Skip to main content
Log in

Quantitative Trait Loci Associated to Drought Adaptation in Pea (Pisum sativum L.)

  • Original Paper
  • Published:
Plant Molecular Biology Reporter Aims and scope Submit manuscript

Abstract

Pea (Pisum sativum L.) is an important grain legume whose yield stability and production is constrained by drought stress in most environments. However, little is known on availability of drought adaptation sources and its genetic control in pea. The aim of this work was to study the genetic of drought adaptation in pea and identify the genomic regions controlling the trait. Towards this objective, in this work, we assessed drought symptoms and relative water content in soil (RWCS) and leaves (RWCL) along a time course of water stress on a pea Recombinant Inbreed Lines (RILs) population from two parents known to segregate for drought adaptation. Drought adaptation in this population was a quantitative trait. QTL analysis using composite interval mapping (CIM) and multiple interval mapping (MIM) allowed us to identify ten quantitative trait loci (QTLs) associated with the traits explaining individually from 9 to 33 % of the phenotypic variation depending on the variable assessed and altogether from 20 to 57 %. A set of reproducible markers linked to these QTLs (A6, AA175, AC74, AD57, AB141, AB64, Psblox2, PsAAP2_SNP4, and DipeptIV_SNP1) were identified. These markers can be used to select the individuals harbouring the desired QTLs in pea breeding programs for drought adaptation.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Aguirreazabal L, Bouchier-Combaud S, Radziejwoski A, Dauzat M, Cookson SJ, Granier C (2006) Plasticity to soil water deficit in Arabidopsis thaliana: dissection of leaf development into underlying growth dynamic and cellular variables reveals invisible phenotypes. Plant, Cell Environ 29:2216–2227

    Article  CAS  Google Scholar 

  • Alexieva V, Sergiev I, Mapelli S, Karanov E (2001) The effect of drought and ultraviolet radiation on growth and stress markers in pea and wheat. Plant, Cell Environ 24:1337–1344

    Article  CAS  Google Scholar 

  • Alonso-Ramírez A, Rodríguez D, Reyes D, Jiménez JA, Nicolás G, López-Climent M, Gómez-Cadenas A, Nicolás C (2009) Cross-talk between gibberellins and salicylic acid in early stress responses in Arabidopsis thaliana seeds. Plant Signal Behav 8:750–751

    Article  Google Scholar 

  • Araújo SS, Beebe S, Crespi M, Delbreil B, González EM, Gruber V, Lejeune-Henaut I, Link W, Monteros MJ, Prats E, Rao I, Vadez V, Vaz Patto MC (2015) Abiotic stress responses in legumes: strategies used to cope with environmental challenges. Crit Rev Plant Sci 34:237–280

  • Aubert G, Morin J, Jacquin LK, Quillet MC, Petit A, Rameau C, Lejeune-Hénaut I, Huget T, Burstin J (2006) Functional mapping in pea, as an aid to the candidate gene selection and for investigating synteny with the model legume Medicago truncatula. Theor Appl Genet 112:1024–1041

    Article  PubMed  CAS  Google Scholar 

  • Bartels D, Sunkar R (2005) Drought and salt tolerance in plants. Crit Rev Plant Sci 24:23–58

    Article  CAS  Google Scholar 

  • Bechtold U, Lawson T, Mejia-Carranza J, Meyer RC, Brown IR, Altmann T, Ton J, Mullineaux PM (2010) Constitutive salicylic acid defences do not compromise seed yield, drought tolerance and water productivity in the Arabidopsis accession C24. Plant, Cell Environ 33:1959–1973

    Article  CAS  Google Scholar 

  • Bell E, Mullet JE (1991) Lipoxygenase gene expression is modulated in plants by water deficit, wounding, and methyl jasmonate. Mol Gen Genet 230:456–462

    Article  PubMed  CAS  Google Scholar 

  • Bordat A, Savois V, Nicolas M, Salse J, Chauveau A, Bourgeois M, Potier J, Houtin H, Ron 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. Gene, Genomes, Genet 1:93–103

    CAS  Google Scholar 

  • Borsani O, Valpuesta V, Botella MA (2001) Evidence for a role of salicylic acid in the oxidative damage generated by NaCl and osmotic stress in Arabidopsis seedlings. Plant Physiol 126:1024–1030

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Cabrera-Bosquet L, Molero G, Bort J, Nogués S, Araus JL (2007) The combined effect of constant water deficit and nitrogen supply on WUE, NUE and ∆13C in durum wheat potted plants. Ann Appl Biol 151:277–289

    Article  CAS  Google Scholar 

  • Carrillo E, Satovic Z, Aubert G, Boucherot K, Rubiales D, Fondevilla S (2014) Identification of quantitative trait loci and candidate genes for specific cellular resistance responses against Didymella pinodes in pea. Plant Cell Rep 33:1133–1145

    Article  PubMed  CAS  Google Scholar 

  • Cattivelli L, Rizza F, Badeck FW, Mazzucotelli E, Mastrangelo AM, Francia E, Marè C, Tondelli A, Stanca AM (2008) Drought tolerance improvement in crop plants: an integrated view from breeding to genomics. Field Crop Res 105:1–14

    Article  Google Scholar 

  • Churchill GA, Doerge RW (1994) Empirical threshold values for quantitative trait mapping. Genetics 138:963–971

    PubMed  PubMed Central  CAS  Google Scholar 

  • Darvasi A, Soller M (1997) A simple method to calculate resolving power and confidence interval of QTL map location. Behav Genet 27:125–132

    Article  PubMed  CAS  Google Scholar 

  • Doré T, Meynard MJ, Sebillotte M (1998) The role of grain number, nitrogen nutrition and stem number in limiting pea crop (Pisum sativum) yield under agricultural conditions. Eur J Agron 8:29–37

    Article  Google Scholar 

  • Dumont E, Fontaine V, Vuylsteker C, Sellier H, Bodèle S, Voedts N, Devaux R, Frise M, Avia K, Hilber JL (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  PubMed  CAS  Google Scholar 

  • Fondevilla S, Ávila CM, Cubero JI, Rubiales D (2005) Response to Mycosphaerella pinodes in a germplasm collection of Pisum spp. Plant Breed 124:313–315

    Article  Google Scholar 

  • Fondevilla S, Fernández-Aparicio M, Satovic Z, Emeran AA, Torres AM, Moreno MT, Rubiales D (2010) Identification of quantitative trait loci for specific mechanisms of resistance to Orobanche crenata in pea. Mol Breed 25:259–272

    Article  CAS  Google Scholar 

  • Fondevilla S, Almeida NF, Satovic Z, Rubiales D, Vaz Patto MC, Cubero JI, Torres AM (2011) Identification of common genomic regions controlling resistance to Mycosphaerella pinodes, earliness and architectural traits in different pea genetic backgrounds. Euphytica 182:43–52

    Article  Google Scholar 

  • Fondevilla S, Martín-Sanz A, Satovic Z, Fernández-Romero MD, Rubiales D, Caminero C (2012) Identification of quantitative trait loci involved in resistance to Pseudomonas syringae pv. syringae in pea (Pisum sativum L.). Euphytica 186:805–812

    Article  Google Scholar 

  • Forrest J, Miller-Russhing AJ (2010) Toward a synthetic understanding of the role of phenology in ecology and evolution. Phil Trans R Soc B 365:3101–3112

    Article  PubMed  PubMed Central  Google Scholar 

  • Gong DS, Xiong YC, Ma BL, Wang TM, Ge JP, Qin XL, Li PF, Kong HY, Li ZZ, Li FM (2010) Early activation of plasma membrane H+-ATPase and its relation to drought adaptation in two contrasting oat Avena sativa L.) genotypes. Environ Exp Bot 69:1–8

    Article  CAS  Google Scholar 

  • Granier C, Aguirrezabal L, Chenu K, Cookson SJ, Dauzat M, Hamard P, Thioux J-J, Rolland G, Bouchier-Combaud S, Lebaudy A, Muller B, Simonneau T, Tardieu F (2006) PHENOPSIS, an automated platform for reproducible phenotyping of plant responses to soil water deficit in Arabidopsis thaliana permitted the identification of an accession with low sensitivity to soil water deficit. New Phytol 169:623–635

    Article  PubMed  Google Scholar 

  • Grzesiak S, Lijima M, Kono Y, Yamauchi A (1997) Differences in drought tolerance between cultivars of field bean and field pea. A comparison of drought-resistant and drought-sensitive cultivars. Acta Physiol Plant 3:349–357

    Article  Google Scholar 

  • Gutierrez M, Reynolds MP, Klatt AR (2010) Association of water spectral indices with plant and soil water relations in contrasting wheat genotypes. J Exp Bot 61:3291–3303

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hao Z, Liu X, Li X, Xie C, Li M, Zhang D, Zhang S, Xu Y (2009) Identification of quantitative trait loci for drought tolerance at seedling stage by screening a large number of introgression lines in maize. Plant Breed 128:337–341

    Article  Google Scholar 

  • Hunt ER, Rock BN, Nobel PS (1987) Measurement of leaf relative water content by infrared reflectance. Remote Sensi Environ 22:429–435

    Article  Google Scholar 

  • Iglesias-García R, Prats E, Rubiales D (2012) Use of physiological parameters as tools to discriminate water stress tolerance in pea. International Conference on Bioscience: Biotechnology and Biodiversity, Novi Sad, Serbia, June 18-20-2012, P:107

  • SAS Institute Inc (2004) SAS/STAT® 9.1 User’s guide, SAS Institute Inc, Cary, NC

  • Kao CH, Zeng ZB, Teasdale RD (1999) Multiple interval mapping for quantitative trait loci. Genetics 152:1203–1216

    PubMed  PubMed Central  CAS  Google Scholar 

  • Keurentjes JJB, Sulpice R, Gibon Y, Steinhauser M-C, Fu J, Koornneef M, Stitt M, Vreughdenhil D (2008) Integrative analyses of genetic variation in enzyme activities of primary carbohydrate metabolism reveal distinct modes of regulation in Arabidopsis thaliana. Genome Biol 9:R129

    Article  PubMed  PubMed Central  Google Scholar 

  • Kottapalli P, Gaur PM, Katiyar SK, Crouch JH, Buhariwalla HK, Pande S, Gali KK (2009) Mapping and validation of QTLs for resistance to an Indian isolate of Ascochyta blight pathogen in chickpea. Euphytica 165:79–88

    Article  Google Scholar 

  • Kramer PJ (1988) Changing concepts regarding plant water relations. Plant, Cell Environ 11:565–568

    Article  Google Scholar 

  • Lange T, Robatzek S, Frisse A (1999) Cloning and expression of a Gibberellin 2b,3b-Hydroxylase cDNA from pumpkin endosperm. Plant Cell 9:1459–1467

    Google Scholar 

  • Lejeune-Hénaut I, Hanocq E, Béthencourt L, Fontaine V, Delbreil B, Morin J, Petit A, Devaux R, Boilleau M, Stempniak JJ (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  CAS  Google Scholar 

  • Lester DR, Ross JJ, Davies PJ, Reid J (1997) Mendel’s stem length gene (Le) encodes a gibberellin 3P-hydroxylase. Plant Cell 9:1435–1443

    PubMed  PubMed Central  CAS  Google Scholar 

  • Ludlow MM (1989) Strategies in response to water stress. In: Kreeb HK, Richter H, Hinkley TM (eds) Structural and functional response to environmental stresses: Water shortage. SPB Academic Press, The Netherlands, pp 269–281

    Google Scholar 

  • O’Toole JC, Moya TB (1978) Genotypic variation in maintenance of leaf water potential in rice. Crop Sci 18:873–876

    Article  Google Scholar 

  • Quach TN, Tran LSP, Valliyodan B, Nguyen HT, Kumar R, Neelakandan AK, Guttikonda SK, Sharp RE, Nguyen HT (2014) Functional analysis of water stress-responsive soybean GmNAC003 and GmNAC004 transcription factors in lateral root development in Arabidopsis. PLoS One 9:e84886

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Rao MV, Lee H, Creelman RA, Mullet JE, Davis KR (2000) Jasmonic acid signaling modulates ozone-induced hypersensitive cell death. Plant Cell 12:1633–1646

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Rao MV, Lee HI, Davis KR (2002) Ozone-induced ethylene production is dependent on salicylic acid, and both salicylic acid and ethylene act in concert to regulate ozone-induced cell death. Plant J 32:447–456

    Article  PubMed  CAS  Google Scholar 

  • Rubiales D, Fernández-Aparicio M, Moral A, Barilli E, Sillero JC, Fondevilla S (2009a) Disease resistance in pea (Pisum sativum L.) types for autumn sowings in Mediterranean environments. Czech J Genet Plant 45:135–142

    Google Scholar 

  • Rubiales D, Fernández-Aparicio M, Pérez-de-Luque A, Prats E, Castillejo MA, Sillero JC, Rispail N, Fondevilla S (2009b) Breeding approaches for crenate broomrape (Orobanche crenata Forsk.) management in pea (Pisum sativum L.). Pest Manag Sci 65:553–559

    Article  PubMed  CAS  Google Scholar 

  • Sánchez-Martín J, Mur LA, Rubiales D, Prats E (2012) Targeting sources of drought tolerance within an Avena spp. collection through multivariate approaches. Planta 236:1529–1545

    Article  PubMed  CAS  Google Scholar 

  • Shinozaki K, Yamaguchi-Shinozaki K (2007) Gene networks involved in drought stress response and tolerance. J Exp Bot 58:221–227

    Article  PubMed  CAS  Google Scholar 

  • Siddique MRB, Hamid A, Islam MS (2000) Drought stress effects on water relations of wheat. Bot Bull Acad Sin 41:35–39

    Google Scholar 

  • Smýkal P, Aubert G, Burstin J, Coyne CJ, Ellis NTH, Flavell AJ, Ford R, Hýbl M, Macas J, Neumann P, Mcphee KE, Redden RJ, Rubiales D, Weller JL, Warkentin TD (2012) Pea (Pisum sativum L.) in the Genomic Era. Agronomy 2:74–115

    Article  Google Scholar 

  • Tripathy JN, Zhang J, Robin S, Nguyen TT, Nguyen HT (2000) QTL for cell-membrane stability mapped in rice (Oryza sativa L.) under drought stress. Theor Appl Genet 100:1197–1202

    Article  CAS  Google Scholar 

  • Turner NC, Wright GC, Siddique KHH (2001) In: Sparks DL (Ed) Adaptation of grain legumes (pulses) to water limited environments, Vol. 71, pp: 193-231

  • Turner JG, Ellis C, Devoto A (2002) The jasmonate signal pathway. Plant Cell 14:S153–S164

    PubMed  PubMed Central  CAS  Google Scholar 

  • Turyagyenda LF, Kizito EB, Ferguson M, Baguma Y, Agaba M, Harvey JJ, Osiru DS (2013) Physiological and molecular characterization of drought responses and identification of candidate tolerance genes in cassava. AoB plants 5: plt007

  • Upreti KK, Murti GSR, Bhatt RM (2000) Response of pea cultivars to water stress: changes in morphophysiological characters, endogenous hormones and yield. Veg Sci 27:57–61

    Google Scholar 

  • Vettakkorumankankav NN, Falk D, Saxena P, Fletcher RA (1999) A crucial role for Gibberellins in stress protection of plants. Plant Cell Physiol 40:542–548

    Article  Google Scholar 

  • Wang S, Basten CJ, Zeng ZB (2011) Windows QTL Cartographer 2.5, Department of Statistics, North Carolina State University, Raleigh, NC (http://statgen.ncsu.edu/qtlcart/WQTLCart.htm)

  • Xiao B, Huang Y, Tang N, Xiong L (2007) Over-expression of a LEA gene in rice improves drought resistance under the field conditions. Theor App Gen 115:35–46

    Article  CAS  Google Scholar 

  • Xiong L, Schumaker KS, Zhu JK (2002) Cell signaling during cold, drought, and salt stress. Plant Cell 14:S165–S183

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Xoconostle-Cázares B, Ramirez-Ortega FA, Flores-Elenes L, Ruiz-Medrano R (2011) Drought tolerance in crop plants. Am J Plant Physiol 5:241–256

    Article  Google Scholar 

  • Yue B, Xiong L, Xue W, Xing Y, Luo L, Xu C (2005) Genetic analysis for drought resistance of rice at reproductive stage in field with different types of soil. Theor Appl Genet 111:1127–1136

    Article  PubMed  Google Scholar 

  • Zahran HH (1999) Rhizobium-legume symbiosis and nitrogen fixation under severe conditions and in an arid climate. Microbiol Mol Biol Rev 63:968–989

    PubMed  PubMed Central  CAS  Google Scholar 

  • Zeng ZB, Kao CH, Basten CJ (1999) Estimating the genetic architecture of quantitative traits. Genetics 74:279–289

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by EU project FP7-KBBE2013.1.2-02-613551 “LEGATO”.

Conflict of Interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to R. Iglesias-García.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(DOCX 725 kb)

ESM 2

(DOCX 16 kb)

ESM 3

(DOCX 17 kb)

ESM 4

(DOC 63.5 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Iglesias-García, R., Prats, E., Fondevilla, S. et al. Quantitative Trait Loci Associated to Drought Adaptation in Pea (Pisum sativum L.). Plant Mol Biol Rep 33, 1768–1778 (2015). https://doi.org/10.1007/s11105-015-0872-z

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11105-015-0872-z

Keywords

Navigation