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A Foundation for Provitamin A Biofortification of Maize: Genome-Wide Association and Genomic Prediction Models of Carotenoid Levels.
Genetics
PUBLISHED: 09-27-2014
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Efforts are underway for development of crops with improved levels of provitamin A carotenoids to help combat dietary vitamin A deficiency. As a global staple crop with considerable variation in kernel carotenoid composition, maize (Zea mays L.) could have widespread impact. We performed a genome-wide association study (GWAS) of quantified seed carotenoids across a panel of maize inbreds ranging from light yellow to dark orange in grain color to identify some of the key genes controlling maize grain carotenoid composition. Significant associations at the genome-wide level were detected within the coding regions of zep1 and lut1, carotenoid biosynthetic genes not previously shown to impact grain carotenoid composition in association studies, as well as within previously associated lcyE and crtRB1 genes. We leveraged existing biochemical and genomic information to identify 58 a priori candidate genes relevant to the biosynthesis and retention of carotenoids in maize to test in a pathway-level analysis. This revealed dxs2 and lut5, genes not previously associated with kernel carotenoids. In genomic prediction models, use of markers that targeted a small set of quantitative trait loci (QTL) associated with carotenoid levels in prior linkage studies were as effective as genome-wide markers for predicting carotenoid traits. Based on our GWAS, pathway-level analysis, and genomic prediction studies, we outline a flexible strategy involving use of a small number of genes that can be selected for rapid conversion of elite white grain germplasm, with minimal amounts of carotenoids, to orange grain versions containing high levels of provitamin A.
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Genome-wide association study and pathway-level analysis of tocochromanol levels in maize grain.
G3 (Bethesda)
PUBLISHED: 06-05-2013
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Tocopherols and tocotrienols, collectively known as tocochromanols, are the major lipid-soluble antioxidants in maize (Zea mays L.) grain. Given that individual tocochromanols differ in their degree of vitamin E activity, variation for tocochromanol composition and content in grain from among diverse maize inbred lines has important nutritional and health implications for enhancing the vitamin E and antioxidant contents of maize-derived foods through plant breeding. Toward this end, we conducted a genome-wide association study of six tocochromanol compounds and 14 of their sums, ratios, and proportions with a 281 maize inbred association panel that was genotyped for 591,822 SNP markers. In addition to providing further insight into the association between ZmVTE4 (?-tocopherol methyltransferase) haplotypes and ?-tocopherol content, we also detected a novel association between ZmVTE1 (tocopherol cyclase) and tocotrienol composition. In a pathway-level analysis, we assessed the genetic contribution of 60 a priori candidate genes encoding the core tocochromanol pathway (VTE genes) and reactions for pathways supplying the isoprenoid tail and aromatic head group of tocochromanols. This analysis identified two additional genes, ZmHGGT1 (homogentisate geranylgeranyltransferase) and one prephenate dehydratase parolog (of four in the genome) that also modestly contribute to tocotrienol variation in the panel. Collectively, our results provide the most favorable ZmVTE4 haplotype and suggest three new gene targets for increasing vitamin E and antioxidant levels through marker-assisted selection.
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High-provitamin A carotenoid (Orange) maize increases hepatic vitamin A reserves of offspring in a vitamin A-depleted sow-piglet model during lactation.
J. Nutr.
PUBLISHED: 05-29-2013
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The relationship of dietary vitamin A transfer from mother to fetus is not well understood. The difference in swine offspring liver reserves was investigated between single-dose vitamin A provided to the mother post-conception compared with continuous provitamin A carotenoid dietary intake from biofortified (enhanced provitamin A) orange maize (OM) fed during gestation and lactation. Vitamin A-depleted sows were fed OM (n = 5) or white maize (WM) + 1.05 mmol retinyl palmitate administered at the beginning of gestation (n = 6). Piglets (n = 102) were killed at 0, 10, 20, and 28 d after birth. Piglets from sows fed OM had higher liver retinol reserves (P < 0.0001) and a combined mean concentration from d 10 to 28 of 0.11 ± 0.030 ?mol/g. Piglets from sows fed WM had higher serum retinol concentrations (0.56 ± 0.25 ?mol/L; P = 0.0098) despite lower liver retinol concentrations of 0.068 ± 0.026 ?mol/g from d 10 to 28. Milk was collected at 0, 5, 10, 20, and 28 d. Sows fed OM had a higher milk retinol concentration (1.36 ± 1.30 ?mol/L; P = 0.038), than those fed WM (0.93 ±1.03 ?mol/L). Sow livers were collected at the end of the study (n = 3/group) and had identical retinol concentrations (0.22 ± 0.05 ?mol/g). Consumption of daily provitamin A carotenoids by sows during gestation and lactation increased liver retinol status in weanling piglets, illustrating the potential for provitamin A carotenoid consumption from biofortified staple foods to improve vitamin A reserves. Biofortified OM could have a measurable impact on vitamin A status in deficient populations if widely adopted.
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Genetic architecture controlling variation in grain carotenoid composition and concentrations in two maize populations.
Theor. Appl. Genet.
PUBLISHED: 04-20-2013
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Genetic control of maize grain carotenoid profiles is coordinated through several loci distributed throughout three secondary metabolic pathways, most of which exhibit additive, and more importantly, pleiotropic effects. The genetic basis for the variation in maize grain carotenoid concentrations was investigated in two F2:3 populations, DEexp × CI7 and A619 × SC55, derived from high total carotenoid and high ?-carotene inbred lines. A comparison of grain carotenoid concentrations from population DEexp × CI7 grown in different environments revealed significantly higher concentrations and greater trait variation in samples harvested from a subtropical environment relative to those from a temperate environment. Genotype by environment interactions was significant for most carotenoid traits. Using phenotypic data in additive, environment-specific genetic models, quantitative trait loci (QTL) were identified for absolute and derived carotenoid traits in each population, including those specific to the isomerization of ?-carotene. A multivariate approach for these correlated traits was taken, using carotenoid trait principal components (PCs) that jointly accounted for 97 % or more of trait variation. Component loadings for carotenoid PCs were interpreted in the context of known substrate-product relationships within the carotenoid pathway. Importantly, QTL for univariate and multivariate traits were found to cluster in close proximity to map locations of loci involved in methyl-erythritol, isoprenoid and carotenoid metabolism. Several of these genes, including lycopene epsilon cyclase, carotenoid cleavage dioxygenase1 and beta-carotene hydroxylase, were mapped in the segregating populations. These loci exhibited pleiotropic effects on ?-branch carotenoids, total carotenoid profile and ?-branch carotenoids, respectively. Our results confirm that several QTL are involved in the modification of carotenoid profiles, and suggest genetic targets that could be used for the improvement of total carotenoid and ?-carotene in future breeding populations.
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Distinct genetic architectures for male and female inflorescence traits of maize.
PLoS Genet.
PUBLISHED: 05-11-2011
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We compared the genetic architecture of thirteen maize morphological traits in a large population of recombinant inbred lines. Four traits from the male inflorescence (tassel) and three traits from the female inflorescence (ear) were measured and studied using linkage and genome-wide association analyses and compared to three flowering and three leaf traits previously studied in the same population. Inflorescence loci have larger effects than flowering and leaf loci, and ear effects are larger than tassel effects. Ear trait models also have lower predictive ability than tassel, flowering, or leaf trait models. Pleiotropic loci were identified that control elongation of ear and tassel, consistent with their common developmental origin. For these pleiotropic loci, the ear effects are larger than tassel effects even though the same causal polymorphisms are likely involved. This implies that the observed differences in genetic architecture are not due to distinct features of the underlying polymorphisms. Our results support the hypothesis that genetic architecture is a function of trait stability over evolutionary time, since the traits that changed most during the relatively recent domestication of maize have the largest effects.
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Genome-wide association study of leaf architecture in the maize nested association mapping population.
Nat. Genet.
PUBLISHED: 01-09-2011
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US maize yield has increased eight-fold in the past 80 years, with half of the gain attributed to selection by breeders. During this time, changes in maize leaf angle and size have altered plant architecture, allowing more efficient light capture as planting density has increased. Through a genome-wide association study (GWAS) of the maize nested association mapping panel, we determined the genetic basis of important leaf architecture traits and identified some of the key genes. Overall, we demonstrate that the genetic architecture of the leaf traits is dominated by small effects, with little epistasis, environmental interaction or pleiotropy. In particular, GWAS results show that variations at the liguleless genes have contributed to more upright leaves. These results demonstrate that the use of GWAS with specially designed mapping populations is effective in uncovering the basis of key agronomic traits.
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Vitamin A equivalence of the ß-carotene in ß-carotene-biofortified maize porridge consumed by women.
Am. J. Clin. Nutr.
PUBLISHED: 09-01-2010
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?-Carotene-biofortified maize is being developed through plant breeding as a sustainable agronomic approach to alleviate vitamin A deficiency.
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Rare genetic variation at Zea mays crtRB1 increases beta-carotene in maize grain.
Nat. Genet.
PUBLISHED: 02-19-2010
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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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Major and minor QTL and epistasis contribute to fatty acid compositions and oil concentration in high-oil maize.
Theor. Appl. Genet.
PUBLISHED: 09-30-2009
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High-oil maize is a useful genetic resource for genomic investigation in plants. To determine the genetic basis of oil concentration and composition in maize grain, a recombinant inbred population derived from a cross between normal line B73 and high-oil line By804 was phenotyped using gas chromatography, and genotyped with 228 molecular markers. A total of 42 individual QTL, associated with fatty acid compositions and oil concentration, were detected in 21 genomic regions. Five major QTL were identified for measured traits, one each of which explained 42.0% of phenotypic variance for palmitic acid, 15.0% for stearic acid, 27.7% for oleic acid, 48.3% for linoleic acid, and 15.7% for oil concentration in the RIL population. Thirty-six loci were involved in 24 molecular marker pairs of epistatic interactions across all traits, which explained phenotypic variances ranging from 0.4 to 6.1%. Seven of 18 mapping candidate genes related to lipid metabolism were localized within or were close to identified individual QTL, explaining 0.7-13.2% of the population variance. These results demonstrated that a few major QTL with large additive effects could play an important role in attending fatty acid compositions and increasing oil concentration in used germplasm. A larger number of minor QTL and a certain number of epistatic QTL, both with additive effects, also contributed to fatty acid compositions and oil concentration.
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The genetic architecture of maize flowering time.
Science
PUBLISHED: 08-08-2009
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Flowering time is a complex trait that controls adaptation of plants to their local environment in the outcrossing species Zea mays (maize). We dissected variation for flowering time with a set of 5000 recombinant inbred lines (maize Nested Association Mapping population, NAM). Nearly a million plants were assayed in eight environments but showed no evidence for any single large-effect quantitative trait loci (QTLs). Instead, we identified evidence for numerous small-effect QTLs shared among families; however, allelic effects differ across founder lines. We identified no individual QTLs at which allelic effects are determined by geographic origin or large effects for epistasis or environmental interactions. Thus, a simple additive model accurately predicts flowering time for maize, in contrast to the genetic architecture observed in the selfing plant species rice and Arabidopsis.
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Natural variation in maize architecture is mediated by allelic differences at the PINOID co-ortholog barren inflorescence2.
Plant J.
PUBLISHED: 01-19-2009
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We characterized allelic variation at barren inflorescence2 (bif2), a maize co-ortholog of the Arabidopsis PINOID protein kinase (PID), and tested for trait associations with bif2 in both an association mapping population of 277 diverse maize inbreds and in the inter-mated B73 x Mo17 (IBM) linkage population. Results from the quantitative analyses were compared with previous reports of bif2 phenotypes in mutagenesis studies. All three approaches (association, linkage, and mutagenesis) detect a significant effect of bif2 on tassel architecture. Association mapping implicates bif2 in an unexpectedly wide range of traits including plant height, node number, leaf length, and flowering time. Linkage mapping finds a significant interaction effect for node number between bif2 and other loci, in keeping with previous reports that bif2;spi1 and Bif2;Bif1 double mutants produce fewer phytomers. The Mo17 allele is associated with a reduced tassel branch zone and shows lower expression than the B73 allele in hybrid B73-Mo17 F(1) inflorescences, consistent with the complete absence of tassel branches in the bif2 knockout mutant. Overall, these data suggest that allelic variation at bif2 affects maize architecture by modulating auxin transport during vegetative and inflorescence development.
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Comparative intake of white- versus orange-colored maize by Zambian children in the context of promotion of biofortified maize.
Food Nutr Bull
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Vitamin A deficiency is associated with poor health outcomes related to reproduction, growth, vision, and immunity. Biofortification of staple crops is a novel strategy for combating vitamin A deficiency in high-risk populations where staple food intakes are high. African populations are proposed beneficiaries of maize (Zea mays) biofortified with provitamin A carotenoids, often called "orange maize" because of its distinctive deep yellow-orange kernels. The color facilitates ready recognition but presents a cultural challenge to maize-consuming populations, including those in much of Africa, who traditionally eat white varieties.
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