temperature tolerance, and the accumulation of two different COR proteins (COR14b and TMC-Ap3) was identified. The HvCBF4 locus, or another member of the CBF loci clustered in this region, is the candidate gene underlying this QTL. There is a CRT/DRE recognition site in the promoter of cor14b with which a CBF protein could interact. These results support the hypothesis that highly conserved regulatory factors, such as members of the CBF gene family, may regulate the stress responses of a wide range of plant species.

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References

  • Alabadi D, Alessandra D, Eckardt N (2002) Arabidopsis research heats up in Seville. Plant Cell 14:1987–1994

    Article  CAS  PubMed  Google Scholar 

  • Baldi P, Grossi M, Pecchioni N, Valè G, Cattivelli L (1999) High expression level of a gene coding for a chloroplastic amino-acid selective channel protein is correlated to cold acclimation in cereals. Plant Mol Biol 41:233–243

    Article  CAS  PubMed  Google Scholar 

  • Becker J, Heun M (1995) Barley microsatellites variation and mapping. Plant Mol Biol 27:835–845

    CAS  PubMed  Google Scholar 

  • Becker J, Vos P, Kuiper F, Salamini F, Heun M (1995) Combined mapping of AFLP and RFLP markers in barley. Mol Gen Genet 249:65–73

    CAS  PubMed  Google Scholar 

  • Butler WL, Kitajima M (1975) Fluorescence quenching in photosystem II of the chloroplast. Biochim Biophys Acta 376:116–125

    CAS  PubMed  Google Scholar 

  • Cattivelli L, Baldi P, Crosatti C, Di Fonzo N, Faccioli P, Grossi M, Mastrangelo AM, Pecchioni N, Stanca AM (2002) Chromosome regions and stress-related sequences involved in resistance to abiotic stress in Triticeae. Plant Mol Biol 48:649–665

    CAS  PubMed  Google Scholar 

  • Choi D-W, Koag MC, Close TJ (2000) Map location of barley Dhn genes determined by gene-specific PCR. Theor Appl Genet 101:350–354

    Article  CAS  Google Scholar 

  • Choi D-W, Rodriguez EM, Close TJ (2002) Barley Cbf3 gene identification, expression pattern, and map location. Plant Physiol 129:1781–1787

    Article  CAS  PubMed  Google Scholar 

  • Costa JM, Corey A, Hayes PM, Jobet C, Kleinhofs A, Kopisch-Obusch A, Kramer SF, Kudrna D, Li M, Riera-Lizarazu O, Sato K, Szucs P, Toojinda T, Vales MI, Wolfe RI (2001) Molecular mapping of the Oregon Wolfe barleys: a phenotypically polymorphic doubled-haploid population. Theor Appl Genet 103:415–424

    CAS  Google Scholar 

  • Crosatti C, Soncini C, Stanca AM, Cattivelli L (1995) The accumulation of a cold-regulated chloroplastic protein is light-dependent. Planta 196:458–463

    CAS  PubMed  Google Scholar 

  • Dal Bosco C, Busconi M, Govoni C, Baldi P, Stanca AM, Crosatti C, Bassi R, Cattivelli L (2003) cor gene expression in barley mutants affected in chloroplast development and photosynthetic electron transport. Plant Physiol 131:793–802

    Article  PubMed  Google Scholar 

  • Drenkard E, Richter BG, Rozen S, Stutius LM, Angell NA, Mindrinos M, Cho RJ, Oefner PJ, Davis RW, Ausubel FM (2000) A simple procedure for the analysis of single nucleotide polymorphisms facilitates map-based cloning in Arabidopsis. Plant Physiol 124:1483–1492

    CAS  PubMed  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

    CAS  Google Scholar 

  • Faccioli P, Terzi V, Monetti A, Nicola J, Pecchioni N (1995) B-hordein STS markers for barley genotype identification: comparison with RFLPs, hordeins A-PAGE and morphophysiological traits. Seed Sci Technol 23:415–427

    Google Scholar 

  • Fowler DB, Chauvin LP, Limin AE, Sarhan F (1996) The regulatory role of vernalization in the expression of low-temperature induced genes in wheat and rye. Theor Appl Genet 93:554–559

    Article  CAS  Google Scholar 

  • Franckowiak JD, Lundqvist U (2002) Current list of new and revised Barley Genetic Stock description. Barley Genetic Newslett 32:47–137

    Google Scholar 

  • Freed RD, Eisensmith SP, Goetz S, Reicosky D, Smail VW, Wolberg P (1988) MSTAT-C user’s guide. Michigan State University, USA

  • Galiba G, Quarrie SA, Sutka J, Morgaunov A, Snape JW (1995) RFLP mapping of the vernalization (Vrn-1) and frost resistance (Fr1) genes on chromosome 5A of wheat. Theor Appl Genet 90:1174–1179

    CAS  Google Scholar 

  • Gilmour SJ, Zarka DG, Stockinger EJ, Salazar MP, Houghton MJ, Thomashow MF (1998) Low-temperature regulation of the Arabidopsis CBF family of AP2 transcriptional activators as an early step in cold-induced COR gene expression. Plant J 16:433–443

    CAS  PubMed  Google Scholar 

  • Giorni E, Crosatti C, Baldi P, Grossi M, Marè C, Stanca AM, Cattivelli L (1999) Cold-regulated gene expression during winter in frost-tolerant and frost-susceptible barley cultivars grown under field conditions. Euphytica 106:149–157

    Article  Google Scholar 

  • Hayes PM, Blake TK, Chen THH, Tragoonrung S, Chen F, Pan A, Liu B (1993) Quantitative trait loci on barley (Hordeum vulgare) chromosome 7 associated with components of winterhardiness. Genome 36:66–71

    Google Scholar 

  • Hayes PM, Chen FQ, Corey A, Pan A, Chen THH, Baird E, Powell W, Thomas W, Waugh R, Bedo Z, Karsai I, Blake T, Oberthur L (1997) The Dicktoo × Morex population: a model for dissecting components of winterhardiness in barley. In: Li PH, Chen THH (eds) Plant cold hardiness. Plenum Press, New York, USA

  • Hayes PM, Castro A, Marquez-Cedillo L, Corey A, Henson C, Jones BL, Kling D, Mather D, Matus I, Rossi C, Sato K (2003) Genetic diversity for quantitatively inherited agronomic and malting quality traits. In: Von Bothmer R et al. (eds) Diversity in barley. Elsevier Science Publishers, Amsterdam (in press)

  • Heun M, Kennedy AE, Anderson JA, Lapitan NLV, Sorrells ME, Tanksley SD (1991) Construction of a restriction fragment length polymorphism map for barley (Hordeum vulgare). Genome 34:437–447

    Google Scholar 

  • Ishimaru K, Yano M, Aoki N, Ono K, Hirose T, Lin SY, Monna L, Sasaki T, Ohsugi R (2001) Toward the mapping of physiological and agronomic characters on a rice function map: QTL analysis and comparison between QTLs and expressed sequence tags. Theor Appl Genet 102:793–800

    Article  CAS  Google Scholar 

  • Ismail AM, Hall AE, Close TJ (1999) Allelic variation of a dehydrin gene co-segregates with chilling tolerance during seedling emergence. Proc Natl Acad Sci USA 96:13566–13570

    CAS  PubMed  Google Scholar 

  • Karsai I, Mészáros K, Szucs P, Hayes P, Láng L, Bedo Z (1999) Effects of loci determining photoperiod sensitivity (Ppd-H1 ) and vernalization response (Sh2) on agronomic traits in the Dicktoo × Morex barley mapping population. Plant Breed 118:399–403

    Article  Google Scholar 

  • Karsai I, Mészáros K, Lang L, Hayes PM, Bedo Z (2001) Multivariate analysis of traits determining adaptation in cultivated barley. Plant Breeding 120:217–222

    Article  Google Scholar 

  • Kilian A, Kudrna D, Kleinhofs A (1999) Genetic and molecular characterization of barley chromosome telomeres. Genome 42:412–419

    Article  CAS  Google Scholar 

  • Lander ES, Botstein D (1989) Mapping Mendelian factors underlying quantitative traits using RFLP linkage maps. Genetics 121:185–199

    CAS  PubMed  Google Scholar 

  • Langridge P, Karakousis A, Collins N, Kretschmer J, Manning S (1995) A consensus linkage map of barley. Mol Breed 1:389–395

    CAS  Google Scholar 

  • Laurie DA, Pratchett N, Bezant JH, Snape JW (1995) RFLP mapping of five major genes and eight quantitative trait loci controlling flowering time in a winter × spring barley (Hordeum vulgare L) cross. Genome 38:575–585

    CAS  Google Scholar 

  • Limin AE, Fowler DB (2002) Developmental traits affecting low-temperature tolerance response in near-isogenic lines for the vernalization locus Vrn-A1 in wheat (Triticum aestivum L. em Thell). Ann Bot 89:579–585

    Article  CAS  Google Scholar 

  • Liu Z-W, Biyashev RM, Saghai Maroof MA (1996) Development of simple sequence repeat DNA markers and their integration into a barley linkage map. Theor Appl Genet 93:869–976

    CAS  Google Scholar 

  • Mano Y, Sayed-Tabatabaei BE, Graner A, Blake T, Takaiwa F, Oka S, Komatsuda T (1999) Map construction of sequence-tagged sites (STSs) in barley (Hordeum vulgare L). Theor Appl Genet 98:937–946

    CAS  Google Scholar 

  • Medina J, Bargues, Terol J, Pérez-Alonso M, Salinas J (1999) The Arabidopsis CBF gene family is composed of three genes encoding AP2 domain-containing proteins whose expression is regulated by low temperature but not by abscisic acid or dehydration. Plant Physiol 119:463–470

    CAS  Google Scholar 

  • Pan A, Hayes PM, Chen F, Chen THH, Blake T, Wright S, Karsai I, Bedö Z (1994) Genetic analysis of the components of winterhardiness in barley (Hordeum vulgare L). Theor Appl Genet 89:900–910

    CAS  Google Scholar 

  • Qi X, Lindhout P (1997) Development of AFLP markers in barley. Mol Gen Genet 254:330–336

    Article  CAS  PubMed  Google Scholar 

  • Qi X, Stam P, Lindhout P (1998) Use of locus-specific AFLP markers to construct a high-density molecular map in barley. Theor Appl Genet 96:376–384

    Article  CAS  Google Scholar 

  • Quarrie SA, Gulli M, Calestani C, Steed A, Marmiroli N (1994) Location of a gene regulating drought-induced abscisic acid production on the long arm of chromosome 5A of wheat. Theor Appl Genet 89:794–800

    CAS  Google Scholar 

  • Ramsay L, Macaulay M, degli Ivanissevich S, MacLean K, Cardle L, Fuller J, Edwards KJ, Tuvesson S, Morgante M, Massari A, Maestri E, Marmiroli N, Sjakste T, Ganal M, Powell W, Waugh R (2000) Simple sequences repeat-based linkage map of barley. Genetics 156:1997–2005

    CAS  PubMed  Google Scholar 

  • Rizza F, Pagani D, Stanca AM, Cattivelli L (2001) Use of chlorophyll fluorescence to evaluate the cold acclimation and freezing tolerance of winter and spring oats. Plant Breed 120:389–396

    Article  Google Scholar 

  • Rozen S, Skaletsky HJ (1998) Primer3. (Available from http://www-genome.wi.mit.edu/genome_software/other/primer3.html)

  • Saghai-Maroof MA, Soliman KA, Jorgensen RA, Allard RW (1984) Ribosomal DNA spacer-length polymorphisms in barley: Mendelian inheritance, chromosomal location, and population dynamics. Proc Natl Acad Sci USA 81:8014–8018

    CAS  PubMed  Google Scholar 

  • Salinas J (2002) Genetic approaches confirm an important role for CBFs in cold acclimation and reveal a complex network for regulating CBF expression. In: XIII Int Conf On Arabidopsis Research, Seville, Spain 2002. http://www.arabidopsis2002.com

  • Salvo-Garrido H, Laurie DA, Jaffé B, Snape JW (2001) An RFLP map of diploid Hordeum bulbosum L. and comparison with maps of barley (H. vulgare L.) and wheat (Triticum aestivum L.). Theor Appl Genet 103:869–880

    CAS  Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York, USA

    Google Scholar 

  • Snape JW, Semikhodskii A, Fish L, Sarma RN, Quarrie SA, Galiba G, Sutka J (1997) Mapping frost tolerance loci in wheat and comparative mapping with other cereals. Acta Agric Hung 45:265–270

    Google Scholar 

  • Stockinger EJ, Gilmour SJ, Thomashow MF (1997) Arabidopsis thaliana CBF1 encodes an AP2 domain-containing transcriptional activator that binds to the C-repeat/DRE, a cis-acting DNA regulatory element that stimulates transcription in response to low temperature and water deficit. Proc Natl Acad Sci USA 94:1035–1040

    CAS  PubMed  Google Scholar 

  • Stracke S, Borner A (1998) Molecular mapping of the photoperiod response gene ea7 in barley. Theor Appl Genet 97:797–800

    Article  CAS  Google Scholar 

  • Sutka J (1981) Genetic studies of frost resistance in wheat. Theor Appl Genet 59:145–152

    Google Scholar 

  • Sutka J, Snape JW (1989) Location of a gene for frost resistance on chromosome 5A of wheat. Euphytica 42:41–44

    Google Scholar 

  • Sutka J, Galiba G, Vaguifalvi A, Gill BS, Snape JW (1999) Physical mapping of the Vrn-A1 and Fr1 genes on chromosome 5A of wheat using deletion lines. Theor Appl Genet 99:199–202

    Article  CAS  Google Scholar 

  • Takahashi R, Yasuda S (1971) Genetics of earliness and growth habit in barley In: Nilan R (ed) Proc 2nd Int Barley Genetics Symposium. Barley Genetics II, Pullman, USA, 1969, pp 388–413

    Google Scholar 

  • Thomashow MF, Gilmour SJ, Stockinger EJ, Jaglo-Ottosen KR, Zarka DG (2001) Role of Arabidopsis CBF transcriptional activators in cold acclimation. Physiol Plant 112:171–175

    CAS  Google Scholar 

  • Tóth B, Galiba G, Fehér E, Sutka J, Snape JW (2003a) Mapping genes affecting flowering time and frost resistance on chromosome 5B of wheat. Theor Appl Genet (in press)

  • Tóth B, Francia E, Rizza R, Stanca AM, Galiba G, Pecchioni N (2003b) Development of PCR-based markers of 5H chromosome for assisted selection of frost-tolerant genotypes in barley. Mol Breed (submitted)

  • Utz HF, Melchinger AE (1996) PLABQTL: a program for composite interval mapping of QTL. J Agric Genomics 2 http://www.ncgr.org/ag/papers96/paper196/indexp196.html

  • Vagujfalvi A, Crosatti C, Galiba G, Dubcovsky J, Cattivelli L (2000) Two loci on wheat chromosome 5A regulate the differential cold-dependent expression of the cor14b gene in frost-tolerant and frost-sensitive genotypes. Mol Gen Genet 263:194–200

    PubMed  Google Scholar 

  • Van Ooijen JW, Boer MP, Jansen RC, Maliepaard C (2002) MapQTL 4.0: software for the calculation of QTL positions on genetic maps. Plant Research International, Wageningen, The Netherlands

  • Von Zitzewitz J, Chen THH, Corey A, Filichkin T, Hayes PM Marquez-Cedillo L, Skinner JS, Szucs P (2003) Mining barley for genes determining winter hardiness phenotypes. PAG XI poster and Abiotic Stress Workshop Presentation, San Diego, California, USA, Jan 11–15, 2003

  • Xue GP (2002) An AP2 domain transcription factor HvCBF1 activates expression of cold-responsive genes in barley through interaction with a (G/a)(C/t)CGAC motif. Biochim Biophys Acta 1577:63–72

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This work was supported by grants from MiUR (Ministero dell’Università e della Ricerca Scientifica) “Progetto FIRB FUNCTIONMAP” (ID: RBAU01MHMR_004), EU INCOA3 Project MABDE No. ICA3-2002-10073, the Hungarian National Research Fund (T034277) and the Hungarian-Italian Intergovernmental Scientific and Technological Cooperation Programme (ID: I-49/99). Funding for Hayes and Skinner was provided by the United States National Science Foundation Project No. DBIO110124. The authors are very grateful to J. Von Zitzewitz (Oregon State University, Oregon, USA) for re-analysis of the chromosome 5H QTL with MapQTL and QTL Cartographer software; and to Mr. Laszlo Stehli and Mrs. Donata Pagani for their excellent technical assistance.

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Authors and Affiliations

  1. Istituto Sperimentale per la Cerealicoltura, 29017, Fiorenzuola d’Arda, Italy

    E. Francia, F. Rizza, L. Cattivelli, A. M. Stanca & N. Pecchioni

  2. Agricultural Research Institute of the Hungarian Academy of Sciences, 2462, Martonvásár, Hungary

    G. Galiba & B. Tóth

  3. Department of Crop and Soil Science and Department of Horticulture, Oregon State University, Corvallis, OR 97331, USA

    P. M. Hayes & J. S. Skinner

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  1. E. Francia
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  2. F. Rizza
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  3. L. Cattivelli
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  4. A. M. Stanca
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  5. G. Galiba
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  6. B. Tóth
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  7. P. M. Hayes
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  8. J. S. Skinner
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  9. N. Pecchioni
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Correspondence to N. Pecchioni.

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Communicated by J.W. Snape

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Francia, E., Rizza, F., Cattivelli, L. et al. Two loci on chromosome 5H determine low-temperature tolerance in a ‘Nure’ (winter) × ‘Tremois’ (spring) barley map. Theor Appl Genet 108, 670–680 (2004). https://doi.org/10.1007/s00122-003-1468-9

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