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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

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Abstract

Freezing is one of the most serious abiotic stress factors that affect cool-season legumes. It limits species geographic distribution and causes severe yield losses. Improving tolerance to freezing has long been a main concern for legume breeders. Medicago truncatula Gaertn. has been selected as a model species for legume biology. Various studies have shown significant macrosynteny between M. truncatula and agronomically important crop legumes. A major freezing tolerance quantitative trait locus (QTL), herein referred to as Mt-FTQTL6, was previously identified on M. truncatula chromosome 6. The physical location of this QTL was determined in this study and its corresponding chromosomal interval was enriched with additional markers. Markers were first developed using the draft sequence of M. truncatula euchromatin (release versions Mt3.0 and Mt3.5). Because Mt-FTQTL6 was found to coincide with an assembly gap, the Glycine max (L.) Merr. genome sequence was also used to generate markers. Five Mt-FTQTL6-linked markers were found to be common to a region on Pisum sativum L. linkage group VI harboring a QTL for freezing damage. A subset of markers was tested for transferability across 11 additional legume species. This study lays the groundwork for identifying the molecular basis of Mt-FTQTL6. Cross-legume markers will be useful in future efforts aiming to investigate the conservation of Mt-FTQTL6 in cool-season legumes and subsequently the existence of common mechanisms for response to freezing between M. truncatula and crop legumes.

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References

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215(3):403–410. doi:10.1016/S0022-2836(05)80360-2

    PubMed  CAS  Google Scholar 

  • Arbaoui M, Link W, Satovic Z, Torres AM (2008) Quantitative trait loci of frost tolerance and physiologically related trait in faba bean (Vicia faba L.). Euphytica 164:93–104. doi:10.1007/s10681-008-9654-0

    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 selection and for investigating synteny with the model legume Medicago truncatula. Theor Appl Genet 112:1024–1041. doi:10.1007/s00122-005-0205-y

    Article  PubMed  CAS  Google Scholar 

  • Bélanger G, Castonguay Y, Bertrand A, Dhont C, Rochette P, Couture L, Drapeau R, Mongrain D, Chalifour FP, Michaud R (2006) Winter damage to perennial forage crops in eastern Canada: causes, mitigation, and prediction. Can J Plant Sci 86:33–47

    Article  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. Genes Genomes Genet 1:93–103. doi:10.1534/g3.111.000349

    CAS  Google Scholar 

  • Brouwer DJ, Duke SH, Osborn TC (2000) Mapping genetic factors associated with winter hardiness, fall growth, and freezing injury in autotetraploid alfalfa. Crop Sci 40:1387–1396

    Article  CAS  Google Scholar 

  • Cannon SB, Sterck L, Rombauts S, Sato S, Cheung F, Gouzy J, Wang X, Mudge J, Vasdewani J, Schiex T, Spannagl M, Monaghan E, Nicholson C, Humphray SJ, Schoof H et al (2006) Legume genome evolution viewed through the Medicago truncatula and Lotus japonicus genomes. Proc Natl Acad Sci USA 103(40):14959–14964. doi:10.1073/pnas.0603228103

    Article  PubMed  CAS  Google Scholar 

  • Casasoli M, Derory J, Morera-Dutrey C, Brendel O, Porth I, Guehl JM, Villani F, Kremer A (2006) Comparison of quantitative trait loci for adaptive traits between oak and chestnut based on an expressed sequence tag consensus map. Genetics 172:533–546. doi:10.1534/genetics.105.048439

    Article  PubMed  CAS  Google Scholar 

  • Castonguay Y, Michaud R, Nadeau P, Bertrand A (2009) An indoor screening method for improvement of freezing tolerance in alfalfa. Crop Sci 49:809–818. doi:10.2135/cropsci2008.09.0539

    Article  Google Scholar 

  • Castonguay Y, Cloutier J, Bertrand A, Michaud R, Laberge S (2010) SRAP polymorphisms associated with superior freezing tolerance in alfalfa (Medicago sativa spp. sativa). Theor Appl Genet 120:1611–1619. doi:10.1007/s00122-010-1280-2

    Article  PubMed  CAS  Google Scholar 

  • Chen H, Wang S, Xing Y, Xu C, Hayes PM, Zhang Q (2003) Comparative analyses of genomic locations and race specificities of loci for quantitative resistance to Pyricularia grisea in rice and barley. Proc Natl Acad Sci USA 100(5):2544–2549. doi:10.1073/pnas.0437898100

    Article  PubMed  CAS  Google Scholar 

  • Chen C, Miller P, Muehlbauer F, Neill K, Wichman D, McPhee K (2006) Winter pea and lentil response to seeding date and micro- and macro-environments. Agron J 98:1655–1663. doi:10.2134/agronj2006.0085

    Article  Google Scholar 

  • Choi HK, Mun JH, Kim DJ, Zhu H, Baek JM, Mudge J, Roe B, Ellis N, Doyle J, Kiss GB, Young ND, Cook DR (2004a) Estimating genome conservation between crop and model legume species. Proc Natl Acad Sci USA 101(43):15289–15294. doi:10.1073/pnas.0402251101

    Article  PubMed  CAS  Google Scholar 

  • Choi HK, Kim D, Uhm T, Limpens E, Lim H, Mun JH, Kalo P, Penmetsa RV, Seres A, Kulikova O, Roe BA, Bisseling T, Kiss GB, Cook DR (2004b) A sequence-based genetic map of Medicago truncatula and comparison of marker colinearity with M. sativa. Genetics 166:1463–1502

    Article  PubMed  CAS  Google Scholar 

  • Cook DR (1999) Medicago truncatula—a model in the making! Curr Opin Plant Biol 2:301–304

    Article  PubMed  CAS  Google Scholar 

  • Corpet F (1988) Multiple sequence alignment with hierarchical clustering. Nucl Acids Res 16(22):10881–10890

    Article  PubMed  CAS  Google Scholar 

  • Cruz-Izquierdo S, Avila CM, Satovic Z, Palomino C, Gutierrez N, Ellwood SR, Phan HTT, Cubero JI, Torres AM (2012) Comparative genomics to bridge Vicia faba with model and closely-related legume species: stability of QTLs for flowering and yield-related traits. Theor Appl Genet 125(8):1767–1782. doi:10.1007/s00122-012-1952-1

    Article  PubMed  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. doi:10.1111/j.1469-8137.2012.04296.x

    Article  PubMed  Google Scholar 

  • Dereeper A, Guignon V, Blanc G, Audic S, Buffet S, Chevenet F, Dufayard JF, Guindon S, Lefort V, Lescot M, Claverie JM, Gascuel O (2008) Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucl Acids Res 36:W465–W469. doi:10.1093/nar/gkn180

    Article  PubMed  CAS  Google Scholar 

  • Distelfeld A, Korol A, Dubcovsky J, Uauy C, Blake T, Fahima T (2008) Colinearity between the barley grain protein content (GPC) QTL on chromosome arm 6HS and the wheat Gpc-B1 region. Mol Breed 22:25–38. doi:10.1007/s11032-007-9153-3

    Article  CAS  Google Scholar 

  • Doyle JJ, Luckow MA (2003) The rest of the iceberg. Legume diversity and evolution in a phylogenetic context. Plant Physiol 131:900–910. doi:10.1104/pp.102.018150

    Article  PubMed  CAS  Google Scholar 

  • Dumont E, Fontaine V, Vuylsteker C, Sellier H, Bodèle S, Voedts N, Devaux R, Frise M, Avia K, Hilbert JL, Bahrman N, Hanocq E, Lejeune-Hénaut 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. doi:10.1007/s00122-009-1004-7

    Article  PubMed  CAS  Google Scholar 

  • Fatokun CA, Menancio-Hautea DI, Danesh D, Young ND (1992) Evidence for orthologous seed weight genes in cowpea and mung bean based on RFLP mapping. Genetics 132:841–846

    PubMed  CAS  Google Scholar 

  • Fırıncıoğlu HK, Erbektaş E, Doğruyol L, Mutlu Z, Ünal S, Karakurt E (2009) Phenotypic variation of autumn and spring-sown vetch (Vicia sativa ssp.) populations in central Turkey. Span. J Agric Res 7(3):596–606

    Google Scholar 

  • Gepts P, Beavis WD, Brummer EC, Shoemaker RC, Stalker HT, Weeden NF, Young ND (2005) Legumes as a model plant family. Genomics for food and feed report of the cross-legume advances through genomics conference. Plant Physiol 137:1228–1235. doi:10.1104/pp.105.060871

    Article  PubMed  CAS  Google Scholar 

  • Gondo T, Sato S, Okumura K, Tabata S, Akashi R, Isobe S (2007) Quantitative trait locus analysis of multiple agronomic traits in the model legume Lotus japonicus. Genome 50:627–637. doi:10.1139/G07-040

    Article  PubMed  Google Scholar 

  • Guy C (1990) Cold acclimation and freezing stress tolerance: role of protein metabolism. Annu Rev Plant Physiol Plant Mol Biol 41:187–223

    Article  CAS  Google Scholar 

  • Joseph B, Schlueter JA, Du J, Graham MA, Ma J, Shoemaker RC (2009) Retrotransposons within syntenic regions between soybean and Medicago truncatula and their contribution to local genome evolution. Plant Gen 2(3):211–223. doi:10.3835/plantgenome2009.01.0001

    Article  CAS  Google Scholar 

  • Julier B, Flajoulot S, Barre P, Cardinet G, Santoni S, Huguet T, Huyghe C (2003) Construction of two genetic linkage maps in cultivated tetraploid alfalfa (Medicago sativa) using microsatellite and AFLP markers. BMC Plant Biol 3:9

    Article  PubMed  Google Scholar 

  • Kahraman A, Kusmenoglu I, Aydin N, Aydogan A, Erskine W, Muehlbauer FJ (2004) QTL mapping of winter hardiness genes in lentil. Crop Sci 44:13–22

    Article  CAS  Google Scholar 

  • Klimenko I, Razgulayeva N, Gau M, Okumura K, Nakaya A, Tabata S, Kozlov NN, Isobe S (2010) Mapping candidate QTLs related to plant persistency in red clover. Theor Appl Genet 120:1253–1263. doi:10.1007/s00122-009-1253-5

    Article  PubMed  Google Scholar 

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

  • Kosambi DD (1944) The estimation of map distances from recombination values. Ann Eugen 12:172–175

    Google Scholar 

  • Kulikova O, Gualtieri G, Geurts R, Kim DJ, Cook D, Huguet T, de Jong JH, Fransz PF, Bisseling T (2001) Integration of the FISH pachytene and genetic maps of Medicago truncatula. Plant J 27:49–58

    Article  PubMed  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 116:1105–1116. doi:10.1007/s00122-008-0739-x

    Article  PubMed  Google Scholar 

  • Loridon K, McPhee K, Morin J, Dubreuil P, Pilet-Nayel ML, Aubert G, Rameau C, Baranger A, Coyne C, Lejeune-Hénaut L, Burstin J (2005) Microsatellite marker polymorphism and mapping in pea (Pisum sativum L.). Theor Appl Genet 111:1022–1031. doi:10.1007/s00122-005-0014-3

    Article  PubMed  CAS  Google Scholar 

  • Maughan PJ, Maroof MAS, Buss GR (1996) Molecular-marker analysis of seed-weight: genomic locations, gene action, and evidence for orthologous evolution among three legume species. Theor Appl Genet 93:574–579

    Article  CAS  Google Scholar 

  • Mudge J, Cannon SB, Kalo P, Oldroyd GE, Roe BA, Town CD, Young ND (2005) Highly syntenic regions in the genomes of soybean, Medicago truncatula, and Arabidopsis thaliana. BMC Plant Biol 5:15. doi:10.1186/1471-2229-5-15

    Article  PubMed  Google Scholar 

  • Rozen S, Skaletsky HJ (2000) Primer3 on the WWW for general users and for biologist programmers. In: Krawetz S, Misener S (eds) Bioinformatics methods and protocols: methods in molecular biology. Humana Press, Totowa, pp 365–386

    Google Scholar 

  • Sadeghipour O, Aghaei P (2012) Comparison of autumn and spring sowing on performance of chickpea (Cicer arietinum L.) varieties. Int J Biosci 2(6):49–58

    Google Scholar 

  • Sato S, Nakamura Y, Kaneko T, Asamizu E, Kato T, Nakao M, Sasamoto S, Watanabe A, Ono A, Kawashima K, Fujishiro T, Katoh M, Kohara M, Kishida Y, Minami C et al (2008) Genome structure of the legume, Lotus japonicus. DNA Res 15:227–239. doi:10.1093/dnares/dsn008

    Article  PubMed  CAS  Google Scholar 

  • Schlueter JA, Scheffler BE, Jackson S, Shoemaker RC (2008) Fractionation of synteny in a genomic region containing tandemly duplicated genes across Glycine max, Medicago truncatula, and Arabidopsis thaliana. J Hered 99(4):390–395. doi:10.1093/jhered/esn010

    Article  PubMed  CAS  Google Scholar 

  • Schmutz J, Cannon SB, Schlueter J, Ma J, Mitros T, Nelson W, Hyten DL, Song Q, Thelen JJ, Cheng J, Xu D, Hellsten U, May GD, Yu Y, Sakurai T et al (2010) Genome sequence of the palaeopolyploid soybean. Nature 463:178–183. doi:10.1038/nature08670

    Article  PubMed  CAS  Google Scholar 

  • Shin JH, Van K, Kim DH, Kim KD, Jang YE, Choi BS, Kim MY, Lee SH (2008) The lipoxygenase gene family: a genomic fossil of shared polyploidy between Glycine max and Medicago truncatula. BMC Plant Biol 8:133. doi:10.1186/1471-2229-8-133

    Article  PubMed  Google Scholar 

  • Timko MP, Rushton PJ, Laudeman TW, Bokowiec MT, Chipumuro E, Cheung F, Town CD, Chen X (2008) Sequencing and analysis of the gene-rich space of cowpea. BMC Genomics 9:103. doi:10.1186/1471-2164-9-103

    Article  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Van Ooijen JW (2006) Joinmap® 4, software for the calculation of genetic linkage maps in experimental populations. Kyazma B.V, Wageningen

    Google Scholar 

  • Van Ooijen JW (2009) MapQTL® 6, software for the mapping of quantitative trait loci in experimental populations of diploid species. Kyazma B.V, Wageningen

    Google Scholar 

  • Varshney RK, Chen W, Li Y, Bharti AK, Saxena RK, Schlueter JA, Donoghue MTA, Azam S, Fan G, Whaley AM, Farmer AD, Sheridan J, Iwata A, Tuteja R, Penmetsa RV et al (2012) Draft genome sequence of pigeonpea (Cajanus cajan), an orphan legume crop of resource-poor farmers. Nat Biotechnol 30(1):83–89. doi:10.1038/nbt.2022

    Article  CAS  Google Scholar 

  • Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93(1):77–78

    Article  PubMed  CAS  Google Scholar 

  • Young ND, Debellé F, Oldroyd GED, Geurts R, Cannon SB, Udvardi MK, Benedito VA, Mayer KFX, Gouzy J, Schoof H, Van De Peer Y, Proost S, Cook DR, Meyers BC, Spannagl M et al (2011) The Medicago genome provides insight into the evolution of rhizobial symbioses. Nature 480:520–524. doi:10.1038/nature10625

    Article  PubMed  CAS  Google Scholar 

  • Zhu H, Cannon SB, Young ND, Cook DR (2002) Phylogeny and genomic organization of the TIR and Non-TIR NBS-LRR resistance gene family in Medicago truncatula. Mol Plant Microbe Interact 15(6):529–539

    Article  PubMed  CAS  Google Scholar 

  • Zorrilla-Fontanesi Y, Cabeza A, Domínguez P, Medina JJ, Valpuesta V, Denoyes-Rothan B, Sánchez-Sevilla JF, Amaya I (2011) Quantitative trait loci and underlying candidate genes controlling agronomical and fruit quality traits in octoploid strawberry (Fragaria x ananassa). Theor Appl Genet 123:755–778. doi:10.1007/s00122-011-1624-6

    Article  PubMed  Google Scholar 

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Acknowledgments

The authors wish to thank Drs. Marie-Christine Quillet and Marie-Laure Pilet-Nayel for helpful discussions concerning this work, Grégoire Aubert for providing P. sativum RNA-seq data, Cécile Godé for assistance in PCR product sequencing and Frédéric Depta for plant care in the greenhouse. They acknowledge Eric Hanocq for providing the initial plant material for the construction of the large P. sativum segregating population. They would also like to thank Pascal Marget and Jean-Bernard Magnin-Robert of GRC of grain legumes, INRA, Dijon, France; Stéphane Fourtier of GRC of forage and turf species, INRA, Lusignan, France; Frederic Ottosson of NordGen, Sweden and Dave Stout of WRPIS, Pullman, Washington, USA for supplying legume seeds. They also thank the GENTYANE platform (INRA UBP, UMR 1095, Clermont-Ferrand) for genotyping. This work was partly financially supported by the Région Nord Pas-de-Calais, France (FEDER ARCIR PLANTEQ3 program). N. Tayeh was the recipient of a Ph.D. fellowship from the Ministère de l’Enseignement supérieur et de la Recherche, France.

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  1. Université Lille 1, UMR 1281 SADV, Bâtiment SN2, 59655, Villeneuve d’Ascq Cedex, France

    Nadim Tayeh, Nasser Bahrman, Aurélie Bluteau & Bruno Delbreil

  2. INRA, UMR 1281 SADV, Estrées-Mons BP50136, 80203, Péronne Cedex, France

    Nasser Bahrman, Rosemonde Devaux, Aurélie Bluteau & Isabelle Lejeune-Hénaut

  3. INRA, UMR AGAP, 2 Place Pierre Viala, 34060, Montpellier Cedex, France

    Jean-Marie Prosperi

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  1. Nadim Tayeh
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  2. Nasser Bahrman
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Correspondence to Bruno Delbreil.

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Tayeh, N., Bahrman, N., Devaux, R. et al. 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 Breeding 32, 279–289 (2013). https://doi.org/10.1007/s11032-013-9869-1

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