Development of low-phytate maize inbred lines through marker-assisted introgression of lpa1
K. R. Yathish A B , Chikkappa G. Karjagi B * , Shivraj S. Gangoliya B C , Raveendra N. Gadag A , M. G. Mallikarjuna A , Javaji C. Sekhar B , Abhijit K. Das B , P. Lakshmi Soujanya B , Ramesh Kumar B , Alla Singh B , Shyam Bir Singh B and Sujay Rakshit BA ICAR-Indian Agricultural Research Institute, Pusa Campus New Delhi, Delhi 110012, India.
B ICAR-Indian Institute of Maize Research, PAU Campus, Ludhiana, Punjab 141004, India.
C Maharana Pratap Government Post Graduate College, Gadarwara, Madhya Pradesh 487551, India.
Crop & Pasture Science 74(9) 843-855 https://doi.org/10.1071/CP22238
Submitted: 11 July 2022 Accepted: 4 February 2023 Published: 14 March 2023
© 2023 The Author(s) (or their employer(s)). Published by CSIRO Publishing
Abstract
Context: Phytic acid is the major storage form of phosphorus in cereals and is considered an anti-nutritional factor because it chelates major mineral micronutrient cations, resulting in micronutrient malnutrition in humans. For monogastric animals fed maize (Zea mays L.) grains, the stored phosphorus does not release into the digestive tract, leading to phosphorus deficiency and environmental pollution.
Aims: The aim of the study was to develop maize lines with a lower level of phytic acid that might substantially enhance the nutritional value of maize.
Methods: The lpa1 mutant allele conferring low phytic acid was transferred into the parental lines of popular maize hybrid DMH 121 (i.e. BML 6 and BML 45) through marker-assisted backcross breeding. Foreground selection was performed using a co-dominant single nucleotide polymorphism marker through a high-resolution melting approach, and background selection was undertaken using 50–55 polymorphic sequence-tagged microsatellite site markers.
Key results: Near-isogeneic lines were produced with >90% recurrent parental genome and reduction of phytic acid content by up to 44–56% compared with the original lines.
Conclusions: The near-isogeneic lines carrying lpa1 can be used to reconstitute DHM 121 with low phytate content.
Implications: The low-phytate maize hybrids produced can be useful in reducing micronutrient malnutrition in humans, as well as environmental pollution.
Keywords: biofortification, high-resolution melting, inorganic phosphorus, maize, malnutrition, marker-assisted backcross breeding, near isogenic lines, phytic acid.
References
Borlini G, Rovera C, Landoni M, Cassani E, Pilu R (2019) lpa1-5525: a new lpa1 mutant isolated in a mutagenized population by a novel non-disrupting screening method. Plants 8, 209| lpa1-5525: a new lpa1 mutant isolated in a mutagenized population by a novel non-disrupting screening method.Crossref | GoogleScholarGoogle Scholar |
Cerino Badone F, Amelotti M, Cassani E, Pilu R (2012) Study of low phytic acid1-7 (lpa1-7), a new ZmMRP4 mutation in maize. Journal of Heredity 103, 598–605.
| Study of low phytic acid1-7 (lpa1-7), a new ZmMRP4 mutation in maize.Crossref | GoogleScholarGoogle Scholar |
Coulibaly A, Kouakou B, Chen J (2010) Phytic acid in cereal grains: structure, healthy or harmful ways to reduce phytic acid in cereal grains and their effects on nutritional quality. American Journal of Plant Nutrition and Fertilization Technology 1, 1–22.
| Phytic acid in cereal grains: structure, healthy or harmful ways to reduce phytic acid in cereal grains and their effects on nutritional quality.Crossref | GoogleScholarGoogle Scholar |
Dellaporta SL, Wood J, Hicks JB (1983) A plant DNA minipreparation: version II. Plant Molecular Biology Reporter 1, 19–21.
| A plant DNA minipreparation: version II.Crossref | GoogleScholarGoogle Scholar |
Dhillon BS (1998) Recurrent selection for combining ability and performance per se of cross-bred and selfed families. Maydica 43, 155–160.
Dorsch JA, Cook A, Young KA, Anderson JM, Bauman AT, Volkmann CJ, Murthy PPN, Raboy V (2003) Seed phosphorus and inositol phosphate phenotype of barley low phytic acid genotypes. Phytochemistry 62, 691–706.
| Seed phosphorus and inositol phosphate phenotype of barley low phytic acid genotypes.Crossref | GoogleScholarGoogle Scholar |
Ertl DS, Young KA, Raboy V (1998) Plant genetic approaches to phosphorus management in agricultural production. Journal of Environmental Quality 27, 299–304.
| Plant genetic approaches to phosphorus management in agricultural production.Crossref | GoogleScholarGoogle Scholar |
FAOSTAT (2020) Crops and livestock products. Available at https://www.fao.org/faostat/en/#data/QCL
Frisch M, Bohn M, Melchinger AA (1999a) Minimum sample size and optimal positioning of flanking markers in marker-assisted backcrossing for transfer of a target gene. Crop Science 39, 967–975.
| Minimum sample size and optimal positioning of flanking markers in marker-assisted backcrossing for transfer of a target gene.Crossref | GoogleScholarGoogle Scholar |
Frisch M, Bohn M, Melchinger AE (1999b) Comparison of selection strategies for marker-assisted backcrossing of a gene. Crop Science 39, 1295–1301.
| Comparison of selection strategies for marker-assisted backcrossing of a gene.Crossref | GoogleScholarGoogle Scholar |
Gupta HS, Hossain F, Muthusamy V (2015) Biofortification of maize: an Indian perspective. Indian Journal of Genetics and Plant Breeding 75, 1–22.
| Biofortification of maize: an Indian perspective.Crossref | GoogleScholarGoogle Scholar |
Guttieri M, Bowen D, Dorsch JA, Raboy V, Souza E (2004) Identification and characterization of a low phytic acid wheat. Crop Science 44, 418–424.
| Identification and characterization of a low phytic acid wheat.Crossref | GoogleScholarGoogle Scholar |
Hospital F, Charcosset A (1997) Marker-assisted introgression of quantitative trait loci. Genetics 147, 1469–1485.
| Marker-assisted introgression of quantitative trait loci.Crossref | GoogleScholarGoogle Scholar |
Jorboe SG, Beavis WD, Openshaw (1994) Prediction of responses to selection in marker-assisted backcross programs by computer simulation. In ‘Abstracts of the second international conference on plant genome’. pp. 38. (Scherago International Inc.: NJ, USA)
Kishor DS, Lee C, Lee D, Venkatesh J, Seo J, Chin JH, Jin Z, Hong S-K, Ham J-K, Koh HJ, Jeon J-S (2019) Novel allelic variant of Lpa1 gene associated with a significant reduction in seed phytic acid content in rice (Oryza sativa L.). PLoS ONE 14, e0209636
| Novel allelic variant of Lpa1 gene associated with a significant reduction in seed phytic acid content in rice (Oryza sativa L.).Crossref | GoogleScholarGoogle Scholar |
Landoni M, Cerino Badone F, Haman N, Schiraldi A, Fessas D, Cesari V, Toschi I, Cremona R, Delogu C, Villa D, Cassani E, Pilu R (2013) Low phytic acid 1 mutation in maize modifies density, starch properties, cations, and fiber contents in the seed. Journal of Agricultural and Food Chemistry 61, 4622–4630.
| Low phytic acid 1 mutation in maize modifies density, starch properties, cations, and fiber contents in the seed.Crossref | GoogleScholarGoogle Scholar |
Larson SR, Young KA, Cook A, Blake TK, Raboy V (1998) Linkage mapping of two mutations that reduce phytic acid content of barley grain. Theoretical and Applied Genetics 97, 141–146.
| Linkage mapping of two mutations that reduce phytic acid content of barley grain.Crossref | GoogleScholarGoogle Scholar |
Larson SR, Rutger JN, Young KA, Raboy V (2000) Isolation and genetic mapping of a non-lethal rice (Oryza sativa L.) low phytic acid 1 mutation. Crop Science 40, 1397–1405.
| Isolation and genetic mapping of a non-lethal rice (Oryza sativa L.) low phytic acid 1 mutation.Crossref | GoogleScholarGoogle Scholar |
Liu Q-L, Xu X-H, Ren X-L, Fu H-W, Wu D-X, Shu Q-Y (2007) Generation and characterization of low phytic acid germplasm in rice (Oryza sativa L.). Theoretical and Applied Genetics 114, 803–814.
| Generation and characterization of low phytic acid germplasm in rice (Oryza sativa L.).Crossref | GoogleScholarGoogle Scholar |
Lorenz AJ, Scott MP, Lamkey KR (2007) Quantitative determination of phytate and inorganic phosphorus for maize breeding. Crop Science 47, 600–604.
| Quantitative determination of phytate and inorganic phosphorus for maize breeding.Crossref | GoogleScholarGoogle Scholar |
Lorenz AJ, Scott MP, Lamkey KR (2008) Genetic variation and breeding potential of phytate and inorganic phosphorus in a maize population. Crop Science 48, 79–84.
| Genetic variation and breeding potential of phytate and inorganic phosphorus in a maize population.Crossref | GoogleScholarGoogle Scholar |
Mallikarjuna MG, Thirunavukkarasu N, Hossain F, Bhat JS, Jha SK, Rathore A, Agrawal PK, Pattanayak A, Reddy SS, Gularia SK, Singh AM, Manjaiah KM, Gupta HS (2015) Stability performance of inductively coupled plasma mass spectrometry-phenotyped kernel minerals concentration and grain yield in maize in different agro-climatic zones. PLoS ONE 10, e0140947
| Stability performance of inductively coupled plasma mass spectrometry-phenotyped kernel minerals concentration and grain yield in maize in different agro-climatic zones.Crossref | GoogleScholarGoogle Scholar |
Mallikarjuna MG, Thirunavukkarasu N, Sharma R, Shiriga K, Hossain F, Bhat JS, Mithra ACR, Marla SS, Manjaiah KM, Rao AR, Gupta HS (2020) Comparative transcriptome analysis of iron and zinc deficiency in maize (Zea mays L.). Plants 9, 1812
| Comparative transcriptome analysis of iron and zinc deficiency in maize (Zea mays L.).Crossref | GoogleScholarGoogle Scholar |
Naidoo R, Watson GMF, Derera J, Tongoona P, Laing MD (2012) Marker-assisted selection for low phytic acid (lpa1-1) with single nucleotide polymorphism marker and amplified fragment length polymorphisms for background selection in a maize backcross breeding programme. Molecular Breeding 30, 1207–1217.
| Marker-assisted selection for low phytic acid (lpa1-1) with single nucleotide polymorphism marker and amplified fragment length polymorphisms for background selection in a maize backcross breeding programme.Crossref | GoogleScholarGoogle Scholar |
Oliver RE, Yang C, Hu G, Raboy V, Zhang M (2009) Identification of PCR-based DNA markers flanking three low phytic acid mutant loci in barley. Journal of Plant Breeding and Crop Science 1, 87–93.
Pilu R, Panzeri D, Gavazzi G, Rasmussen SK, Consonni G, Nielsen E (2003) Phenotypic, genetic and molecular characterization of a maize low phytic acid mutant (lpa241). Theoretical and Applied Genetics 107, 980–987.
| Phenotypic, genetic and molecular characterization of a maize low phytic acid mutant (lpa241).Crossref | GoogleScholarGoogle Scholar |
Raboy V (1997) Accumulation and storage of phosphate and minerals. In ‘Cellular and molecular biology of plant seed development. Vol. 4. Advances in cellular and molecular biology of plants’. (Eds BA Larkins, IK Vasil) pp. 441–477. (Springer: Dordrecht, Netherlands)
Raboy V (2002) Progress in breeding low phytate crops. The Journal of Nutrition 132, S503–S505.
| Progress in breeding low phytate crops.Crossref | GoogleScholarGoogle Scholar |
Raboy V (2007) The ABCs of low-phytate crops. Nature Biotechnology 25, 874–875.
| The ABCs of low-phytate crops.Crossref | GoogleScholarGoogle Scholar |
Raboy V, Gerbasi P (1996) Genetics of myo-inositol phosphate synthesis and accumulation. In ‘Myo-Inositol phosphates, phosphoinositides, and signal transduction. Vol. 26. Subcellular biochemistry’. (Eds BB Biswas, S Biswas) pp. 257–285. (Springer)
Raboy V, Gerbasi PF, Young KA, Stoneberg SD, Pickett SG, Bauman AT, Murthy PPN, Sheridan WF, Ertl DS (2000) Origin and seed phenotype of maize low phytic acid 1-1 and low phytic acid 2-1. Plant Physiology 124, 355–368.
| Origin and seed phenotype of maize low phytic acid 1-1 and low phytic acid 2-1.Crossref | GoogleScholarGoogle Scholar |
Rasmussen SK, Hatzack F (1998) Identification of two low-phytate barley (Hordeum vulgare L.) grain mutants by TLC and genetic analysis. Hereditas 129, 107–112.
| Identification of two low-phytate barley (Hordeum vulgare L.) grain mutants by TLC and genetic analysis.Crossref | GoogleScholarGoogle Scholar |
Roslinsky V, Eckstein PE, Raboy V, Rossnagel BG, Scoles GJ (2007) Molecular marker development and linkage analysis in three low phytic acid barley (Hordeum vulgare) mutant lines. Molecular Breeding 20, 323–330.
| Molecular marker development and linkage analysis in three low phytic acid barley (Hordeum vulgare) mutant lines.Crossref | GoogleScholarGoogle Scholar |
Sharpley AN, Chapra SC, Wedepohl R, Sims JT, Daniel TC, Reddy KR (1994) Managing agricultural phosphorus for protection of surface waters: issues and options. Journal of Environmental Quality 23, 437–451.
| Managing agricultural phosphorus for protection of surface waters: issues and options.Crossref | GoogleScholarGoogle Scholar |
Shi J, Wang H, Wu Y, Hazebroek J, Meeley RB, Ertl DS (2003) The maize low-phytic acid mutant lpa2 is caused by mutation in an inositol phosphate kinase gene. Plant Physiology 131, 507–515.
| The maize low-phytic acid mutant lpa2 is caused by mutation in an inositol phosphate kinase gene.Crossref | GoogleScholarGoogle Scholar |
Shi J, Wang H, Hazebroek J, Ertl DS, Harp T (2005) The maize low-phytic acid 3 encodes a myo-inositol kinase that plays a role in phytic acid biosynthesis in developing seeds. The Plant Journal 42, 708–719.
| The maize low-phytic acid 3 encodes a myo-inositol kinase that plays a role in phytic acid biosynthesis in developing seeds.Crossref | GoogleScholarGoogle Scholar |
Shi J, Wang H, Schellin K, Li B, Faller M, Stoop JM, Meeley RB, Ertl DS, Ranch JP, Glassman K (2007) Embryo-specific silencing of a transporter reduces phytic acid content of maize and soybean seeds. Nature Biotechnology 25, 930–937.
| Embryo-specific silencing of a transporter reduces phytic acid content of maize and soybean seeds.Crossref | GoogleScholarGoogle Scholar |
Singh BD, Singh AK (2015) ‘Marker-assisted plant breeding: principles and practices.’ (Springer)
Sparvoli F, Cominelli E (2015) Seed biofortification and phytic acid reduction: a conflict of interest for the plant? Plants 4, 728–755.
| Seed biofortification and phytic acid reduction: a conflict of interest for the plant?Crossref | GoogleScholarGoogle Scholar |
Sureshkumar S, Tamilkumar P, Senthil N, Nagarajan P, Thangavelu AU, Raveendran M, Vellaikumar S, Ganesan KN, Balagopal R, Vijayalakshmi G, Shobana V (2014a) Marker assisted selection of low phytic acid trait in maize (Zea mays L.). Hereditas 151, 20–27.
| Marker assisted selection of low phytic acid trait in maize (Zea mays L.).Crossref | GoogleScholarGoogle Scholar |
Sureshkumar S, Tamilkumar P, Thangavelu AU, Senthil N, Nagarajan P, Vellaikumar S, Ganesan KN, Balagopal R, Raveendran M (2014b) Marker-assisted introgression of lpa2 locus responsible for low-phytic acid trait into an elite tropical maize inbred (Zea mays L.). Plant Breeding 133, 566–578.
| Marker-assisted introgression of lpa2 locus responsible for low-phytic acid trait into an elite tropical maize inbred (Zea mays L.).Crossref | GoogleScholarGoogle Scholar |
Tamilkumar P, Senthil N, Sureshkumar S, Thangavelu AU, Nagarajan P, Vellaikumar S, Ganesan KN, Natarajan N, Balagopal R, Nepolean T, Raveendran M (2014) Introgression of low phytic acid locus (lpa2-2) into an elite Maize (Zea mays L.) inbred through marker assisted backcross breeding. Australian Journal of Crop Science 8, 1224–1231.
van Berloo R (2008) GGT 2.0: Versatile software for visualization and analysis of genetic data. Journal of Heredity 99, 232–236.
| GGT 2.0: Versatile software for visualization and analysis of genetic data.Crossref | GoogleScholarGoogle Scholar |
Wilcox JR, Premachandra GS, Young KA, Raboy V (2000) Isolation of high seed inorganic P, low-phytate soybean mutants. Crop Science 40, 1601–1605.
| Isolation of high seed inorganic P, low-phytate soybean mutants.Crossref | GoogleScholarGoogle Scholar |
Yathish KR, Gangoliya SS, Ghoshal T, Singh A, Phagna RK, Das AK, Neelam S, Singh SB, Kumar A, Rakshit S, Gadag RN, Hossain F, Karjagi CG (2021) Biochemical estimation of phytic acid and inorganic phosphate in diverse maize germplasm to identify potential donor for low phytic acid (Lpa) trait in tropical genetic background. Indian Journal of Genetics and Plant Breeding 81, 245–254.
| Biochemical estimation of phytic acid and inorganic phosphate in diverse maize germplasm to identify potential donor for low phytic acid (Lpa) trait in tropical genetic background.Crossref | GoogleScholarGoogle 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, 127
| Introgression of the low phytic acid locus (lpa2) into elite maize (Zea mays L.) inbreds through marker-assisted backcross breeding (MABB).Crossref | GoogleScholarGoogle Scholar |
Yuan F-J, Zhao H-J, Ren X-L, Zhu S-L, Fu X-J, Shu Q-Y (2007) Generation and characterization of two novel low phytate mutations in soybean (Glycine max L. Merr.). Theoretical and Applied Genetics 115, 945–957.
| Generation and characterization of two novel low phytate mutations in soybean (Glycine max L. Merr.).Crossref | GoogleScholarGoogle Scholar |
Zhou JR, Erdman JW (1995) Phytic acid in health and disease. Critical Reviews in Food Science and Nutrition 35, 495–508.
| Phytic acid in health and disease.Crossref | GoogleScholarGoogle Scholar |