Advertisement

Introgression of an expressed HMW 1Ay glutenin subunit allele into bread wheat cv. Lincoln increases grain protein content and breadmaking quality without yield penalty

  • Nandita Roy
  • Shahidul Islam
  • Zitong Yu
  • Meiqin Lu
  • Domenico Lafiandra
  • Yun Zhao
  • Masood Anwar
  • Jorge E. Mayer
  • Wujun MaEmail author
Original Article

Abstract

Key message

An expressed HMW glutenin subunit Glu-Ay showed positive impacts on a range of wheat processing quality and yield traits. The grain protein compositions are significantly optimised for baking, resulting in a better breadmaking quality.

Abstract

The unique breadmaking properties of wheat flour are related to the quality and quantity of high-molecular weight glutenin subunits (HMW-GSs) present in the grain. In the current study, the silent 1Ay HMW-GS allele, present in most bread wheat cultivars, was replaced by the expressed 1Ay21* allele, which was introgressed into Australian bread wheat cultivar Lincoln by a backcrossing and selfing scheme. Stability of gene expression and the effect of the introgressed 1Ay21* subunit on protein composition, agronomic traits, flour functionality, and breadmaking quality were studied using BC4F5 grain grown in glasshouse and field. Field phenotyping and grain quality testing showed that the 1Ay21* gene conferred significant improvements to a range of traits, including an increase in grain protein content by up to 9%, UPP% by up to 24%, bread volume by up to 28%. The glasshouse experiment and one of the field trials showed positive 1Ay21* effects on yield, while one field trial showed one significant effects. This indicates that expression of the 1Ay21* gene has the potential of simultaneously increasing protein content and grain yield under certain environment. The qualitative improvements of the grain also led to a reduction of the energy required during the baking process in addition to the significant positive effects on bread quality.

Keywords

Expressed Glu-Ay subunit Grain yield Protein content HMW glutenin Wheat Breadmaking 

Notes

Acknowledgements

This research is financially supported by the Australian Grain Research and Development Corporation Projects UMU00036 and UMU00043. On behalf of all authors, the corresponding author states that there is no conflict of interest.

Authors' contribution

NR conducted the experiments and wrote the manuscript; SI involved in laboratory work, supervision, and manuscript writing; ZY conducted HPLC work; ML performed field trial and quality testing; DL supplied the germplasm and revised the manuscript; YZ involved in HPLC work; MA involved in phenotyping work; JEM contributed to experiment design, result interpretation, and manuscript writing; WM designed and supervised the study as well as finalised the manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare no conflict of interest.

References

  1. Bogard M, Allard V, Brancourt-Hulmel M, Heumez E, Machet J-M, Jeuffroy M-H, Le Gouis J (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(15):4303–4312PubMedCrossRefPubMedCentralGoogle Scholar
  2. Bushuk W (1997) Wheat breeding for end-product use. In: Braun HJ, Altay F, Kronstad WE, Beniwal SPS, McNab A (eds) Wheat: prospects for global improvement. Developments in plant breeding, vol 6. Springer, DordrechtGoogle Scholar
  3. Bushuk W, Briggs K, Shebeski L (1969) Protein quantity and quality as factors in the evaluation of bread wheats. Can J Plant Sci 49(2):113–122CrossRefGoogle Scholar
  4. Butow BJ, Ma W, Gale KR, Cornish GB, Rampling L, Larroque O, Morell MK, Békés F (2003) Molecular discrimination of Bx7 alleles demonstrates that a highly expressed high-molecular-weight glutenin allele has a major impact on wheat flour dough strength. Theor Appl Genet 107:1524–1532PubMedCrossRefPubMedCentralGoogle Scholar
  5. Cornish G, Bekes F, Allen H, Martin D (2001) Flour proteins linked to quality traits in an Australian doubled haploid wheat population. Crop Pasture Sci 52(12):1339–1348CrossRefGoogle Scholar
  6. Dowla NU, Edwards I, O'Hara G, Islam S, Ma W (2018) Developing Wheat for improved yield and adaptation under a changing climate: optimization of a few key genes. Engineering 4(4):514–522CrossRefGoogle Scholar
  7. Galili G (1997) The prolamin storage proteins of wheat and its relatives. In: Larkins BA, Vasil IK (eds) Cellular and molecular biology of plant seed development. Advances in cellular and molecular biology of plants, vol 4. Springer, DordrechtGoogle Scholar
  8. Gao L, Wang A, Li X, Dong K, Wang K, Appels R, Ma W, Yan Y (2009) Wheat quality related differential expression of albumins and globulins revealed by two-dimensional difference gel electrophoresis (2-D DIGE). J Proteom 73(2):279–296CrossRefGoogle Scholar
  9. Gao L, Ma W, Chen J, Wang K, Li J, Wang S, Bekes F, Appels R, Yan Y (2010) Characterization and comparative analysis of wheat high molecular weight glutenin subunits by SDS-PAGE, RP-HPLC, HPCE, and MALDI-TOF-MS. J Agric Food Chem 58(5):2777–2786PubMedCrossRefGoogle Scholar
  10. Gupta RB, MacRitchie F (1994) Allelic variation at glutenin subunit and gliadin loci, Glu-1, Glu-3 and Gli-1, of common wheats. II. Biochemical basis of the allelic effects on dough properties. J Cereal Sci 19:19–29CrossRefGoogle Scholar
  11. Jiang P, Xue J, Duan L, Gu Y, Mu J, Han S, Chen L, Li Y, Ma W, Yan Y, Li X (2019) Effects of high-molecular weight glutenin subunit combination in common wheat on the quality of crumb structure. J Sci Food Agric 99(4):1501–1508PubMedCrossRefPubMedCentralGoogle Scholar
  12. Koekemoer F, Labuschagne M, Van Deventer C (1999) A selection strategy for combining high grain yield and high protein content in South African wheat cultivars. Cereal Res Commun 27:107–114Google Scholar
  13. León E, Marín S, Giménez MJ, Piston F, Rodríguez-Quijano M, Shewry PR, Barro F (2009) Mixing properties and dough functionality of transgenic lines of a commercial wheat cultivar expressing the 1Ax1, 1Dx5 and 1Dy10 HMW glutenin subunit genes. J Cereal Sci 49(1):148–156CrossRefGoogle Scholar
  14. Liu L, Wang A, Appels R, Ma J, Xia X, Lan P, Ma W (2009) A MALDI-TOF based analysis of high-molecular weight glutenin subunits for wheat breeding. J Cereal Sci 50(2):295–301CrossRefGoogle Scholar
  15. Ma W, Zhang W, Gale KR (2003) Multiplex-PCR typing of high-molecular weight glutenin alleles in wheat. Euphytica 134:51–60CrossRefGoogle Scholar
  16. Ma W, Appels R, Bekes F, Larroque O, Morell MK, Gale KR (2005) Genetic characterisation of dough rheological properties in a wheat doubled-haploid population: additive genetic effects and epistatic interactions. Theor Appl Genet 111:410–422PubMedCrossRefGoogle Scholar
  17. Ma W, Sutherland M, Kammholz S, Banks P, Brennan P, Bovill W, Daggard G (2007) Wheat flour protein content and water absorption analysis in a doubled-haploid population. J Cereal Sci 45:302–308CrossRefGoogle Scholar
  18. Mann G, Diffey S, Cullis B, Azanza F, Martin D, Kelly A, McIntyre L, Schmidt A, Ma W, Nath Z, Kutty I, Leyne E, Rampling L, Quail K, Morell M (2009) Genetic control of wheat quality: interactions between chromosomal regions determining protein content and composition, dough rheology, and sponge and dough baking properties. Theor Appl Genet 118:1519–1537PubMedCrossRefGoogle Scholar
  19. Marchylo B, Kruger J, Hatcher D (1989) Quantitative reversed-phase high-performance liquid chromatographic analysis of wheat storage proteins as a potential quality prediction tool. J Cereal Sci 9(2):113–130CrossRefGoogle Scholar
  20. Margiotta B, Urbano M, Colaprico G, Johansson E, Buonocore F, D'Ovidio R, Lafiandra D (1996) Detection of y-type subunit at the Glu-A1 locus in some Swedish bread wheat lines. J Cereal Sci 23:203–211CrossRefGoogle Scholar
  21. McKendry AL, McVetty P, Evans L (1995) Selection criteria for combining high grain yield and high grain protein concentration in bread wheat. Crop Sci 35(6):1597–1602CrossRefGoogle Scholar
  22. Oury F-X, Godin C (2007) Yield and grain protein concentration in bread wheat: how to use the negative relationship between the two characters to identify favourable genotypes? Euphytica 157(1–2):45–57CrossRefGoogle Scholar
  23. Oury F-X, Berard P, Brancourt-Hulmel M, Heumez E, Pluchard P, Rousset M, Giraud A (2003) Yield and grain protein concentration in bread wheat: a review and a study of multi-annual data from a French breeding program [Triticum aestivum L.]. J Genet Breed 57(1):59–68Google Scholar
  24. Oury F-X, Chiron H, Faye A, Gardet O, Giraud A, Heumez E, Charmet G (2010) The prediction of bread wheat quality: joint use of the phenotypic information brought by technological tests and the genetic information brought by HMW and LMW glutenin subunits. Euphytica 171(1):87CrossRefGoogle Scholar
  25. Payne PI (1987) Genetics of wheat storage proteins and the effect of allelic variation on breadmaking quality. Ann Rev Plant Physiol 38(1):141–153CrossRefGoogle Scholar
  26. Penfield MP, Campbell AM (1990) Experimental food science. Academic Press, CambridgeGoogle Scholar
  27. Peng Y, Yu K, Zhang Y, Islam S, Sun D, Ma W (2015) Two novel Y-Type high-molecular weight glutenin genes in Chinese wheat landraces of the Yangtze-River region. PLoS ONE 10(11):e0142348PubMedPubMedCentralCrossRefGoogle Scholar
  28. Roy N, Islam S, Ma J, Lu M, Torok K, Tomoskozi S, Bekes F, Lafiandra D, Appels R, Ma W (2018) Expressed Ay HMW glutenin subunit in Australian wheat cultivars indicates a positive effect on wheat quality. J Cereal Sci 79:494–500.  https://doi.org/10.1016/j.jcs.2017.12.009 CrossRefGoogle Scholar
  29. She M, Ye X, Yan Y, Howit C, Belgard M, Ma W (2011) Gene networks in the synthesis and deposition of protein polymers during grain development of wheat. Funct Integr Genom 11:23–35CrossRefGoogle Scholar
  30. Shewry PR, Halford NG, Tatham AS (1992) High-molecular weight subunits of wheat glutenin. J Cereal Sci 15(2):105–120CrossRefGoogle Scholar
  31. Sliwinski E, Kolster P, Van Vliet T (2004) On the relationship between large-deformation properties of wheat flour dough and baking quality. J Cereal Sci 39(2):231–245CrossRefGoogle Scholar
  32. Uauy C, Distelfeld A, Fahima T, Blechl A, Dubcovsky J (2006) A NAC gene regulating senescence improves grain protein, zinc, and iron content in wheat. Science 314(5803):1298–1301PubMedPubMedCentralCrossRefGoogle Scholar
  33. Vasil IK, Anderson OD (1997) Genetic engineering of wheat gluten. Trends Plant Sci 2(8):292–297CrossRefGoogle Scholar
  34. Vasil IK, Bean S, Zhao J, McCluskey P, Lookhart G, Zhao H-P, Altpeter F, Vasil V (2001) Evaluation of baking properties and gluten protein composition of field grown transgenic wheat lines expressing high molecular weight glutenin gene 1Ax1. J Plant Physiol 158(4):521–528CrossRefGoogle Scholar
  35. Vawser M, Cornish GB (2004) Over-expression of HMW glutenin subunit Glu-B1 7x in hexaploid wheat varieties (Triticum aestivum). Aust J Agric Res 55(5):577–588CrossRefGoogle Scholar
  36. Wang S, Yu Z, Cao M, Shen X, Li N, Li X, Ma W, Weißgerber H, Zeller FJ, Hsam SLK, Yan Y (2013) Molecular mechanisms of HMW glutenin subunits from 1Sl genome of Aegilops longissima positively affecting wheat breadmaking quality. PLoS ONE 8(4):e58947PubMedPubMedCentralCrossRefGoogle Scholar
  37. Wang K, Islam S, Ma J, Anwar M, Chen J, Yan Y, Appels R, Ma W (2015) An improved MALDI-TOF mass spectrometry procedure and a novel DNA marker for identifying over-expressed Bx7 glutenin protein subunit in wheat. Hereditas 151(6):196–200CrossRefGoogle Scholar
  38. Weegels P, Hamer R, Schofield J (1996) Functional properties of wheat glutenin. J Cereal Sci 23(1):1–17CrossRefGoogle Scholar
  39. Yu Z, Islam S, She M, Diepeveen D, Zhang Y, Tang G, Zhang J, Juhasz A, Yang R, Ma W (2018) Wheat grain protein accumulation and polymerization mechanisms driven by nitrogen fertilization. Plant J 96(6):1160–2117PubMedCrossRefGoogle Scholar
  40. Yu Z, Peng Y, Islam S, She M, Lu M, Lafiandra D, Roy N, Juhasz A, Yan G, Ma W (2019) Molecular characterization and phylogenetic analysis of active y-type high molecular weight glutenin subunit genes at Glu-A1 locus in wheat. J Cereal Sci 86:9–14CrossRefGoogle Scholar
  41. Zaidel DA, Chin N, Yusof Y (2010) A review on rheological properties and measurements of Dough and gluten. J Appl Sci 10(20):2478–2490CrossRefGoogle Scholar
  42. Zhang H, Turner NC, Poole ML (2010) Source–sink balance and manipulating sink–source relations of wheat indicate that the yield potential of wheat is sink-limited in high-rainfall zones. Crop Pasture Sci 61(10):852–861CrossRefGoogle Scholar
  43. Zhang Y, Hu X, Islam S, She M, Peng Y, Yu Z, Wylie S, Juhasz A, Dowla M, Yang R, Zhang J, Wang X, Dell B, Chen X, Nevo E, Sun D, Ma W (2018) New insights into the evolution of wheat avenin-like proteins in wild emmer wheat (Triticum dicoccoides). Proc Natl Acad Sci 115(52):13312–13317PubMedCrossRefGoogle Scholar
  44. Zuwariah I, Noor A (2009) Physicochemical properties of wheat breads substituted with banana flour and modified banana flour. J Trop Agric Food Sci 37(1):33–42Google Scholar

Copyright information

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

Authors and Affiliations

  1. 1.Australia-China Joint Centre for Wheat Improvement, State Agriculture Biotechnology CentreMurdoch UniversityPerthAustralia
  2. 2.Australian Grain TechnologiesNarrabriAustralia
  3. 3.Department of Sciences and Technology for Agriculture, Forest, Environment and EnergyTuscia UniversityViterboItaly
  4. 4.Ag RD&IP Consult P/LCanberraAustralia

Personalised recommendations