Skip to main content
SpringerLink
Log in

QTL analysis of frost damage in pea suggests different mechanisms involved in frost tolerance

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

Abstract

Key message

Avoidance mechanisms and intrinsic resistance are complementary strategies to improve winter frost tolerance and yield potential in field pea.

Abstract

The development of the winter pea crop represents a major challenge to expand plant protein production in temperate areas. Breeding winter cultivars requires the combination of freezing tolerance as well as high seed productivity and quality. In this context, we investigated the genetic determinism of winter frost tolerance and assessed its genetic relationship with yield and developmental traits. Using a newly identified source of frost resistance, we developed a population of recombinant inbred lines and evaluated it in six environments in Dijon and Clermont-Ferrand between 2005 and 2010. We developed a genetic map comprising 679 markers distributed over seven linkage groups and covering 947.1 cM. One hundred sixty-one quantitative trait loci (QTL) explaining 9–71 % of the phenotypic variation were detected across the six environments for all traits measured. Two clusters of QTL mapped on the linkage groups III and one cluster on LGVI reveal the genetic links between phenology, morphology, yield-related traits and frost tolerance in winter pea. QTL clusters on LGIII highlighted major developmental gene loci (Hr and Le) and the QTL cluster on LGVI explained up to 71 % of the winter frost damage variation. This suggests that a specific architecture and flowering ideotype defines frost tolerance in winter pea. However, two consistent frost tolerance QTL on LGV were independent of phenology and morphology traits, showing that different protective mechanisms are involved in frost tolerance. Finally, these results suggest that frost tolerance can be bred independently to seed productivity and quality.

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

References

  • Avia K, Pilet-Nayel ML, Bahrman N, Baranger A, Delbreil B, Fontaine V, Hamon C, Hanocq E, Niarquin M, Sellier H, Vuylsteker C, Prosperi JM, Lejeune-Henaut I (2013) Genetic variability and QTL mapping of freezing tolerance and related traits in Medicago truncatula. Theor Appl Genet 126:2353–2366

    Article  CAS  PubMed  Google Scholar 

  • Bordat A, Savois V, Nicolas M, Salse J, Chauveau A, Bourgeois M, Potier J, Houtin H, Rond C, Murat F, Marget P, Aubert G, Burstin J (2011) Translational Genomics in Legumes Allowed Placing In Silico 5460 Unigenes on the Pea Functional Map and Identified Candidate Genes in Pisum sativum L. G3-Genes Genomes Genet 1:93-103

    Google Scholar 

  • Bourion V, Rizvi SMH, Fournier S, de Larambergue H, Galmiche F, Marget P, Duc G, Burstin J (2010) Genetic dissection of nitrogen nutrition in pea through a QTL approach of root, nodule, and shoot variability. Theor Appl Genet 121:71–86

    Article  PubMed  Google Scholar 

  • Burstin J, Marget P, Huart M, Moessner A, Mangin B, Duchene C, Desprez B, Munier-Jolain N, Gr Duc (2007) Developmental genes have pleiotropic effects on plant morphology and source capacity, eventually impacting on seed protein content and productivity in pea. Plant Physiol 144:768–781

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Cunningham SM, Nadeau P, Castonguay Y, Laberge S, Volenec JJ (2003) Raffinose and stachyose accumulation, galactinol synthase expression, and winter injury of contrasting alfalfa germplasms. Crop Sci 43:562–570

    Article  CAS  Google Scholar 

  • D’Erfurth I, Le Signor C, Aubert G, Sanchez M, Vernoud V, Darchy B, Lherminier J, Bourion V, Bouteiller N, Bendahmane A, Buitink J, Prosperi JM, Thompson R, Burstin J, Gallardo K (2012) A role for an endosperm-localized subtilase in the control of seed size in legumes. New Phytol 196:738–751

    Article  PubMed  Google Scholar 

  • Deulvot C, Charrel H, Marty A, Jacquin F, Donnadieu C, Lejeune-Henaut I, Burstin J, Aubert G (2010) Highly-multiplexed SNP genotyping for genetic mapping and germplasm diversity studies in pea. BMC Genomics 11:468

    Google Scholar 

  • Dhillon T, Pearce SP, Stockinger EJ, Distelfeld A, Li CX, Knox AK, Vashegyi I, Vagujfalvi A, Galiba G, Dubcovsky J (2010) Regulation of freezing tolerance and flowering in temperate cereals: the VRN-1 Connection. Plant Physiol 153:1846–1858

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Dong MA, Farre EM, Thomashow MF (2011) Circadian clock-associated 1 and late elongated hypocotyl regulate expression of the c-repeat binding factor (CBF) pathway in Arabidopsis. Proc Natl Acad Sci USA 108:7241–7246

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Dumont E, Fontaine V, Vuylsteker C, Sellier H, Bodele S, Voedts N, Devaux R, Frise M, Avia K, Hilbert JL, Bahrman N, Hanocq E, Lejeune-Henaut I, Delbreil B (2009) Association of sugar content QTL and PQL with physiological traits relevant to frost damage resistance in pea under field and controlled conditions. Theor Appl Genet 118:1561–1571

    Article  CAS  PubMed  Google Scholar 

  • Foucher F, Morin J, Courtiade J, Cadioux S, Ellis N, Banfield MJ, Rameau C (2003) DETERMINATE and LATE FLOWERING are two TERMINAL FLOWER1/CENTRORADIALIS homologs that control two distinct phases of flowering initiation and development in pea. Plant Cell 15:2742–2754

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Franklin KA, Whitelam GC (2007) Light-quality regulation of freezing tolerance in Arabidopsis thaliana. Nature Genet 39:1410–1413

    Article  CAS  PubMed  Google Scholar 

  • Jourjon MF, Jasson S, Marcel J, Ngom B, Mangin B (2005) MCQTL: multi-allelic QTL mapping in multi-cross design. Bioinformatics 21:128–130

    Article  CAS  PubMed  Google Scholar 

  • Krajewski P, Bocianowski J, Gawłowska M, Kaczmarek Z, Pniewski T, Święcicki W, Wolko B (2011) QTL for yield components and protein content: a multienvironment study of two pea (Pisum sativum L.) populations. Euphytica 183:323–336

    Article  Google Scholar 

  • Lander ES, Green P, Abrahamson J, Barlow A, Daly MJ, Lincoln SE, Newburg L (1987) MAPMAKER: an interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. Genomics 1:174–181

    Article  CAS  PubMed  Google Scholar 

  • Larmure A, Munier-Jolain NG (2004) A crop model component simulating N partitioning during seed filling in pea. Fields Crops Res 85:135–148

    Article  Google Scholar 

  • Lejeune-Hénaut I, Hanocq E, Bethencourt L, Fontaine V, Delbreil B, Morin J, Petit A, Devaux R, Boilleau M, Stempniak JJ, Thomas M, Laine AL, Foucher F, Baranger A, Burstin J, Rameau C, Giauffret C (2008) The flowering locus Hr colocalizes with a major QTL affecting winter frost tolerance in Pisum sativum L. Theor Appl Genet 116:1105–1116

    Article  PubMed  Google Scholar 

  • Levitt J (1980) Responses of plants to environmental stress, vol 1, 2nd edn. Chilling, freezing, and high temperature stresses p. 497

  • Loridon K, McPhee K, Morin J, Dubreuil P, Pilet-Nayel ML, Aubert G, Rameau C, Baranger A, Coyne C, Lejeune-Henaut I, Burstin J (2005) Microsatellite marker polymorphism and mapping in pea (Pisum sativum L.). Theor Appl Genet 111:1022–1031

    Article  CAS  PubMed  Google Scholar 

  • Mikkelsen MD, Thomashow MF (2009) A role for circadian evening elements in cold-regulated gene expression in Arabidopsis. Plant J 60:328–339

    Article  CAS  PubMed  Google Scholar 

  • Murfet IC (1985) In: Halevy A (ed) Handbook of flowering. CRC Press, Boca Raton, pp 97–126

    Google Scholar 

  • Murfet IC, Reid JB (1993) Developmental mutants. Peas: genetics, molecular biology and biotechnology. CAB International, Wallingford, pp 165–216

    Google Scholar 

  • Nishizawa A, Yabuta Y, Shigeoka S (2008) Galactinol and Raffinose constitute a novel function to protect plants from oxidative damage. Plant Physiol 147:1251–1263

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • R Development Core Team (2013) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org

  • SAS (1999) SAS/STAT® User’s Guide, version 8. SAS Institute, Cary, NC pp. 3884

    Google Scholar 

  • Stoddard FL, Balko C, Erskine W, Khan HR, Link W, Sarker A (2006) Screening techniques and sources of resistance to abiotic stresses in cool-season food legumes. Euphytica 147:167–186

    Article  Google Scholar 

  • Taji T, Ohsumi C, Iuchi S, Seki M, Kasuga M, Kobayashi M, Yamaguchi-Shinozaki K, Shinozaki K (2002) Important roles of drought- and cold-inducible genes for galactinol synthase in stress tolerance in Arabidopsis thaliana. Plant J 29:417–426

    Article  CAS  PubMed  Google Scholar 

  • Tar’an B, Warkentin T, Somers DJ, Miranda D, Vandenberg A, Blade S, Bing D (2004) Identification of quantitative trait loci for grain yield, seed protein concentration and maturity in field pea (Pisum sativum L.). Euphytica 136:297–306

    Article  Google Scholar 

  • Tayeh N, Bahrman N, Devaux R, Bluteau A, Prosperi JM, Delbreil B, Lejeune-Henaut I (2013a) A high-density genetic map of the Medicago truncatula major freezing tolerance QTL on chromosome 6 reveals colinearity with a QTL related to freezing damage on Pisum sativum linkage group VI. Mol Breed 32:279–289

    Article  CAS  Google Scholar 

  • Tayeh N, Bahrman N, Sellier H, Bluteau A, Blassiau C, Fourment J, Bellec A, Debelle F, Lejeune-Hénaut I, Delbreil B (2013b) A tandem array of CBF/DREB1 genes is located in a major freezing tolerance QTL region on Medicago truncatula chromosome 6. BMC Genom 14:814

    Article  CAS  Google Scholar 

  • Timmerman-Vaughan GM, Mills A, Whitfield C, Frew T, Butler R, Murray S, Lakeman M, McCallum J, Russell A, Wilson D (2005) Linkage mapping of QTL for seed yield, yield components, and developmental traits in pea. Crop Sci 45:1336–1344

    Article  CAS  Google Scholar 

  • Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78

    Article  CAS  PubMed  Google Scholar 

  • Weller JL, Hecht V, Liew LC, Sussmilch FC, Wenden B, Knowles CL, Schoor JKV (2009) Update on the genetic control of flowering in garden pea. J Exp Bot 60:2493–2499

    Article  CAS  PubMed  Google Scholar 

  • Weller JL, Liew LC, Hecht VFG, Rajandran V, Laurie RE, Ridge S, Wenden B, Vander Schoor JK, Jaminon O, Blassiau C, Dalmais M, Rameau C, Bendahmane A, Macknight RC, Lejeune-Henaut I (2012) A conserved molecular basis for photoperiod adaptation in two temperate legumes. Proc Natl Acad Sci USA 109:21158–21163

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zhuo CL, Wang T, Lu SY, Zhao YQ, Li XG, Guo ZF (2013) A cold responsive galactinol synthase gene from Medicago falcata (MfGolS1) is induced by myo-inositol and confers multiple tolerances to abiotic stresses. Physiol Plant 149:67–78

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The authors thank Catherine Desmetz, Chantal Martin and Emilie Vieille (INRA Dijon—UMR Agroécologie) for their implication in the genotyping, Norbert Blanc and Pierre Mangin (INRA Dijon—UE Domaine d’Epoisses), Bernard Debote and Florent Batifoy (INRA Clermont-Ferrand—UE phénotypage au champ des céréales) for technical assistance in the field experiments, Michael Touratier and Jennifer Bour-Schmitt (INRA Dijon—UMR Agroécologie) for the seed protein analysis. We thank Christophe Lecomte (INRA Dijon—UMR Agroécologie) for the pea frost data at Chaux-des-Prés (France). We thank Grégoire Aubert (INRA Dijon—UMR Agroécologie) for his helpful suggestions on the manuscript.

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical standards

The experiments comply with the current laws of the country in which they were performed.

Author information

Authors and Affiliations

  1. INRA, UMR 1347 Agroécologie, BP 86510, 21000, Dijon Cedex, France

    Anthony Klein, Hervé Houtin, Céline Rond, Pascal Marget, Françoise Jacquin, Karen Boucherot, Myriam Huart & Judith Burstin

  2. Biogemma, Route d’Ennezat, CS 90126, 63720, Chappes, France

    Nathalie Rivière

  3. INRA, UMR 1349 IGEPP, BP 35327, 35653, Le Rheu Cedex, France

    Gilles Boutet

  4. INRA, UMR 1281 SADV, Estrées-Mons, BP 50136, 80203, Péronne Cedex, France

    Isabelle Lejeune-Hénaut

Authors
  1. Anthony Klein
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hervé Houtin
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Céline Rond
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Pascal Marget
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Françoise Jacquin
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Karen Boucherot
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Myriam Huart
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Nathalie Rivière
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Gilles Boutet
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Isabelle Lejeune-Hénaut
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Judith Burstin
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Anthony Klein.

Additional information

Communicated by I. Rajcan.

Electronic supplementary material

Below is the link to the electronic supplementary material.

122_2014_2299_MOESM1_ESM.pdf

Frequency distribution of Pop9 lines adjusted means observed on one-row field trial between 2005 and 2010 at INRA Dijon and INRA Clermont-Ferrand. The arrowheads indicate the mean value of parental lines: Ch, China; Ca, Caméor. BegFlo beginning of flowering, BSF beginning of seed filling, EndFlo end of the flowering, Harvest maturity, Flo flowering period, Fill filling period, Repro reproductive period, WFD winter frost damage, NB branching type, Area1 and Area2 leaf projected area before and after the winter respectively, Chloro SPAD chlorophyll measurements, hBSF height at BSF, hHarvest height at harvest, NBB number of basal branches per plant, PN pod number per plant, SN seed number per plant, SNP seed number per pod, SW seed weight per plant, TSW thousand seed weight, SDW straw dry weight per plant, BDW biomass dry weight per plant, HI harvest index and SPC seed protein content (PDF 132 kb)

122_2014_2299_MOESM2_ESM.pdf

Mean parental and recombinant inbred values, standard deviation, heritabilities and significance of genotype effect measured on one-row field trial between 2005 and 2010 at INRA Dijon and INRA Clermont-Ferrand. a Cler06 Clermont-Ferrand autumn sowing in 2005, Cler10 Clermont-Ferrand autumn sowing in 2009, Dij08 Dijon autumn sowing in 2007, Dij08S Dijon spring sowing in 2008, Dij09 Dijon autumn sowing in 2008, Dij10 Dijon autumn sowing in 2009, b BegFlo beginning of flowering, BSF beginning of seed filling, EndFlo end of the flowering, Harvest maturity, Flo flowering period, Fill filling period, Repro reproductive period, WFD winter frost damage, NB branching type, Area1, Area2 leaf projected area before and after the winter respectively, Chloro SPAD chlorophyll measurements, hBSF height at BSF, hHarvest height at harvest, NBB number of basal branches per plant, PN pod number per plant, SN seed number per plant, SNP seed number per pod, SW seed weight per plant, TSW thousand seed weight, SDW straw dry weight per plant, BDW biomass dry weight per plant, HI harvest index and SPC seed protein content (PDF 74 kb)

122_2014_2299_MOESM3_ESM.pdf

Climatic data recorded at INRA Dijon and INRA Clermont-Ferrand between 2005 and 2010. Dij08 Dijon autumn sowing in 2007, Dij09 Dijon autumn sowing in 2008, Dij10 Dijon autumn sowing in 2009, Cler06 Clermont-Ferrand autumn sowing in 2005, Cler10 Clermont-Ferrand autumn sowing in 2009, Tmin minimal temperature (°C), Tmax maximal temperature (°C), Tavg average temperature (°C), rainfall (millimeter) (PDF 26 kb)

122_2014_2299_MOESM4_ESM.pdf

Pearson correlation coefficients between phenotypic traits recorded from 2005 to 2010 in Pop9 at INRA Dijon and INRA Clermont-Ferrand. BegFlo beginning of flowering, BSF beginning of seed filling, EndFlo end of the flowering, Harvest maturity, Flo flowering period, Fill filling period, Repro reproductive period, WFD winter frost damage, NB branching type, Area1, Area2 leaf projected area before and after the winter respectively, Chloro SPAD chlorophyll measurements, hBSF height at BSF, hHarvest height at harvest, NBB number of basal branches per plant, PN pod number per plant, SN seed number per plant, SNP seed number per pod, SW seed weight per plant, TSW thousand seed weight, SDW straw dry weight per plant, BDW biomass dry weight per plant, HI harvest index and SPC seed protein content, *, ** and *** significant correlation at the P < 0.05, P < 0.01 and P < 0.001 probability level, respectively (PDF 33 kb)

122_2014_2299_MOESM5_ESM.pdf

QTL parameters detected in Pop9 from 2005 to 2010 at INRA Dijon and INRA Clermont-Ferrand. a Name of QTL defined by trait and condition, b Area1, Area2 leaf projected area before and after the winter respectively, BDW biomass dry weight per plant, BegFlo beginning of flowering, BSF beginning of seed filling, Chloro SPAD chlorophyll measurements, EndFlo end of the flowering, Fill filling period, Flo flowering period, Harvest maturity, hBSF height at BSF, hHarvest height at harvest, HI harvest index, NB branching type, NBB number of basal branches per plant, PN pod number per plant, Repro reproductive period, SDW straw dry weight per plant, SN seed number per plant, SNP seed number per pod, SPC seed protein content, SW seed weight per plant, TSW thousand seed weight and WFD winter frost damage, c Cler06 Clermont-Ferrand autumn sowing in 2005, Cler10 Clermont-Ferrand autumn sowing in 2009, Dij08 Dijon autumn sowing in 2007, Dij08S Dijon spring sowing in 2008, Dij09 Dijon autumn sowing in 2008, Dij10 Dijon autumn sowing in 2009, d QTL position from the first marker of the linkage group (in cM Kosambi), e Position of the lower and upper ends of the QTL confidence intervals, from the first marker of the linkage group (in cM Kosambi), f P peak value at the QTL position for each variable, g Phenotypic variance explained by each QTL, h Allelic value of Caméor (PDF 148 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Klein, A., Houtin, H., Rond, C. et al. QTL analysis of frost damage in pea suggests different mechanisms involved in frost tolerance. Theor Appl Genet 127, 1319–1330 (2014). https://doi.org/10.1007/s00122-014-2299-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00122-014-2299-6

Keywords

Search

Navigation