Abstract
Sweet corn has emerged as a favorite food item worldwide owing to its kernel sweetness. However, traditional sweet corn cultivars are poor in provitamin-A (proA) and essential amino acids, viz., lysine and tryptophan. So far, no sweet corn hybrid with high nutritional qualities has been commercialized elsewhere. Here, we analyzed accumulation of provitamin-A (proA), lysine, and tryptophan in a set of mutant versions of (i) crtRB1-, (ii) o2-, and (iii) crtRB1 + o2-based sweet corn inbreds and hybrids with (iv) traditional sweet corn (wild-type: O2 + CrtRB1). The crtRB1- and crtRB1 + o2-based genotypes possessed significantly higher proA (17.31 ppm) over traditional sweet corn (2.83 ppm), while o2- and crtRB1 + o2-based genotypes possessed significantly higher lysine (0.345%) and tryptophan (0.080%) over traditional sweet corn (lysine 0.169%, tryptophan 0.036%). Late sowing favored high kernel lysine, proA, and green cob yield among hybrids. Sweetness (17.87%) among the improved inbreds and hybrids was comparable to the original sweetcorn genotypes (17.84%). Among the four genotypic classes, crtRB1 + o2-based improved genotypes showed stronger association among traits over genotypes with o2 and crtRB1 genes alone. Significant association was observed among (i) proA and BC (r = 0.99), (ii) proA and BCX (r = 0.93), (iii) lysine and tryptophan (r = 0.99), and (iv) green cob yield with fodder yield (r = 0.73) in sweet corn hybrids. The study demonstrated that combining crtRB1 and o2 genes did not pose any negative impact on nutritional, yield, and agronomic performance. Sweet corn with crtRB1 + o2 assumes significance for alleviating malnutrition through sustainable and cost-effective approach.
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The datasets generated analyzed during the current study are available from corresponding author on reasonable request.
References
Aluru M, Xu Y, Guo R, Wang Z, Li S, White W, Wang K, Rodermel S (2008) Generation of transgenic maize with enhanced provitamin a content. J Exp Bot 59:3551–3562
Andersson MS, Saltzman A, Virk PS, Pfeiffer WH (2017) Progress update: crop development of biofortified staple food crops under HarvestPlus. Afr J Food Agric Nutr Dev 17(2):11905–35. https://doi.org/10.18697/ajfand.78.harvestplus05
Anjorin FB, Ogunniyan DJ (2014) Comparison of growth and yield components of five quality protein maize varieties. Int j Res Agric 4(1):1–5. https://doi.org/10.5923/j.ijaf.20140401.01
Azevedo RA, Lea PJ (2001) Lysine metabolism in higher plants. Amino Acids 20(3):261–279. https://doi.org/10.1007/s007260170043
Azevedo RA, Damerval C, Landry J, Lea PJ, Bellato CM, Meinhardt LW, Le Guilloux M, Delhaye S, Toro AA, Gaziola SA, Berdejo BD (2003) Regulation of maize lysine metabolism and endosperm protein synthesis by opaque and floury mutations. Eur J Biochem 270(24):4898–4908
Babu R, Rojas NP, Gao S, Yan J, Pixley K (2013) Validation of the effects of molecular marker polymorphisms in LcyE and CrtRB1 on provitamin A concentrations for 26 tropical maize populations. Züchter Genet Breed Res 126(2):389–399. https://doi.org/10.1007/s00122-012-1987-3
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. J Appl Genet. https://doi.org/10.1007/s13353-021-00633-4
Baveja A, Chhabra R, Panda KK, Muthusamy V, Mehta BK, Mishra SJ, Zunjare RU, Hossain F (2022) Expression analysis of opaque2, crtRB1 and shrunken2 genes during different stages of kernel development in biofortified sweet corn. J Cereal Sci 105(103466):103466. https://doi.org/10.1016/j.jcs.2022.103466
Bouis H (2018) Reducing mineral and vitamin deficiencies through biofortification: progress under HarvestPlus. World Rev Nutr Diet 118:112–122. https://doi.org/10.1159/000484342
Bouis HE, Saltzman A, Birol E (2019) Improving nutrition through biofortification. Agriculture for improved nutrition: seizing the momentum. CAB International, UK, pp 47–57
Castelli S, Mascheretti I, Cosentino C, Lazzari B, Pirona R, Ceriotti A, Viotti A, Lauria M (2018) Uniparental and transgressive expression of α- zeins in maize endosperm of o2 hybrid lines. PLoS One 13(11). https://doi.org/10.1371/journal.pone.0206993
Chand G, Zunjare RU, Allen T, Muthusamy V, Mishra SJ, Kasana RK, Bhatt V, Ismail RI, Sarika K, Guleria SK, Hossain F (2022b) Genetic analysis of maize genotypes possessing novel combination of opaque2 and opaque16 genes affecting higher accumulation of lysine and tryptophan in kernels. J Cereal Sci 107(103534):103534. https://doi.org/10.1016/j.jcs.2022.103534
Chand G, Muthusamy V, Allen T, Zunjare RU, Mishra SJ, Singh B, Mehta BK, Talukder ZA, Ismail MR, Sairka K, Kamboj MC, Singh S, Hossain F (2022a) Composition of lysine and tryptophan among biofortified-maize possessing novel combination of opaque2 and opaque16 genes. J Food Compost Anal 107(104376):104376. https://doi.org/10.1016/j.jfca.2021.104376
Chauhan HS, Chhabra R, Rashmi T, Muthusamy V, Zunjare RU, Mishra SJ, Gain N, Mishra BK, Singh AK, Gupta HS, Hossain F (2022) Impact of vte4 and crtRB1 genes on composition of vitamin-E and provitamin-A carotenoids during kernel-stages in sweet corn. J Food Compos Anal. https://doi.org/10.1016/j.jfca.2021.104264
Chhabra R, Muthusamy V, Gain N, Katral A, Prakash NR, Zunjare RU, Hossain F (2021) Allelic variation in sugary1 gene affecting kernel sweetness among diverse-mutant and -wild-type maize inbreds. Mol Genet Genomics 296(5):1085–1102. https://doi.org/10.1007/s00438-021-01807-9
Chhabra R, Muthusamy V, Baveja A, Katral A, Mehta B, Zunjare RU et al (2022) Allelic variation in shrunken2 gene affecting kernel sweetness in exotic-and indigenous-maize inbreds. PLoS ONE 17(9):e0274732. https://doi.org/10.1371/journal.pone.0274732
Cunningham FX, Gantt E (1998) Genes and enzymes of carotenoid biosynthesis in plants. Annu Rev Plant Physiol Plant Mol Biol 49(1):557–583. https://doi.org/10.1146/annurev.arplant.49.1.557
De Moura FF, Miloff A, Boy E (2015) Retention of provitamin a carotenoids in staple crops targeted for biofortification in Africa: cassava, maize and sweet potato. Crit Rev Food Sci Nutr 55(9):1246–1269. https://doi.org/10.1080/10408398.2012.724477
Dutta S, Muthusamy V, Hossain F, Baveja A, Abhijith KP, Saha S, Zunjare RU, Yadava DK (2020) Effect of storage period on provitamin-A carotenoids retention in biofortified maize hybrids. Int J Food Sci Technol. https://doi.org/10.1111/ijfs.14785
FAO, IFAD, UNICEF, WFP and WHO (2022). The state of food security and nutrition in the world. Rome, FAO. https://doi.org/10.4060/cc0639en
FAOSTAT (2023) Prevalence of undernourishment. Fao.org. https://www.fao.org/sustainable-developmentgoals/indicators/211/en/. Accessed 23 Jun 2023
Goswami R, Zunjare RU, Khan S, Baveja A, Muthusamy V, Hossain F (2019) Marker-assisted introgression of rare allele of β-carotene hydroxylase (crtRB1) gene into elite quality protein maize inbred for combining high lysine, tryptophan and provitamin A in maize. Plant Breed 138(2):174–183. https://doi.org/10.1111/pbr.12676
Gunjaca J, Buhinicek I, Jukic M, Sarcevic H, Vragolovic A, Kozic Z, Jambrovic A, Pejic I (2008) Discriminating maize inbred lines using molecular and DUS data. Euphytica 161:165–172. https://doi.org/10.1007/s10681-007-9518-z
Gupta HS, Hossain F, Muthusamy V, Zunjare RU (2019) Marker-assisted breeding for enrichment of provitamin A in maize. In: Qureshi A, Dar Z, Wani S (eds) Quality Breeding in Field Crops. Springer, Cham, pp 139–157
Gupta HS, Raman B, Agrawal PK et al (2013) Accelerated development of qualityprotein maize hybrid through marker-assisted introgression of opaque-2 allele. Plant Breed 132:77–82. https://doi.org/10.1111/pbr.12009
Gyenes-Hegyi Z, Pók I, Kizmus L (2002) Plant height and height of the main ear in maize (Zea mays L.) at different locations and different plant densities. Acta Agron Hungar 50(1):75–84. https://doi.org/10.1556/aagr.50.2002.1.9
Herrmann KM, Weaver LM (1999) The shikimate pathway. Annu Rev Plant Physiol Plant Mol Biol 50(1):473–503
Hossain F, Nepolean T, Vishwakarma AK, Pandey N, Prasanna BM, Gupta HS (2015) Mapping and validation of microsatellite markers linked to sugary1 and shrunken2 genes in maize (Zea mays L.). J Plant Biochem Biotechnol 24(2):135–42. https://doi.org/10.1007/s13562-013-0245-3
Hossain F, Sarika K, Muthusamy V, Zunjare RU, Gupta HS (2019) Quality proteinmaize for nutritional security. In: Qureshi AMI et al (eds) Quality breeding in field crops. Springer, Switzerland, pp 217–237. https://doi.org/10.1007/978-3-030-04609-5_11
Hossain F, Jaiswal SK, Muthusamy V, Zunjare RU, Mishra SJ, Chand G, Bhatt V, Bhat JS, Das AK, Chauhan HS, Gupta HS (2023) Enhancement of nutritional quality in maize kernel through genomics-assisted breeding for vte4, crtRB1 and opaque2 genes. J Applied Genetics. https://doi.org/10.1007/s13353-023-00768-6
Jia M, Wu H, Clay KL, Jung R, Larkins BA, Gibbon BC (2013) Identification and characterization of lysine-rich proteins and starch biosynthesis genes in the opaque2 mutant by transcriptional and proteomic analysis. BMC Plant Biol 13(1):60. https://doi.org/10.1186/1471-2229-13-60
Kemper EL, Neto GC, Papes F, Moraes KCM, Leite A, Arruda P (1999) The role of Opaque2 in the control of lysine-degrading activities in developing maize endosperm. Plant Cell 11(10):1981. https://doi.org/10.2307/3871092
Khush GS, Lee S, Cho J-I, Jeon J-S (2012) Biofortification of crops for reducing malnutrition. Plant Biotechnol Rep 6(3):195–202. https://doi.org/10.1007/s11816-012-0216-5
Kiani AK, Dhuli K, Donato K, Aquilanti B, Velluti V, Matera G, Iaconelli A, Connelly ST, Bellinato F, Gisondi P, Bertelli M (2022) Main nutritional deficiencies. J Prev Med Hyg 63(2Suppl3):E93–101. https://doi.org/10.15167/2421-4248/jpmh2022.63.2S3.2752
Kodrzycki R, Boston RS, Larkins BA (1989) The opaque-2 mutation of maize differentially reduces zein gene transcription. Plant Cell 1(1):105–114. https://doi.org/10.1105/tpc.1.1.105
Kurilich AC, Juvik JA (1999) Quantification of carotenoid and tocopherol antioxidants in Zea mays. J Agric Food Chem 47(5):1948–1955. https://doi.org/10.1021/jf981029d
Larkin DF, Berry M, Easty DL (1991) In vitro corneal pathogenicity of Acanthamoeba. EYE 5(5):560–8. https://doi.org/10.1038/eye.1991.98
Letrat K, Pulam T (2007) Breeding for increased sweetness in sweet corn. Int J Plant Breed Genet 1:27–30
Mehta BK, Chauhan HS, Basu S, Anand A, Baveja A, Kumar A, Zunjare RU, Muthusamy V, Singh AK, Hossain F (2024) Mutant crtRB1 gene negates the unfavourable effects of opaque2 gene on germination and seed vigour among shrunken2-based biofortified sweet corn genotypes. Funct Plant Biol. https://doi.org/10.1071/FP23179
Mehta BK, Hossain F, Muthusamy V, Zunjare RU, Sekhar JC, Gupta HS (2017a) Analyzing the role of sowing and harvest time as factors for selecting super sweet (-sh2sh2) corn hybrids. Indian J Genet Plant Breed 77:348–56. https://doi.org/10.31742/ijgpb.v77i03.3
Mehta BK, Hossain F, Muthusamy V, Zunjare RU, Sekhar JC, Gupta HS (2017b) Analysis of responses of novel double mutant (sh2sh2/su1su1) sweet corn hybrids for kernel sweetness under different sowing-and harvest-time. Indian J Agric Sci 87:1543–8. https://doi.org/10.56093/ijas.v87i11.75787
Mehta BK, Muthusamy V, Zunjare RU, Baveja A, Chauhan HS, Chhabra R, Singh AK, Hossain F (2020) Biofortification of sweet corn hybrids for provitamin-A, lysine and tryptophan using molecular breeding. J Cereal Sci 96(103093):103093. https://doi.org/10.1016/j.jcs.2020.103093
Mehta BK, Chhabra R, Muthusamy V, Zunjare RU, Baveja A, Chauhan HS, Prakash NR, Chalam VC, Singh Ak, Hossain F (2021) Expression analysis of β-carotene hydroxylase1 and opaque2 genes governing accumulation of provitamin-A, lysine and tryptophan during kernel development in biofortified sweet corn. 3 Biotech 11(7):325. https://doi.org/10.1007/s13205-021-02837-1
Mertz ET, Bates LS, Nelson OE (1964) Mutant gene that changes protein composition and increases lysine content of maize endosperm. Science 145(3629):279–280. https://doi.org/10.1126/science.145.3629.279
Muthusamy V, Hossain F, Thirunavukkarasu N, Choudhary M, Saha S, Bhat JS, Prasanna BM, Gupta HS (2014) Development of β-carotene rich maize hybrids through marker-assisted introgression of β-carotene hydroxylase allele. PLoS ONE 9(12):e113583. https://doi.org/10.1371/journal.pone.0113583
Nyakurwa CS, Gasura E, Mabasa S (2017) Potential for quality protein maize for reducing proteinenergy undernutrition in maize dependent Sub-Saharan African countries: a review. Afr Crop Sci J 25(4):521–537. https://doi.org/10.4314/acsj.v25i4.9
Ortiz-Covarrubias Y, Dhliwayo T, Palacios-Rojas N, Ndhlela T, Magorokosho C, Aguilar-Rincón VH, Cruz-Morales AS, Trachsel S (2019) Effects of drought and low nitrogen stress on provitamin A carotenoid content of biofortified maize hybrids. Crop Sci 59(6):2521–2532. https://doi.org/10.2135/cropsci2019.02.0100
Pandey N, Hossain F, Kumar K, Vishwakarma A, Muthusamy V, Manjaiah K, Agrawal PK, Guleria SK, Reddy SS, Thirunavukkarasu N, Gupta HS (2015) Microsatellite marker-based genetic diversity among quality protein maize (QPM) inbreds differing for kernel iron and zinc. Mol Plant Breed. https://doi.org/10.5376/mpb.2015.06.0003
Pixley K, Rojas NP, Babu R, Mutale R, Surles R, Simpungwe E (2013) Biofortification of maize with provitamin A carotenoids. In: Tanumihardjo SA (ed) Carotenoids and human health, nutrition and health. Humana Press, pp 271–292. https://doi.org/10.1007/978-1-62703-203-2_17
Prasanna BM, Palacios-Rojas N, Hossain F, Muthusamy V, Menkir A, Dhliwayo T, Ndhlela T, Vicente FS, Nair SK, Vivek BS, Zhang X, Olsen M, Fan X (2020) Molecular breeding for nutritionally enriched maize: status and prospects. Front Genet. https://doi.org/10.3389/fgene.2019.01392
Protection of Plant Varieties and Farmers’ Rights Authority (PPVFRA) (2007) Guidelines for the conduct of test for distinctiveness, uniformity and stability on maize (Zea mays L.) pp 1–13. https://plantauthority.gov.in/sites/default/fles/gmaize.pdf. Accessed 18 Sept 2023
Qi X, Zhao Y, Jiang L, Cui Y, Wang Y, Liu B (2009) QTL analysis of kernel soluble sugar content in supersweet corn. Afr J Biotechnol 8(24):6913–6917
Radwanski ER, Last RL (1995) Tryptophan biosynthesis and metabolism: biochemical and molecular genetics. Plant Cell 7(7):921–934
Revilla P, Anibas CM, Tracy WF (2021) Sweet corn research around the world 2015–2020. Agronomy (Basel) 11(3):534. https://doi.org/10.3390/agronomy11030534
Sarika K, Hossain F, Muthusamy V, Zunjare RU, Baveja A, Goswami R, Bhat JS, Saha S, Gupta HS (2018) Marker-assisted pyramiding of opaque2 and novel opaque16 genes for further enrichment of lysine and tryptophan in sub-tropical maize. Plant Sci 272:142–152. https://doi.org/10.1016/j.plantsci.2018.04.014
Sethi M, Singh A, Kaur H, Phagna RK, Rakshit S, Chaudhary DP (2021) Expression profile of protein fractions in the developing kernel of normal, Opaque-2 and quality protein maize. Sci Rep 11(1):2469. https://doi.org/10.1038/s41598-021-81906-0
Singh B, Zunjare RU, Shrivastava S, Chand G, Gain N, Bhatt V, Muthusamy V, Hossain F (2023) Provitamin A, lysine and tryptophan enrichment in shrunken2-based sweet corn genotypes through genomics-assisted breeding for crtRB1 and opaque2 genes. Mol Biol Rep 50(6):4965–4974. https://doi.org/10.1007/s11033-023-08446-w
Tracy WF (2001) Sweet corn. In: Hallauer AR (ed) Specialty corns, 2nd edn. CRC Press, Boca Raton, Fla, University of Florida, pp 155–197
Vasal SK, Villegas E, Bjarnason M, Gelaw B, Goertz P (1980) Genetic modifiers and breeding strategies in developing hard endosperm opaque-2 materials. In: Pollmer WG, Phipps RH (eds) Improvement of quality traits for silage use. Martinus Nijhoff Publishers, pp 37–71
World Health Organization (2021) Levels and trends in child malnutrition: UNICEF. https://www.who.int/data/gho/data/themes/topics/joint-child-malnutrition-estimates-unicef-who-wb. Accessed 23 June 2023
Wurtzel ET, Cuttriss A, Vallabhaneni R (2012) Maize provitamin a carotenoids, current resources, and future metabolic engineering challenges. Front Plant Sci 3:29. https://doi.org/10.3389/fpls.2012.00029
Yan J, Kandianis CB, Harjes CE, Bai L, Kim EH, Yang X, Skinner DJ, Fu Z, Mitchell S, Li Q, Fernandez MGS, Zaharieva M, Babu R, Fu Y, Palacios N, Li J, DellaPenna D, Brutnell T, Buckler ES, Warburton ML, Rocheford T (2010) Rare genetic variation at Zea mays crtRB1 increases β-carotene in maize grain. Nat Genet 42:322–327. https://doi.org/10.1038/ng.551
Zunjare RU, Hossain F, Muthusamy V, Baveja A, Chauhan HS, Thirunavukkarasu N, Saha S, Gupta HS (2017) Influence of rare alleles of ß-carotene hydroxylase and lycopene epsilon cyclase genes on accumulation of provitamin A carotenoids in maize kernels. Plant Breed 136(6):872–880
Zunjare RU, Chhabra R, Hossain F, Muthusamy V, Baveja A, Gupta HS (2018b) Development and validation of multiplex-PCR assay for simultaneous detection of rare alleles of crtRB1 and lcyE governing higher accumulation of provitamin A in maize. J Plant Biochem Biotechnol 27:208–214. https://doi.org/10.1007/s13562-017-0432-8
Zunjare RU, Hossain F, Muthusamy V, Baveja A, Chauhan HS, Bhat JS, Nepolean T, Saha S, Gupta HS (2018a) Development of biofortified maize hybrids through marker-assisted stacking of β-carotene hydroxylase, lycopene- ε-cyclase and opaque2 genes. Front Plant Sci 9:178. https://doi.org/10.3389/fpls.2018.00178
Acknowledgements
We acknowledge the financial support received from ICAR under the Consortia Research Platform on Biofortification of Selected Crops for Nutritional Security-Maize component (12-131). We thank ICAR-IARI, New Delhi, for providing the lab and field facility.
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We are thankful to the ICAR-IARI, New Delhi, for financial support.
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Conduct of the experiment: BS; generation of crosses: RUZ; raising of hybrid trials: VM; recording of phenotypic data: GC and VB; estimation of quality parameters: NG; statistical analysis: VM; writing and editing of manuscript: BS, FH, and SS; designing of experiment: FH and SS.
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Singh, B., Muthusamy, V., Shrivastava, S. et al. Analysis of nutritional composition in opaque2- and crtRB1-based single- and double-biofortified super sweet corn. J Appl Genetics (2024). https://doi.org/10.1007/s13353-024-00873-0
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DOI: https://doi.org/10.1007/s13353-024-00873-0