Advertisement

Planta

pp 1–19 | Cite as

Candidate genes and genome-wide association study of grain protein content and protein deviation in durum wheat

  • D. Nigro
  • A. GadaletaEmail author
  • G. Mangini
  • P. Colasuonno
  • I. Marcotuli
  • A. Giancaspro
  • S. L. Giove
  • R. Simeone
  • A. Blanco
Original Article

Abstract

Main conclusion

Stable QTL for grain protein content co-migrating with nitrogen-related genes have been identified by the candidate genes and genome-wide association mapping approaches useful for marker-assisted selection.

Grain protein content (GPC) is one of the most important quality traits in wheat, defining the nutritional and end-use properties and rheological characteristics. Over the years, a number of breeding programs have been developed aimed to improving GPC, most of them having been prevented by the negative correlation with grain yield. To overcome this issue, a collection of durum wheat germplasm was evaluated for both GPC and grain protein deviation (GPD) in seven field trials. Fourteen candidate genes involved in several processes related to nitrogen metabolism were precisely located on two high-density consensus maps of common and durum wheat, and six of them were found to be highly associated with both traits. The wheat collection was genotyped using the 90 K iSelect array, and 11 stable quantitative trait loci (QTL) for GPC were detected in at least three environments and the mean across environments by the genome-wide association mapping. Interestingly, seven QTL were co-migrating with N-related candidate genes. Four QTL were found to be significantly associated to increases of GPD, indicating that selecting for GPC could not affect final grain yield per spike. The combined approaches of candidate genes and genome-wide association mapping led to a better understanding of the genetic relationships between grain storage proteins and grain yield per spike, and provided useful information for marker-assisted selection programs.

Keywords

Genome-wide association mapping Grain protein content Grain protein deviation Grain yield GPC and grain yield relationships Nitrogen-related genes QTL mapping SNP markers 

Abbreviations

AlaAT

Alanine aminotransferase

ASN

Asparagine synthetase

CG

Candidate gene

GDH

Glutamate dehydrogenase

GOGAT

Glutamate synthetase

GPC

Grain protein content

GPD

Grain protein deviation

GS

Glutamine synthetase

GWAS

Genome-wide association study

GY

Grain yield

GYS

Grain yield per spike

NIR

Nitrite reductase

NR

Nitrate reductase

NRT2

Nitrate transporter

NUE

Nitrogen use efficiency

PPDK

Pyruvate orthophosphate dikinase

QTL

Quantitative trait locus

Notes

Acknowledgements

The research project was supported by grants from Ministero dell’Istruzione, dell’Università e della Ricerca, project ‘ISCOCEM’, and from Regione Puglia “Programma regionale a sostegno della specializzazione intelligente e della sostenibilità sociale ed ambientale-FutureInResearch”.

Compliance with ethical standards

Conflict of interest

The authors declare no conflict of interest.

Supplementary material

425_2018_3075_MOESM1_ESM.docx (185 kb)
Supplementary material 1 (DOCX 185 kb)

References

  1. Acreche MM, Slafer GA (2009) Grain weight, radiation interception and use efficiency as affected by sink-strength in Mediterranean wheats released from 1940 to 2005. Field Crops Res 110(2):98–105CrossRefGoogle Scholar
  2. Akhunov E, Nicolet C, Dvorak J (2009) Single nucleotide polymorphism genotyping in polyploid wheat with the Illumina GoldenGate assay. Theor Appl Genet 119(3):507–517CrossRefGoogle Scholar
  3. Balyan HS, Gahlaut V, Kumar A, Jaiswal V, Dhariwal R, Tyagi S, Agarwal P, Kumari S, Gupta PK (2016) Nitrogen and phosphorus use efficiencies in wheat: physiology, phenotyping, genetics, and breeding. In: Janick J (ed) Plant breeding reviews, vol 40. Wiley, Hoboken, pp 167–234CrossRefGoogle Scholar
  4. Blanco A, Mangini G, Giancaspro A, Giove S, Colasuonno P, Simeone R, Gadaleta A (2012) Relationships between grain protein content and grain yield components through quantitative trait locus analyses in a recombinant inbred line population derived from two elite durum wheat cultivars. Mol Breed 30(1):79–92CrossRefGoogle Scholar
  5. Bogard M, Allard V, Brancourt-Hulmel M, Heumez E, Machet JM, Jeuffroy MH et al (2010) Deviation from the grain protein concentration-grain yield negative relationship is highly correlated to post-anthesis N uptake in winter wheat. J Exp Bot 61:4303–4312CrossRefGoogle Scholar
  6. Bordes J, Ravel C, Jaubertie JP, Duperrier B, Gardet O, Heumez E, Balfourier F (2013) Genomic regions associated with the nitrogen limitation response revealed in a global wheat core collection. Theor Appl Genet 126(3):805–822CrossRefGoogle Scholar
  7. Börner A, Schumann E, Fürste A, Cöster H, Leithold B, Röder M, Weber W (2002) Mapping of quantitative trait loci determining agronomic important characters in hexaploid wheat (Triticum aestivum L.). Theor Appl Genet 105(6–7):921–936CrossRefGoogle Scholar
  8. Breseghello F, Sorrells ME (2006) Association analysis as a strategy for improvement of quantitative traits in plants. Crop Sci 46(3):1323–1330CrossRefGoogle Scholar
  9. Brevis JC, Dubcovsky J (2010) Effects of the chromosome region including the grain protein content locus Gpc-B1 on wheat grain and protein yield. Crop Sci 50:93–104CrossRefGoogle Scholar
  10. Castaings L, Camargo A, Pocholle D, Gaudon V, Texier Y et al (2009) The nodule inception-like protein 7 modulates nitrate sensing and metabolism in Arabidopsis. Plant J 57:426–435CrossRefGoogle Scholar
  11. Clarke JM, McCaig TN, DePauw RM, Knox RE, Clarke FR, Fernandez MR, Ames NP (2005) Strongfield durum wheat. Can J Plant Sci 85:651–654CrossRefGoogle Scholar
  12. Colasuonno P, Lozito ML, Marcotuli I, Nigro D, Giancaspro A, Mangini G et al (2017) The carotenoid biosynthetic and catabolic genes in wheat and their association with yellow pigments. BMC Genomics 18:122.  https://doi.org/10.1186/s12864-016-3395-6 CrossRefGoogle Scholar
  13. Collins NC, Tardieu F, Tuberosa R (2008) Quantitative trait loci and crop performance under abiotic stress: where do we stand? Plant Physiol 147(2):469–486CrossRefGoogle Scholar
  14. Curci PL, Bergès H, Marande W, Maccaferri M, Tuberosa R, Sonnante G (2018) Asparagine synthetase genes (AsnS1 and AsnS2) in durum wheat: structural analysis and expression under nitrogen stress. Euphytica 214(2):36.  https://doi.org/10.1007/s10681-017-2105-z CrossRefGoogle Scholar
  15. Cuthbert JL, Somers DJ, Brûlé-Babel AL, Brown PD, Crow GH (2008) Molecular mapping of quantitative trait loci for yield and yield components in spring wheat (Triticum aestivum L.). Theor Appl Genet 117:595–608CrossRefGoogle Scholar
  16. Donnelly P (2008) Progress and challenges in genome-wide association studies in humans. Nature 456:728–731CrossRefGoogle Scholar
  17. Gadaleta A, Nigro D, Giancaspro A, Blanco A (2011) The glutamine synthetase (GS2) genes in relation to grain protein content of durum wheat. Funct Integr Genomics 11:665–670CrossRefGoogle Scholar
  18. Gadaleta A, Nigro D, Marcotuli I, Giancaspro A, Giove SL, Blanco A (2014) Isolation and characterization of cytosolic glutamine synthetase (GSe) genes and association with grain protein content in durum wheat. Crop Pasture Sci 65:38–45CrossRefGoogle Scholar
  19. Gao R, Curtis TY, Powers SJ, Xu H, Huang J, Halford NG (2016) Food safety: structure and expression of the asparagine synthetase gene family of wheat. J Cereal Sci 68:122–131CrossRefGoogle Scholar
  20. Garnett T, Conn V, Kaiser BN (2009) Root based approaches to improving nitrogen use efficiency in plants. Plant Cell Environ 32:1272–1283CrossRefGoogle Scholar
  21. Giancaspro A, Giove SL, Zito D, Blanco A, Gadaleta A (2016) Mapping QTLs for Fusarium head blight resistance in an interspecific wheat population. Front Plant Sci 7:1381.  https://doi.org/10.3389/fpls.2016.01381 CrossRefGoogle Scholar
  22. Good AG, Johnson SJ, De Pauw M, Carroll RT, Savidov N, Vidmar J, Stroeher V (2007) Engineering nitrogen use efficiency with alanine aminotransferase. Botany 85(3):252–262Google Scholar
  23. 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 106:1032–1040CrossRefGoogle Scholar
  24. Gu R, Duan F, An X, Zhang F, von Wiren N, Yuan L (2013) Characterization of AMT-mediated high-affinity ammonium uptake in roots of maize (Zea mays L.). Plant Cell Physiol 54:1515–1524CrossRefGoogle Scholar
  25. Gupta PK, Kulwal PL, Jaiswal V (2014) Association mapping in crop plants: opportunities and challenges. Adv Genet 85:109–147CrossRefGoogle Scholar
  26. Habash DZ, Bernard S, Schondelmaier J, Weyen J, Quarrie SA (2007) The genetics of nitrogen use in hexaploid wheat: N utilisation, development and yield. Theor Appl Genet 114:403–419CrossRefGoogle Scholar
  27. Hu M, Zhao X, Liu Q, Hong X, Zhang W, Zhang Y, Tong Y (2018) Transgenic expression of plastidic glutamine synthetase increases nitrogen uptake and yield in wheat. Plant Biotechnol J 16(11):1858–1867CrossRefGoogle Scholar
  28. 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 Crops Res 102:22–32CrossRefGoogle Scholar
  29. Kotur Z, Mackenzie N, Ramesh S, Tyerman SD, Kaiser BN, Glass AD (2012) Nitrate transport capacity of the Arabidopsis thaliana NRT2 family members and their interactions with AtNAR2.1. New Phytol 194(3):724–731CrossRefGoogle Scholar
  30. Krapp A (2015) Plant nitrogen assimilation and its regulation: a complex puzzle with missing pieces. Curr Opin Plant Biol 25:115–122CrossRefGoogle Scholar
  31. Krapp A, Berthomé R, Orsel M, Mercey-Boutet S, Yu A, Castaings L, Daniel-Vedele F (2011) Arabidopsis roots and shoots show distinct temporal adaptation pattern towards N starvation. Plant Physiol 157(3):1255–1282CrossRefGoogle Scholar
  32. Kumar A, Jain S, Elias EM, Ibrahim M, Sharma LK (2018) An overview of QTL identification and marker-assisted selection for grain protein content in wheat. In: Sengar RS, Singh A (eds) Eco-friendly agro-biological techniques for enhancing crop productivity. Springer, Singapore, pp 245–274CrossRefGoogle Scholar
  33. Laidò G, Marone D, Russo MA, Colecchia SA, Mastrangelo AM, De Vita P et al (2014) Linkage disequilibrium and genome-wide association mapping in tetraploid wheat (Triticum turgidum L.). PLoS One 9(4):e95211.  https://doi.org/10.1371/journal.pone.0095211 CrossRefGoogle Scholar
  34. Lea PJ, Azevedo RA (2007) Nitrogen use efficiency. 2. Amino acid metabolism. Ann Appl Biol 15(3):269–275CrossRefGoogle Scholar
  35. Li W, Wang Y, Okamoto M, Crawford NM, Siddiqi MY, Glass AD (2007) Dissection of the AtNRT2. 1: AtNRT2. 2 inducible high-affinity nitrate transporter gene cluster. Plant Physiol 143(1):425–433CrossRefGoogle Scholar
  36. Lipka AE, Gore MA, Magallanes-Lundback M, Mesberg A, Lin H, Tiede T, DellaPenna D (2013) Genome-wide association study and pathway level analysis of tocochromanol levels in maize grain. G3-Genes Genom Genet 3(8):1287–1299Google Scholar
  37. Lu Y, Luo F, Yang M, Li X, Lian X (2011) Suppression of glutamate synthase genes significantly affects carbon and nitrogen metabolism in rice (Oryza sativa L.). Sci China Life Sci 54:651–663CrossRefGoogle Scholar
  38. Maccaferri M, Cane MA, Sanguineti MC, Salvi S, Colalongo MC, Massi A, Fahima T (2014) A consensus framework map of durum wheat (Triticum durum Desf.) suitable for linkage disequilibrium analysis and genome-wide association mapping. BMC Genomics 15(1):873.  https://doi.org/10.1186/1471-2164-15-873 CrossRefGoogle Scholar
  39. Mahjourimajd S, Taylor J, Rengel Z, Khabaz-Saberi H, Kuchel H, Okamoto M, Langridge P (2016) The genetic control of grain protein content under variable nitrogen supply in an Australian wheat mapping population. PLoS One 11(7):e0159371.  https://doi.org/10.1371/journal.pone.0159371 CrossRefGoogle Scholar
  40. Mangini G, Gadaleta A, Colasuonno P, Marcotuli I, Signorile AM, Simeone R et al (2018) Genetic dissection of the relationships between grain yield components by genome-wide association mapping in a collection of tetraploid wheats. PLoS One 13(1):e0190162.  https://doi.org/10.1371/journal.phone.0190162 CrossRefGoogle Scholar
  41. Marcotuli I, Houston K, Waugh R, Fincher GB, Burton RA, Blanco A, Gadaleta A (2015) Genome wide association mapping for arabinoxylan content in a collection of tetraploid wheats. PLoS One 10(7):e0132787.  https://doi.org/10.1371/journal.pone.0132787 CrossRefGoogle Scholar
  42. Marcotuli I, Colasuonno P, Blanco A, Gadaleta A (2018) Expression analysis of cellulose synthase-like genes in durum wheat. Sci Rep 8:15675.  https://doi.org/10.1038/s41598-018-34013-6 CrossRefGoogle Scholar
  43. Marjoram P, Zubair A, Nuzhdin SV (2014) Post-GWAS: where next? More samples, more SNPs or more biology? Heredity 112(1):79–88CrossRefGoogle Scholar
  44. Monaghan JM, Snape JW, Chojecki AJS, Kettlewell PS (2001) The use of grain protein deviation for identifying wheat cultivars with high grain protein concentration and yield. Euphytica 122(2):309–317CrossRefGoogle Scholar
  45. Nigro D, Gu YQ, Huo N, Marcotuli I, Blanco A, Gadaleta A, Anderson OD (2013) Structural analysis of the wheat genes encoding NADH-dependent glutamine-2-oxoglutarate amidotransferases genes and correlation with grain protein content. PLoS One 8:e73751.  https://doi.org/10.1371/journal.pone.0073751 CrossRefGoogle Scholar
  46. Nigro D, Blanco A, Anderson OD, Gadaleta A (2014) Characterization of ferredoxin-dependent glutamine-oxoglutarate amidotransferase (Fd-GOGAT) genes and their relationship with grain protein content QTL in wheat. PLoS One 9:e103869.  https://doi.org/10.1371/journal.pone.0103869 CrossRefGoogle Scholar
  47. Nigro D, Fortunato S, Giove SL, Paradiso A, Gu YQ, Blanco A, de Pinto MC, Gadaleta A (2016) Glutamine synthetase in durum wheat: genotypic variation and relationship with grain protein content. Front Plant Sci 7:971.  https://doi.org/10.3389/fpls.2016.00971 CrossRefGoogle Scholar
  48. Nigro D, Fortunato S, Giove SL, Mangini G, Yacoubi I, Simeone R, BlancoA Gadaleta A (2017a) Allelic variants of glutamine synthetase and glutamate synthase genes in a collection of durum wheat and association with grain protein content. Diversity 9(4):52.  https://doi.org/10.3390/d9040052 CrossRefGoogle Scholar
  49. Nigro D, Laddomada B, Mita G, Blanco E, Colasuonno P, Simeone R, Gadaleta A, Pasqualone A, Blanco A (2017b) Genome-wide association mapping of phenolic acids in tetraploid wheats. J Cereal Sci 75:25–34CrossRefGoogle Scholar
  50. Oury FX, Berard P, Brancourt-Hulmel M, Depatureaux C, Doussignault G, Galic N, Giraud A, Heumez E, Lecompte 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 57:59–68Google Scholar
  51. Quraishi UM, Abrouk M, Murat F, Pont C, Foucrier S et al (2011) Cross-genome map based dissection of a nitrogen use efficiency ortho-metaQTL in bread wheat unravels concerted cereal genome evolution. Plant J 65:745–756CrossRefGoogle Scholar
  52. Quraishi UM, Pont C, Ain QU, Flores R, Burlot L, Alaux M, Salse J (2017) Combined genomic and genetic data integration of major agronomical traits in bread wheat (Triticum aestivum L.). Front Plant Sci 8:1843.  https://doi.org/10.3389/fpls.2017.01843 CrossRefGoogle Scholar
  53. Rapp M, Lein V, Lacoudre F, Lafferty J, Müller E, Vida G, Leiser WL (2018) Simultaneous improvement of grain yield and protein content in durum wheat by different phenotypic indices and genomic selection. Theor Appl Genet 131(6):1315–1329CrossRefGoogle Scholar
  54. Salse J, Quraishi UM, Pont C, Murat F, Le Gouis J, Lafarge S (2013) Grain filling of a plant through the modulation of NADH-glutamate synthase. Patent Application No. 13/576,610Google Scholar
  55. Sears RG (1998) Improving grain protein concentration and grain yield in USA hard winter wheat. In: Fowler DB, Geddes WE, Johnston AM, Preston KR (eds) Wheat protein production and marketing. In: Proceedings of Wheat Symposium, Saskatoon, Printcrafters Inc., Winnipeg, Canada, pp 63–67Google Scholar
  56. Sharp PJ, Kreis M, Shewry PR, Gale MD (1988) Location of β-amylase sequences in wheat and its relatives. Theor Appl Genet 75:286–290CrossRefGoogle Scholar
  57. Shrawat AK, Carroll RT, DePauw M, Taylor GJ, Good AG (2008) Genetic engineering of improved nitrogen use efficiency in rice by the tissue-specific expression of alanine aminotransferase. Plant Biotechnol J 6:722–732CrossRefGoogle Scholar
  58. Simmonds NW (1995) The relation between yield and protein in cereal grain. J Sci Food Agric 67:309–315CrossRefGoogle Scholar
  59. Simons M, Saha R, Guillard L, Clément G, Armengaud P, Cañas R, Maranas CD, Lea PJ, Hirel B (2014) Nitrogen use efficiency in maize (Zea mays L.): from omics studies to metabolic modelling. J Exp Bot 65:5657–5671CrossRefGoogle Scholar
  60. Suprayogi Y, Pozniak CJ, Clarke FR, Clarke JM, Knox RE, Singh AK (2009) Identification and validation of quantitative trait loci for grain protein concentration in adapted Canadian durum wheat populations. Theor Appl Genet 119(3):437–448CrossRefGoogle Scholar
  61. Tabuchi M, Abiko T, Yamaya T (2007) Assimilation of ammonium ions and reutilization of nitrogen in rice. J Exp Bot 58:2319–2327CrossRefGoogle Scholar
  62. Taulemesse F, Le Gouis J, Gouache D, Gibon Y, Allard V (2015) Post-flowering nitrate uptake in wheat is controlled by N status at flowering, with a putative major role of root nitrate transporter NRT2.1. PLoS One 10(3):e0120291.  https://doi.org/10.1371/journal.pone.0120291 CrossRefGoogle Scholar
  63. Taylor L, Nunes-Nesi A, Parsley K, Leiss A, Leach G, Coates S, Hibberd JM (2010) Cytosolic pyruvate, orthophosphate dikinase functions in nitrogen remobilization during leaf senescence and limits individual seed growth and nitrogen content. Plant J 62(4):641–652CrossRefGoogle Scholar
  64. Thomsen HC, Eriksson D, Møller IS, Schjoerring JK (2014) Cytosolic glutamine synthetase: a target for improvement of crop nitrogen use efficiency? Trends Plant Sci 19:656–663CrossRefGoogle Scholar
  65. Thorwarth P, Piepho HP, Zhao Y, Ebmeyer E, Schacht J, Schachschneider R, Kazman E, Reif JC, Wurschum T, Friedrich C, Longin CFH (2018) Higher grain yield and higher grain protein deviation underline the potential of hybrid wheat for a sustainable agriculture. Plant Breed 137(3):326–337CrossRefGoogle Scholar
  66. Tian H, Fu J, Drijber RA, Gao Y (2015) Expression patterns of five genes involved in nitrogen metabolism in two winter wheat (Triticum aestivum L.) genotypes with high and low nitrogen utilization efficiencies. J Cereal Sci 61:48–54CrossRefGoogle Scholar
  67. Uauy C, Brevis JC, Dubcovsky J (2006) The high grain protein content gene Gpc-B1 accelerates senescence and has pleiotropic effects on protein content in wheat. J Exp Bot 57:2785–2794CrossRefGoogle Scholar
  68. Wang LIN, Cui FA, Wang J, Jun LI, Ding A, Zhao C, Wang H (2012) Conditional QTL mapping of protein content in wheat with respect to grain yield and its components. Thai J Genet 91(3):303–312CrossRefGoogle Scholar
  69. Wang SW, Forrest D, Allen K, Chao A, Huang SBE, Maccaferri M et al (2014) Characterization of polyploid wheat genomic diversity using a high-density 90,000 single nucleotide polymorphism array. Plant Biotechnol J 12(6):787–796CrossRefGoogle Scholar
  70. Weng J, Xie C, Hao Z, Wang J, Liu C, Li M, Li X (2011) Genome-wide association study identifies candidate genes that affect plant height in Chinese elite maize (Zea mays L.) inbred lines. PLoS One 6(12):e29229.  https://doi.org/10.1371/journal.pone.0029229 CrossRefGoogle Scholar
  71. Xu G, Fan X, Miller AJ (2012) Plant nitrogen assimilation and use efficiency. Annu Rev Plant Biol 63:153–182CrossRefGoogle Scholar
  72. Yamaya T, Obara M, Nakajima H, Sasaki S, Hayakawa T et al (2002) Genetic manipulation and quantitative-trait loci mapping for nitrogen recycling in rice. J Exp Bot 53:917–925CrossRefGoogle Scholar
  73. Zanetti S, Winzeler M, Feuillet C, Keller B, Messmer M (2001) Genetic analysis of bread–making quality in wheat and spelt. Plant Breed 120:13–19CrossRefGoogle Scholar
  74. Zeng DD, Qin R, Li M et al (2017) The ferredoxin-dependent glutamate synthase (OsFd-GOGAT) participates in leaf senescence and the nitrogen remobilization in rice. Mol Genet Genomics 292(2):385–395CrossRefGoogle Scholar
  75. Zhao XQ, Nie XL, Xiao XG (2013) Over-expression of a tobacco nitrate reductase gene in wheat (Triticum aestivum L.) increases seed protein content and weight without augmenting nitrogen supplying. PloS One 8(9):74678.  https://doi.org/10.1371/journal.pone.0074678 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • D. Nigro
    • 1
  • A. Gadaleta
    • 2
  • G. Mangini
    • 1
  • P. Colasuonno
    • 2
  • I. Marcotuli
    • 2
  • A. Giancaspro
    • 2
  • S. L. Giove
    • 2
  • R. Simeone
    • 1
  • A. Blanco
    • 1
  1. 1.Department of Soil, Plant and Food Sciences, Genetics and Plant Breeding SectionUniversity of BariBariItaly
  2. 2.Department of Agricultural and Environmental Science, Research Unit of “Genetics and Plant Biotechnology”University of BariBariItaly

Personalised recommendations