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Article << Previous     |     Next >>   Contents Vol 41(9)

Genetic variability and identification of quantitative trait loci affecting plant growth and chlorophyll fluorescence parameters in the model legume Medicago truncatula under control and salt stress conditions

Maryam Foroozanfar A B F , Sarah Exbrayat C , Laurent Gentzbittel A B , Georges Bertoni D , Pierre Maury E , Mohamad Reza Naghavie F , Ali Peyghambari F , Mounavar Badri G , Cécile Ben A B , Frédéric Debelle C and Ahmad Sarrafi A B H

A Institut National Polytechnique (INP), Université Paul Sabatier(UPS), Laboratoire D’Ecologie Fonctionnelle et Environnement, Ecole Nationale Supérieure Agronomique de Toulouse, Université de Toulouse, 18 Chemin de Borde Rouge, BP 32607 Auzeville, 31326 Castanet-Tolosan, France.
B Centre National de la Recherche Scientifique (CNRS), Unité Mixte Recherche 5245, Laboratoire D’Ecologie Fonctionnelle et Environnement (EcoLab), 18 Chemin de Borde Rouge, 31326 Castanet-Tolosan, France.
C Centre National de la Recherche Scientifique (CNRS), Institut National de la Recherche Agronomique, Laboratoire des Interactions Plantes-Microorganismes (UMR441 and UMR 2594), 18 Chemin de Borde Rouge, 31326 Castanet-Tolosan, France.
D Institut National Polytechnique (INP), Ecole Nationale Supérieure Agronomique de Toulouse (ENSAT), Unité Mixte Recherche DYNAFOR (Dynamiques et Écologie des Paysages Agriforestiers), Université de Toulouse, BP 32607, 31326 Castanet-Tolosan, France.
E Institut National Polytechnique (INP), Ecole Nationale Supérieure Agronomique de Toulouse (ENSAT), Institut National de la Recherche Agronomique (INRA), Unité Mixte Recherche AGIR (Agroécologies, Innovations et Ruralités), Université de Toulouse, BP 52627, 31326 Castanet-Tolosan, France.
F Agronomy and Plant Breeding Department, Agricultural & Natural Resources College, University of Tehran, Karaj, 31587-11167, Iran.
G Center of Biotechnology of Borj Cedria, BP 901, Hammam-Lif 2050, Tunisia.
H Corresponding author. Email: sarrafi@ensat.fr

Functional Plant Biology 41(9) 983-1001 http://dx.doi.org/10.1071/FP13370
Submitted: 13 January 2014  Accepted: 14 April 2014   Published: 4 July 2014


 
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Abstract

Salinity is one of the major stresses that limits crop production worldwide and affects most physiological activities in plants. In order to study the genetic control of salt stress in the model legume Medicago truncatula Gaertn., an experiment was undertaken to determine the genetic variability and to identify quantitative trait loci (QTLs) controlling several traits related to plant growth and physiology in a population of recombinant inbred lines. Shoot and root DW, relative water content, leaf area, chlorophyll content, chlorophyll fluorescence parameters, and Na+ and K+ in shoots and roots were measured. The experiment was carried out with three replications. ANOVA showed a large genetic variation and transgressive segregation for the traits studied, suggesting putative complex tolerance mechanisms. A total of 21 QTLs were detected under control conditions and 19 QTLs were identified under 100 mm salt stress conditions, with three QTLs being common to both situations. The percentage of total phenotypic variance explained by the QTLs ranged from 4.6% to 23.01%. Overlapping QTLs for different traits were also observed, which enables us to discriminate independent traits from linked ones. The results should be helpful information for further functional analysis of salt tolerance in M. truncatula.

Additional keywords: K+ content, Na+ content, Photosystem II efficiency, recombinant inbred lines.


References

Apostolova EL, Dobrikova AG, Ivanova PI, Petkanchin IB, Taneva SG (2006) Relationship between the organization of the supercomplex and the functions of the photosynthetic apparatus. Journal of Photochemistry and Photobiology. B, Biology 83, 114–122.
CrossRef | CAS | PubMed |

Arends D, Prins P, Jansen RC, Broman KW (2010) R/qtl: high-throughput multiple QTL mapping. Bioinformatics 26, 2990–2992.
CrossRef | CAS | PubMed |

Ariel F, Diet A, Verdenaud M, Gruber V, Frugier F, Chan R, Crespi M (2010) Environmental regulation of lateral root emergence in Medicago truncatula requires the HD-Zip I transcription factor HB1. The Plant Cell 22, 2171–2183.
CrossRef | CAS | PubMed |

Arraouadi S, Chardon F, Huguet T, Aouani ME, Badri M (2011) QTLs mapping of morphological traits related to salt tolerance in Medicago truncatula. Acta Physiologiae Plantarum 33, 917–926.
CrossRef |

Arraouadi S, Badri M, Abdelly C, Huguet T, Aouani ME (2012) QTL mapping of physiological traits associated with salt tolerance in Medicago truncatula recombinant inbred lines. Genomics 99, 118–125.
CrossRef | CAS | PubMed |

Ashraf M, Foolad MR (2007) Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environmental and Experimental Botany 59, 206–216.
CrossRef | CAS |

Ashraf M, Harris PJC (2013) Photosynthesis under stressful environments: an overview. Photosynthetica 51, 163–190.
CrossRef | CAS |

Avia K, Pilet-Nayel M-L, Bahrman N, Baranger A, Delbreil B, Fontaine V, Hamon C, Hanocq E, Niarquin M, Sellier H, Vuylsteker C, Prosperi J-M, Lejeune-Hénaut I (2013) Genetic variability and QTL mapping of freezing tolerance and related traits in Medicago truncatula. Theoretical and Applied Genetics 126, 2353–2366.
CrossRef | CAS | PubMed |

Badri M, Chardon F, Huguet T, Aouani ME (2011) Quantitative trait loci associated with drought tolerance in the model legume Medicago truncatula. Euphytica 181, 415–428.
CrossRef |

Baker NR (2008) Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annual Review of Plant Biology 59, 89–113.
CrossRef | CAS | PubMed |

Ben C, Toueni M, Montanari S, Tardin MC, Fervel M, Negahi A, Saint-Pierre L, Mathieu G, Gras MC, Noël D, Prospéri JM, Pilet-Nayel ML, Baranger A, Huguet T, Julier B, Rickauer M, Gentzbittel L (2013a) Natural diversity in the model legume Medicago truncatula allows identification of distinct genetic mechanisms conferring partial resistance to Verticillium wilt. Journal of Experimental Botany 64, 317–332.
CrossRef | CAS | PubMed |

Ben C, Debellé F, Berges H, Bellec A, Jardinaud MF, Anson A, Huguet T, Gentzbittel L, Vailleau F (2013b) MtQRRS1, an R-locus required for Medicago truncatula quantitative resistance to Ralstonia solanacearum. New Phytologist 199, 758–772.

Broman KW, Wu H, Sen Ś, Churchill GA (2003) R/qtl: QTL mapping in experimental crosses. Bioinformatics 19, 889–890.
CrossRef | CAS | PubMed |

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

de Givry S, Bouchez M, Chabrier P, Milan D, Schiex T (2005) CarthaGene: multipopulation integrated genetic and radiation hybrid mapping. Bioinformatics 21, 1703–1704.
CrossRef | CAS | PubMed |

de Lorenzo L, Merchan F, Laporte P, Thompson R, Clarke J, Sousa C, Crespi M (2009) A novel plant LRR receptor kinase regulates the response of Medicago truncatula roots to salt stress. The Plant Cell 21, 668–680.
CrossRef | CAS | PubMed |

Dias PM, Brunel-Muguet S, Dürr C, Huguet T, Demilly D, Wagner MH, Teulat-Merah B (2011) QTL analysis of seed germination and pre-emergence growth at extreme temperatures in Medicago truncatula. Theoretical and Applied Genetics 122, 429–444.
CrossRef | PubMed |

Duzan HM, Zhou X, Souleimanov A, Smith DL (2004) Perception of Bradyrhizobium japonicum Nod factor by soybean (Glycine max (L.) Merr.) root hairs under abiotic stress conditions. Journal of Experimental Botany 55, 2641–2646.
CrossRef | CAS | PubMed |

Edmeades GO, Cooper M, Lafitte R, Zinselmeier C, Ribaut JM, Habben JE, Löffler C, Bänziger M (2001) Abiotic stresses and staple crops. In ‘Crop science: progress and prospects. Proceedings of the Third International Crops Science Congress’. August 18–23, 2000, Hamburg, Germany, CABI. pp. 17–21.

Espinoza Ldel C, Huguet T, Julier B (2012) Multi-population QTL detection for aerial morphogenetic traits in the model legume Medicago truncatula. Theoretical and Applied Genetics 124, 739–754.
CrossRef | PubMed |

Flexas J, Bota J, Loreto F, Cornic G, Sharkey TD (2004) Diffusive and metabolic limitations to photosynthesis under drought and salinity in C3 plants. Plant Biology 6, 269–279.

Friesen ML, Cordeiro MA, Penmetsa RV, Badri M, Huguet T, Aouani ME, Cook DR, Nuzhdin SV (2010) Population genomic analysis of Tunisian Medicago truncatula reveals candidates for local adaptation. The Plant Journal 63, 623–635.
CrossRef | CAS | PubMed |

Ganieva RA, Allahverdiyev SR, Guseinova NB, Kavakli HI, Nafisi S (1998) Effect of salt stress and synthetic hormone polystimuline K on the photosynthetic activity of cotton (Gossypium hirsutum). Turkish Journal of Botany 22, 217–221.

Genty B, Briantais JM, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochimica et Biophysica Acta 990, 87–92.
CrossRef | CAS |

Graham PH, Vance CP (2003) Legumes: importance and constraints to greater use. Plant Physiology 131, 872–877.
CrossRef | CAS | PubMed |

Gruber V, Blanchet S, Diet A, Zahaf O, Boualem A, Kakar K, Alunni B, Udvardi M, Frugier F, Crespi M (2009) Identification of transcription factors involved in root apex responses to salt stress in Medicago truncatula. Molecular Genetics and Genomics 281, 55–66.
CrossRef | CAS | PubMed |

Hamon C, Baranger A, Miteul H, Lecointe R, Le Goff I, Deniot G, Onfroy C, Moussart A, Prosperi JM, Tivoli B, Delourme R, Pilet-Nayel ML (2010) A complex genetic network involving a broad-spectrum locus and strain-specific loci controls resistance to different pathotypes of Aphanomyces euteiches in Medicago truncatula. Theoretical and Applied Genetics 120, 955–970.
CrossRef | PubMed |

Jansen RC (1993) Interval mapping of multiple quantitative trait loci. Genetics 135, 205–211.

Jansen RC, Stam P (1994) High resolution of quantitative traits into multiple loci via interval mapping. Genetics 136, 1447–1455.

Jeranyama P, DeMoranville CJ (2009) Gas exchange and chlorophyll content of cranberry under salt stress. Acta Horticulturae 810, 753–758.

Julier B, Huguet T, Chardon F, Ayadi R, Pierre JB, Prosperi JM, Barre P, Huyghe C (2007) Identification of quantitative trait loci influencing aerial morphogenesis in the model legume Medicago truncatula. Theoretical and Applied Genetics 114, 1391–1406.
CrossRef | PubMed |

Kearsey MJ, Pooni HSJ (1996) ‘The genetical analysis of quantitative traits.’ (Stanley Thornes Ltd: Cheltenham, UK)

Koyama ML, Levesley A, Koebner RMD, Flowers TJ, Yeo AR (2001) Quantitative trait loci for component physiological traits determining salt tolerance in rice. Plant Physiology 125, 406–422.
CrossRef | CAS | PubMed |

Krause GH, Weis E (1991) Chlorophyll fluorescence and photosynthesis – the basics. Annual Review of Plant Physiology and Plant Molecular Biology 42, 313–349.
CrossRef | CAS |

Lagunes Espinoza LD, Julier B (2013) QTL detection for forage quality and stem histology in four connected mapping populations of the model legume Medicago truncatula. Theoretical and Applied Genetics 126, 497–509.
CrossRef |

Lazrek F, Roussel V, Ronfort J, Cardinet G, Chardon F, Aouani ME, Huguet T (2009) The use of neutral and non-neutral SSRs to analyse the genetic structure of a Tunisian collection of Medicago truncatula lines and to reveal associations with eco-environmental variables. Genetica 135, 391–402.
CrossRef | CAS | PubMed |

Li D, Kinkema M, Gresshoff PM (2009) Autoregulation of nodulation (AON) in Pisum sativum (pea) involves signalling events associated with both nodule primordia development and nitrogen fixation. Journal of Plant Physiology 166, 955–967.
CrossRef | CAS | PubMed |

Li D, Zhang Y, Hu X, Shen X, Ma L, Su Z, Wang T, Dong J (2011) Transcriptional profiling of Medicago truncatula under salt stress identified a novel CBF transcription factor MtCBF4 that plays an important role in abiotic stress responses. BMC Plant Biology 11, 109
CrossRef | CAS | PubMed |

Long NV, Dolstra O, Malosetti M, Kilian B, Graner A, Richard GF, Visser RGF, van der Linden CG (2013) Association mapping of salt tolerance in barley (Hordeum vulgare L.). Theoretical and Applied Genetics 126, 2335–2351.
CrossRef | CAS | PubMed |

López M, Herrera-Cervera JA, Iribarne C, Tejera NA, Lluch C (2008a) Growth and nitrogen fixation in Lotus japonicus and Medicago truncatula under NaCl stress: nodule carbon metabolism. Journal of Plant Physiology 165, 641–650.
CrossRef | PubMed |

López M, Noel A, Lluch C (2008b) Differential strategies of model legume Lotus japonicus and Medicago truncatula in the adaptation to salt stress: photosynthetic and nutritional response. American Journal of Plant Physiology 3, 121–130.
CrossRef |

Ma HC, Fung L, Wang SS, Altman A, Hüttermann A (1997) Photosynthetic response of Populus euphratica to salt stress. Forest Ecology and Management 93, 55–61.
CrossRef |

Masood MS, Seiji Y, Shinwari ZK, Anwar R (2004) Mapping quantitative trait loci (QTL) for salt tolerance in rice (Oryza sativa) using RFLPs. Pakistan Journal of Botany 36, 825–834.

Maury P, Mojayad F, Berger M, Planchon C (1996) Photochemical response to drought acclimation in two sunflower genotypes. Physiologia Plantarum 98, 57–66.
CrossRef | CAS |

May GD, Dixon RA (2004) Medicago truncatula. Current Biology 14, R180–R181.
CrossRef | CAS | PubMed |

Merchan F, de Lorenzo L, González-Rizzo S, Niebel A, Megías M, Frugier F, Sousa C, Crespi M (2007) Analysis of regulatory pathways involved in the reacquisition of root growth after salt stress in Medicago truncatula. The Plant Journal 51, 1–17.
CrossRef | CAS | PubMed |

Misra AN, Srivastava A, Strasser RJ (2001) Utilization of fast chlorophyll fluorescence technique in assessing the salt/ion sensitivity of mung bean and Brassica seedlings. Journal of Plant Physiology 158, 1173–1181.
CrossRef | CAS |

Moreau D, Burstin J, Aubert G, Huguet T, Ben C, Prosperi JM, Salon C, Munier-Jolain N (2012) Using a physiological framework for improving the detection of quantitative trait loci related to nitrogen nutrition in Medicago truncatula. Theoretical and Applied Genetics 124, 755–768.
CrossRef | CAS | PubMed |

Mun JH, Kim DJ, Choi HK, Gish J, Debellé F, Mudge J, Denny R, Endré G, Saurat O, Dudez AM, Kiss GB, Roe B, Young ND, Cook DR (2006) Distribution of microsatellites in the genome of Medicago truncatula: a resource of genetic markers that integrate genetic and physical maps. Genetics 172, 2541–2555.
CrossRef | CAS | PubMed |

Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annual Review of Plant Biology 59, 651–681.
CrossRef | CAS | PubMed |

Munns R, Schachtman DP, Condon AG (1995) The significance of a two-phase growth response to salinity in wheat and barley. Australian Journal of Plant Physiology 22, 561–569.

Munns R, Wallace PA, Teakle NL, Colmer TD (2010) Measuring soluble ion concentrations (Na+, K+, Cl) in salt treated plants in R. sunkar (ed), plant stress tolerance. Methods in Molecular Biology 639, 371–382.
CrossRef | CAS | PubMed |

Negahi A, Ben C, Gentzbittel L, Maury P, Nabipour AR, Ebrahimi A, Sarrafi A, Rickauer M (2014) Quantitative trait loci associated with resistance to a potato isolate of Verticillium albo-atrum in Medicago truncatula. Plant Pathology 63, 308–315.
CrossRef | CAS |

Netondo GW, Onyango J, Beck E (2004) Sorghum and salinity: II. Gas exchange and chlorophyll fluorescence of sorghum under salt stress. Crop Science 44, 806–811.
CrossRef |

Nyquist WE (1991) Estimates of heritability and prediction of selection response in plant populations. Critical Reviews in Plant Sciences 10, 235–322.
CrossRef |

Osmond CB, Ramus J, Levavasseur G, Franklin LA, Henley WJ (1993) Fluorescence quenching during photoinhibition of Ulva rotundata Blid. Planta 190, 97–106.
CrossRef | CAS |

Palma F, Tejera NA, Lluch C (2013) Nodule carbohydrate metabolism and polyols involvement in the response of Medicago sativa to salt stress. Environmental and Experimental Botany 85, 43–49.
CrossRef | CAS |

Pérez-López U, Robredo A, Lacuesta M, Mena-Petite A, Muñoz-Rueda A (2012) Elevated CO2 reduces stomatal and metabolic limitations on photosynthesis caused by salinity in Hordeum vulgare. Photosynthesis Research 111, 269–283.
CrossRef | PubMed |

Pierre JB, Huguet T, Barre P, Huyghe C, Julier B (2008) Detection of QTL for flowering date in three mapping populations of the model legume species Medicago truncatula. Theoretical and Applied Genetics 117, 609–620.
CrossRef | CAS | PubMed |

Putterill J, Zhang L, Yeoh CC, Balcerowicz M, Jaudal M, Gasic EV (2013) FT genes and regulation of flowering in the legume Medicago truncatula. Functional Plant Biology 40, 1199–1207.
CrossRef |

Qiu N, Lu Q, Lu C (2003) Photosynthesis, photosystem II efficiency and the xanthophylls cycle in the salt adapted halophyte Atriplex centralasiatica. New Phytologist 159, 479–486.
CrossRef | CAS |

Rose RJ (2008) Medicago truncatula as a model for understanding plant interactions with other organisms, plant development and stress biology: past, present and future. Functional Plant Biology 35, 253–264.
CrossRef |

Santos CV, Falcao IP, Pinto GC, Oliveira H, Oureiro JL (2002) Nutrient responses and glutamate and proline metabolism in sunflower plants and calli under Na2SO4 stress. Journal of Plant Nutrition and Soil Science 165, 366–372.
CrossRef | CAS |

Schreiber U, Bilger W, Neubauer C (1995) Chlorophyll fluorescence as a non intrusive indicator for rapid assessment of vivo photosynthesis. In ‘Ecophysiology of photosynthesis’. (Eds ED Schulze, MM Caldwell) pp. 49–70. (Springer: New York)

Smethurst CF, Rix K, Garnett T, Auricht G, Bayart A, Lane P, Wilson SJ, Shabala S (2008) Multiple traits associated with salt tolerance in lucerne: revealing the underlying cellular mechanisms. Functional Plant Biology 35, 640–650.
CrossRef | CAS |

Staudinger C, Mehmeti V, Turetschek R, Lyon D, Egelhofer V, Wienkoop S (2012) Possible role of nutritional priming for early salt and drought stress responses in Medicago truncatula. Frontiers in Plant Science 3, 285
CrossRef | PubMed |

Vadez V, Rodier F, Payre’ H, Drevon JJ (1996) Nodule permeability to O2 and nitrogenase-linked respiration in bean genotypes varying in the tolerance of N2 fixation to P deficiency. Plant Physiology and Biochemistry 34, 871–878.

Vailleau F, Sartorel E, Jardinaud MF, Chardon F, Genin S, Huguet T, Gentzbittel L, Petitprez M (2007) Characterization of the interaction between the bacterial wilt pathogen Ralstonia solanacearum and the model legume plant Medicago truncatula. Molecular Plant—Microbe Interactions 20, 159–167.
CrossRef | CAS | PubMed |

Vandecasteele C, Teulat-Merah B, Morère-Le Paven MC, Leprince O, Ly Vu B, Viau L, Ledroit L, Pelletier S, Payet N, Satour P, Lebras C, Gallardo K, Huguet T, Limami A, Prosperi JM, Buitink J (2011) Quantitative trait loci analysis reveals a correlation between the ratio of sucrose/raffinose family oligosaccharides and seed vigour in Medicago truncatula. Plant, Cell & Environment 34, 1473–1487.
CrossRef | CAS |

Veatch ME, Smith SE, Vandemark G (2004) Shoot biomass production among accessions of Medicago truncatula exposed to NaCl. Crop Science 44, 1008–1013.
CrossRef |

Vinocur B, Altman A (2005) Recent advances in engineering plant tolerance to abiotic stress: achievements and limitations. Current Opinion in Biotechnology 16, 123–132.
CrossRef | CAS | PubMed |

Yadav NS, Shukla PS, Jha A, Agarwal PK, Jha B (2012) The SbSOS1 gene from the extreme halophyte Salicornia brachiata enhances Na+ loading in xylem and confers salt tolerance in transgenic tobacco. BMC Plant Biology 12, 188
CrossRef | CAS | PubMed |

Yamaguchi-Shinozaki K, Shinozaki , K (2006) Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annual Review of Plant Biology 57, 781–803.

Zahaf O, Blanchet S, De Zelicourt A, Alunni B, Plet J, Laffont C, De Lorenzo L, Imbeaud S, Ichante JL, Diet A, Badri M, Zabalza A, Gonzalez EM, Delacroix H, Gruber V, Frugier F, Crespi M (2012) Comparative transcriptomic analysis of salt adaptation in roots of contrasting Medicago truncatula genotypes. Molecular Plant 5, 1068–1081.
CrossRef | CAS | PubMed |


   
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