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Genomic regions associated with the nitrogen limitation response revealed in a global wheat core collection

Theoretical and Applied Genetics volume 126, pages 805–822 (2013)Cite this article

Abstract

Modern wheat (Triticum aestivum L.) varieties in Western Europe have mainly been bred, and selected in conditions where high levels of nitrogen-rich fertilizer are applied. However, high input crop management has greatly increased the risk of nitrates leaching into groundwater with negative impacts on the environment. To investigate wheat nitrogen tolerance characteristics that could be adapted to low input crop management, we supplied 196 accessions of a wheat core collection of old and modern cultivars with high or moderate amounts of nitrogen fertilizer in an experimental network consisting of three sites and 2 years. The main breeding traits were assessed including grain yield and grain protein content. The response to nitrogen level was estimated for grain yield and grain number per m2 using both the difference and the ratio between performance at the two input levels and the slope of joint regression. A large variability was observed for all the traits studied and the response to nitrogen level. Whole genome association mapping was carried out using 899 molecular markers taking into account the five ancestral group structure of the collection. We identified 54 main regions involving almost all chromosomes that influence yield and its components, plant height, heading date and grain protein concentration. Twenty-three regions, including several genes, spread over 16 chromosomes were involved in the response to nitrogen level. These chromosomal regions may be good candidates to be used in breeding programs to improve the performance of wheat varieties at moderate nitrogen input levels.

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References

  • Agarwal PK, Agarwal P, Reddy MK, Sopory SK (2006) Role of DREB transcription factors in abiotic and biotic stress tolerance in plants. Plant Cell Rep 25:1263–1274

    PubMed  Article  CAS  Google Scholar 

  • An DG, Su JY, Liu QY, Zhu YG, Tong YP, Li JM, Jing RL, Li B, Li ZS (2006) Mapping QTLs for nitrogen uptake in relation to the early growth of wheat (Triticum aestivum L.). Plant Soil 284:73–84

    Article  CAS  Google Scholar 

  • Austin RB, Ford MA, Edrich JA, Blackwell RD (1977) The nitrogen economy of winter wheat. J Agric Sci 88:159–167

    Article  Google Scholar 

  • Balfourier F, Roussel V, Strelchenko P, Exbrayat-Vinson F, Sourdille P, Boutet G, Koenig J, Ravel C, Mitrofanova O, Beckert M, Charmet G (2007) A worldwide bread wheat core collection arrayed in a 384-well plate. Theor Appl Genet 114:1265–1275

    PubMed  Article  Google Scholar 

  • Barraclough PB, Howarth JR, Jones J, Lopez-Bellido R, Parmar S, Caroline E, Shepherd CE, Hawkesford MJ (2010) Nitrogen efficiency of wheat: genotypic and environmental variation and prospects for improvement. Eur J Agron 33:1–11

    Article  CAS  Google Scholar 

  • Blanco A, Simeone R, Gadaleta A (2006) Detection of QTLs for grain protein content in durum wheat. Theor Appl Genet 113:563–565

    Article  CAS  Google Scholar 

  • Bonnin I, Rousset M, Madur D, Sourdille P, Dupuits C, Brunel D, Goldringer I (2008) FT genome A and D polymorphisms are associated with the variation of earliness components in hexaploid wheat. Theor Appl Genet 116:383–394

    PubMed  Article  CAS  Google Scholar 

  • Bordes J, Branlard G, Oury FX, Charmet G, Balfourier F (2008) Agronomic characteristics, grain quality and flour rheology of 372 bread wheats in a worldwide core collection. J Cereal Sci 48:569–579

    Article  CAS  Google Scholar 

  • Bordes J, Ravel C, Le Gouis J, Charmet G, Balfourier F (2011) Use of global wheat core collection for association analysis of flour and dough quality traits. J Cereal Sci 54:137–147

    Article  Google Scholar 

  • Börner A, Schumann E, Fürste A, Cöster H, Leithold B, Röder MS, Weber WE (2002) Mapping of quantitative trait loci determining agronomic important characters in hexaploid wheat (Triticum aestivum L.). Theor Appl Genet 105:921–936

    PubMed  Article  Google Scholar 

  • Bradbury PJ, Zhang ZC, Kroon D, Casstevens TM, Ramdoss Y, Buckler ES (2007) TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics 23:2633–2635

    PubMed  Article  CAS  Google Scholar 

  • Brancourt-Hulmel M, Lecomte C-M, Bérard P, Galic N, Trouvé B, Sausseau C (1994) Sélection et stabilité du rendement chez le blé tendre d’hiver. Agronomie 14:611–625

    Article  Google Scholar 

  • Branlard G, Dardevet M, Amiour N, Igrejas G (2003) Allelic diversity of HMW and LMW glutenin subunits and omega gliadins in French bread wheat (Triticum aestivum L.). Genet Resour Crop Evol 50:669–679

    Article  CAS  Google Scholar 

  • Breseghello F, Sorrells ME (2006) Association mapping of kernel size and milling quality in wheat (Triticum aestivum L.) cultivars. Genetics 172:1165–1177

    PubMed  Article  Google Scholar 

  • Castleden CK, Aoki N, Gillespie VJ, MacRae EA, Quick WP, Buchner P, Foyer CH, Furbank RT, Lunn JE (2004) Evolution and function of the sucrose-phosphate synthase gene families in wheat and other grasses. Plant Physiol 135:1753–1764

    PubMed  Article  CAS  Google Scholar 

  • Charmet G, Robert N, Branlard G, Linossier P, Martre P, Triboi (2005) Genetic analysis of dry matter and nitrogen accumulation and protein composition in wheat kernels. Theor Appl Genet 111:540–550

  • Crossa J, Burgueno J, Dreisickacker S, Vargas M, Herrera-Foessel SA, Lillemo M, Singh RP, Trethowan R, Warburton M, Franco J, Reynolds M, Crouch JH, Ortiz R (2007) Association analysis of historical bread wheat germplasm using additive genetic covariance of relatives and population structure. Genetics 177:1889–1913

    PubMed  Article  CAS  Google Scholar 

  • Donmez E, Sears RG, Shroyer JP, Paulsen GM (2001) Genetic gain in yield attributes of winter wheat in the Great Plains. Crop Sci 41:1412–1419

    Article  Google Scholar 

  • Dreccer F, Ogbonnaya G, Borgognone J, Wilson J (2004) Variation in shoot and root growth in primary synthetic wheats—implications for overcoming water deficits in marginal environments. In: Proceedings of the 4th international crop science congress, Brisbane, 26 Sept–1 Oct 2004 (http://www.cropscience.org.au/icsc2004/poster/1/3/2/637_dreccer.htm)

  • Dubois F, Terce´-laforgue T, Gonzalez Moro MB, Estavillo JM, Sangwan R, Gallais A, Hirel B (2003) Glutamate dehydrogenase in plants: is there a new story for an old enzyme? Plant Physiol Biochem 41:565–576

    Article  CAS  Google Scholar 

  • Ehdaie B, Waines JG (2003) 1RS translocation increases root biomass in Very-type wheat isogenic lines and associates with grain yield. In: Pogna NE, Romano M, Pogna EA, Galterio G, eds. Proceedings of the 10th International Wheat Genetics Symposium, Vol. 2. ISC: Paestum, Italy, p 693–695

  • Finlay KW, Wilkinson GN (1963) The analysis of adaptation in a plant breeding programme. Aust J Agric Res 14:742–754

    Article  Google Scholar 

  • Fontaine JX, Ravel C, Pageau K, Heumez E, Dubois F, Hirel B, Le Gouis J (2009) A quantitative genetic study for elucidating the contribution of glutamine synthetase, glutamate dehydrogenase and other nitrogen-related physiological traits to the agronomic performance of common wheat. Theor Appl Genet 119:645–662

    PubMed  Article  CAS  Google Scholar 

  • Foulkes MJ, Hawkesford MJ, Barraclough PB, Holdsworth MJ, Kerr S, Kightley S, Shewry PR (2009) Identifying traits to improve the nitrogen economy of wheat: recent advances and future prospects. Field Crops Res 114:329–342

    Article  Google Scholar 

  • Gaju O, Allard V, Martre P, Snape J, Heumez E, Le Gouis J, Moreau D, Bogard M, Griffiths S, Orford S, Hubbart S, Foulkes J (2011) Identification of traits to improve the N-use efficiency of wheat genotypes. Field Crops Res 123:139–152

    Article  Google Scholar 

  • García-Suárez JV, Röder MS, Díaz De León JL (2010) Identification of QTLs and associated molecular markers of agronomic traits in wheat (Triticum aestivum L.) under two conditions of nitrogen fertilization. Cereal Res Commun 38:459–470

    Article  Google Scholar 

  • Gou J, Strauss SH, Tsai CJ, Fang K, Chen Y, Jiang X, Busov VB (2010) Gibberellins regulate lateral root formation in Populus through interactions with auxin and other hormones. Plant Cell 22:623–639

    PubMed  Article  CAS  Google Scholar 

  • Groos C, Gay G, Perretant M-R, Gervais L, Bernard M, Dedryver F, Charmet G (2002) Study of the relationship between pre-harvest sprouting and grain color by quantitative trait loci analysis in a white red grain breadwheat cross. Theor Appl Genet 104:39–47

    PubMed  Article  CAS  Google Scholar 

  • Groos C, Robert N, Bervas E, Charmet G (2003) Genetic analysis of grain protein content, grain yield and thousand kernel weight in bread wheat. Theor Appl Genet 106:1032–1040

    PubMed  CAS  Google Scholar 

  • Habash D, Bernard S, Schondelmaier J, Weyen J, Quarrie S (2007) The genetics of nitrogen use in hexaploid wheat: n utilisation, development and yield. Theor Appl Genet 114:403–419

    PubMed  Article  CAS  Google Scholar 

  • Hirel B, Le Gouis J, Ney B, Gallais A (2007) The challenge of improving nitrogen use efficiency in crop plants: towards a more central role for genetic variability and quantitative genetics within integrated approaches. J Exp Bot 58:2369–2387

    PubMed  Article  CAS  Google Scholar 

  • Horvath A, Didier A, Koenig J, Exbrayat F, Charmet G, Balfourier F (2009) Diversity and linkage disequilibrium analysis along the chromosome 3B of bread wheat (Triticum aestivum L.) in contrasted plant materials. Theor Appl Genet 119:1523–1537

    PubMed  Article  CAS  Google Scholar 

  • Johansson E, Prieto-Linde ML, Jönsson JÖ (2001) Effects of wheat cultivar and nitrogen application on storage protein composition and bread making quality. Cereal Chem 78:19–25

    Article  CAS  Google Scholar 

  • Kichey T, Heumez E, Pocholle P, Pageau K, Vanacker H, Dubois F, Le Gouis J, Hirel B (2006) Combined agronomic and physiological aspects of nitrogen management in wheat (Triticum aestivum L.). Dynamic and integrated views highlighting the central role for the enzyme glutamine synthetase. New Phytol 169:265–278

    PubMed  Article  CAS  Google Scholar 

  • Kichey T, Hirel B, Heumez E, Dubois F, Le Gouis J (2007) In winter wheat (Triticum aestivum L.), post-anthesis nitrogen uptake and remobilisation to the grain correlates with agronomic traits and nitrogen physiological markers. Field Crop Res 102:22–32

    Article  Google Scholar 

  • Kim W, Johnson JW, Baenziger PS, Lukaszewski AJ, Gaines CS (2004) Agronomic effect of wheat–rye translocation carrying rye chromatin (1R) from different sources. Crop Sci 44:1254–1258

    Article  Google Scholar 

  • Koch W, Kwart M, Laubner M, Heineke D, Stransky H, Frommer WB, Tegeder M (2003) Reduced amino acid content in transgenic potato tubers due to antisense inhibition of the leaf H+/amino acid symporter StAAP1. Plant J 33:211–220

    PubMed  Article  CAS  Google Scholar 

  • Krapp A, Saliba-Colombani V, Daniel-Vedele F (2005) Analysis of C and N metabolisms and of C/N interactions using quantitative genetics. Photosynth Res 83:251–263

    PubMed  Article  CAS  Google Scholar 

  • Kuchel H, Williams K, Langridge P, Eagles HA, Jefferies SP (2007) Genetic dissection of grain yield in bread wheat II. QTL-by-environment interaction. Theor Appl Genet 115:1015–1027

    PubMed  Article  CAS  Google Scholar 

  • Laperche A, Brancourt-Hulmel M, Heumez E, Gardet O, Le Gouis J (2006) Estimation of genetic parameters of a DH wheat population grown at different N stress levels characterized by probe genotypes. Theor Appl Genet 112:797–807

    PubMed  Article  CAS  Google Scholar 

  • Laperche A, Brancourt-Hulmel M, Heumez E, Gardet O, Hanocq E, Devienne-Barret F, Le Gouis J (2007) Using genotype × nitrogen interaction variables to evaluate the QTL involved in wheat tolerance to nitrogen constraints. Theor Appl Genet 115:399–415

    PubMed  Article  CAS  Google Scholar 

  • Laperche A, Le Gouis J, Hanocq E, Brancourt-Hulmel M (2008) Modelling nitrogen stress with probe genotypes to assess genetic parameters and genetic determinism of winter wheat tolerance to nitrogen constraint. Euphytica 16:259–271

    Article  Google Scholar 

  • Law CN, Worland AJ, Giorgi B (1976) Genetic-control of ear-emergence time by chromosomes-5a and chromosomes-5D of wheat. Heredity 36:49–58

    Article  Google Scholar 

  • Le Gouis J, Beghin D, Heumez E, Pluchard P (2000) Genetic differences for nitrogen uptake and nitrogen utilisation efficiencies in winter wheat. Eur J Agron 12:163–173

    Article  Google Scholar 

  • Le Gouis J, Bordes J, Ravel C, Heumez E, Faure S, Praud S, Galic N, Remoué C, Balfourier F, Allard V, Rousset M (2011) Genome wide association analysis to identify chromosomal regions determining components of earliness in wheat. Theor Appl Genet. doi:10.1007/s00122-011-1732-3

    Google Scholar 

  • Lee JH, Graybosch RA, Peterson CJ (1995) Quality and biochemical effects of 1BL/1RS wheat–rye translocation in wheat. Theor Appl Genet 90:105–112

    Article  CAS  Google Scholar 

  • Lid SE, Olsen L, Nestestog R, Aukerman M, Brown RC, Lemmon B, Mucha M, Opsahl-Sorteberg HG, Olsen OA (2005) Mutation in the Arabidopisis thaliana DEK1 calpain gene perturbs endosperm and embryo development while over expression affects organ development globally. Planta 221:339–351

    PubMed  Article  CAS  Google Scholar 

  • Masood Quraishi U, Abrouk M, Murat F, Pont C, Foucrier S, Desmaizieres G, Confolent C, Rivière N, Charmet G, Paux E, Murigneux A, Guerreiro L, Lafarge S, Le Gouis J, Feuillet C, Salse J (2011) Cross-genome map based dissection of a nitrogen use efficiency ortho-metaQTL in bread wheat unravels concerted cereal genome evolution. Plant J 65:745–756

    Article  Google Scholar 

  • McIntosh RA, Hart GE, Devos KM Gale MD, Rogers WJ (1998) Catalogue of gene symbols for wheat. In: Proceedings of the 9th international wheat genetics symposium, Saska toon, Canada, pp 1–235 (1998)

  • Neumann K, Kobiljski B, Dencie S, Varshney RK, Borner A (2011) Genome-wide association mapping: a case study in bread wheat (Triticum aestivum L.). Mol Breeding 27:37–58

    Article  Google Scholar 

  • Okumoto S, Koch W, Tegeder M, Fischer WN, Biehl A, Leister D, Stierhof YD, Frommer WB (2004) Root phloem-specific expression of the plasma membrane amino acid proton co-transporter AAP3. J Exp Bot 55:2155–2168

    PubMed  Article  CAS  Google Scholar 

  • Oury FX, Godin C (2007) Yield and grain protein concentration in bread wheat: how to use the negative relationship between the two characters to identify favorable genotypes? Euphytica 157:45–57

    Article  CAS  Google Scholar 

  • Oury FX, Bérard P, Brancourt-Hulmel M, Depatureaux C, Doussinault G, Galic N, Giraud A, Heumez E, Lecomte C, Pluchard P, Rolland B, Rousset M, Trottet M (2003) Yield and grain protein concentration in bread wheat: a review and a study of multi-annual data from a French breeding program. J Genet Breed 57:59–68

    Google Scholar 

  • Paux E, Sourdille P, Salse J, Saintenac C, Choulet F, Leroy P, Korol A, Michalak M, Kianian S, Spielmeyer W, Lagudah E, Somers D, Kilian A, Alaux M, Vautrin S, Bergès H, Eversole K, Appels R, Safar J, Simkova H, Dolezel J, Bernard M, Feuillet C (2008) A physical map of the 1-gigabase bread wheat chromosome 3B. Science 322:101–104

    PubMed  Article  CAS  Google Scholar 

  • Payne PI (1987) Genetics of wheat storage proteins and the effect of allelic variation on breadmaking quality. Annu Rev Plant Physiol 38:141–153

    Article  CAS  Google Scholar 

  • Pena RJ, Amaya A, Rajaram S, Mujeeb-Kazi A (1990) Variation in quality characteristics associated with some spring 1B/1R translocation wheats. J Cereal Sci 12:105–112

    Article  Google Scholar 

  • Peng J, Richards DE, Hartley NM, Murphy GP, Devos KM, Flintham JE, Beales J, Fish LJ, Worland AJ, Pelica F, Sudhakar D, Christou P, Snape JW, Gale MD, Harberd NP (1999) ‘Green revolution’ genes encode mutant gibberellin response modulators. Nature 400:256–261

    PubMed  Article  CAS  Google Scholar 

  • Prasad M, Kumar N, Kulwal PL, Röder MS, Balyan HS, Dhaliwal HS, Gupta PK (2003) QTL analysis for grain protein content using SSR markers and validation studies using NILs in bread wheat. Theor Appl Genet 106:659–667

    PubMed  CAS  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    PubMed  CAS  Google Scholar 

  • Quarrie SA, Steed A, Calestani C, Semikhodskii A, Lebreton C, Chinoy C, Steele N, Pljevljakusic D, Waterman E, Weyen J, Schondelmaier J, Habash DZ, Farmer P, Saker L, Clarkson DT, Abugalieva A, Yessimbekova M, Turuspekov Y, Abugalieva S, Tuberosa R, Sanguineti MC, Hollington PA, Aragues R, Royo A, Dodig D (2005) A high-density genetic map of hexaploid wheat (Triticum aestivum L.) from the cross Chinese Spring × SQ1 and its use to compare QTLs for grain yield across a range of environments. Theor Appl Genet 110:865–880

    PubMed  Article  CAS  Google Scholar 

  • Ravel C, Martre P, Romeuf I, Dardevet M, El-Malki R, Bordes J, Duchateau N, Brunel D, Balfourier F, Charmet G (2009) Nucleotide polymorphism in the wheat transcriptional activator Spa influences its pattern of expression and has pleiotropic effects on grain protein composition, dough viscoelasticity and grain hardness. Plant Physiol 151:33–44

    Article  Google Scholar 

  • Rousset M, Bonnin I, Remoué C, Falque M, Rhoné B, Veyrieiras J-B, Madur D, Balfourier F, Le Gouis J, Santoni S, Goldringer I (2011) Deciphering the genetics of growth habit by an association study on candidate genes in bread wheat (Triticum aestivum L.). Theor Appl Genet. doi:10.1007/s00122-011-1636-2

  • Roy JK, Bandopadhyay R, Rustgi S, Balyan HS, Gupta PK (2006) Association analysis of agronomically important traits using SSR, SAMPL and AFLP markers in bread wheat. Curr Sci 90:683–689

    CAS  Google Scholar 

  • Sabelli PA, Larkins BA (2009) The development of endosperm in grasses. Plant Physiol 149:14–26

    PubMed  Article  CAS  Google Scholar 

  • Somers D, Isaac P, Edwards K (2004) A high-density microsatellite consensus map for bread wheat (Triticum aestivum L.). Theor Appl Genet 109:1105–1114

    PubMed  Article  CAS  Google Scholar 

  • Veyrieras J-B, Goffinet B, Charcosset A (2007) MetaQTL: a package of new computational methods for the meta-analysis of QTL mapping experiments. BMC Bioinformatics 8:1–16

    Article  Google Scholar 

  • Viglasi P (1968) Short strawed mutants of Karcagi 522 winter wheat induced by gamma rays. Acta Agron Hung 17:205–214

    Google Scholar 

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

    PubMed  Article  CAS  Google Scholar 

  • Weir BS (1996) Genetic data analysis II Methods for discrete population genetic data. Sinauer Associates Inc, Sunderlan, p 376

    Google Scholar 

  • Wieser H, Kieffer R, Lelley T (2000) The influence of 1B/1R chromosome translocation on gluten protein composition and technological properties of bread wheat. J Sci Food Agric 80:1640–1647

    Article  CAS  Google Scholar 

  • Willats WGT, McCartney L, Mackie W, Knox JP (2001) Pectin: cell biology and prospects for functional analysis. Plant Mol Biol 47:9–27

    PubMed  Article  CAS  Google Scholar 

  • Witcombe JR, Hollington PR, Howarth CJ, Reader S, Steele KA (2008) Breeding for abiotic stresses for sustainable agriculture. Phil Trans R Soc Biol 363:703–716

    Article  CAS  Google Scholar 

  • Worland AJ, Sayer EJ, Borner A (1994) The genetics and breeding potential of Rht12, a dominant dwarfing gene in wheat. Plant Breed 113:187–196

    Article  Google Scholar 

  • Yamaguchi S (2008) Gibberellin metabolism and its regulation. Annu Rev Plant Biol 59:225–251

    PubMed  Article  CAS  Google Scholar 

  • Zhang Y, Tang J, Zhang Y, Yan J, Xiao Y, Zhang Y, Xia X, He Z (2011) QTL mapping for quantities of protein fractions in bread wheat (Triticum aestivum L.). Theor Appl Genet 122:971–987

    PubMed  Article  CAS  Google Scholar 

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Acknowledgments

The experimental work was partly supported by the Enterprise Competitiveness Fund Project “Semences de Demain”.

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Affiliations

  1. INRA, UMR 1095 Génétique, Diversité Et Ecophysiologie Des Céréales, 234 Avenue Du Brézet, 63100, Clermont-Ferrand, France

    Jacques Bordes, C. Ravel, G. Charmet, J. Le Gouis & F. Balfourier

  2. Université Blaise Pascal, UMR 1095 Génétique, Diversité Et Ecophysiologie Des Céréales, 63177, Aubière Cedex, France

    Jacques Bordes, C. Ravel, G. Charmet, J. Le Gouis & F. Balfourier

  3. Agri Obtentions Chemin de La Petite, Minière, Guyancourt, 78280, France

    J. P. Jaubertie & A. L. Pissavy

  4. Limagrain Europe, BP3, 77390, Verneuil l’Etang, France

    B. Duperrier

  5. INRA-UPS-CNRS-AgroParisTech, UMR de Génétique Végétale, Ferme Du Moulon, 91190, Gif-sur-Yvette, France

    O. Gardet

  6. INRA, UMR 1281 Stress Abiotiques Et Différenciation Des Végétaux Cultivés, Estrées-Mons, 80203, Péronne, France

    E. Heumez

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  1. Jacques Bordes
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  2. C. Ravel
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  3. J. P. Jaubertie
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  5. O. Gardet
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  6. E. Heumez
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  7. A. L. Pissavy
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  9. J. Le Gouis
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  10. F. Balfourier
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Correspondence to Jacques Bordes.

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Communicated by A. Graner.

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Bordes, J., Ravel, C., Jaubertie, J.P. et al. Genomic regions associated with the nitrogen limitation response revealed in a global wheat core collection. Theor Appl Genet 126, 805–822 (2013). https://doi.org/10.1007/s00122-012-2019-z

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Keywords

  • Simple Sequence Repeat Marker
  • Glutamine Synthetase
  • Core Collection
  • Grain Yield
  • Favorable Allele