Skip to main content
SpringerLink
Log in

Low-temperature tolerance and genetic potential in wheat (Triticum aestivum L.): response to photoperiod, vernalization, and plant development

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

It is frequently observed that winter habit types are more low-temperature (LT) tolerant than spring habit types. This raises the question of whether this is due to pleiotropic effects of the vernalization loci or to the linkage of LT-tolerance genes to these vernalization loci. Reciprocal near-isogenic lines (NILs) for alleles at the Vrn-A1 locus, Vrn-A1 and vrn-A1, determining spring and winter habit respectively, in two diverse genetic backgrounds of wheat (Triticum aestivum L.) were used to separate the effects of vernalization, photoperiod, and development on identical, or near identical, genetic backgrounds. The vrn-A1 allele in the winter lines allowed full expression of genotype dependent LT tolerance potential. The winter allele (vrn-A1) in a very cold tolerant genetic background resulted in 11°C, or a 2.4-fold, greater LT tolerance compared to the spring allele. Similarly, the delay in development caused by short-day (SD) versus long-day (LD) photoperiod in the identical spring habit NIL resulted in an 8.5°C or 2.1-fold, increase in LT tolerance. The duration of time in early developmental stages was shown to underlie full expression of genetic LT-tolerance potential. Therefore, pleiotropic effects of the vernalization loci can explain the association of LT tolerance and winter habit irrespective of either the proposed closely linked Fr-A1 or the more distant Fr-A2 LT-tolerance QTLs. Plant development progressively reduced LT-acclimation ability, particularly after the main shoot meristem had advanced to the double ridge reproductive growth stage. The Vrn-1 genes, or other members of the flowering induction pathway, are discussed as possible candidates for involvement in LT-tolerance repression.

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

Similar content being viewed by others

Abbreviations

AP1 :

APETALA 1

CBF:

C-repeat/dehydration-responsive element binding factor

Cor :

Cold-responsive

DR:

Double ridge

LD:

Long day

LT:

Low-temperature

NIL:

Near-isogenic line

SD:

Short day

TaVRT-1 :

Triticum aestivum vegetative to reproductive transition-1

References

  • Amasino R (2004) Vernalization, competence, and the epigenetic memory of winter. Plant Cell 16:2553–2559

    Article  PubMed  CAS  Google Scholar 

  • Blake T, Tragoonrung S, Walton M, Wright S, Jones B, Chen T, Hayes P (1993) Mapping the genes for cold tolerance in barley. In: Close TJ, Bray EA (eds) Plant responses to cellular dehydration during environmental stress. The American Society of Plant Physiologists, Rockville, pp 202–210

    Google Scholar 

  • Brule-Babel AL, Fowler DB (1988) Genetic control of cold hardiness and vernalization requirement in winter wheat. Crop Sci 28:879–884

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Danyluk J, Kane NA, Breton G, Limin AE, Fowler DB, Sarhan F (2003) TaVRT-1, a putative transcription factor associated with vegetative to reproductive transition in cereals. Plant Physiol 132:1849–1860

    Article  PubMed  CAS  Google Scholar 

  • de-Folter S, Immink RGH, Kieffer M, Parenicova L, Henz SR, Weigel D Busscher M, Kooiker M, Colombo L, Kater MM, Davies B, Angenent GC (2005) Comprehensive interaction map of the Arabidopsis MADS box transcription factors. Plant Cell 17:1424–1433

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Fowler DB, Chauvin LP, Limin AE, Sarhan F (1996a) 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 

  • Fowler DB, Limin AE, Wang S, Ward RW (1996b) Relationship between low-temperature tolerance and vernalization response in wheat and rye. Can J Plant Sci 76:37–42

    Google Scholar 

  • Fowler DB, Limin AE, Ritchie JT (1999) Low-temperature tolerance in cereals: model and genetic interpretation. Crop Sci 39:626–633

    Article  Google Scholar 

  • Fowler DB, Breton G, Limin AE, Mahfoozi S, Sarhan F (2001) Photoperiod and temperature interactions regulate low-temperature-induced gene expression in barley. Plant Physiol 127:1676–1681

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Galiba G, Quarrie SA, Sutka J, Morgounov A, Snape JW (1995) RFLP mapping of the vernalization (Vrn1) and frost resistance (Fr1) genes on chromosome 5A of wheat. Theor Appl Genet 90:174–1179

    Article  Google Scholar 

  • Gilmour SJ, Sebolt AM, Salazar MP, Everard JD, Thomashow MF (2000) Overexpression of the Arabidopsis CBF3 transcriptional activator mimics multiple biochemical changes associated with cold acclimation. Plant Physiol 124:1854–1865

    Article  PubMed  CAS  Google Scholar 

  • Hayes HK, Aamodt OS (1927) Inheritance of winter hardiness and growth habit in crosses of Marquis with Minhardi and Minturki wheats. J Agric Res 35:223–236

    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

    Article  PubMed  CAS  Google Scholar 

  • Henderson IR, Shindo C, Dean C (2003) The need for winter in the switch to flowering. Annu Rev Genet 37:371–392

    Article  PubMed  CAS  Google Scholar 

  • Houde M, Danyluk J, Laliberté JF, Rassart E, Dhindsa DS, Sarhan F (1992) A molecular marker to select for freezing tolerance in Gramineae. Mol Gen Genet 234:43–48

    PubMed  CAS  Google Scholar 

  • Jaglo-Ottosen KR, Gilmour SJ, Zarka DG, Schabenberger O, Thomashow MF (1998) Arabidopsis CBF1 overexpression induces COR genes and enhances freezing tolerance. Science 280:104–106

    Article  PubMed  CAS  Google Scholar 

  • Jaglo KR, Kleff S, Amundsen KL, Zhang X, Haake V, Zhang JZ, Deits T, Thomashow MF (2001) Components of the Arabidopsis C-repeat/dehydration-responsive element binding factor cold-response pathway are conserved in Brassica napus and other plant species. Plant Physiol 127:910–917

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Levy YY, Dean C (1998) The transition to flowering. Plant Cell 10:1973–1989

    Article  PubMed  CAS  Google Scholar 

  • Limin AE, Danyluk J, Chauvin L-P, Fowler DB, Sarhan F (1997) Chromosome mapping of low-temperature induced Wcs 120 family genes and regulation of cold-tolerance expression in wheat. Mol and Gen Genet 253:720–727

    Article  CAS  Google Scholar 

  • Limin AE, Fowler DB (1988) Cold hardiness expression in interspecific hybrids and amphiploids of the Triticeae. Genome 30:261–265

    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  PubMed  CAS  Google Scholar 

  • Mahfoozi S, Limin AE, Fowler DB (2001a) Developmental regulation of low-temperature tolerance in winter wheat. Ann Bot 87:751–757

    Article  Google Scholar 

  • Mahfoozi S, Limin AE, Fowler DB (2001b) Influence of vernalization and photoperiod responses on cold hardiness in winter cereals. Crop Sci 41:1006–1011

    Article  Google Scholar 

  • Mahfoozi S, Limin AE, Hayes PM, Hucl P, Fowler DB (2000) Influence of photoperiod response on the expression of cold hardiness in cereals. Can J Plant Sci 80:721–724

    Google Scholar 

  • Murai K, Miyamae M, Kato H, Takumi S, Ogihara Y (2003) WAP1, a wheat APETALA1 homolog, plays a central role in the phase transition from vegetative to reproductive growth. Plant Cell Physiol 44:255–1265

    Article  Google Scholar 

  • Prasil IT, Prasilova P, Pankova K (2004) Relationships among vernalization, shoot apex development and frost tolerance in wheat. Ann Bot 94:413–418

    Article  PubMed  Google Scholar 

  • Quisenberry KS (1931) Inheritance of winter hardiness, growth habit, and stem-rust reaction in crosses between Minhardi winter and H-44 spring wheat. USDA Bul, p 218

  • Rawson HM, Zajac M, Penrose LDJ (1998) Effect of seedling temperature and its duration on development of wheat cultivars differing in vernalization response. Field Crops Res 57:289–300

    Article  Google Scholar 

  • Toth B, Galiba G, Feher E, Sutka J, Snape JW (2003) Mapping genes affecting flowering time and frost resistance on chromosome 5B in wheat. Theor Appl Genet 107:509–514

    Article  PubMed  CAS  Google Scholar 

  • Trevaskis B, Bagnall DJ, Ellis MH, Peacock WJ, Dennis ES (2003) MADS box genes control vernalization-induced flowering in cereals. Proc Natl Acad Sci USA 100:13099–13104

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Vagujfalvi A, Galiba G, Cattivelli L, Dubcovsky J (2003) The cold-regulated transcriptional activator Cbf3 is linked to the frost-tolerance locus Fr-A2 on wheat chromosome 5A. Mol Gen Genom 269:60–67

    CAS  Google Scholar 

  • Welch SM, Dong Z, Roe JL (2004) Modelling gene networks controlling transition to flowering in Arabidopsis. “New directions for a diverse planet’’. In: Proceedings 4th international crop science congress,September 26–October 1 2004, Brisbane, Australia. Published on CDROM. Web site www.cropscience.org.au

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

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

Financial support from Genome Canada/Genome Prairie and Ducks Unlimited Canada is gratefully acknowledged. The excellent technical assistance of Garcia Schellhorn and Twyla Chastain is greatly appreciated.

Author information

Authors and Affiliations

  1. Department of Plant Sciences, University of Saskatchewan, 51 Campus Drive, S7N 5A8, Saskatoon , SK, Canada

    Allen E. Limin & D. Brian Fowler

Authors
  1. Allen E. Limin
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. D. Brian Fowler
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Allen E. Limin.

Rights and permissions

Reprints and permissions

About this article

Cite this article

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-006-0219-y

Keywords

Search

Navigation