Skip to main content

Advertisement

Log in

Genetic dissection of nitrogen nutrition in pea through a QTL approach of root, nodule, and shoot variability

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

Abstract

Pea (Pisum sativum L.) is the third most important grain legume worldwide, and the increasing demand for protein-rich raw material has led to a great interest in this crop as a protein source. Seed yield and protein content in crops are strongly determined by nitrogen (N) nutrition, which in legumes relies on two complementary pathways: absorption by roots of soil mineral nitrogen, and fixation in nodules of atmospheric dinitrogen through the plant–Rhizobium symbiosis. This study assessed the potential of naturally occurring genetic variability of nodulated root structure and functioning traits to improve N nutrition in pea. Glasshouse and field experiments were performed on seven pea genotypes and on the ‘Cameor’ × ‘Ballet’ population of recombinant inbred lines selected on the basis of parental contrast for root and nodule traits. Significant variation was observed for most traits, which were obtained from non-destructive kinetic measurements of nodulated root and shoot in pouches, root and shoot image analysis, 15N quantification, or seed yield and protein content determination. A significant positive relationship was found between nodule establishment and root system growth, both among the seven genotypes and the RIL population. Moreover, several quantitative trait loci for root or nodule traits and seed N accumulation were mapped in similar locations, highlighting the possibility of breeding new pea cultivars with increased root system size, sustained nodule number, and improved N nutrition. The impact on both root or nodule traits and N nutrition of the genomic regions of the major developmental genes Le and Af was also underlined.

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
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Ali-Khan ST, Snoad B (1977) Root and shoot development in peas. I. Variability in seven root and shoot characters of seedlings. Ann Appl Biol 85:131–136

    Article  Google Scholar 

  • Ané JM, Kiss GB, Riely BK, Penmetsa RV, Olroyd G, Ayax C, Levy J, Debelle F, Baek JM, Kalo P, Rosenberg C, Roe BA, Long SR, Denarié J, Cook D (2004) Medicago truncatula DMI1 required for bacterial and fungal symbiosis in legumes. Science 393:1364–1366

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Baranger A, Aubert G, Arnau G, Lainé A-L, Deniot G, Potier J, Weinachter C, Lejeune-Hénaut I, Lallemand J, Burstin J (2004) Genetic diversity within Pisum sativum using protein- and PCR-based markers. Theor Appl Genet 108:1309–1321

    Article  CAS  PubMed  Google Scholar 

  • Barbulova A, Rogato A, D’Apuzzo E, Omrane S, Chiurazzi M (2007) Differential effects of combined N sources on early steps of the nod factor–dependent transduction pathway in Lotus japonicus. Mol Plant Microbe Interact 20:994–1003

    Article  CAS  PubMed  Google Scholar 

  • Bourion V, Laguerre G, Depret G, Voisin A-S, Salon C, Duc G (2007) Genetic variability in nodulation and root growth affects nitrogen fixation and accumulation in pea. Ann Bot 100:589–598

    Article  CAS  PubMed  Google Scholar 

  • Bright LJ, Liang Y, Mitchell DM, Harris JM (2005) The LATD gene of Medicago truncatula is required for both nodule and root development. Mol Plant Microbe Interact 18:521–532

    Article  CAS  PubMed  Google Scholar 

  • Burstin J, Marget P, Huart M, Moessner A, Mangin B, Duchene C, Desprez B, Munier-Jolain N, Duc G (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  Google Scholar 

  • Caroll BJ, Mathews A (1990) Nitrate inhibition of nodulation in legumes. In: Gresshoff PM (ed) Molecular biology of symbiotic nitrogen fixation. CRC Press, Boca Raton, pp 159–180

    Google Scholar 

  • Catoira R, Galera C, de Billy F, Penmetsa RV, Journet EP, Maillet F, Rosenberg C, Cook D, Gough C, Denarié J (2000) Four genes of Medicago truncatula controlling components of a Nod factor transdution pathway. Plant cell 12:1647–1665

    Article  CAS  PubMed  Google Scholar 

  • Charcosset A, Gallais A (1996) Estimation of the contribution of quantitative trait loci (QTL) to the variance of a quantitative trait by means of genetic markers. Theor Appl Gen 93:1193–1201

    Article  Google Scholar 

  • Coque M, Gallais A (2006) Genomics region involved in response to grain yield selection at high and low nitrogen fertilization in maize. Theor Appl Genet 112:1205–1220

    Article  CAS  PubMed  Google Scholar 

  • de Billy F, Grosjean C, May S, Bennett M, Cullimore JV (2001) Expression studies on AUX1-like genes in Medicago truncatula suggest that auxin is required at two steps in early nodule development. Mol Plant Microbe Interact 14:267–277

    Article  PubMed  Google Scholar 

  • Dénarié J, Cullimore J (1993) Lipo-oligosaccharide nodulation factors: a new class of signaling molecules mediating recognition and morphogenesis. Cell 74:951–954

    Article  PubMed  Google Scholar 

  • Duc G, Mariotti A, Amarger N (1988) Measurements of genetic variability for symbiotic dinitrogen fixation in field-grown faba bean (Vicia faba L.) using a low level 15 N-tracer technique. Plant Soil 106:269–276

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Edwards A, Heckmann AB, Yousafzai F, Duc G, Downie A (2007) Structural implications of mutations in the pea SYM8 symbiosis gene, the DMI1 ortholog, encoding a predicted ion channel. Mol Plant Microbe Interact 20:1183–1191

    Article  CAS  PubMed  Google Scholar 

  • Endre G, Kereszt A, Kevei Z, Mihacea S, Kalo P, Kiss GB (2002) A receptor kinase gene regulating symbiotic nodule development. Nature 417:962–966

    Article  CAS  PubMed  Google Scholar 

  • FAOSTAT (2007) Food and Agriculture Organisation website. http://faostat.fao.org

  • Frugier F, Kosuta S, Murray JD, Crespi M, Szczyglowski K (2008) Cytokinin: secret agent of symbiosis. Trends Plant Sci 13:115–120

    Article  CAS  PubMed  Google Scholar 

  • Gonzalez-Rizzo S, Crespi M, Frugier F (2006) The Medicago truncatula CRE1 cytokinin receptor regulates lateral root development and early symbiotic interaction with Sinorhizobium meliloti. Plant Cell 18:2680–2693

    Article  CAS  PubMed  Google Scholar 

  • Jeuffroy MH, Warembourg FR (1991) Carbon transfer and partitioning between vegetative and reproductive organs in Pisum sativum L. Plant Physiol 97:440–448

    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 

  • Kiniry JR, Jones CA, O’Toole JC, Blanchet R, Cabelguenne Spanel DA (1989) Radiation-use efficiency in biomass accumulation prior to grain-filling for five grain-crop species. Field Crops Res 20:51–64

    Article  Google Scholar 

  • Kof EM, Vinogradova IA, Oorzhak AS, Kalibernaya ZV (2006) The rates of shoot and root growth in intact plants of pea mutants in leaf morphology. Russ J Plant Physiol 53:116–125

    Article  CAS  Google Scholar 

  • Kraft JM, Boge W (2001) Root characteristics in pea in relation to compaction and fusarium root rot. Plant Dis 85:939–940

    Article  Google Scholar 

  • Krusell L, Madsen LH, Sato S, Aubert G, Genua A, Szczyglowski K, Duc G, Kaneto T, Tabata S, de Bruijn F, Pajuelo E, Sandal N, Stougaard J (2002) Shoot control of root development and nodulation is mediated by a receptor-like kinase. Nature 420:422–425

    Article  CAS  PubMed  Google Scholar 

  • Kuang RB, Liao H, Yan XL, Dong YS (2005) Phosphorus and Nitrogen Interactions in Field-Grown Soybean as Related to Genetic Attributes of Root Morphological and Nodular Traits. J Integr Plant Biol 47:549–559

    Article  CAS  Google Scholar 

  • Laguerre G, Depret G, Bourion V, Duc G (2007) Rhizobium leguminosarum bv. viciae genotypes interact with pea plants in developmental responses of nodules, roots and shoots. New Phytol 176:680–690

    Article  PubMed  Google Scholar 

  • Laperche A, Devienne-Barret F, Maury O, Le Gouis J, Ney B (2006) A simplified conceptual model of carbon/nitrogen functioning for QTL analysis of winter wheat adaptation to nitrogen deficiency. Theor Appl Genet 113:1131–1146

    Article  CAS  PubMed  Google Scholar 

  • Larigauderie A, Reynolds JF, Strain BR (1994) Root response to CO2 enrichment and nitrogen supply in loblolly pine. Plant Soil 165:21–32

    Article  CAS  Google Scholar 

  • Lejeune-Hénaut I, Hanocq E, Béthencourt L, Fontaine V, Delbreil B, Morin J, Petit A, Devaux R, Boilleau M, Stempniak JJ, Thomas M, Lainé 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(8):1105–1116

    Article  PubMed  CAS  Google Scholar 

  • Lévy J, Bres J, Geurts R, Chalhoub B, Kulikova O, Duc G, Journet EP, Ané JM, Lauber E, Bisseling T, Dénarié J, Rosenberg C, Debellé F (2004) A putative Ca2+ and calmodulin-dependent protein kinase required for bacterial and fungal Symbioses. Science 303:1361–1364

    Article  PubMed  CAS  Google Scholar 

  • Liang Y, Mitchell DM, Harris JM (2007) Abscisic acid rescues the root meristem defects of the Medicago truncatula latd mutant. Dev Biol 304:297–307

    Article  CAS  PubMed  Google Scholar 

  • Lira Junior MA, Lima AST, Arruda JRF, Smith DL (2005) Effect of root temperature on nodule development of bean, lentil and pea. Soil Biol Biochem 37:235–239

    Article  CAS  Google Scholar 

  • Loridon K, McPhee K, Morin J, Dubreuil P, Pilet-Nayel ML, Aubert G, Rameau C, Baranger A, Coyne C, Lejeune-Hénaut 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 

  • Magori S, Kawaguchi M (2009) Long-distance control of nodulation: molecules and models. Mol Cells 27:129–134

    Article  CAS  PubMed  Google Scholar 

  • Mathesius U (2008) Auxin: at the root of nodule development? Funct Plant Biol 35:651–668

    Article  CAS  Google Scholar 

  • McPhee K (2005) Variation for seedling root architecture in the core collection of pea germplasm. Crop Sci 45:1758–1763

    Article  Google Scholar 

  • Melchinger AE, Chandra S, Utz HF (2000) New ways in quantitative genetics: results of QTL analyses revisited by cross validation and bootstrapping. In: INRA (ed) Paris (France) August 30/31–September 1, 2000, Paris, 2001 (Les Colloques, n 96)

  • Moreau D (2007) Réponse du développement et de la croissance de Medicago truncatula aux facteurs environnementaux : contribution à l’élaboration d’outils de phénotypage pour l’analyse de la variabilité génétique associée à la nutrition azotée. Thèse de doctorat, Université de Bourgogne, Dijon (France), 148 pp

  • Moreau D, Schneider C, Huguet T, Salon C, Munier-Jolain N (2009) Can differences of nitrogen nutrition level among Medicago truncatula genotypes be assessed non-destructively? Probing with a recombinant inbred lines population. Plant Signal Behav 4:30–32

    CAS  PubMed  Google Scholar 

  • Ney B, Turc O (1993) Heat-unit based description of the reproductive development of pea. Crop Sci 33:510–514

    Article  Google Scholar 

  • Nicolas MF, Hungria M, Arias AA (2006) Identification of quantitative trait loci controlling nodulation and shoot mass in progenies from two Brazilian soybean cultivars. Field Crops Res 95:355–356

    Article  Google Scholar 

  • Nodari RO, Tsai SM, Guzman P, Gilbertson RL, Gepts P (1993) Toward an integrated linkage map of common bean. III. Mapping genetic factors controlling host bacteria interactions. Genetics 134:341–350

    CAS  PubMed  Google Scholar 

  • Novak K, Chovanec P, Skrdleta V, Kropacova M, Lisa L, Nemcova M (2002) Effect of exogenous flavonoids on nodulation of pea (Pisum sativum L.). J Exp Bot 53:1735–1745

    Article  CAS  PubMed  Google Scholar 

  • Novak K, Biedermannova E, Vondrys J (2009) Symbiotic and growth performance of supernodulating forage pea line. Crop Sci 49:1227–1234

    Article  Google Scholar 

  • Oka-Kira E, Kawaguchi M (2006) Long-distance signaling to control root nodule number. Curr Opin Plant Biol 9:496–502

    Article  CAS  PubMed  Google Scholar 

  • Okamoto S, Ohnishi E, Sato S, Takahashi H, Nakazono M, Tabata S, Kawaguchi M (2009) Nod factor/nitrate-induced CLE genes that drive HAR1-mediated systemic regulation of nodulation. Plant Cell Physiol 50:67–77

    Article  CAS  PubMed  Google Scholar 

  • Pilet-Nayel ML, Muehlbauer FJ, McGee RJ, Kraft JM, Baranger A, Coyne CJ (2002) Quantitative trait loci for partial resistance to Aphanomyces root rot in pea. Theor Appl Genet 106:28–39

    CAS  PubMed  Google Scholar 

  • Postma JG, Jacobsen E, Feenstra WJ (1988) Three pea mutants with an altered nodulation studied by genetic analysis and grafting. J Plant Physiol 132:424–430

    Google Scholar 

  • Sagan M, Duc G (1996) Sym28 and Sym29. two new genes involved in regulation of nodulation in pea (Pisum sativum L.). Symbiosis 20:229–245

    Google Scholar 

  • Sagan M, Ney B, Duc G (1993) Plant symbiotic mutants as a tool to analyse nitrogen and yield relationship in field-grown peas (Pisum sativum L.). Plant Soil 153:33–45

    Article  CAS  Google Scholar 

  • Salon C, Munier-Jolain NG, Duc G, Voisin A-S, Grandgirard D, Larmure A, Emery JN, Ney B (2001) Grain legume seed filling in relation to nitrogen acquisition: a review and prospects with particular reference to pea. Agronomie 21:539–552

    Article  Google Scholar 

  • Santalla M, Amurrio JM, Ron AM (2001) Symbiotic interactions between Rhizobium leguminosarum strains and elite cultivars of Pisum sativum L. J Agron Crop Sci 187:59–68

    Article  Google Scholar 

  • Schnabel E, Journet EP, de Carvalho-Niebel F, Duc G, Frugoli J (2005) The Medicago truncatula SUNN gene encodes a CLV1-like leucine-rich repeat receptor kinase that regulates nodule number and root length. Plant Mol Biol 58:809–822

    Article  PubMed  CAS  Google Scholar 

  • Sinclair TR, Horie T (1989) Leaf nitrogen, photosynthesis, and crop radiation use efficiency: a review. Crop Sci 29:90–98

    Article  Google Scholar 

  • Smith GB, Wollum AG (1989) Nodulation of Glycine max by six Bradyrhizobium japonicum strains with different competitive abilities. Appl Environ Microbiol 55:1957–1962

    PubMed  Google Scholar 

  • Souza AA, Boscariol RL, Moon DH, Camargo LEA, Tsai SM (2000) Effects of Phaseolus vulgaris QTL in controlling host-bacteria interaction under two levels of nitrogen fertilization. Genet Mol Biol 23:155–161

    CAS  Google Scholar 

  • Tar’an B, Warkentin T, Somers DJ, Miranda D, Vandenberg A, Blade S, Woods 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 

  • Thorup-Kristensen K (1998) Root growth of green pea (Pisum sativum L.) genotypes. Crop Sci 38:1445–1451

    Article  Google Scholar 

  • Timmerman-Vaughan GM, McCallum JA, Frew TJ, Butler R, Weeden NF, Russell AC (1996) Linkage mapping of quantitative loci controlling seed weight in pea (Pisum sativum L.). Theor Appl Genet 93:431–439

    Article  CAS  Google Scholar 

  • Timmerman-Vaughan GM, Mills A, Whitfield C, Frew TJ, Butler R, Murray S, Lakeman M, McCallum JA, Russell AC, 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 

  • Tricot F, Crozat Y, Pellerin S (1997) Root system growth and nodule establishment on pea (Pisum sativum L.). J Exp Bot 48:1935–1941

    CAS  Google Scholar 

  • Tuberosa R, Sanguinetti MC, Landi P, Giuliani MM, Salvi S, Conti S (2002) Identification of QTLs for root characteristics in maize grown in hydroponics and analysis of their overlap with QTLs for grain yield in the field at two water regimes. Plant Mol Biol 48:697–712

    Article  CAS  PubMed  Google Scholar 

  • Voisin A-S, Salon C, Munier-Jolain NG, Ney B (2002) Effect of mineral nitrogen on nitrogen nutrition and biomass partitioning between the shoot and roots of pea (Pisum sativum L.). Plant Soil 242:251–262

    Article  CAS  Google Scholar 

  • Voisin A-S, Salon C, Jeudy C, Warembourg FR (2003a) Symbiotic N2 fixation activity in relation to C economy of Pisum sativum L. as a function of plant phenology. J Exp Bot 54:2733–2744

    Article  CAS  PubMed  Google Scholar 

  • Voisin A-S, Salon C, Jeudy C, Warembourg FR (2003b) Root and nodule growth in Pisum sativum L. in relation with photosynthesis: analysis using 13C-labelling. Ann Bot 92:557–563

    Article  CAS  PubMed  Google Scholar 

  • Voisin A-S, Bourion V, Duc G, Salon C (2007) Using an ecophysiological analysis to dissect genetic variability and to propose an ideotype for nitrogen nutrition in pea. Ann Bot 100:1525–1536

    Article  CAS  PubMed  Google Scholar 

  • Weeden NF, Moffet M (2002) Identification of genes affecting root mass and root/shoot ratio in a JI1794 x “Slow” RILL population. Pisum Genet 34:28–31

    Google Scholar 

  • Weeden NF, Tonguc M, Boone WE (1999) Mapping coding sequences in pea by PCR. Pisum Genet 31:30–32

    Google Scholar 

  • Wopereis J, Pajuelo E, Dazzo FB, Jiang Q, Gresshoff PM, de Bruijn FJ, Stougaard J, Szczyglowski K (2000) Short root mutant of Lotus japonicus with a dramatically altered symbiotic phenotype. Plant J 23:97–114

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank, for their help in the experimental work, Hervé Houtin, Céline Rond, Nicolas Jeannin, Abdelkrim Souiah and Chantal Martin of the UMR102, and Nouredine El Mjiyad of the Experimental Unit (UE115, Dijon). We also thank Laurence Moreau (INRA, UMR320, Gif-sur-Yvette) for useful help in statistical analysis and Olivier Delfosse (INRA, UMR614, Reims) for 15N analyses. Gisèle Laguerre (INRA, UMR113, Montpellier) and Céline Faivre (INRA, UMR1229, Dijon) are acknowledged for their guidance in the use of growth pouches. This work was supported by the French programme Genoplante (GOP PeaC and GOP PeaC2), and by the European Union (Grain Legumes Integrated Project, a Framework Programme 6 project, grant no. FOOD-CT-2004-506223). We are grateful to the anonymous referees for their constructive remarks.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Virginie Bourion.

Additional information

Communicated by H. T. Nguyen.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplemental Figures (PDF 33 kb)

Supplemental Tables (PDF 60 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bourion, V., Rizvi, S.M.H., Fournier, S. et al. Genetic dissection of nitrogen nutrition in pea through a QTL approach of root, nodule, and shoot variability. Theor Appl Genet 121, 71–86 (2010). https://doi.org/10.1007/s00122-010-1292-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00122-010-1292-y

Keywords

Navigation