Skip to main content
Log in

Marker-trait association identified candidate starch biosynthesis pathway genes for starch and amylose–lipid complex gelatinization in wheat (Triticum aestivum L.)

  • Published:
Euphytica Aims and scope Submit manuscript

Abstract

During processing of wheat flour, its starch component undergoes gelatinization, an important physicochemical property, affecting cooking and nutrition quality of food products. Genetic loci controlling gelatinization properties of starch and amylose–lipid complex is unknown in wheat. In this study gelatinization properties were measured in a set of 226 wheat varieties using differential scanning calorimetry and their thermograms identified two endothermic peaks: first peak of starch gelatinization and second peak of amylose–lipid complex. The four parameters (onset temp, peak temp, conclusion temp, and enthalpy) of both gelatinization peaks showed wide variation among the varieties. Marker-trait association studies using the genotyping data of 258 SSRs and gelatinization data on the wheat varieties identified 24 and 6 markers associated for starch and amylose–lipid complex gelatinization properties, respectively. Using wheat reference genome sequence and LD decay information, 12 starch biosynthesis pathway genes were identified, which were co-located within 50 Mb of the associated markers. Four out of 12 genes (SSIV, SBEIIb, PHO, and PUL) were located within 5.2 Mb. Out of 24, 17 markers were involved in epistatic interactions. These markers are novel for wheat starch gelatinization properties, and would be useful for gene discovery and marker assisted selection for the improvement of starch quality in wheat.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Alcazar-Alay SC, Meireles MAA (2015) Physicochemical properties, modifications and applications of starches from different botanical sources. Food Sci Technol 35(2):215–236

    Article  Google Scholar 

  • Bao JS, Corke H, Sun M (2006) Microsatellites, single nucleotide polymorphisms and a sequence tagged site in starch-synthesizing genes in relation to starch physicochemical properties in nonwaxy rice (Oryza sativa L.). Theor Appl Genet 113(7):1185–1196

    Article  CAS  PubMed  Google Scholar 

  • Bao JS, Wu YR, Hu B, Wu P, Cui HR, Shu QY (2002) QTL for rice grain quality based on a DH population derived from parents with similar apparent amylose content. Euphytica 128(3):317–324

    Article  CAS  Google Scholar 

  • Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc 57(1):289–300

    Google Scholar 

  • Bhupender SK, Rajneesh B, Baljeet SY (2013) Physicochemical, functional, thermal and pasting properties of starches isolated from pearl millet cultivars. Int Food Res J 20(4):1555–1561

    Google Scholar 

  • Birt DF, Boylston T, Hendrich S, Jane JL, Hollis J, Li L, Schalinske K (2013) Resistant starch: promise for improving human health. Adv Nutr 4(6):587–601

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bland JM, Altman DG (1995) Multiple significance tests: the Bonferroni method. BMJ 310(6973):170

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Breseghello F, Sorrells ME (2006b) Association analysis as a strategy for improvement of quantitative traits in plants. Crop Sci 46(3):1323–1330

    Article  Google Scholar 

  • Breseghello F, Sorrells ME (2006a) Association mapping of kernel size and milling quality in wheat (Triticum aestivum L.) cultivars. Genetics 172(2):1165–1177

    Article  PubMed  PubMed Central  Google Scholar 

  • Breseghello F, Sorrells ME (2007) QTL analysis of kernel size and shape in two hexaploid wheat mapping populations. Field Crops Res 101(2):172–179

    Article  Google Scholar 

  • Ciesla K, Eliasson AC (2002) Influence of gamma radiation on potato starch gelatinization studied by differential scanning calorimetry. Radiat Phys Chem 64(2):137–148

    Article  CAS  Google Scholar 

  • Cooke D, Gidley MJ (1992) Loss of crystalline and molecular order during starch gelatinisation: origin of the enthalpic transition. Carbohydr Res 227:103–112

    Article  CAS  Google Scholar 

  • Coral DF, Pineda-Gómez P, Rosales-Rivera A, Rodriguez-Garcia ME (2009) Determination of the gelatinization temperature of starch presented in maize flours. J Phys Conf Ser 167(1):012057

    Article  CAS  Google Scholar 

  • Covarrubias-Pazaran G (2018) Quantitative genetics using the Sommer package. R Found. Stat. Comput., Vienna. https://cran.r-project.org/web/packages/sommer/vignettes/sommer.pdf. Accessed 22 Mar 2018

  • Deepa G, Singh V, Naidu KA (2010) A comparative study on starch digestibility, glycemic index and resistant starch of pigmented (‘Njavara’ and ‘Jyothi’) and a non-pigmented (‘IR 64’) rice varieties. J Food Sci Technol 47(6):644–649

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Edwards MA, Osborne BG, Henry RJ (2008) Effect of endosperm starch granule size distribution on milling yield in hard wheat. J Cereal Sci 48(1):180–192

    Article  CAS  Google Scholar 

  • Eliasson AC (1994) Interactions between starch and lipids studied by DSC. Thermo Chim Acta 246(2):343–356

    Article  CAS  Google Scholar 

  • Ellis RP, Cochrane MP, Dale MFB, Duffus CM, Lynn A, Morrison IM, Tiller SA (1998) Starch production and industrial use. J Sci Food Agric 77(3):289–311

    Article  CAS  Google Scholar 

  • Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14(8):2611–2620

    Article  CAS  PubMed  Google Scholar 

  • Faridi HA, Rubenthaler GL (1984) Effect of baking time and temperature on bread quality, starch gelatinization and staling of Egyptian Balady bread. Cereal Chem 61(2):151–154

    CAS  Google Scholar 

  • Ferng LH, Chen SH, Lin YA (2011) Effect of steam jet cooking on the destruction of corn starches. Procedia Food Sci 1:1295–1300

    Article  CAS  Google Scholar 

  • Flint-Garcia SA, Thuillet AC, Yu J, Pressoir G, Romero SM, Mitchell SE, Buckler ES (2005) Maize association population: a high-resolution platform for quantitative trait locus dissection. Plant J 44(6):1054–1064

    Article  CAS  PubMed  Google Scholar 

  • Gonzalez JR, Armengol L, Sole X, Guino E, Mercader JM, Estivill X, Moreno V (2007) SNPassoc: an R package to perform whole genome association studies. Bioinformatics 23(5):654–655

    Article  CAS  Google Scholar 

  • Gupta PK, Kulwal PL, Jaiswal V (2019) Association mapping in plants in the post-GWAS genomics era. Adv Genet 104:75–154

    Article  PubMed  Google Scholar 

  • Gupta PK, Rustgi S, Kulwal PL (2005) Linkage disequilibrium and association studies in higher plants: present status and future prospects. Plant Mol Biol 57(4):461–485

    Article  CAS  PubMed  Google Scholar 

  • Hao C, Wang L, Ge H, Dong Y, Zhang X (2011) Genetic diversity and linkage disequilibrium in Chinese bread wheat (Triticum aestivum L.) revealed by SSR markers. PLoS ONE 6(2):e17279

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hoove R, Vasanthan T (1993) The effect of annealing on the physicochemical properties of wheat, oat, potato and lentil starches. J Food Biochem 17(5):303–325

    Article  Google Scholar 

  • Hoover R, Li YX, Hynes G, Senanayake N (1997) Physicochemical characterization of mung bean starch. Food Hydrocoll 11(4):401–408

    Article  CAS  Google Scholar 

  • Jaiswal V, Gahlaut V, Meher PK, Mir RR, Jaiswal JP, Rao AR, Gupta PK (2016) Genome wide single locus single trait, multi-locus and multi-trait association mapping for some important agronomic traits in common wheat (T. aestivum L.). PLoS ONE 11(7):e0159343

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Jaiswal V, Mir RR, Mohan A, Balyan HS, Gupta PK (2012) Association mapping for pre-harvest sprouting tolerance in common wheat (Triticuma estivum L.). Euphytica 188(1):89–102

    Article  CAS  Google Scholar 

  • Jannink JL, Bink MC, Jansen RC (2001) Using complex plant pedigrees to map valuable genes. Trends Plant Sci 6(8):337–342

    Article  CAS  PubMed  Google Scholar 

  • Jin H, Wen W, Liu J, Zhai S, Zhang Y, Yan J, He Z (2016) Genome-wide QTL mapping for wheat processing quality parameters in a Gaocheng 8901/Zhoumai 16 recombinant inbred line population. Front Plant Sci 7:1032

    PubMed  PubMed Central  Google Scholar 

  • Jugran AK, Bhatt ID, Rawal RS (2015) Identification of ISSR markers associated with valerenic acid content and antioxidant activity in Valeriana jatamansi Jones in the West Himalaya. Mol Breed 35(2):73

    Article  CAS  Google Scholar 

  • Jugran A, Rawat S, Dauthal P, Mondal S, Bhatt ID, Rawal RS (2013) Association of ISSR markers with some biochemical traits of Valeriana jatamansi Jones. Ind Crops Prod 44:671–676

    Article  CAS  Google Scholar 

  • Juliano BO (1999) Comparative nutritive value of various staple foods. Food Rev Int 15(4):399–434

    Article  CAS  Google Scholar 

  • Kharabian-Masouleh A, Waters DL, Reinke RF, Ward R, Henry RJ (2012) SNP in starch biosynthesis genes associated with nutritional and functional properties of rice. Sci Rep 2:557

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lang NT, Buu BC (2004) Quantitative analysis on amylose content by DNA markers through backcross populations of rice (Oryza sativa L.). OMonRice 12:12–17

    Google Scholar 

  • Madhawan A, Sharma A, Bhandawat A, Rahim MS, Kumar P, Mishra A et al (2020) Identification and characterization of long non-coding RNAs regulating resistant starch biosynthesis in bread wheat (Triticum aestivum L.). Genomics 3065–3074

  • Massaux C, Sindic M, Lenartz J, Sinnaeve G, Bodson B, Falisse A, Deroanne C (2008) Variations in physicochemical and functional properties of starches extracted from European soft wheat (Triticum aestivum L.): The importance to preserve the varietal identity. Carbohydr Polym 71(1):32–41

    Article  CAS  Google Scholar 

  • Morrison WR, Tester RF (1993) Some properties of the four major polysaccharide fractions in cereal starches. Conference paper. Chemistry in Australia (Australia)

  • Okumus BN, Tacer-Caba Z, Kahraman K, Nilufer-Erdil D (2018) Resistant starch type V formation in brown lentil (Lens culinaris Medikus) starch with different lipids/fatty acids. Food Chem 240:550–558

    Article  CAS  PubMed  Google Scholar 

  • Paton DAVID (1987) Differential scanning calorimetry of oat starch pastes. Cereal Chem 64(6):394–399

    CAS  Google Scholar 

  • Peng M, Gao M, Abdel-Aal ES, Hucl P, Chibbar RN (1999) Separation and characterization of A-and B-type starch granules in wheat endosperm. Cereal Chem 76(3):375–379

    Article  CAS  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000a) Inference of population structure using multilocus genotype data. Genetics 155(2):945–959

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pritchard JK, Stephens M, Rosenberg NA, Donnelly P (2000b) Association mapping in structured populations. Am J Hum Genetics 67(1):170–181

    Article  CAS  Google Scholar 

  • Rahim MS, Sharma H, Parveen A, Roy JK (2018) Trait mapping approaches through association analysis in plants. In: Plant genetics and molecular biology. Springer, Cham, pp 83–108 (2018)

  • Rahman S, Li Z, Batey I, Cochrane MP, Appels R, Morell M (2000) Genetic alteration of starch functionality in wheat. J Cereal Sci 31(1):91–110

    Article  CAS  Google Scholar 

  • Ramírez-Miranda M, Ribotta PD, Silva-González AZZ, Salgado-Cruz MDLP, Andraca-Adame JA, Chanona-Pérez JJ, Calderón-Domínguez G (2017) Morphometric and crystallinity changes on jicama starch (Pachyrizus erosus) during gelatinization and their relation with in vitro glycemic index. Starch Stärke 69(7–8):1600281

    Article  CAS  Google Scholar 

  • Ravel C, Martre P, Romeuf I, Dardevet M, El-Malki R, Bordes J, 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(4):2133–2144

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Roy JK, Smith KP, Muehlbauer GJ, Chao S, Close TJ, Steffenson BJ (2010) Association mapping of spot blotch resistance in wild barley. Mol Breeding 26(2):243–256

    Article  Google Scholar 

  • Sandhu KS, Singh N (2007) Some properties of corn starches II: Physicochemical, gelatinization, retrogradation, pasting and gel textural properties. Food Chem 101(4):1499–1507

    Article  CAS  Google Scholar 

  • Satbhai SB, Setzer C, Freynschlag F, Slovak R, Kerdaffrec E, Busch W (2017) Natural allelic variation of FRO2 modulates Arabidopsis root growth under iron deficiency. Nat Commun 8:15603

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shetty RM, Lineback DR, Seib PA (1974) Determining the degree of starch gelatinization. Cereal Chem 51:364–375

    CAS  Google Scholar 

  • Singh J, Dartois A, Kaur L (2010) Starch digestibility in food matrix: a review. Trends Food Sci Technol 21(4):168–180

    Article  CAS  Google Scholar 

  • Singh A, Kumar P, Sharma M, Tuli R, Dhaliwal HS, Chaudhury A, Roy J (2015) Expression patterns of genes involved in starch biosynthesis during seed development in bread wheat (Triticum aestivum). Mol Breeding 35(9):184

    Article  CAS  Google Scholar 

  • Singh N, Singh J, Kaur L, Sodhi NS, Gill BS (2003) Morphological, thermal and rheological properties of starches from different botanical sources. Food Chem 81(2):219–231

    Article  CAS  Google Scholar 

  • Somers DJ, Isaac P, Edwards K (2004) A high-density microsatellite consensus map for bread wheat (Triticum aestivum L.). Theor Appl Genet 109(6):1105–1114

    Article  CAS  PubMed  Google Scholar 

  • Steffenson BJ, Olivera P, Roy JK, Jin Y, Smith KP, Muehlbauer GJ (2007) A walk on the wild side: mining wild wheat and barley collections for rust resistance genes. Aust J Agric Res 58(6):532–544

    Article  Google Scholar 

  • Stich B, Möhring J, Piepho HP, Heckenberger M, Buckler ES, Melchinger AE (2008) Comparison of mixed-model approaches for association mapping. Genetics 178(3):1745–1754

    Article  PubMed  PubMed Central  Google Scholar 

  • Tako M, Tamaki Y, Teruya T, Takeda Y (2014) The principles of starch gelatinization and retrogradation. Food Nutr Sci 5(03):280

    Google Scholar 

  • Tanaka N, Fujita N, Nishi A, Satoh H, Hosaka Y, Ugaki M, Nakamura Y (2004) The structure of starch can be manipulated by changing the expression levels of starch branching enzyme IIb in rice endosperm. Plant Biotechnol J 2(6):507–516

    Article  CAS  PubMed  Google Scholar 

  • Varriano-Marston E, Ke V, Huang G, Ponte J (1980) Comparison of methods to determine starch gelatinization in bakery foods. Cereal Chem 57(4):242–248

    CAS  Google Scholar 

  • Wang S, Copeland L (2013) Molecular disassembly of starch granules during gelatinization and its effect on starch digestibility: a review. Food Funct 4(11):1564–1580

    Article  CAS  PubMed  Google Scholar 

  • Wang S, Li C, Copeland L, Niu Q, Wang S (2015) Starch retrogradation: a comprehensive review. Compr Rev Food Sci Food Saf 14(5):568–585

    Article  CAS  Google Scholar 

  • Wang FF, Liu TT, Li QF, An YL, Xie CP, Sun X, Chen JS (2017) QTL mapping of the pasting properties of wheat flour treated by papain digestion. Starch Starke 69(3–4):1600077

    Article  CAS  Google Scholar 

  • Wani AA, Singh P, Shah MA, Wani IA, Gotz A, Schott M, Zacherl C (2013) Physico-chemical, thermal and rheological properties of starches isolated from newly released rice cultivars grown in Indian temperate climates. LWT Food Sci Technol 53(1):176–183

    Article  CAS  Google Scholar 

  • Wani IA, Sogi DS, Wani AA, Gill BS, Shivhare US (2010) Physico-chemical properties of starches from Indian kidney bean (Phaseolus vulgaris) cultivars. Int J Food Sci Technol 45(10):2176–2185

    Article  CAS  Google Scholar 

  • Wen W, Mei H, Feng F, Yu S, Huang Z, Wu J, Luo L (2009) Population structure and association mapping on chromosome 7 using a diverse panel of Chinese germplasm of rice (Oryza sativa L.). Theor Appl Genet 119(3):459–470

    Article  PubMed  Google Scholar 

  • Xu F, Zhang G, Tong C, Sun X, Corke H, Sun M, Bao J (2013) Association mapping of starch physicochemical properties with starch biosynthesizing genes in waxy rice (Oryza sativa L.). J Agric Food Chem 61(42):10110–10117

    Article  CAS  PubMed  Google Scholar 

  • Yan CJ, Tian ZX, Fang YW, Yang YC, Li J, Zeng SY, Gu MH (2011) Genetic analysis of starch paste viscosity parameters in glutinous rice (Oryza sativa L.). Theor Appl Genet 122(1):63–76

    Article  CAS  PubMed  Google Scholar 

  • Yan CJ, Xu CW, Yi CD, Liang GH, Zhu LH, Gu MH (2001) Genetic analysis of gelatinization temperature in rice via microsatellite (SSR) markers. Yi chuanxuebao Acta genetica Sinica 28(11):1006–1011

    CAS  PubMed  Google Scholar 

  • Yang F, Chen Y, Tong C, Huang Y, Xu F, Li K, Bao J (2014) Association mapping of starch physicochemical properties with starch synthesis-related gene markers in nonwaxy rice (Oryza sativa L.). Mol Breeding 34(4):1747–1763

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We would like to thank National Agri-Food Biotechnology Institute (NABI), Department of Biotechnology, Government of India, for providing funding and facilities to carry out this work. MSR acknowledges Central University of Punjab, Bathinda, India for PhD registration. We acknowledge Indian Institute of Wheat and Barley Research, Karnal, Haryana, India for providing wheat germplasm. We acknowledge DeLCON (DBT-electronic library consortium), Gurugram, India, for the online access to e-resources.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Joy Roy.

Ethics declarations

Conflict of interest

The authors declare that they have no potential conflict of interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

10681_2020_2688_MOESM1_ESM.tif

Fig. S1. Adaptation regions of bread wheat varieties clustered in 8-sub-populations (Q1, Q2, Q3, Q4, Q5, Q6, Q7, & Q8) in India: The outline (political) map India showing 6 adapted (growing) regions of Indian wheat varieties used in this study and their sub-population classifications (Q1 to Q8) indicated by different color symbols. (TIFF 1578 kb)

10681_2020_2688_MOESM2_ESM.tif

Fig. S2. Manhattan plots representing the chromosome-wise distribution of the association data of starch quality traits of year 2018 (a) and 2017 (b). The X-axis represents all 21 chromosomes (1A to 7D) of bread wheat (T. aestivum L.) and Y-axis the –log10 (P) values of SSRs. The significant (P ≤ 0.05) associated SSRs are represented by dots above the red horizontal line. The color of dots corresponds to different starch quality traits: SGTo (starch gelatinization onset temp), SGTp (starch gelatinization peak temp), SGTc (starch gelatinization conclusion temp), SGTr (starch gelatinization range temp), SGTe (starch gelatinization enthalpy), ALCGTo (Amylose–lipid complex gelatinization onset temp), ALCGTp (Amylose–lipid complex gelatinization peak temp), ALCGTc (Amylose–lipid complex gelatinization conclusion temp), ALCGTr (Amylose–lipid complex gelatinization range temp), and ALCGTe (Amylose–lipid complex gelatinization enthalpy). (TIFF 184 kb)

Supplementary material 3 (XLSX 20 kb)

Supplementary material 4 (XLSX 17 kb)

Supplementary material 5 (XLSX 21 kb)

Supplementary material 6 (XLSX 220 kb)

Supplementary material 7 (DOCX 17 kb)

Supplementary material 8 (XLSX 424 kb)

Supplementary material 9 (XLSX 196 kb)

Supplementary material 10 (DOCX 18 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Rahim, M.S., Mishra, A., Katyal, M. et al. Marker-trait association identified candidate starch biosynthesis pathway genes for starch and amylose–lipid complex gelatinization in wheat (Triticum aestivum L.). Euphytica 216, 151 (2020). https://doi.org/10.1007/s10681-020-02688-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s10681-020-02688-6

Keywords

Navigation