Development of high-amylose maize (Zea mays L.) genotypes adapted to Indian conditions through molecular breeding
Arushi Arora A B , Deepak Bhamare A B C , Abhijit Kumar Das
A * , Shubhank Dixit A , Sreya Venadan A B C , Yathish K. R. C , Ramesh Kumar A , Dharam Paul A , J. C. Sekhar C , Sunil Neelam C , Sudip Nandi A , M. C. Kamboj D and Sujay Rakshit A E *
A
B
C
D
E
Abstract
Amylose is a type of resistant starch with numerous health benefits and industrial applications. Starch from maize (Zea mays L.) usually has an amylose content of ~25%.
The aim was to develop high-amylose maize genotypes suitable for human consumption and adapted to Indian conditions.
Marker-assisted backcross breeding was used to transfer the mutant ae1 allele from a high-amylose donor from the USA into the three parents (HKI 1344, HKI 1378, HKI 1348-6-2) of two high-yielding white maize hybrids (HM5 and HM12) grown in India.
In converted lines, amylose content was 40.40–58.10% of total kernel starch, compared with 22.25–26.39% in parents. The percentage increase in amylose content was 63.70–153.03%. There was a significant amount of background recovery in each backcross generation: 66.80–79% in BC1F1, 72.85–88.60% in BC2F1, and 84.45–93.70% in BC2F2. Overall, the total kernel starch content was reduced (by ~22%) in the ae1-introgressed families.
The converted lines developed in the study are enriched with kernel amylose while showing significant background recovery.
The high-amylose lines developed may be highly beneficial for diabetic patients and in the bioplastics industry, and should be suitable for growing under Indian conditions.
Keywords: ae1, amylose, diabetes, maize, marker-assisted backcross breeding, SBEs, SSR, starch.
References
Abidin MZAZ, Julkapli NM, Juahir H, Azaman F, Sulaiman NH, Abidin IZ (2015) Fabrication and properties of chitosan with starch for packaging application. Malaysian Journal of Analytical Sciences 19, 1032-1042.
| Google Scholar |
Babu R, Nair SK, Kumar A, Venkatesh S, Sekhar JC, Singh NN, Srinivasan G, Gupta HS (2005) Two-generation marker-aided backcrossing for rapid conversion of normal maize lines to quality protein maize (QPM). Theoretical and Applied Genetics 111, 888-897.
| Crossref | Google Scholar | PubMed |
Baveja A, Muthusamy V, Panda KK, Zunjare RU, Das AK, Chhabra R, Mishra SJ, Mehta BK, Saha S, Hossain F (2021) Development of multinutrient-rich biofortified sweet corn hybrids through genomics-assisted selection of shrunken2, opaque2, lcyE and crtRB1 genes. Journal of Applied Genetics 62, 419-429.
| Crossref | Google Scholar | PubMed |
Bear RP, Vineyard ML, MacMasters MM, Deatherage WL (1958) Development of “Amylomaize”—corn hybrids with high amylose starch: II. Results of breeding efforts 1. Agronomy Journal 50(10), 598-602.
| Crossref | Google Scholar |
Behall KM, Scholfield DJ, Hallfrisch JG (2006) Barley β-glucan reduces plasma glucose and insulin responses compared with resistant starch in men. Nutrition Research 26(12), 644-650.
| Crossref | Google Scholar |
Bishop G, Styles D, Lens PN (2022) Land-Use change and valorisation of feedstock side-streams determine the climate mitigation potential of bioplastics. Resources, Conservation and Recycling 180, 106185.
| Crossref | Google Scholar |
Blennow A, Skryhan K, Tanackovic V, Krunic SL, Shaik SS, Andersen MS, Kirk H-G, Nielsen KL (2020) Non-GMO potato lines, synthesizing increased amylose and resistant starch, are mainly deficient in isoamylase debranching enzyme. Plant Biotechnology Journal 18(10), 2096-2108.
| Crossref | Google Scholar | PubMed |
Boren M, Glaring MA, Ghebremedhin H, Olsson H, Blennow A, Jansson C (2008) Molecular and physicochemical characterization of the high-amylose barley mutant Amo1. Journal of Cereal Science 47(1), 79-89.
| Crossref | Google Scholar |
Cameron JW (1947) Chemico-Genetic bases for the reserve carbohydrates in maize endosperm. Genetics 32(5), 459.
| Crossref | Google Scholar |
Campbell MR, Jane J-L, Pollak L, Blanco M, O’Brien A (2007) Registration of maize germplasm line GEMS-0067. Journal of Plant Registrations 1(1), 60-61.
| Crossref | Google Scholar |
Ceseracciu L, Heredia-Guerrero JA, Dante Athanassiou A, Bayer IS (2015) Robust and biodegradable elastomers based on corn starch and polydimethylsiloxane (PDMS). ACS Applied Materials Interfaces 7, 3742-3753.
| Crossref | Google Scholar |
Chai XJ, Wang PW, Guan SY, Xu YW (2005) Reducing the maize amylopectin content through RNA interference manipulation. Zhi wu Sheng li yu fen zi Sheng wu xue xue bao= Journal of Plant Physiology and Molecular Biology 31(6), 625-630.
| Google Scholar |
Chen F, Zhu SW, Xiang Y, Jiang HY, Cheng BJ (2010) Molecular marker-assisted selection of the ae alleles in maize. Genetics and Molecular Research 9(2), 1074-1084.
| Crossref | Google Scholar |
Chen T, Ning L, Liu X, Cui D, Zhang H, Li D, Zhao L, Chen H (2013) Development of functional molecular markers of Sbe I and Sbe IIb for the high amylose maize germplasm line GEMS-0067. Crop Science 53(2), 482-490.
| Crossref | Google Scholar |
Cho NH, Shaw JE, Karuranga S, Huang Y, da Rocha Fernandes JD, Ohlrogge AW, Malanda B (2018) IDF diabetes atlas: global estimates of diabetes prevalence for 2017 and projections for 2045. Diabetes Research and Clinical Practice 138, 271-281.
| Crossref | Google Scholar | PubMed |
Chourey PS, Nelson OE (1976) The enzymatic deficiency conditioned by the shrunken-1 mutations in maize. Biochemical Genetics 14, 1-6.
| Crossref | Google Scholar |
Chukwu SC, Rafii MY, Ramlee SI, Ismail SI, Oladosu Y, Muhammad I, Musa I, Ahmed M, Jatto MI, Yusuf BR (2020) Recovery of recurrent parent genome in a marker-assisted backcrossing against rice blast and blight infections using functional markers and SSRs. Plants 9(11), 1411.
| Crossref | Google Scholar |
Cimini A, Sestili F, Moresi M (2022) Environmental profile of a novel high-amylose bread wheat fresh pasta with low glycemic index. Foods 11(20), 3199.
| Crossref | Google Scholar | PubMed |
Clendenning KA (1945) Polarimetric determination of starch in cereal products: IV. critical studies of methods for the determination of starch in whole wheat, granular, and patent flours. Canadian Journal of Research 23(6), 239-259.
| Crossref | Google Scholar |
Das AK, Gowda MM, Muthusamy V, Zunjare RU, Chauhan HS, Baveja A, Bhatt V, Chand G, Bhat JS, Guleria SK, Saha S, Gupta HS, Hossain F (2021) Development of maize hybrids with enhanced vitamin-E, vitamin-A, lysine, and tryptophan through molecular breeding. Frontiers in Plant Science 12, 659381.
| Crossref | Google Scholar | PubMed |
Dhir A, Kaur C, Devi V, Singh A, Das AK, Rakshit S, Chaudhary DP (2022) A rapid single kernel screening method for preliminary estimation of amylose in maize. Food Analytical Methods 15(8), 2163-2171.
| Crossref | Google Scholar |
Duncan KA, Hardin SC, Huber SC (2006) The three maize sucrose synthase isoforms differ in distribution, localization, and phosphorylation. Plant and Cell Physiolog 47, 959-971.
| Crossref | Google Scholar |
Dunn G, Kramer H, Whistler RL (1953) Gene dosage effects on corn endosperm carbohydrates 1. Agronomy Journal 45, 101-104.
| Google Scholar |
Eleazu CO (2016) The concept of low glycemic index and glycemic load foods as panacea for type 2 diabetes mellitus; prospects, challenges and solutions. African Health Sciences 16(2), 468-479.
| Crossref | Google Scholar | PubMed |
Flury M, Narayan R (2021) Biodegradable plastic as an integral part of the solution to plastic waste pollution of the environment. Current Opinion in Green and Sustainable Chemistry 30, 125-137.
| Crossref | Google Scholar |
Guan S, Wang P, Liu H, Liu G, Ma Y, Zhao L (2011) Production of high-amylose maize lines using RNA interference in sbe2a. African Journal of Biotechnology 10(68), 15229-15237.
| Crossref | Google Scholar |
Guan H, Dong Y, Liu C, He C, Liu C, Liu Q, Dong R, Li Y, Liu T, Wang L (2017) A splice site mutation in shrunken1-m causes the shrunken 1 mutant phenotype in maize. Plant Growth Regulation 83, 429-439.
| Crossref | Google Scholar |
Guo X, Song X, Zhang X (2010) Increasing amylose content by silencing SBEI using RNA interference in maize. Chinese Bulletin of Botany 45(06), 670 Available at https://www.chinbullbotany.com/EN/10.3969/j.issn.1674-3466.2010.06.004.
| Google Scholar |
Guo J, Wang Z, Qu L, Hao D, Lu D (2023) Comparison of the physicochemical properties of starches from maize reciprocal F1 hybrids and their parental lines. Food Chem.: X 17, 100561.
| Crossref | Google Scholar |
Han J, Guo Z, Wang M, Liu S, Hao Z, Zhang D, Yong H, Weng J, Zhou Z, Li M, Li X (2022) Using the dominant mutation gene Ae1-5180 (amylose extender) to develop high-amylose maize. Molecular Breeding 42(10), 57.
| Crossref | Google Scholar |
Hossain F, Jaiswal SK, Muthusamy V, et al. (2023) Enhancement of nutritional quality in maize kernel through marker-assisted breeding for vte4, crtRB1, and opaque2 genes. Journal of Applied Genetics 64, 431-443.
| Crossref | Google Scholar |
Jeevetha S, Barakatun-Nisak MY, Beng Ngan H, Ismail A, Azlan A (2014) Relationship between amylose content and glycemic index of commonly consumed white rice. Journal of Agriculture and Veterinary Science 7(9), 12-18.
| Crossref | Google Scholar |
King RA, Noakes M, Bird AR, Morell MK, Topping DL (2008) An extruded breakfast cereal made from a high amylose barley cultivar has a low glycemic index and lower plasma insulin response than one made from a standard barley. Journal of Cereal Science 48(2), 526-530.
| Crossref | Google Scholar |
Koch KE, Nolte KD, Duke ER, McCarty DR, Avigne WT (1992) Sugar levels modulate differential expression of maize sucrose synthase genes. The Plant Cell 4(1), 59-69.
| Crossref | Google Scholar |
Kostadinović M, Nikolić A, Ristić D, Božinović S, Đorđević-Melnik O, Ignjatović-Micić D, Vančetović J (2019) Marker assisted backcross breeding in Maize Research Institute Zemun Polje. Selekcija i semenarstvo 25(1), 41-47.
| Crossref | Google Scholar |
Kramer HH, Whistler RL (1949) Quantitative effects of certain genes on the amylose content of corn endosperm starch. Agronomy Journal 41, 409-411.
| Crossref | Google Scholar |
Li ZW, Zhong YY, Wu QM, Wang WB, Gao J, Liu XX, Kang HM, Guo DW, Xue JQ (2014) Physicochemical properties of high-amylose maize starch. Journal of Northwest University(Natural Science Edition) 42(7), 53-60.
| Crossref | Google Scholar |
Li C, Huang Y, Huang R, Wu Y, Wang W (2018) The genetic architecture of amylose biosynthesis in maize kernel. Plant Biotechnology Journal 16(2), 688-695.
| Crossref | Google Scholar |
Li C, Dhital S, Gidley MJ (2023) High amylose wheat foods: a new opportunity to improve human health. Trends in Food Science & Technology 135, 93-101.
| Crossref | Google Scholar |
Lim SM, Choo JM, Li H, O’rielly R, Carragher J, Rogers GB, Muhlhausler B (2021) A high amylose wheat diet improves gastrointestinal health parameters and gut microbiota in male and female mice. Foods 10(2), 220-229.
| Crossref | Google Scholar |
Lin X, Xu Y, Pan X, et al. (2020) Global, regional, and national burden and trend of diabetes in 195 countries and territories: an analysis from 1990 to 2025. Scientific Reports 10, 14790.
| Crossref | Google Scholar | PubMed |
Liu D, Wu Y, Gao Z, Yun YH (2019) Comparative non-destructive classification of partial waxy wheats using near-infrared and Raman spectroscopy. Crop & Pasture Science 70(5), 437-441.
| Crossref | Google Scholar |
MacLeod M, Arp HP, Tekman MB, Jahnke A (2021) The global threat from plastic pollution. Science 373(6550), 61-65.
| Crossref | Google Scholar |
McWhirter KS, Dunn CF (1986) Development of high amylose maize production in Australia. Special publication-Agronomy Society of New Zealand 5, 86-91.
| Google Scholar |
Miller JC (1994) Importance of glycemic index in diabetes. The American Journal of Clinical Nutrition 59(3), 747S-752S.
| Crossref | Google Scholar |
Moore CW, Creech RG (1972) Genetic fine structure analysis of the amylose-extender locus in Zea mays L. Genetics 70(4), 611-619.
| Crossref | Google Scholar |
Mukri G, Kumar R, Rajendran Kumar B, Hooda KS, Karjagi CG, Singh V, Jat SL, Das AK, Sekhar JC, Singh SB (2018) Strategic selection of white maize inbred lines for tropical adaptation and their utilization in developing stable, medium to long duration maize hybrids. Maydica 63(16), 1-8.
| Google Scholar |
Murray MG, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Research 8(19), 4321-4326.
| Crossref | Google Scholar | PubMed |
Prasanna BM, Pixley K, Warburton ML, Xie C-X (2010) Molecular marker-assisted breeding options for maize improvement in Asia. Molecular Breeding 26, 339-356.
| Crossref | Google Scholar |
Pukalenthy B, Manickam D, Chandran S, Adhimoolam K, Sampathrajan V, Rajasekaran R, Arunachalam K, Ganapathyswamy H, Chocklingam V, Muthusamy V, Hossain F, Natesan S (2019) Incorporation of opaque-2 into ‘UMI 1200’, an elite maize inbred line, through marker-assisted backcross breeding. Biotechnology & Biotechnological Equipment 33(1), 144-153.
| Crossref | Google Scholar |
Qin Y, Zhang H, Dai Y, Hou H, Dong H (2019) Effect of alkali treatment on structure and properties of high amylose corn starch film. Materials 12(10), 1705-1723.
| Crossref | Google Scholar |
Ranum P, Rosas JP, Casal MN (2014) Global maize production, utilization, and consumption. Annals of the New York Academy of Sciences 1312, 105-112.
| Crossref | Google Scholar |
Semagn K, Bjørnstad Å, Ndjiondjop MN (2006) Progress and prospects of marker assisted backcrossing as a tool in crop breeding programs. African Journal of Biotechnology 5(25), 2588-2603.
| Google Scholar |
Semagn K, Magorokosho C, Vivek BS, Makumbi D, Beyene Y, Mugo S, Prasanna BM, Warburton ML (2012) Molecular characterization of diverse CIMMYT maize inbred lines from eastern and southern Africa using single nucleotide polymorphic markers. BMC Genomics 13(1), 113.
| Crossref | Google Scholar |
Singh BD, Singh AK (2015) Marker-assisted selection. In ‘Marker-assisted plant breeding: principles and practices’, pp. 259-293. (Springer: India) doi:10.1007/978-81-322-2316-0_9
Slade AJ, McGuire C, Loeffler D, Mullenberg J, Skinner W, Fazio G, Holm A, Brandt KM, Steine MN, Goodstal JF, Knauf VC (2012) Development of high amylose wheat through TILLING. BMC Plant Biology 12(1), 69.
| Crossref | Google Scholar |
Tuncel A, Okita TW (2013) Improving starch yield in cereals by over-expression of ADPglucose pyrophosphorylase: expectations and unanticipated outcomes. Plant Science 211, 52-60.
| Crossref | Google Scholar |
van Berloo R (1999) Computer note. GGT: software for the display of graphical genotypes. Journal of Heredity 90(2), 328-329.
| Google Scholar |
Venadan S, Das AK, Yathish KR, Chaudhary DP, Arora A, Rakshit S (2023) Variability for kernel starch components in Indian maize germplasm and identification of polymorphic molecular marker for selected waxy maize genotypes. Cereal Research Communications 1, 1-3.
| Crossref | Google Scholar |
Wang J, Hu P, Chen Z, Liu Q, Wei C (2017) Progress in high-amylose cereal crops through inactivation of starch branching enzymes. Frontiers in Plant Science 8, 469.
| Crossref | Google Scholar | PubMed |
Whitt SR, Wilson LM, Tenaillon MI, Gaut BS, Buckler ES (2002) Genetic diversity and selection in the maize starch pathway. Proceedings of the National Academy of Sciences 99, 12959-12962.
| Crossref | Google Scholar |
Xu J, Sagnelli D, Faisal M, Perzon A, Taresco V, Mais M, Giosafatto CVL, Hebelstrup KH, Ulvskov P, Jorgensen B, Chen L (2021) Amylose/cellulose nanofiber composites for all-natural, fully biodegradable and flexible bioplastics. Carbohydrate Polymers 253, 1172-1187.
| Crossref | Google Scholar |
Yathish KR, Karjagi CG, Gangoliya SS, Kumar A, Preeti J, Yadav HK, Srivastava S, Kumar S, Swamy HKM, Singh A, Phagna RK, Das AK, Sekhar JC, Hossain F, Rakshit S, Gadag RN (2022) Introgression of the low phytic acid locus (lpa2) into elite maize (Zea mays L.) inbreds through marker-assisted backcross breeding (MABB). Euphytica 218(9), 127.
| Crossref | Google Scholar |
Yathish KR, Karjagi CG, Gangoliya SS, Gadag RN, Mallikarjuna MG, Sekhar JC, Das AK, Lakshmi Soujanya P, Kumar R, Singh A, Singh SB, Rakshit S (2023) Development of low-phytate maize inbred lines through marker-assisted introgression of lpa1. Crop & Pasture Science 74(9), 843-855.
| Crossref | Google Scholar |
Yusof BNM, Talib R, Kamaruddin N, Karim N, Chinna K, Gilbertson H (2009) A low-GI diet is associated with a short-term improvement of glycaemic control in Asian patients with type 2 diabetes. Diabetes, Obesity and Metabolism 11(4), 387-396.
| Crossref | Google Scholar |
Zhang W-L, Yang W-P, Chen Z-W, Wang M-C, Yang L-Q, Cai Y-L (2010) Molecular marker-assisted selection for o2 introgression lines with o16 gene in corn. Acta Agronomica Sinica 36(8), 1302-1309.
| Crossref | Google Scholar |
Zhang XD, Gao XC, Li ZW, Xu LC, Li YB, Zhang RH, Xue JQ, Gus DW (2020) The effect of amylose on kernel phenotypic characteristics, starch-related gene expression and amylose inheritance in naturally mutated high-amylose maize. Journal of Integrative Agriculture 19(6), 1554-1564.
| Crossref | Google Scholar |
Zhao Y, Li N, Li B, Li Z, Xie G, Zhang J (2015) Reduced expression of starch branching enzyme IIa and IIb in maize endosperm by RNAi constructs greatly increases the amylose content in kernel with nearly normal morphology. Planta 241, 449-461.
| Crossref | Google Scholar |
Zhu L, Gu M, Meng X, Cheung SCK, Yu H, Huang J, Sun Y, Shi Y, Liu Q (2012) High-amylose rice improves indices of animal health in normal and diabetic rats. Plant Biotechnology Journal 10(3), 353-362.
| Crossref | Google Scholar | PubMed |
Zunjare RU, Hossain F, Muthusamy V, Baveja A, Chauhan HS, Bhat JS, Thirunavukkarasu N, Saha S, Gupta HS (2018) Development of biofortified maize hybrids through marker-assisted stacking of β-carotene hydroxylase, lycopene-ε-cyclase and opaque2 genes. Frontiers in Plant Science 9, 178.
| Crossref | Google Scholar |
