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Overexpressing wheat low-molecular-weight glutenin subunits in rice (Oryza sativa L. japonica cv. Koami) seeds

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Abstract

Genes encoding wheat low-molecular-weight glutenin subunits (LMW-GSs) that confer dough strength and extensibility were previously identified from Korean wheat cultivars. To improve low viscoelasticity of rice (Oryza sativa L.) dough caused by the lack of seed storage proteins comparable to wheat gluten, two genes, LMW03 and LMW28, encoding LMW-GSs are cloned from Korean wheat cultivar Jokyoung. The LMW genes are inserted into binary vectors under the control of the rice endosperm-specific Glu-B1 promoter. Transgenic rice plants expressing LMW03 or LMW28 in their seeds are generated using Agrobacterium-mediated transformation. The expression of recombinant wheat LMW-GS in the transgenic rice seeds was confirmed by SDS-PAGE and immunoblot analysis. Their accumulation in the endosperm and aleurone layers of rice seeds was observed through in situ immuno-hybridization.

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References

  • Altpeter F, Popelka JC, Wieser H (2004) Stable expression of 1Dx5 and 1Dy10 high-molecular-weight glutenin subunit genes in transgenic rye drastically increases the polymeric glutelin fraction in rye flour. Plant Mol Biol 54(6):783–792. https://doi.org/10.1007/s11103-004-0122-5

    Article  CAS  PubMed  Google Scholar 

  • Beom H-R, Kim JS, Jang Y-R, Lim S-H, Kim C-K, Lee CK, Lee J-Y (2018) Proteomic analysis of low-molecular-weight glutenin subunits and relationship with their genes in a common wheat variety. 3 Biotech 8(1):56

    Article  Google Scholar 

  • Cameron-Mills V, Brandt A (1988) A gamma-hordein gene. Plant Mol Biol (4):449–461. https://doi.org/10.1007/BF00039026

    Article  CAS  Google Scholar 

  • Cho K, Lee H-J, Jo Y-M, Lim S-H, Rakwal R, Lee J-Y, Kim Y-M (2016) RNA interference-mediated simultaneous suppression of seed storage proteins in rice grains. Front Plant Sci 7:1624

    PubMed  PubMed Central  Google Scholar 

  • Cho K, Beom H-R, Jang Y-R, Altenbach S, Vensel WH, Simon-Buss A, Lim S-H, Kim MG, Kim JS, Lee J-Y (2018) Proteomic profiling and epitope analysis of the complex α-, γ-and ω-gliadin families in a commercial bread wheat. Front Plant Sci 9:818

    Article  Google Scholar 

  • Cornish GB, Bekes F, Allen H, Martin D (2001) Flour proteins linked to quality traits in an Australian doubled haploid wheat population. Aust J Agric Res 52(12):1339–1348

    Article  CAS  Google Scholar 

  • D’Ovidio R, Masci S (2004) The low-molecular-weight glutenin subunits of wheat gluten. J Cereal Sci 39(3):321–339

    Article  Google Scholar 

  • Delcour JA, Joye IJ, Pareyt B, Wilderjans E, Brijs K, Lagrain B (2012) Wheat gluten functionality as a quality determinant in cereal-based food products. Annu Rev Food Sci Technol 3:469–492

    Article  CAS  Google Scholar 

  • Dong L, Zhang X, Liu D, Fan H, Sun J, Zhang Z, Qin H, Li B, Hao S, Li Z (2010) New insights into the organization, recombination, expression and functional mechanism of low molecular weight glutenin subunit genes in bread wheat. PLoS One 5(10):e13548

    Article  Google Scholar 

  • Gadaleta A, Blechl AE, Nguyen S, Cardone MF, Ventura M, Quick JS, Blanco A (2008) Stably expressed d-genome-derived HMW glutenin subunit genes transformed into different durum wheat genotypes change dough mixing properties. Mol Breed 22(2):267–279. https://doi.org/10.1007/s11032-008-9172-8

    Article  CAS  Google Scholar 

  • Gao S, Gu YQ, Wu J, Coleman-Derr D, Huo N, Crossman C, Jia J, Zuo Q, Ren Z, Anderson OD, Kong X (2007) Rapid evolution and complex structural organization in genomic regions harboring multiple prolamin genes in the polyploid wheat genome. Plant Mol Biol 65(1–2):189–203. https://doi.org/10.1007/s11103-007-9208-1

    Article  CAS  PubMed  Google Scholar 

  • Gupta RB, Shepherd K (1990) Two-step one-dimensional SDS-PAGE analysis of LMW subunits of glutelin. Theor Appl Genet 80(1):65–74

    Article  CAS  Google Scholar 

  • Gupta RB, Singh NK, Shepherd K (1989) The cumulative effect of allelic variation in LMW and HMW glutenin subunits on dough properties in the progeny of two bread wheats. Theor Appl Genet 77(1):57–64

    Article  CAS  Google Scholar 

  • Jeong N, Jeon S-H, Kim D-Y, Lee C, Ok H-C, Park K-D, Hong H-C, Lee S-S, Moon J-K, Park S-K (2016) Development of marker-free TaGlu-Ax1 transgenic rice harboring a wheat high-molecular-weight glutenin Subunit (HMW-GS) protein. J Life Sci 26(10):1121–1129

    Article  Google Scholar 

  • Jo Y-M, Cho K, Lee H-J, Lim S-H, Kim JS, Kim Y-M, Lee J-Y (2017) Cellular localization of wheat high molecular weight glutenin subunits in transgenic rice grain. Int J Mol Sci 18(11):2458

    Article  Google Scholar 

  • Karimi M, Inze D, Depicker A (2002) GATEWAY((TM)) vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci 7(5):193–195. https://doi.org/10.1016/S1360-1385(02)02251-3

    Article  CAS  PubMed  Google Scholar 

  • Kawakatsu T, Yamamoto MP, Hirose S, Yano M, Takaiwa F (2008) Characterization of a new rice glutelin gene GluD-1 expressed in the starchy endosperm. J Exp Bot 59(15):4233–4245. https://doi.org/10.1093/jxb/ern265

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kawakatsu T, Hirose S, Yasuda H, Takaiwa F (2010) Reducing rice seed storage protein accumulation leads to changes in nutrient quality and storage organelle formation. Plant Physiol 154(4):1842–1854. https://doi.org/10.1104/pp.110.164343

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim Y-M, Lee J-Y, Yoon U-H, Choi S-B, Ha S-H, Lim S-H (2011) New design of rice seed storage proteins. J Plant Biotechnol 38(4):263–271

    Article  Google Scholar 

  • Kim Y-M, Lee J-Y, Lee T, Lee Y-H, Kim S-H, Kang S-H, Yoon U-H, Ha S-H, Lim S-H (2012) The suppression of the glutelin storage protein gene in transgenic rice seeds results in a higher yield of recombinant protein. Plant Biotechnol Rep 6(4):347–353

    Article  Google Scholar 

  • Koehler P, Wieser H (2013) Chemistry of cereal grains. In: Gobbetti M, Gänzle M (eds) Handbook on sourdough biotechnology. Springer, Boston, pp 11–45. https://doi.org/10.1007/978-1-4614-5425-0_2

    Chapter  Google Scholar 

  • Kohler P, Belitz HD, Wieser H (1993) Disulphide bonds in wheat gluten: further cystine peptides from high molecular weight (HMW) and low molecular weight (LMW) subunits of glutenin and from gamma-gliadins. Z Lebensm Unters Forsch 196(3):239–247

    Article  CAS  Google Scholar 

  • Kreis M, Forde BG, Rahman S, Miflin BJ, Shewry PR (1985) Molecular evolution of the seed storage proteins of barley, rye and wheat. J Mol Biol 183(3):499–502

    Article  CAS  Google Scholar 

  • Lee J-Y, Kim Y-T, Kim B-M, Lee J-H, Lim S-H, Ha S-H, Ahn S-N, Nam M-H, Kim Y-M (2010) Cloning of low-molecular-weight glutenin subunit genes and identification of their protein products in common wheat (Triticum aestivum L.). Korean J Breed Sci 42(5):547–554

    Google Scholar 

  • Lee HJ, Jo YM, Lee JY, Lim SH, Kim YM (2015) Lack of globulin synthesis during seed development alters accumulation of seed storage proteins in rice. Int J Mol Sci 16(7):14717–14736. https://doi.org/10.3390/ijms160714717

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee JY, Beom HR, Altenbach SB, Lim SH, Kim YT, Kang CS, Yoon UH, Gupta R, Kim ST, Ahn SN, Kim YM (2016) Comprehensive identification of LMW-GS genes and their protein products in a common wheat variety. Funct Integr Genom 16(3):269–279. https://doi.org/10.1007/s10142-016-0482-3

    Article  CAS  Google Scholar 

  • Motoyama T, Maruyama N, Amari Y, Kobayashi K, Washida H, Higasa T, Takaiwa F, Utsumi S (2009) α′ Subunit of soybean β-conglycinin forms complex with rice glutelin via a disulphide bond in transgenic rice seeds. J Exp Bot 60(14):4015–4027

    Article  CAS  Google Scholar 

  • Okita TW, Cheesbrough V, Reeves CD (1985) Evolution and heterogeneity of the alpha-/beta-type and gamma-type gliadin DNA sequences. J Biol Chem 260(13):8203–8213

    CAS  PubMed  Google Scholar 

  • Orsi A, Sparvoli F, Ceriotti A (2001) Role of individual disulfide bonds in the structural maturation of a low molecular weight glutenin subunit. J Biol Chem 276(34):32322–32329

    Article  CAS  Google Scholar 

  • Oszvald M, Jenes B, Tömösközi S, Bekes F, Tamas L (2007) Expression of the 1D × 5 high molecular weight glutenin subunit protein in transgenic rice. Cereal Res Commun 35(4):1543–1549

    Article  CAS  Google Scholar 

  • Oszvald M, Balázs G, Pólya S, Tömösközi S, Békés F, Tamás L (2013) Wheat storage proteins in transgenic rice endosperm. J Agric Food Chem 61(31):7606–7614

    Article  CAS  Google Scholar 

  • Park S-K, Shin D, Hwang W-H, Hur Y-J, Kim T-H, Oh S-Y, Cho J-H, Han S-I, Lee S-S, Nam M-H (2014) Development of marker-free transgenic rice expressing the wheat storage protein, Glu-1Dy10, for increasing quality processing of bread and noodles. J Life Sci 24(6):618–625

    Article  Google Scholar 

  • Payne PI (1987) Genetics of wheat storage proteins and the effect of allelic variation on bread-making quality. Annu Rev Plant Physiol 38(1):141–153

    Article  CAS  Google Scholar 

  • Popineau Y, Deshayes G, Lefebvre J, Fido R, Tatham AS, Shewry PR (2001) Prolamin aggregation, gluten viscoelasticity, and mixing properties of transgenic wheat lines expressing 1Ax and 1Dx high molecular weight glutenin subunit transgenes. J Agric Food Chem 49(1):395–401

    Article  CAS  Google Scholar 

  • Qian D, Tian L, Qu L (2015) Proteomic analysis of endoplasmic reticulum stress responses in rice seeds. Sci Rep 5:14255

    Article  CAS  Google Scholar 

  • Qu LQ, Xing YP, Liu WX, Xu XP, Song YR (2008) Expression pattern and activity of six glutelin gene promoters in transgenic rice. J Exp Bot 59(9):2417–2424. https://doi.org/10.1093/jxb/ern110

    Article  CAS  PubMed Central  Google Scholar 

  • Rasheed A, Xia XC, Yan YM, Appels R, Mahmood T, He ZH (2014) Wheat seed storage proteins: advances in molecular genetics, diversity and breeding applications. J Cereal Sci 60(1):11–24. https://doi.org/10.1016/j.jcs.2014.01.020

    Article  CAS  Google Scholar 

  • Rooke L, Bekes F, Fido R, Barro F, Gras P, Tatham AS, Barcelo P, Lazzeri P, Shewry PR (1999) Overexpression of a gluten protein in transgenic wheat results in greatly increased dough strength. J Cereal Sci 30(2):115–120. doi:https://doi.org/10.1006/jcrs.1999.0265

    Article  CAS  Google Scholar 

  • Shin M (2009) Rice-processed food. Food Sci Ind 42:2–18

    Google Scholar 

  • Shyur L-F, Wen T-N, Chen C-S (1994) Purification and characterization of rice prolamins. Bot Bull Acad Sin 35:65–71

    CAS  Google Scholar 

  • Sivaramakrishnan HP, Senge B, Chattopadhyay PK (2004) Rheological properties of rice dough for making rice bread. J Food Eng 62(1):37–45. https://doi.org/10.1016/S0260-8774(03)00169-9

    Article  Google Scholar 

  • Takaiwa F, Wakasa Y, Takagi H, Hiroi T (2015) Rice seed for delivery of vaccines to gut mucosal immune tissues. Plant biotechnol J 13(8):1041–1055

    Article  CAS  Google Scholar 

  • Tosi P, Parker M, Gritsch CS, Carzaniga R, Martin B, Shewry PR (2009) Trafficking of storage proteins in developing grain of wheat. J Exp Bot 60(3):979–991

    Article  CAS  Google Scholar 

  • Wakasa Y, Yasuda H, Takaiwa F (2013) Secretory type of recombinant thioredoxin h induces ER stress in endosperm cells of transgenic rice. J Plant Physiol 170(2):202–210

    Article  CAS  Google Scholar 

  • Wang Y, Zhen S, Luo N, Han C, Lu X, Li X, Xia X, He Z, Yan Y (2016) Low molecular weight glutenin subunit gene Glu-B3h confers superior dough strength and breadmaking quality in wheat (Triticum aestivum L.). Sci Rep 6:27182

    Article  CAS  Google Scholar 

  • Xu JH, Messing J (2009) Amplification of prolamin storage protein genes in different subfamilies of the Poaceae. Theor Appl Genet 119(8):1397–1412. https://doi.org/10.1007/s00122-009-1143-x

    Article  CAS  PubMed  Google Scholar 

  • Yamagata H, Tanaka K (1986) The site of synthesis and accumulation of rice storage proteins. Plant Cell Physiol 27(1):135–145

    CAS  Google Scholar 

  • Zhang X, Jin H, Zhang Y, Liu D, Li G, Xia X, He Z, Zhang A (2012) Composition and functional analysis of low-molecular-weight glutenin alleles with Aroona near-isogenic lines of bread wheat. BMC Plant Biol 12:243. https://doi.org/10.1186/1471-2229-12-243

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang XF, Liu DC, Zhang JH, Jiang W, Luo GB, Yang WL, Sun JZ, Tong YP, Cui DQ, Zhang AM (2013) Novel insights into the composition, variation, organization, and expression of the low-molecular-weight glutenin subunit gene family in common wheat. J Exp Bot 64(7):2027–2040. https://doi.org/10.1093/jxb/ert070

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This work was supported by grants from the National Institute of Agricultural Science (RDA PJ012458) and the Next-Generation BioGreen 21 Program (RDA PJ013149 and RDA PJ013159), South Korea. This study was also supported by the Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Education (2016R1A6A3A11931182) to KC.

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  1. Kyoungwon Cho and Yeong-Min Jo contributed equally to this work.

Authors and Affiliations

  1. National Institute of Agricultural Science, RDA, Chonju, 54874, South Korea

    Kyoungwon Cho, Yeong-Min Jo, Sun-Hyung Lim, Joo Yeol Kim & Jong-Yeol Lee

  2. Department of Biotechnology, College of Agriculture and Life Sciences, Chonnam National University, Gwangju, 500-757, South Korea

    Kyoungwon Cho & Oksoo Han

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  1. Kyoungwon Cho
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  2. Yeong-Min Jo
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YMJ designed and conducted the experiments; KC conducted the experiments and wrote the manuscript; SHL, JYK, and OH contributed critical reading and revision of the manuscript; JYL contributed scientific advice and corrected the manuscript. All authors have read and approved the manuscript.

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Correspondence to Jong-Yeol Lee.

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Cho, K., Jo, YM., Lim, SH. et al. Overexpressing wheat low-molecular-weight glutenin subunits in rice (Oryza sativa L. japonica cv. Koami) seeds. 3 Biotech 9, 49 (2019). https://doi.org/10.1007/s13205-019-1579-x

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