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      Carotenoids modulate kernel texture in maize by influencing amyloplast envelope integrity

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          Abstract

          The mechanism that creates vitreous endosperm in the mature maize kernel is poorly understood. We identified Vitreous endosperm 1 ( Ven1) as a major QTL influencing this process. Ven1 encodes β-carotene hydroxylase 3, an enzyme that modulates carotenoid composition in the amyloplast envelope. The A619 inbred contains a nonfunctional Ven1 allele, leading to a decrease in polar and an increase in non-polar carotenoids in the amyloplast. Coincidently, the stability of amyloplast membranes is increased during kernel desiccation. The lipid composition in endosperm cells in A619 is altered, giving rise to a persistent amyloplast envelope. These changes impede the gathering of protein bodies and prevent them from interacting with starch grains, creating air spaces that cause an opaque kernel phenotype. Genetic modifiers were identified that alter the effect of Ven1 A619 , while maintaining a high β-carotene level. These studies provide insight for breeding vitreous kernel varieties and high vitamin A content in maize.

          Abstract

          Very little is known about how vitreous endosperm in the mature maize kernel is created. Here, via map-based cloning, the authors find that mutation of a β-carotene hydroxylase 3 encoding gene Ven1 affects carotenoids and lipids composition, which consequently influences amyloplast envelope integrity.

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          Most cited references41

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          Natural genetic variation in lycopene epsilon cyclase tapped for maize biofortification.

          Dietary vitamin A deficiency causes eye disease in 40 million children each year and places 140 to 250 million at risk for health disorders. Many children in sub-Saharan Africa subsist on maize-based diets. Maize displays considerable natural variation for carotenoid composition, including vitamin A precursors alpha-carotene, beta-carotene, and beta-cryptoxanthin. Through association analysis, linkage mapping, expression analysis, and mutagenesis, we show that variation at the lycopene epsilon cyclase (lcyE) locus alters flux down alpha-carotene versus beta-carotene branches of the carotenoid pathway. Four natural lcyE polymorphisms explained 58% of the variation in these two branches and a threefold difference in provitamin A compounds. Selection of favorable lcyE alleles with inexpensive molecular markers will now enable developing-country breeders to more effectively produce maize grain with higher provitamin A levels.
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            1-Deoxy-D-xylulose-5-phosphate synthase, a limiting enzyme for plastidic isoprenoid biosynthesis in plants.

            The initial step of the plastidic 2C-methyl-D-erythritol 4-phosphate (MEP) pathway that produces isopentenyl diphosphate is catalyzed by 1-deoxy-d-xylulose-5-phosphate synthase. To investigate whether or not 1-deoxy-d-xylulose-5-phosphate synthase catalyzes a limiting step in the MEP pathway in plants, we produced transgenic Arabidopsis plants that over- or underexpress this enzyme. Compared with non-transgenic wild-type plants, the transgenic plants accumulate different levels of various isoprenoids such as chlorophylls, tocopherols, carotenoids, abscisic acid, and gibberellins. Phenotypically, the transgenic plants had slight alterations in growth and germination rates. Because the levels of several plastidic isoprenoids correlate with changes in 1-deoxy-D-xylulose-5-phosphate synthase levels, we conclude that this enzyme catalyzes one of the rate-limiting steps of the MEP biosynthetic pathway. Furthermore, since the product of the MEP pathway is isopentenyl diphosphate, our results suggest that in plastids the pool of isopentenyl diphosphate is limiting to isprenoid production.
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              Rare genetic variation at Zea mays crtRB1 increases beta-carotene in maize grain.

              Breeding to increase beta-carotene levels in cereal grains, termed provitamin A biofortification, is an economical approach to address dietary vitamin A deficiency in the developing world. Experimental evidence from association and linkage populations in maize (Zea mays L.) demonstrate that the gene encoding beta-carotene hydroxylase 1 (crtRB1) underlies a principal quantitative trait locus associated with beta-carotene concentration and conversion in maize kernels. crtRB1 alleles associated with reduced transcript expression correlate with higher beta-carotene concentrations. Genetic variation at crtRB1 also affects hydroxylation efficiency among encoded allozymes, as observed by resultant carotenoid profiles in recombinant expression assays. The most favorable crtRB1 alleles, rare in frequency and unique to temperate germplasm, are being introgressed via inexpensive PCR marker-assisted selection into tropical maize germplasm adapted to developing countries, where it is most needed for human health.
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                Author and article information

                Contributors
                yrwu@cemps.ac.cn
                Journal
                Nat Commun
                Nat Commun
                Nature Communications
                Nature Publishing Group UK (London )
                2041-1723
                22 October 2020
                22 October 2020
                2020
                : 11
                : 5346
                Affiliations
                [1 ]GRID grid.507734.2, National Key Laboratory of Plant Molecular Genetics, CAS Center for Excellence in Molecular Plant Sciences, Shanghai Institute of Plant Physiology & Ecology, ; Shanghai, 200032 China
                [2 ]GRID grid.410726.6, ISNI 0000 0004 1797 8419, University of the Chinese Academy of Sciences, ; Beijing, 100049 China
                [3 ]GRID grid.16821.3c, ISNI 0000 0004 0368 8293, School of Agriculture and Biology, , Shanghai Jiao Tong University, ; Shanghai, 200240 China
                [4 ]GRID grid.134563.6, ISNI 0000 0001 2168 186X, School of Plant Sciences, , University of Arizona, ; Tucson, Arizona 85721 USA
                Author information
                http://orcid.org/0000-0002-5615-4215
                http://orcid.org/0000-0002-5143-9051
                http://orcid.org/0000-0001-6427-6338
                http://orcid.org/0000-0003-3822-0511
                Article
                19196
                10.1038/s41467-020-19196-9
                7582188
                33093471
                f5377202-7a56-4844-bc2f-df082b6e1ce5
                © The Author(s) 2020

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

                History
                : 5 June 2020
                : 3 October 2020
                Funding
                Funded by: FundRef https://doi.org/10.13039/501100002855, Ministry of Science and Technology of the People's Republic of China (Chinese Ministry of Science and Technology);
                Award ID: 2016YFD0100500
                Award Recipient :
                Funded by: FundRef https://doi.org/10.13039/501100001809, National Natural Science Foundation of China (National Science Foundation of China);
                Award ID: 31830063
                Award ID: 31925030
                Award Recipient :
                Categories
                Article
                Custom metadata
                © The Author(s) 2020

                Uncategorized
                agricultural genetics,natural variation in plants,plant breeding
                Uncategorized
                agricultural genetics, natural variation in plants, plant breeding

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