Next-generation technologies for iron and zinc biofortification and bioavailability in cereal grains
S. Ibrahim A , B. Saleem A B , M. K. Naeem B , S. M. Arain C and M. R. Khan B DA National Centre for Bioinformatics, Quaid-i-Azam University, Islamabad, Pakistan.
B National Institute for Genomics and Advanced Biotechnology, National Agricultural Research Centre, Islamabad, Pakistan.
C Plant Breeding and Genetics Division, Nuclear Institute of Agriculture, NIA Tando Jam, Sindh, Pakistan.
D Corresponding author. Email: drmrkhan_nigab@yahoo.com
Crop and Pasture Science - https://doi.org/10.1071/CP20498
Submitted: 16 December 2020 Accepted: 13 July 2021 Published online: 3 November 2021
Abstract
Iron (Fe) and zinc (Zn) are recognised as micronutrients of clinical significance to public health globally. Major staple crops (wheat, rice and maize) contain insufficient levels of these micronutrients. Baseline concentrations in wheat and maize grains are 30 µg/g for Fe and 25 µg/g for Zn, and in rice grains, 2 µg/g for Fe and 16 µg/g for Zn. However, wheat grains should contain 59 μg Fe/g and 38 μg Zn/g if they are to meet 30–40% of the average requirement of an adult diet. Scientists are addressing malnutrition problems by trying to enhance Fe and Zn accumulation in grains through conventional and next-generation techniques. This article explores the applicability and efficiency of novel genome editing tools compared with conventional breeding for Fe and Zn biofortification and for improving the bioavailability of cereal grains. Some wheat varieties with large increases in Zn concentration have been developed through conventional breeding (e.g. BHU1, BHU-6 and Zincol-2016, with 35–42 µg Zn/g); however, there has been little such success with Fe concentration. Similarly, no rice variety has been developed through conventional breeding with the required grain Fe concentration of 14.5 µg/g. Transgenic approaches have played a significant role for Fe and Zn improvement in cereal crops but have the limitations of low acceptance and strict regulatory processes. Precise editing by CRISPR-Cas9 will help to enhance the Fe and Zn content in cereals without any linkage drag and biosafety issues. We conclude that there is an urgent need to biofortify cereal crops with Fe and Zn by using efficient next-generation approaches such as CRISPR/Cas9 so that the malnutrition problem, especially in developing countries, can be addressed.
Keywords: biofortification, CRISPR/Cas9, cereals, Fe, Zn, micronutrients, next-generation technologies, undernutrition.
References
Abid N, Khatoon A, Maqbool A, Irfan M, Bashir A, Asif I, et al (2017) Transgenic expression of phytase in wheat endosperm increases bioavailability of iron and zinc in grains. Transgenic Research 26, 109–122.| Transgenic expression of phytase in wheat endosperm increases bioavailability of iron and zinc in grains.Crossref | GoogleScholarGoogle Scholar | 27687031PubMed |
Agrawal PK, Kohli A, Twyman RM, Christou P (2005) Transformation of plants with multiple cassettes generates simple transgene integration patterns and high expression levels. Molecular Breeding 16, 247–260.
| Transformation of plants with multiple cassettes generates simple transgene integration patterns and high expression levels.Crossref | GoogleScholarGoogle Scholar |
Ahmar S, Gill RA, Jung KH, Faheem A, Qasim MU, Mubeen M, Zhou W (2020) Conventional and molecular techniques from simple breeding to speed breeding in crop plants: recent advances and future outlook. International Journal of Molecular Sciences 21, 2590
| Conventional and molecular techniques from simple breeding to speed breeding in crop plants: recent advances and future outlook.Crossref | GoogleScholarGoogle Scholar |
Alomari DZ, Eggert K, von Wiren N, Alqudah AM, Polley A, Plieske J, Ganal MW, Pillen K, Roder MS (2018) Identifying candidate genes for enhancing grain Zn concentration in wheat. Frontiers in Plant Science 9, 1313
| Identifying candidate genes for enhancing grain Zn concentration in wheat.Crossref | GoogleScholarGoogle Scholar | 30271416PubMed |
Aluru M, Xu Y, Guo R, Wang Z, Li S, White W, et al (2008) Generation of transgenic maize with enhanced provitamin A content. Journal of Experimental Botany 59, 3551–3562.
| Generation of transgenic maize with enhanced provitamin A content.Crossref | GoogleScholarGoogle Scholar | 18723758PubMed |
Aluru MR, Rodermel SR, Reddy MB (2011) Genetic modification of low phytic acid 1-1 maize to enhance iron content and bioavailability. Journal of Agricultural and Food Chemistry 59, 12954–12962.
| Genetic modification of low phytic acid 1-1 maize to enhance iron content and bioavailability.Crossref | GoogleScholarGoogle Scholar | 22088162PubMed |
Anandan A, Rajiv G, Eswaran R, Prakash M (2011) Genotypic variation and relationships between quality traits and trace elements in traditional and improved rice (Oryza sativa L.) genotypes. Journal of Food Science 76, H122–H130.
| Genotypic variation and relationships between quality traits and trace elements in traditional and improved rice (Oryza sativa L.) genotypes.Crossref | GoogleScholarGoogle Scholar | 22417360PubMed |
Anuradha K, Agarwal S, Rao YV, Rao KV, Viraktamath BC, Sarla N (2012) Mapping QTLs and candidate genes for iron and zinc concentrations in unpolished rice of Madhukar × Swarna RILs. GEN 508, 233–240.
| Mapping QTLs and candidate genes for iron and zinc concentrations in unpolished rice of Madhukar × Swarna RILs.Crossref | GoogleScholarGoogle Scholar |
Araki M, Nojima K, Ishii T (2014) Caution required for handling genome editing technology. Trends in Biotechnology 32, 234–237.
| Caution required for handling genome editing technology.Crossref | GoogleScholarGoogle Scholar | 24767735PubMed |
Banakar R, Alvarez-Fernandez A, Abadia J, Capell T, Christou P (2017a) The expression of heterologous Fe (III) phytosiderophore transporter HvYS1 in rice increases Fe uptake, translocation and seed loading and excludes heavy metals by selective Fe transport. Plant Biotechnology Journal 15, 423–432.
| The expression of heterologous Fe (III) phytosiderophore transporter HvYS1 in rice increases Fe uptake, translocation and seed loading and excludes heavy metals by selective Fe transport.Crossref | GoogleScholarGoogle Scholar | 27633505PubMed |
Beasley JT, Bonneau JP, Sánchez‐Palacios JT, Moreno‐Moyano LT, Callahan DL, Tako E, Johnson AA (2019) Metabolic engineering of bread wheat improves grain iron concentration and bioavailability. Plant Biotechnology Journal 17, 1514–1526.
| Metabolic engineering of bread wheat improves grain iron concentration and bioavailability.Crossref | GoogleScholarGoogle Scholar | 30623558PubMed |
Bhatti KK, Alok A, Kumar A, Kaur J, Tiwari S, Pandey AK (2016) Silencing of ABCC13 transporter in wheat reveals its involvement in grain development, phytic acid accumulation and lateral root formation. Journal of Experimental Botany 67, 4379–4389.
| Silencing of ABCC13 transporter in wheat reveals its involvement in grain development, phytic acid accumulation and lateral root formation.Crossref | GoogleScholarGoogle Scholar |
Blancquaert D, De-Steur H, Gellynck X, Van-Der Straeten D (2014) Present and future of folate biofortification of crop plants. Journal of Experimental Botany 65, 895–906.
| Present and future of folate biofortification of crop plants.Crossref | GoogleScholarGoogle Scholar | 24574483PubMed |
Blancquaert D, Van-daele J, Strobbe S, Kiekens F, Storozhenko S, De-Steur H, et al (2015) Improving folate (vitamin B9) stability in biofortified rice through metabolic engineering. Nature Biotechnology 33, 1076–1078.
| Improving folate (vitamin B9) stability in biofortified rice through metabolic engineering.Crossref | GoogleScholarGoogle Scholar | 26389575PubMed |
Borg S, Brinch-Pedersen H, Tauris B, Holm P (2009) Iron transport, deposition and bioavailability in the wheat and barley grain. Plant and Soil 325, 15–24.
| Iron transport, deposition and bioavailability in the wheat and barley grain.Crossref | GoogleScholarGoogle Scholar |
Borg S, Brinch-Pedersen H, Tauris B, Madsen LH, Darbani B, Noeparvar S, et al (2012) Wheat ferritins: improving the iron content of the wheat grain. Journal of Cereal Science 56, 204–213.
| Wheat ferritins: improving the iron content of the wheat grain.Crossref | GoogleScholarGoogle Scholar |
Borrill P, Connorton JM, Balk J, Miller AJ, Sanders D, Uauy C (2014) Biofortification of wheat grain with iron and zinc: integrating novel genomic resources and knowledge from model crops. Frontiers in Plant Science 5, article 53
| Biofortification of wheat grain with iron and zinc: integrating novel genomic resources and knowledge from model crops.Crossref | GoogleScholarGoogle Scholar |
Bouis HE, Saltzman A (2017) Improving nutrition through biofortification: a review of evidence from harvest plus, 2003 through 2016. Global Food Security 12, 49–58.
| Improving nutrition through biofortification: a review of evidence from harvest plus, 2003 through 2016.Crossref | GoogleScholarGoogle Scholar | 28580239PubMed |
Cakmak I, Torun A, Millet E, Feldman M, Fahima T, Korol A, et al (2004) Triticum dicoccoides: an important genetic resource for increasing zinc and iron concentration in modern cultivated wheat. Soil Science and Plant Nutrition 50, 1047–1054.
| Triticum dicoccoides: an important genetic resource for increasing zinc and iron concentration in modern cultivated wheat.Crossref | GoogleScholarGoogle Scholar |
Cakmak I, Pfeiffer WH, McClafferty B (2010) Biofortification of durum wheat with zinc and iron: a review. Cereal Chemistry 87, 10–20.
| Biofortification of durum wheat with zinc and iron: a review.Crossref | GoogleScholarGoogle Scholar |
Chang S, El Arifeen S, Bari S, Wahed MA, Rahman KM, Rahman MT, et al (2010) Supplementing iron and zinc: double blind, randomized evaluation of separate or combined delivery. European Journal of Clinical Nutrition 64, 153–160.
| Supplementing iron and zinc: double blind, randomized evaluation of separate or combined delivery.Crossref | GoogleScholarGoogle Scholar | 19904293PubMed |
Chen R, Xue G, Chen P, Yao B, Yang W, Ma Q, Fan Y, Zhao Z, Tarczynski MC, Shi J (2008) Transgenic maize plants expressing a fungal phytase gene. Transgenic Research 17, 633–643.
| Transgenic maize plants expressing a fungal phytase gene.Crossref | GoogleScholarGoogle Scholar | 17932782PubMed |
Chhuneja P, Dhaliwal HS, Bains NS, Singh K (2006) Aegilops kotschyi and Ae. tauschii are the sources for high grain iron and zinc. Plant Breeding 125, 529–531.
| Aegilops kotschyi and Ae. tauschii are the sources for high grain iron and zinc.Crossref | GoogleScholarGoogle Scholar |
Christian M, et al (2010) Targeting DNA double-strand breaks with TAL effector nucleases. Genetics 186, 757–761.
| Targeting DNA double-strand breaks with TAL effector nucleases.Crossref | GoogleScholarGoogle Scholar | 20660643PubMed |
CIMMYT (2016) Biofortification to fight hidden hunger in Zimbabwe. CIMMYT, El Batán, Mexico. Available at: http://www.cimmyt.org/biofortification-to-fight-hidden-hunger-in-zimbabwe/.
Connorton JM, Jones ER, Rodríguez-Ramiroetal I (2017) Wheat vacuolar iron transporter TaVIT2 transports Fe and Mn and is effective for biofortification. Plant Physiology 174, 2434–2444.
| Wheat vacuolar iron transporter TaVIT2 transports Fe and Mn and is effective for biofortification.Crossref | GoogleScholarGoogle Scholar | 28684433PubMed |
Crespo-Herrera LA, Velu G, Singh RP (2016) Quantitative trait loci mapping reveals pleiotropic effect for grain iron and zinc concentrations in wheat. Annals of Applied Biology 169, 27–35.
| Quantitative trait loci mapping reveals pleiotropic effect for grain iron and zinc concentrations in wheat.Crossref | GoogleScholarGoogle Scholar |
Das JK, Kumar R, Salam RA, Bhutta ZA (2013) Systematic review of zinc fortification trials. Annals of Nutrition & Metabolism 62, 44–56.
| Systematic review of zinc fortification trials.Crossref | GoogleScholarGoogle Scholar |
Demirci Y, Zhang B, Unver T (2018) CRISPR/Cas9: an RNA guided highly precise synthetic tool for plant genome editing. Journal of Cellular Physiology 233, 1844–1859.
| CRISPR/Cas9: an RNA guided highly precise synthetic tool for plant genome editing.Crossref | GoogleScholarGoogle Scholar | 28430356PubMed |
Díaz-Benito P, Banakar R, Rodríguez-Menéndez S, Capell T, Pereiro R, Christou P, Álvarez-Fernández A (2018) Iron and zinc in the embryo and endosperm of rice (Oryza sativa L.) seeds in contrasting 2′-deoxymugineic acid/nicotianamine scenarios. Frontiers in Plant Science 9, 1190
| Iron and zinc in the embryo and endosperm of rice (Oryza sativa L.) seeds in contrasting 2′-deoxymugineic acid/nicotianamine scenarios.Crossref | GoogleScholarGoogle Scholar | 30186295PubMed |
Dong W, Cheng Z, Wang X, Wang B, Zhang H, Su N, Yamamaro C, Lei C, Wang J, et al (2011) Determination of folate content in rice germplasm (Oryza sativa L.) using tri-enzyme extraction and microbiological assays. International Journal of Food Sciences and Nutrition 62, 537–543.
| Determination of folate content in rice germplasm (Oryza sativa L.) using tri-enzyme extraction and microbiological assays.Crossref | GoogleScholarGoogle Scholar | 21438705PubMed |
Drakakaki G, Marcel S, Glahn RP, Lund EK, Pariagh S, Fischer R, Christou P, Stoger E (2005) Endosperm-specific co-expression of recombinant soybean ferritin and Aspergillus phytase in maize results in significant increases in the levels of bioavailable iron. Plant Molecular Biology 59, 869–880.
Dubock A (2017) An overview of agriculture, nutrition and fortification, supplementation and biofortification: Golden Rice as an example for enhancing micronutrient intake. Agriculture & Food Security 6, 59
| An overview of agriculture, nutrition and fortification, supplementation and biofortification: Golden Rice as an example for enhancing micronutrient intake.Crossref | GoogleScholarGoogle Scholar |
EFSA (2012) Scientific opinion addressing the safety assessment of plants developed using Zinc Finger Nuclease 3 and other Site-Directed Nucleases with similar function. EFSA Journal 10, 2943
| Scientific opinion addressing the safety assessment of plants developed using Zinc Finger Nuclease 3 and other Site-Directed Nucleases with similar function.Crossref | GoogleScholarGoogle Scholar |
FAO, IFAD, WFP (2015) ‘The state of food insecurity in the world 2015: meeting the 2015 international hunger targets: taking stock of uneven progress.’ (FAO: Rome) http://www.fao.org/3/a-i4646e.pdf
Farhad M, Velu G, Hakim MA, Kabir MR, Alam MA, Mandal MS (2018) Development and deployment of biofortified and blast resistant wheat variety in Bangladesh. In ‘Book of Abstracts of the 13th International Gluten Workshop’. pp. 14–17. (UCOPress: Córdoba, Spain)
Feng Z, Mao Y, Xu N, Zhang B, Wei P, Yang DL, Wang Z, Zhang Z, Zheng R, Yang L, Zeng L, Liu X, Zhu JK (2014) Multigeneration analysis reveals the inheritance, specificity, and patterns of CRISPR/Cas induced gene modifications in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America 111, 4632–4637.
| Multigeneration analysis reveals the inheritance, specificity, and patterns of CRISPR/Cas induced gene modifications in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 24550464PubMed |
Fernie AR, Yan J (2019) De novo domestication: an alternative route toward new crops for the future. Molecular Plant 12, 615–631.
| De novo domestication: an alternative route toward new crops for the future.Crossref | GoogleScholarGoogle Scholar | 30999078PubMed |
Freeland-Graves JH, Sachdev PK, Binderberger AZ, Sosanya ME (2020) Global diversity of dietary intakes and standards for zinc, iron, and copper. Journal of Trace Elements in Medicine and Biology 61, 126515
| Global diversity of dietary intakes and standards for zinc, iron, and copper.Crossref | GoogleScholarGoogle Scholar | 32450495PubMed |
Garcia-Oliveira AL, Tan L, Fu Y, Sun C (2009) Genetic identification of quantitative trait loci for contents of mineral nutrients in rice grain. Journal of Integrative Plant Biology 51, 84–92.
| Genetic identification of quantitative trait loci for contents of mineral nutrients in rice grain.Crossref | GoogleScholarGoogle Scholar | 19166498PubMed |
Garcia-Oliveira AL, Chander S, Ortiz R, Menkir A, Gedil M (2018) Genetic basis and breeding perspectives of grain iron and zinc enrichment in cereals. Frontiers in Plant Science 9, 937
| Genetic basis and breeding perspectives of grain iron and zinc enrichment in cereals.Crossref | GoogleScholarGoogle Scholar | 30013590PubMed |
Garg M, Sharma N, Sharma S, Kapoor P, Kumar A, Chunduri V, Arora P (2018) Biofortified crops generated by breeding, agronomy, and transgenic approaches are improving lives of millions of people around the world. Frontiers in Nutrition 5, 12
| Biofortified crops generated by breeding, agronomy, and transgenic approaches are improving lives of millions of people around the world.Crossref | GoogleScholarGoogle Scholar | 29492405PubMed |
Gil-Humanes J, Wang Y, Liang Z, et al (2017) High-efficiency gene targeting in hexaploid wheat using DNA replicons and CRISPR/Cas9. The Plant Journal 89, 1251–1262.
| High-efficiency gene targeting in hexaploid wheat using DNA replicons and CRISPR/Cas9.Crossref | GoogleScholarGoogle Scholar | 27943461PubMed |
Gomez-Becerra HF, Erdem H, Yazici A, Tutus Y, Torun B, Ozturk L, Cakmak I (2010a) Grain concentrations of protein and mineral nutrients in a large collection of spelt wheat grown under different environments. Journal of Cereal Science 52, 342–349.
| Grain concentrations of protein and mineral nutrients in a large collection of spelt wheat grown under different environments.Crossref | GoogleScholarGoogle Scholar |
Gomez-Becerra HF, Yazici A, Ozturk L, Budak H, Peleg Z, Morgounov A, Fahima T, Saranga Y, Cakmak I (2010b) Genetic variation and environmental stability of grain mineral nutrient concentrations in Triticum dicoccoides under five environments. Euphytica 171, 39–52.
| Genetic variation and environmental stability of grain mineral nutrient concentrations in Triticum dicoccoides under five environments.Crossref | GoogleScholarGoogle Scholar |
Goto F, Yoshihara T, Shigemoto N, Toki S, Takaiwa F (1999) Iron fortification of rice seed by the soybean ferritin gene. Nature Biotechnology 17, 282–286.
| Iron fortification of rice seed by the soybean ferritin gene.Crossref | GoogleScholarGoogle Scholar | 10096297PubMed |
Gould J (2017) Nutrition: a world of insecurity. Nature 544, S6–S7.
| Nutrition: a world of insecurity.Crossref | GoogleScholarGoogle Scholar | 28445448PubMed |
Graham RD, Knez M, Welch RM (2012) How much nutritional iron deficiency in humans globally is due to an underlying zinc deficiency? Advances in Agronomy 115, 1–40.
| How much nutritional iron deficiency in humans globally is due to an underlying zinc deficiency?Crossref | GoogleScholarGoogle Scholar |
Gregorio GB, Senadhira D, Htut H, Graham RD (2000) Breeding for trace mineral density in rice. Food and Nutrition Bulletin 21, 382–386.
| Breeding for trace mineral density in rice.Crossref | GoogleScholarGoogle Scholar |
Guttieri MJ, 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 |
Guttieri MJ, Baenziger PS, Frels K, Carver B, Arnall B, Waters BM (2015) Variation for grain mineral concentration in a diversity panel of current and historical great plains hard winter wheat germplasm. Crop Science 55, 1035–1052.
| Variation for grain mineral concentration in a diversity panel of current and historical great plains hard winter wheat germplasm.Crossref | GoogleScholarGoogle Scholar |
Hartung F, Schiemann J (2014) Precise plant breeding using new genome editing techniques: opportunities, safety and regulation in the EU. The Plant Journal 78, 742–752.
| Precise plant breeding using new genome editing techniques: opportunities, safety and regulation in the EU.Crossref | GoogleScholarGoogle Scholar | 24330272PubMed |
HarvestPlus (2014) Biofortification progress briefs. HarvestPlus, Washington, DC. Available at: www.HarvestPlus.org
HarvestPlus (2018) Biofortification: the evidence: a summary of research that supports scaling up of biofortification to improve nutrition and health globally. HarvestPlus, Washington, DC. Available at: https://www.harvestplus.org/evidence-document
Haydon MJ, Kawachi M, Wirtz M, Hillmer S, Hell R, Krämer U (2012) Vacuolar nicotianamine has critical and distinct roles under iron deficiency and for zinc sequestration in Arabidopsis. Plant Cell 24, 724–737.
Hefferon KL (2016) Can biofortified crops help attain food security? Current Molecular Biology Reports 2, 180–185.
| Can biofortified crops help attain food security?Crossref | GoogleScholarGoogle Scholar |
Herzig P, Backhaus A, Seiffert U, Wirén N, Pillen K, Maurer A (2019) Genetic dissection of grain elements predicted by hyperspectral imaging associated with yield-related traits in a wild barley NAM population. Plant Science 285, 151–164.
| Genetic dissection of grain elements predicted by hyperspectral imaging associated with yield-related traits in a wild barley NAM population.Crossref | GoogleScholarGoogle Scholar | 31203880PubMed |
Hindu V, Palacios-Rojas N, Babu R, Suwarno WB, Rashid Z, Usha R, et al (2018) Identification and validation of genomic regions influencing kernel zinc and iron in maize. Theoretical and Applied Genetics 131, 1443–1457.
| Identification and validation of genomic regions influencing kernel zinc and iron in maize.Crossref | GoogleScholarGoogle Scholar | 29574570PubMed |
Holm PB, Kristiansen KN, Pedersen HB (2002) Transgenic approaches in commonly consumed cereals to improve iron and zinc content and bioavailability. The Journal of Nutrition 132, 514S–516S.
| Transgenic approaches in commonly consumed cereals to improve iron and zinc content and bioavailability.Crossref | GoogleScholarGoogle Scholar | 11880583PubMed |
Hsu PD, Lander ES, Zhang F (2014) Review development and applications of CRISPR/Cas9 for genome engineering. Cell 157, 1262–1278.
| Review development and applications of CRISPR/Cas9 for genome engineering.Crossref | GoogleScholarGoogle Scholar | 24906146PubMed |
Huang S, Weigel D, Beachy RN, Li J (2016) A proposed regulatory framework for genome-edited crops. Nature Genetics 48, 109–111.
| A proposed regulatory framework for genome-edited crops.Crossref | GoogleScholarGoogle Scholar | 26813761PubMed |
Imbard A, Benoist JF, Blom HJ (2013) Neural tube defects, folic acid and methylation. International Journal of Environmental Research and Public Health 10, 4352–4389.
| Neural tube defects, folic acid and methylation.Crossref | GoogleScholarGoogle Scholar | 24048206PubMed |
Jin T, Zhou J, Chen J, Zhu L, Zhao Y, Huang Y (2013) The genetic architecture of zinc and iron content in maize grains as revealed by QTL mapping and meta-analysis. Breeding Science 63, 317–324.
| The genetic architecture of zinc and iron content in maize grains as revealed by QTL mapping and meta-analysis.Crossref | GoogleScholarGoogle Scholar | 24273427PubMed |
Jinek M, Chylinski K, Fonfara I, Hauer M, Doudna JA, Charpentier E (2012) A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 337, 816–821.
| A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity.Crossref | GoogleScholarGoogle Scholar | 22745249PubMed |
Johnson JA (2018) Better together: partnership around zinc maize improves nutrition in Guatemala. CIMMYT, El Batán, Mexico. Available at: www.cimmyt.org/news/better-together-partnership-around-zinc-maize-improves-nutrition-in-guatemala
Johnson AA, Kyriacou B, Callahan DL, Carruthers L, Stangoulis J, Lombi E, Tester M (2011) Constitutive overexpression of the OsNAS gene family reveals single-gene strategies for effective iron-and zinc-biofortification of rice endosperm. PLoS One 6, e24476
| Constitutive overexpression of the OsNAS gene family reveals single-gene strategies for effective iron-and zinc-biofortification of rice endosperm.Crossref | GoogleScholarGoogle Scholar | 21915334PubMed |
Joshi AK, Crossa J, Arun B, et al (2010) Genotype×environment interaction for zinc and iron concentration of wheat grain in eastern Gangetic plains of India. Field Crops Research 116, 268–277.
| Genotype×environment interaction for zinc and iron concentration of wheat grain in eastern Gangetic plains of India.Crossref | GoogleScholarGoogle Scholar |
Kanchiswamy CN (2016) DNA-free genome editing methods for targeted crop improvement. Plant Cell Reports 35, 1469–1474.
| DNA-free genome editing methods for targeted crop improvement.Crossref | GoogleScholarGoogle Scholar | 27100964PubMed |
Kassebaum NJ, Jasrasaria R, Naghavi M, Wulf SK, Johns N, Lozano R, et al (2014) A systematic analysis of global anemia burden from 1990 to 2010. Blood 123, 615–624.
| A systematic analysis of global anemia burden from 1990 to 2010.Crossref | GoogleScholarGoogle Scholar | 24297872PubMed |
Khatodia S, Bhatotia K, Passricha N, et al (2016) The CRISPR/Cas genome-editing tool: application in improvement of crops. Frontiers in Plant Science 7, 506
| The CRISPR/Cas genome-editing tool: application in improvement of crops.Crossref | GoogleScholarGoogle Scholar | 27148329PubMed |
Kotla A, Phuke R, Hariprasanna K, et al (2019) Identification of QTLs and candidate genes for high grain Fe and Zn concentration in sorghum [Sorghum bicolor (L.) Moench]. Journal of Cereal Science 90, 102850
| Identification of QTLs and candidate genes for high grain Fe and Zn concentration in sorghum [Sorghum bicolor (L.) Moench].Crossref | GoogleScholarGoogle Scholar |
Kumar J, Mir RR, Kumar N, Kumar A, Mohan A, Prabhu KV, Balyan HS, Gupta PK (2010) Marker-assisted selection for pre-harvest sprouting tolerance and leaf rust resistance in bread wheat. Plant Breeding 129, 617–621.
| Marker-assisted selection for pre-harvest sprouting tolerance and leaf rust resistance in bread wheat.Crossref | GoogleScholarGoogle Scholar |
Kumar J, Jaiswal V, Kumar A, Kumar N, Mir RR, Kumar S, Dhariwal R, Tyagi S, Khandelwal M, Prabhu KV, et al (2011) Introgression of a major gene for high grain protein content in some Indian bread wheat cultivars. Field Crops Research 123, 226–233.
| Introgression of a major gene for high grain protein content in some Indian bread wheat cultivars.Crossref | GoogleScholarGoogle Scholar |
Lassoued R, Macall DM, Hesseln H, Phillips PW, Smyth SJ (2019) Benefits of genome-edited crops: expert opinion. Transgenic Research 28, 247–256.
| Benefits of genome-edited crops: expert opinion.Crossref | GoogleScholarGoogle Scholar | 30830581PubMed |
Lee S, An G (2009) Over-expression of OsIRT1 leads to increased iron and zinc accumulations in rice. Plant, Cell & Environment 32, 408–416.
| Over-expression of OsIRT1 leads to increased iron and zinc accumulations in rice.Crossref | GoogleScholarGoogle Scholar |
Lee S, Jeon US, Lee SJ, et al (2009) Iron fortification of rice seeds through activation of the nicotianamine synthase gene. Proceedings of the National Academy of Sciences of the United States of America 106, 22014–22019.
| Iron fortification of rice seeds through activation of the nicotianamine synthase gene.Crossref | GoogleScholarGoogle Scholar | 20080803PubMed |
Lee S, Persson DP, Hansen TH, Husted S, et al (2011) Bio-available zinc in rice seeds is increased by activation tagging of nicotianamine synthase. Plant Biotechnology Journal 9, 865–873.
Lei Y, Lu L, Liu HY, Li S, Xing F, Chen LL (2014) CRISPR-P: a web tool for synthetic single-guide RNA design of CRISPR-system in plants. Molecular Plant 7, 1494–1496.
| CRISPR-P: a web tool for synthetic single-guide RNA design of CRISPR-system in plants.Crossref | GoogleScholarGoogle Scholar | 24719468PubMed |
Li M, Li X, Zhou Z, Wu P, Fang M, Pan X, Lin Q, Luo W, Wu G, Li H (2016) Reassessment of the four yield-related genes Gn1a, DEP1, GS3, and IPA1 in rice using a CRISPR/Cas9 system. Frontiers in Plant Science 7, 377
| Reassessment of the four yield-related genes Gn1a, DEP1, GS3, and IPA1 in rice using a CRISPR/Cas9 system.Crossref | GoogleScholarGoogle Scholar | 27066031PubMed |
Liang Z, Zhang K, Chen K, Gao C (2014) Targeted mutagenesis in Zea mays using TALENs and the CRISPR/Cas system. Journal of Genetics and Genomics 41, 63–68.
| Targeted mutagenesis in Zea mays using TALENs and the CRISPR/Cas system.Crossref | GoogleScholarGoogle Scholar | 24576457PubMed |
Liang G, Huimin Z, Dengji L, Diqiu Y (2016) Selection of highly efficient sgRNAs for CRISPR/Cas9-based plant genome editing. Scientific Reports 6, 21451
| Selection of highly efficient sgRNAs for CRISPR/Cas9-based plant genome editing.Crossref | GoogleScholarGoogle Scholar | 26891616PubMed |
Liang Z, Chen K, Li T, Zhang Y, Wang Y, Zhao Q, Liu J, Zhang H, Liu C, Ran Y, Gao C (2017) Efficient DNA-free genome editing of bread wheat using CRISPR/Cas9 ribonucleoprotein complexes. Nature Communications 8, 14261
| Efficient DNA-free genome editing of bread wheat using CRISPR/Cas9 ribonucleoprotein complexes.Crossref | GoogleScholarGoogle Scholar | 28098143PubMed |
Liu QL, Xu XH, Ren XL, Fu HW, Wu DX, Shu QY (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 | 17219209PubMed |
Liu S, Rudd JC, Bai G, Haley SD, et al (2014) Molecular markers linked to important genes in hard winter wheat. Crop Science 54, 1304–1321.
| Molecular markers linked to important genes in hard winter wheat.Crossref | GoogleScholarGoogle Scholar |
Lu K, Li L, Zheng X, Zhang Z, Mou T, Hu Z (2008) Quantitative trait loci controlling Cu, Ca, Zn, Mn and Fe content in rice grains. Journal of Genetics 87, 305–310.
| Quantitative trait loci controlling Cu, Ca, Zn, Mn and Fe content in rice grains.Crossref | GoogleScholarGoogle Scholar | 19147920PubMed |
Mackelprang R, Lemaux PG (2020) Genetic engineering and editing of plants: an analysis of new and persisting questions. Annual Review of Plant Biology 71, 659–687.
| Genetic engineering and editing of plants: an analysis of new and persisting questions.Crossref | GoogleScholarGoogle Scholar | 32023090PubMed |
Maganti S, Swaminathan R, Parida A (2020) Variation in iron and zinc content in traditional rice genotypes. Agricultural Research 9, 316–328.
Mageto EK, Crossa J, Pérez-Rodríguez P, Dhliwayo T, Palacios-Rojas N, Lee M, Guo R, San Vicente F, Zhang X, Hindu V (2020) Genomic prediction with genotype by environment interaction analysis for kernel zinc concentration in tropical maize germplasm. G3 10, 2629–2639.
| Genomic prediction with genotype by environment interaction analysis for kernel zinc concentration in tropical maize germplasm.Crossref | GoogleScholarGoogle Scholar | 32482728PubMed |
Mali P, Esvelt KM, Church GM (2013) Cas9 as a versatile tool for engineering biology. Nature Methods 10, 957–963.
| Cas9 as a versatile tool for engineering biology.Crossref | GoogleScholarGoogle Scholar | 24076990PubMed |
Manickavelu A, Hattori T, Yamaoka S, Yoshimura K, Kondou Y, Onogi A, Matsui M, Iwata H, Ban T (2017) Genetic nature of elemental contents in wheat grains and its genomic prediction: toward the effective use of wheat landraces from Afghanistan. PLoS One 12, e0169416
| Genetic nature of elemental contents in wheat grains and its genomic prediction: toward the effective use of wheat landraces from Afghanistan.Crossref | GoogleScholarGoogle Scholar | 28072876PubMed |
Masuda H, Suzuki M, Morikawa KC, Kobayashi T, Nakanishi H, Takahashi M, et al (2008) Increase in iron and zinc concentrations in rice grains via the introduction of barley genes involved in phytosiderophore synthesis. Rice 1, 100–108.
| Increase in iron and zinc concentrations in rice grains via the introduction of barley genes involved in phytosiderophore synthesis.Crossref | GoogleScholarGoogle Scholar |
Meng X, Yu H, Zhang Y, Zhuang F, Song X, Gao S, Gao C, Li J (2017) Construction of a genome-wide mutant library in rice using CRISPR/Cas9. Molecular Plant 10, 1238–1241.
| Construction of a genome-wide mutant library in rice using CRISPR/Cas9.Crossref | GoogleScholarGoogle Scholar | 28645639PubMed |
Mikkelsen MD, Pedas P, Schiller M, et al (2012) Barley HvHMA1 is a heavy metal pump involved in mobilizing organellar Zn and Cu and plays a role in metal loading into grains. PLoS One 7, e49027
| Barley HvHMA1 is a heavy metal pump involved in mobilizing organellar Zn and Cu and plays a role in metal loading into grains.Crossref | GoogleScholarGoogle Scholar | 23155447PubMed |
Miladinovic D, Antunes D, Yildirim K, Bakhsh A, Cvejić S, Kondić-Špika A, et al (2021) Targeted plant improvement through genome editing: from laboratory to field. Plant Cell Reports 40, 935–951.
Miller JC, Holmes MC, Wang J, Guschin DY, Lee YL, Rupniewski I, Beausejour CM, Waite AJ, Wang NS, Kim KA, Gregory PD, Pabo CO, Rebar EJ (2007) An improved zinc-finger nuclease architecture for highly specific genome editing. Nature Biotechnology 25, 778–785.
| An improved zinc-finger nuclease architecture for highly specific genome editing.Crossref | GoogleScholarGoogle Scholar | 17603475PubMed |
Monasterio I, Graham RD (2000) Breeding for trace minerals in wheat. Food and Nutrition Bulletin 21, 392–396.
| Breeding for trace minerals in wheat.Crossref | GoogleScholarGoogle Scholar |
Muthayya A, Rah JH, Sugimoto JD, Roos F, Kraemer K, Black RE (2013) The global hidden hunger indices and maps: an advocacy tool for action. PLoS One 8, e67860
| The global hidden hunger indices and maps: an advocacy tool for action.Crossref | GoogleScholarGoogle Scholar |
Neelam K, Rawat N, Tiwari V, Prasad R, Tripathi S, Randhawa G, Dhaliwal H (2012) Evaluation and identification of wheat-Aegilops addition lines controlling high grain iron and zinc concentration and mugineic acid production. Cereal Research Communications 40, 53–61.
| Evaluation and identification of wheat-Aegilops addition lines controlling high grain iron and zinc concentration and mugineic acid production.Crossref | GoogleScholarGoogle Scholar |
Norton GJ, Deacon CM, Xiong L, Huang S, Meharg AA, Price AH (2010) Genetic mapping of the rice ionome in leaves and grain: identification of QTLs for 17 elements including arsenic, cadmium, iron and selenium. Plant and Soil 329, 139–153.
| Genetic mapping of the rice ionome in leaves and grain: identification of QTLs for 17 elements including arsenic, cadmium, iron and selenium.Crossref | GoogleScholarGoogle Scholar |
Ortiz-Monasterio I, Palacios-Rojas N, Meng E, Pixley K, Trethowan R, Pena RJ (2007) Enhancing the mineral and vitamin content of wheat and maize through plant breeding. Journal of Cereal Science 46, 293–307.
| Enhancing the mineral and vitamin content of wheat and maize through plant breeding.Crossref | GoogleScholarGoogle Scholar |
Pachón H, Ortiz DA, Araujo C, Blair MW, Restrepo J (2009) Iron, zinc, and protein bioavailability proxy measures of meals prepared with nutritionally enhanced beans and maize. Journal of Food Science 74, H147–H154.
| Iron, zinc, and protein bioavailability proxy measures of meals prepared with nutritionally enhanced beans and maize.Crossref | GoogleScholarGoogle Scholar | 19646048PubMed |
Pearce S, Tabbita F, Cantu D, et al (2014) Regulation of Zn and Fe transporters by the GPC1gene during early wheat monocarpic senescence. BMC Plant Biology 14, 368
| Regulation of Zn and Fe transporters by the GPC1gene during early wheat monocarpic senescence.Crossref | GoogleScholarGoogle Scholar | 25524236PubMed |
Phuke RM, Anuradha K, Radhika K, Jabeen F, Anuradha G, Ramesh T, Hariprasanna K, Mehtre SP, et al (2017) Genetic variability, genotype × environment interaction, correlation, and GGE biplot analysis for grain iron and zinc concentration and other agronomic traits in RIL population of sorghum (Sorghum bicolor L. Moench). Frontiers in Plant Science 8, 712
| Genetic variability, genotype × environment interaction, correlation, and GGE biplot analysis for grain iron and zinc concentration and other agronomic traits in RIL population of sorghum (Sorghum bicolor L. Moench).Crossref | GoogleScholarGoogle Scholar | 28529518PubMed |
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 | 14523526PubMed |
Poutanen K, Shepherd R, Shewry P, Delcour J, Bjorck I, van-der Kamp J (2008) Beyond whole grain: the European HEALTHGRAIN project aims at healthier cereal foods. Cereal Foods World 53, 32–35.
| Beyond whole grain: the European HEALTHGRAIN project aims at healthier cereal foods.Crossref | GoogleScholarGoogle Scholar |
Prasanna BM, Palacios-Rojas N, Hossain F, Muthusamy V, Menkir A, Dhliwayo T, et al (2020) Molecular breeding for nutritionally enriched maize: status and prospects. Frontiers in Genetics 10, 1392
| Molecular breeding for nutritionally enriched maize: status and prospects.Crossref | GoogleScholarGoogle Scholar | 32153628PubMed |
Prom-u-thai C, Fukai S, Godwin ID, Huang L (2007) Genotypic variation of iron partitioning in rice grain. Journal of the Science of Food and Agriculture 87, 2049–2054.
| Genotypic variation of iron partitioning in rice grain.Crossref | GoogleScholarGoogle Scholar |
Qamar ZU, Hameed A, Ashraf M, Rizwan M, Akhtar M (2019) Development and molecular characterization of low phytate basmati rice through induced mutagenesis, hybridization, backcross, and marker assisted breeding. Frontiers in Plant Science 10, 1525
| Development and molecular characterization of low phytate basmati rice through induced mutagenesis, hybridization, backcross, and marker assisted breeding.Crossref | GoogleScholarGoogle Scholar | 31850026PubMed |
Qin H, Cai Y, Liu Z, Wang G, Wang J, Guo Y, Wang H (2012) Identification of QTL for zinc and iron concentration in maize kernel and cob. Euphytica 187, 345–358.
| Identification of QTL for zinc and iron concentration in maize kernel and cob.Crossref | GoogleScholarGoogle Scholar |
Ramirez CL, et al (2008) Unexpected failure rates for modular assembly of engineered zinc fingers. Nature Methods 5, 374–375.
| Unexpected failure rates for modular assembly of engineered zinc fingers.Crossref | GoogleScholarGoogle Scholar | 18446154PubMed |
Rawat N, Tiwari VK, Singh N, Randhawa GS, Singh K, Chhuneja P, et al (2009) Evaluation and utilization of Aegilops and wild Triticum species for enhancing iron and zinc content in wheat. Genetic Resources and Crop Evolution 56, 53–64.
| Evaluation and utilization of Aegilops and wild Triticum species for enhancing iron and zinc content in wheat.Crossref | GoogleScholarGoogle Scholar |
Rayman MP, Infante HG, Sargent M (2008) Food-chain selenium and human health: spotlight on speciation. British Journal of Nutrition 100, 238–253.
| Food-chain selenium and human health: spotlight on speciation.Crossref | GoogleScholarGoogle Scholar |
Reuscher S, Kolter A, Hoffmann A, Pillen K, Krämer U (2016) Quantitative trait loci and inter-organ partitioning for essential metal and toxic analogue accumulation in barley. PLoS One 11, e0153392
| Quantitative trait loci and inter-organ partitioning for essential metal and toxic analogue accumulation in barley.Crossref | GoogleScholarGoogle Scholar | 27078500PubMed |
Schmidt C, Pacher M, Puchta H (2019) Efficient induction of heritable inversions in plant genomes using the CRISPR/Cas system. The Plant Journal 98, 577–589.
| Efficient induction of heritable inversions in plant genomes using the CRISPR/Cas system.Crossref | GoogleScholarGoogle Scholar | 30900787PubMed |
Shan Q, Wang Y, Li J, Zhang Y, Chen K, Liang Z, Zhang K, Liu J, Xi JJ, Qiu JL, Gao C (2013) Targeted genome modification of crop plants using a CRISPR-Cas system. Nature Biotechnology 31, 686–688.
| Targeted genome modification of crop plants using a CRISPR-Cas system.Crossref | GoogleScholarGoogle Scholar | 23929338PubMed |
Shan Q, Wang Y, Li J, Gao C (2014) Genome editing in rice and wheat using the CRISPR/Cas system. Nature Protocols 9, 2395–2410.
| Genome editing in rice and wheat using the CRISPR/Cas system.Crossref | GoogleScholarGoogle Scholar | 25232936PubMed |
Shan Q, Zhang Y, Chen K, Zhang K, Gao C (2015) Creation of fragrant rice by targeted knockout of the OsBADH2 gene using TALEN technology. Plant Biotechnology Journal 13, 791–800.
| Creation of fragrant rice by targeted knockout of the OsBADH2 gene using TALEN technology.Crossref | GoogleScholarGoogle Scholar | 25599829PubMed |
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 | 12586875PubMed |
Shi R, Li H, Tong Y, Jing R, Zhang F, Zou C (2008) Identification of quantitative trait locus of zinc and phosphorus density in wheat (Triticum aestivum L.) grain. Plant and Soil 306, 95–104.
| Identification of quantitative trait locus of zinc and phosphorus density in wheat (Triticum aestivum L.) grain.Crossref | GoogleScholarGoogle Scholar |
Shukla VK, Doyon Y, Miller JC, DeKelver RC, Moehle EA, Worden SE, Mitchell JC, Arnold NL, Gopalan S, Meng X, Choi VM, Rock JM, Wu YY, et al (2009) Precise genome modification in the crop species Zea mays using zinc-finger nucleases. Nature 459, 437–441.
| Precise genome modification in the crop species Zea mays using zinc-finger nucleases.Crossref | GoogleScholarGoogle Scholar | 19404259PubMed |
Singh SP, Keller B, Gruissem W, Bhullar NK (2017) Rice NICOTIANAMINE SYNTHASE 2 expression improves dietary iron and zinc levels in wheat. Theoretical and Applied Genetics 130, 283–292.
| Rice NICOTIANAMINE SYNTHASE 2 expression improves dietary iron and zinc levels in wheat.Crossref | GoogleScholarGoogle Scholar | 27722771PubMed |
Smith J, Grizot S, Arnould S, Duclert A, Epinat JC, Chames P, Montoya G (2006) A combinatorial approach to create artificial homing endonucleases cleaving chosen sequences. Nucleic Acids Research 34, e149
| A combinatorial approach to create artificial homing endonucleases cleaving chosen sequences.Crossref | GoogleScholarGoogle Scholar | 17130168PubMed |
Srinivasa J, Arun B, Mishra VK, Singh GP, Velu G, Babu R, Vasistha NK, Joshi AK (2014) Zinc and iron concentration QTL mapped in a Triticum spelta × T. aestivum cross. Theoretical and Applied Genetics 127, 1643–1651.
| Zinc and iron concentration QTL mapped in a Triticum spelta × T. aestivum cross.Crossref | GoogleScholarGoogle Scholar | 24865507PubMed |
Storozhenko S, De Brouwer V, Volckaert M, Navarrete O, Blancquaert D, Zhang GF, et al (2007) Folate fortification of rice by metabolic engineering. Nature Biotechnology 25, 1277–1279.
| Folate fortification of rice by metabolic engineering.Crossref | GoogleScholarGoogle Scholar | 17934451PubMed |
Sui X, Zhao Y, Wang S, et al (2012) Improvement Fe content of wheat (Triticum aestivum) grain by soybean ferritin expression cassette without vector backbone sequence. Journal of Agricultural Biotechnology 20, 766–773.
Suzuki M, Morikawa KC, Nakanishi H, et al (2008) Transgenic rice lines that include barley genes have increased tolerance to low iron availability in a calcareous paddy soil. Soil Science & Plant Nutrition 54, 77–85.
Takahashi M, Nakanishi H, Kawasaki S, Nishizawa NK, Mori S (2001) Enhanced tolerance of rice to low iron availability in alkaline soils using barley nicotianamine aminotransferase genes. Nature Biotechnology 19, 466–469.
| Enhanced tolerance of rice to low iron availability in alkaline soils using barley nicotianamine aminotransferase genes.Crossref | GoogleScholarGoogle Scholar | 11329018PubMed |
Taylor G, Petrucci L, Lambert A, Baxter S, Jarjour J, Stoddard B (2012) LAHEDES: the LAGLIDADG homing endonuclease database and engineering server. Nucleic Acids Research 40, W110–W116.
| LAHEDES: the LAGLIDADG homing endonuclease database and engineering server.Crossref | GoogleScholarGoogle Scholar | 22570419PubMed |
Tiwari VK, Rawat N, Chhuneja P, Neelam K, Aggarwal R, Randhawa GS, et al (2009) Mapping of quantitative trait loci for grain iron and zinc concentration in diploid A genome wheat. The Journal of Heredity 100, 771–776.
| Mapping of quantitative trait loci for grain iron and zinc concentration in diploid A genome wheat.Crossref | GoogleScholarGoogle Scholar | 19520762PubMed |
Tiwari VK, Rawat N, Neelam K, Kumar S, Randhawa GS, Dhaliwal HS (2010) Substitutions of 2S and 7U chromosomes of Aegilops kotschyi in wheat enhance grain iron and zinc concentration. Theoretical and Applied Genetics 121, 259–269.
| Substitutions of 2S and 7U chromosomes of Aegilops kotschyi in wheat enhance grain iron and zinc concentration.Crossref | GoogleScholarGoogle Scholar | 20221581PubMed |
Tiwari C, Wallwork H, Balasubramaniam A, Mishra VK, Velu G, Stangoulis J, Kumar U, Joshi AK (2016) Molecular mapping of quantitative trait loci for zinc, iron and protein content in the grains of hexaploid wheat. Euphytica 207, 563–570.
| Molecular mapping of quantitative trait loci for zinc, iron and protein content in the grains of hexaploid wheat.Crossref | GoogleScholarGoogle Scholar |
Tyagi S, Mir RR, Kaur H, Chhuneja P, Ramesh B, Balyan HS, Gupta PK (2014) Marker-assisted pyramiding of eight QTLs/genes for seven different traits in common wheat (Triticum aestivum L.). Molecular Breeding 34, 167–175.
| Marker-assisted pyramiding of eight QTLs/genes for seven different traits in common wheat (Triticum aestivum L.).Crossref | GoogleScholarGoogle Scholar |
Tyagi S, Choudhary R, Das A, Won SY, Shukla P (2020) CRISPR/Cas9 system: a genome-editing tool with endless possibilities. Journal of Biotechnology 319, 36–53.
| CRISPR/Cas9 system: a genome-editing tool with endless possibilities.Crossref | GoogleScholarGoogle Scholar | 32446977PubMed |
Uauy C, Distelfeld A, Fahima T, Blechl A, Dubcovsky J (2006) A NAC Gene regulating senescence improves grain protein, zinc, and iron content in wheat. Science 314, 1298–1301.
| A NAC Gene regulating senescence improves grain protein, zinc, and iron content in wheat.Crossref | GoogleScholarGoogle Scholar | 17124321PubMed |
Vasconcelos M, Datta K, Oliva N, Khalekuzzaman M, Torrizo L, Krishnan S, et al (2003) Enhanced iron and zinc accumulation in transgenic rice with the ferritin gene. Plant Science 164, 371–378.
| Enhanced iron and zinc accumulation in transgenic rice with the ferritin gene.Crossref | GoogleScholarGoogle Scholar |
Velu G, Singh RP, Huerta-Espino J, Peña RJ, Arun B, Mahendru-Singh A, Yaqub Mujahid M, Sohu VS, Mavi GS, Crossa J, Alvarado G, Joshi AK, Pfeiffer WH (2012) Performance of biofortified spring wheat genotypes in target environments for grain zinc and iron concentrations. Field Crops Research 137, 261–267.
| Performance of biofortified spring wheat genotypes in target environments for grain zinc and iron concentrations.Crossref | GoogleScholarGoogle Scholar |
Velu G, Ortiz-Monasterio I, Cakmak I, Hao I, Singh RP (2014) Biofortification strategies to increase grain zinc and iron concentrations in wheat. Journal of Cereal Science 59, 365–372.
| Biofortification strategies to increase grain zinc and iron concentrations in wheat.Crossref | GoogleScholarGoogle Scholar |
Velu G, Crossa J, Singh RP, Hao Y, Dreisigacker S, Perez‐Rodriguez P, Joshi AK, Chatrath R, Gupta V, Balasubramaniam A, Tiwari C, Mishra VK, Sohu VS, Mavi GS (2016a) Genomic prediction for grain zinc and iron concentrations in spring wheat. Theoretical and Applied Genetics 129, 1595–1605.
| Genomic prediction for grain zinc and iron concentrations in spring wheat.Crossref | GoogleScholarGoogle Scholar | 27170319PubMed |
Velu G, Tutus Y, Gomez-Becerra HF, Hao Y, Demir L, Kara R, CrespoHerrera LA, Orhan S, Yazici A, Singh RP, Cakmak I (2017) QTL mapping for grain zinc and iron concentrations and zinc efficiency in a tetraploid and hexaploid wheat mapping populations. Plant and Soil 411, 81–99.
| QTL mapping for grain zinc and iron concentrations and zinc efficiency in a tetraploid and hexaploid wheat mapping populations.Crossref | GoogleScholarGoogle Scholar |
Velu G, Singh RP, Crespo-Herrera L, Juliana P, Dreisigacker S, Valluru R, Stangoulis J, Sohu VS, Mavi GS, Mishra VK, Balasubramaniam A, Chatrath R, Gupta V, Singh GP, Joshi AK (2018) Genetic dissection of grain zinc concentration in spring wheat for mainstreaming biofortification in CIMMYT wheat breeding. Scientific Reports 8, 13526
| Genetic dissection of grain zinc concentration in spring wheat for mainstreaming biofortification in CIMMYT wheat breeding.Crossref | GoogleScholarGoogle Scholar | 30201978PubMed |
Velu G, Crespo Herrera L, Guzman C, Huerta J, Payne T, Singh RP (2019) Assessing genetic diversity to breed competitive biofortified wheat with enhanced grain Zn and Fe concentrations. Frontiers in Plant Science 9, 1971
| Assessing genetic diversity to breed competitive biofortified wheat with enhanced grain Zn and Fe concentrations.Crossref | GoogleScholarGoogle Scholar | 30687366PubMed |
Vishwakarma MK, Mishra V, Gupta P, Yadav P, Kumar H, Joshi AK (2014) Introgression of the high grain protein gene Gpc-B1 in an elite wheat variety of Indo-Gangetic plains through marker assisted backcross breeding. Current Plant Biology 1, 60–67.
| Introgression of the high grain protein gene Gpc-B1 in an elite wheat variety of Indo-Gangetic plains through marker assisted backcross breeding.Crossref | GoogleScholarGoogle Scholar |
Voytas DF, Gao C (2014) Precision genome engineering and agriculture: opportunities and regulatory challenges. PLoS Biology 12, e1001877
| Precision genome engineering and agriculture: opportunities and regulatory challenges.Crossref | GoogleScholarGoogle Scholar | 24915127PubMed |
Waltz E (2018) With a free pass, CRISPR-edited plants reach market in record time. Nature Biotechnology 36, 6–7.
| With a free pass, CRISPR-edited plants reach market in record time.Crossref | GoogleScholarGoogle Scholar | 29319694PubMed |
Wang Y, Cheng X, Shan Q, Zhang Y, Liu J, Gao C, Qiu JL (2014) Simultaneous editing of three homoeoalleles in hexaploid bread wheat confers heritable resistance to powdery mildew. Nature Biotechnology 32, 947–951.
| Simultaneous editing of three homoeoalleles in hexaploid bread wheat confers heritable resistance to powdery mildew.Crossref | GoogleScholarGoogle Scholar | 25038773PubMed |
Wang W, Akhunova A, Chao S, Akhunov E (2016) Optimizing multiplex CRISPR/Cas9-based genome editing for wheat. bioRxiv 15, 35
| Optimizing multiplex CRISPR/Cas9-based genome editing for wheat.Crossref | GoogleScholarGoogle Scholar |
Weeks DP, Spalding MH, Yang B (2016) Use of designer nucleases for targeted gene and genome editing in plants. Plant Biotechnology Journal 14, 483–495.
| Use of designer nucleases for targeted gene and genome editing in plants.Crossref | GoogleScholarGoogle Scholar | 26261084PubMed |
Welch RM, Graham RD (2004) Breeding for micronutrients in staple food crops from a human nutrition perspective. Journal of Experimental Botany 55, 353–364.
| Breeding for micronutrients in staple food crops from a human nutrition perspective.Crossref | GoogleScholarGoogle Scholar | 14739261PubMed |
WHO (2016) Global and regional trends by UN Regions, 1990–2025. Stunting: 1990–2025. WHO Global Health Observatory Data Repository. World Health Organization, Geneva. Available at: http://apps.who.int/gho/data/node.main
Woo JW, Kim J, Kwon S, Corvala’n C, Cho SW, Kim H, Kim SG, Kim ST, Choe S, Kim J (2015) DNA-free genome editing in plants with preassembled CRISPR/Cas9 ribonucleoproteins. Nature Biotechnology 33, 1162–1164.
| DNA-free genome editing in plants with preassembled CRISPR/Cas9 ribonucleoproteins.Crossref | GoogleScholarGoogle Scholar | 26479191PubMed |
Xiaoyan S, Yan Z, Shubin W (2012) Improvement Fe content of wheat (Triticum aestivum) grain by soybean ferritin expression cassette without vector backbone sequence. Journal of Agricultural Biotechnology 20, 766–773.
Xie K, Minkenberg B, Yang Y (2015) Boosting CRISPR/Cas9 multiplex editing capability with the endogenous tRNA processing system. Proceedings of the National Academy of Sciences of the United States of America 112, 3570–3575.
| Boosting CRISPR/Cas9 multiplex editing capability with the endogenous tRNA processing system.Crossref | GoogleScholarGoogle Scholar | 25733849PubMed |
Xu YF, An DG, Liu DC, Zhang AM, Xu HX, Li B (2012) Molecular mapping of QTLs for grain zinc, iron and protein concentration of wheat across two environments. Field Crops Research 138, 57–62.
| Molecular mapping of QTLs for grain zinc, iron and protein concentration of wheat across two environments.Crossref | GoogleScholarGoogle Scholar |
Xu R, Yang Y, Qin R, Li H, Qiu C, Li L, Wei P, Yang J (2016) Rapid improvement of grain weight via highly efficient CRISPR/Cas9-mediated multiplex genome editing in rice. Journal of Genetics and Genomics 43, 529–532.
| Rapid improvement of grain weight via highly efficient CRISPR/Cas9-mediated multiplex genome editing in rice.Crossref | GoogleScholarGoogle Scholar | 27543262PubMed |
Ye X, Al-Babili S, Kloti A, Zhang J, Lucca P, Beyer P, et al (2000) Engineering the provitamin A (β-carotene) biosynthetic pathway into (carotenoids-free) rice endosperm. Science 287, 303–305.
| Engineering the provitamin A (β-carotene) biosynthetic pathway into (carotenoids-free) rice endosperm.Crossref | GoogleScholarGoogle Scholar | 10634784PubMed |
Yilmaz O, Kazar GA, Cakmak I, Ozturk L (2017) Differences in grain zinc are not correlated with root uptake and grain translocation of zinc in wild emmer and durum wheat genotypes. Plant and Soil 411, 69–79.
| Differences in grain zinc are not correlated with root uptake and grain translocation of zinc in wild emmer and durum wheat genotypes.Crossref | GoogleScholarGoogle Scholar |
Zhang Y, Xu YH, Yi HY, Gong JM (2012) Vacuolar membrane transporters OsVIT1 and OsVIT2 modulate iron translocation between flag leaves and seeds in rice. The Plant Journal 72, 400–410.
| Vacuolar membrane transporters OsVIT1 and OsVIT2 modulate iron translocation between flag leaves and seeds in rice.Crossref | GoogleScholarGoogle Scholar | 22731699PubMed |
Zhang Y, Liang Z, Zong Y, Wang Y, Liu J, Chen K, Qiu JL, Gao C (2016) Efficient and transgene-free genome editing in wheat through transient expression of CRISPR/Cas9 DNA or RNA. Nature Communications 7, 12617
| Efficient and transgene-free genome editing in wheat through transient expression of CRISPR/Cas9 DNA or RNA.Crossref | GoogleScholarGoogle Scholar | 27558837PubMed |
Zhang J, Zhang H, Botella JR, Zhu JK (2018) Generation of new glutinous rice by CRISPR/Cas9-targeted mutagenesis of the Waxy gene in elite rice varieties. Journal of Integrative Plant Biology 60, 369–375.
| Generation of new glutinous rice by CRISPR/Cas9-targeted mutagenesis of the Waxy gene in elite rice varieties.Crossref | GoogleScholarGoogle Scholar | 29210506PubMed |
Zheng L, Cheng Z, Ai C, Jiang X, Bei X, Zheng Y, Glahn RP, Welch RM, Miller DD, Lei XG (2010) Nicotianamine, a novel enhancer of rice iron bioavailability to humans. PLoS One 5, e10190
| Nicotianamine, a novel enhancer of rice iron bioavailability to humans.Crossref | GoogleScholarGoogle Scholar | 20419136PubMed |
Zong Y, Wang Y, Li C, Zhang R, Chen K, Ran Y, Qiu JL, Wang D, Gao C (2017) Precise base editing in rice, wheat and maize with a Cas9-cytidine deaminase fusion. Nature Biotechnology 35, 438–440.
| Precise base editing in rice, wheat and maize with a Cas9-cytidine deaminase fusion.Crossref | GoogleScholarGoogle Scholar | 28244994PubMed |
Zsögön A, Čermák T, Naves E, et al (2018) De novo domestication of wild tomato using genome editing. Nature Biotechnology 36, 1211–1216.
| De novo domestication of wild tomato using genome editing.Crossref | GoogleScholarGoogle Scholar |