Quantitative trait loci and differential gene expression analyses reveal the genetic basis for negatively associated β-carotene and starch content in hexaploid sweetpotato [Ipomoea batatas (L.) Lam.].
Journal
TAG. Theoretical and applied genetics. Theoretische und angewandte Genetik
ISSN: 1432-2242
Titre abrégé: Theor Appl Genet
Pays: Germany
ID NLM: 0145600
Informations de publication
Date de publication:
Jan 2020
Jan 2020
Historique:
received:
12
07
2019
accepted:
17
09
2019
pubmed:
9
10
2019
medline:
17
9
2020
entrez:
10
10
2019
Statut:
ppublish
Résumé
β-Carotene content in sweetpotato is associated with the Orange and phytoene synthase genes; due to physical linkage of phytoene synthase with sucrose synthase, β-carotene and starch content are negatively correlated. In populations depending on sweetpotato for food security, starch is an important source of calories, while β-carotene is an important source of provitamin A. The negative association between the two traits contributes to the low nutritional quality of sweetpotato consumed, especially in sub-Saharan Africa. Using a biparental mapping population of 315 F
Identifiants
pubmed: 31595335
doi: 10.1007/s00122-019-03437-7
pii: 10.1007/s00122-019-03437-7
pmc: PMC6952332
doi:
Substances chimiques
beta Carotene
01YAE03M7J
Starch
9005-25-8
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
23-36Subventions
Organisme : Bill and Melinda Gates Foundation
ID : OPP1052983
Références
Alexa A, Rahnenfuhrer J (2019) topGO: enrichment analysis for gene ontology. R package version 2.36.0. https://doi.org/10.18129/B9.bioc.topGO
Anders S, Pyl PT, Huber W (2015) HTSeq—a Python framework to work with high-throughput sequencing data. Bioinformatics 31:166–169
pubmed: 25260700
pmcid: 25260700
Andrade MI et al (2016) Alisha’, ‘Anamaria’, ‘Bie’, ‘Bita’, ‘Caelan’, ‘Ivone’, ‘Lawrence’, ‘Margarete’, ‘Victoria’, Sweetpotato. Hort Sci 51:597–600
Baroja-Fernández E, Muñoz FJ, Zandueta-Criado A, Morán-Zorzano MT, Viale AM, Alonso-Casajús N, Javier Pozueta-Romero J (2004) Most of ADP-glucose linked to starch biosynthesis occurs outside the chloroplast in source leaves. PNAS 101(35):13080–13085
pubmed: 15326306
Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B Methodol 57:289–300
Burgos G, Caprio R, Sanchez C, Sosa P, Porras E, Espinoza J, Grüneberg W (2009) Guide for using the RHS color chart for selecting for high β-Carotene sweet potato. Poster at ISTRC, Lima
Cao H et al (2015) Carotenoid accumulation affects redox status, starch metabolism, and flavonoid/anthocyanin accumulation in citrus. BMC Plant Biol 15:27. https://doi.org/10.1186/s12870-015-0426-4
doi: 10.1186/s12870-015-0426-4
pubmed: 25644332
pmcid: 4323224
Carvalho LJCB et al (2016) Natural variation in expression of genes associated with carotenoid biosynthesis and accumulation in cassava (Manihot esculenta Crantz) storage roots. BMC Plant Biol 16:133
pubmed: 27286876
pmcid: 4902922
Cervantes-Flores JC et al (2011) Identification of quantitative trait loci for dry-matter, starch, and β-carotene content in sweetpotato. Mol Breed 28:201–216
CIP/AVRDC/IBPGR (1991) Descriptors for sweetpotato. In: Huaman Z (ed) International board for plant genetic resources, Rome
Covarrubias-Pazaran G (2016) Genome-assisted prediction of quantitative traits using the R package sommer. PLoS ONE 11(6):e0156744
pubmed: 27271781
pmcid: 4894563
Dejardin A, Rochat C, Wuilleme S, Boutin J-P (1997) Contribution of sucrose synthase, ADP-glucose pyro-phosphorylase and starch synthase to starch synthesis in developing pea seeds. Plant Cell Environ 20:1421–1430
Dufresne F, Stift M, Vergilino R, Mable BK (2014) Recent progress and challenges in population genetics of polyploid organisms: an overview of current state-of-the-art molecular and statistical tools. Mol Ecol 23(1):40–69
pubmed: 24188632
Ellison SL et al (2018) Carotenoid presence is associated with the Or gene in domesticated carrot. Genetics 210:1497–1508
pubmed: 30352832
pmcid: 6283172
Foss EJ et al (2007) Genetic basis of proteome variation in yeast. Nat Genet 39:1369–1375
pubmed: 17952072
Glaubitz JC et al (2014) TASSEL-GBS: a high capacity genotyping by sequencing analysis pipeline. PLoS ONE 9(2):e90346
pubmed: 3938676
pmcid: 3938676
Goo YM et al (2015) Overexpression of the sweetpotato IbOr gene results in the increased accumulation of carotenoid and confers tolerance to environmental stresses in transgenic potato. C R Biol 338:12–20
pubmed: 25528672
Goulet BE, Roda F, Hopkins R (2017) Hybridization in plants, old ideas, new techniques. Plant Physiol 173:65–78
pubmed: 27895205
Gruneberg WJ, Manrique K, Zhang D, Hermann M (2005) G x E interaction for a diverse set of sweetpotato genotypes evaluated across varying ecogeographic conditions in Peru. Crop Sci 45:2160–2171
Grüneberg WJ et al (2012) Advances in sweetpotato breeding from 1992 to 2012. In: Low JW, Nyongesa M, Quinn S, Parker M (eds) Potato and Sweetpotato in Africa: transforming the value chains for food and nutrition security. CABI, Wallingford, pp 3–68
Jarvis P, Lopez-Juez E (2013) Biogenesis and homeostasis of chloroplasts and other plastids. Nat Rev Mol Cell Biol 14:787–802
pubmed: 24263360
Kang L et al (2017) Suppression of the b-carotene hydroxylase gene increases b-carotene content and tolerance to abiotic stress in transgenic sweetpotato plants. Plant Physiol Biochem 117:24–33
pubmed: 28587990
Kim SH et al (2013) Cloning and characterization of an Orange gene that increases carotenoid accumulation and salt stress tolerance in transgenic sweetpotato cultures. Plant Physiol Biochem 70:445–454
pubmed: 23835362
Kitahara et al (2017) Carbohydrate components in sweetpotato storage roots: their diversities and genetic improvement. Breed Sci 67:62–72
pubmed: 28465669
pmcid: 5407920
Kriegner A, Cervantes JC, Burg K, Mwanga ROM, Zhang DA (2003) A genetic linkage map of sweetpotato (Ipomoea batatas (L.) Lam.) based on AFLP markers. Mol Breed 11:169–185
Langmead B, Salzberg SL (2012) Fast gapped-read alignment with Bowtie 2. Nat Methods 9(4):357
pubmed: 3322381
pmcid: 3322381
Lau et al (2018) Transcriptomic analysis of sweet potato under dehydration stress identifies candidate genes for drought tolerance. Plant Direct. https://doi.org/10.1002/pld3.92
doi: 10.1002/pld3.92
pubmed: 31245692
pmcid: 6508841
Li J et al (2013) Enhancing sucrose synthase activity results in increased levels of starch and ADP-glucose in maize (Zea mays L.) seed endosperms. Plant Cell Physiol 54(2):282–294
pubmed: 23292602
Love MI, Huber W, Anders S (2014) Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 15:550
pubmed: 4302049
pmcid: 4302049
Low JW et al (2009) Sweetpotato in Sub-Saharan Africa. In: Loebenstein G, Thottappilly G (eds) The Sweetpotato. Springer, Dordrecht, pp 359–390
Low JW, Mwanga ROM, Andrade M, Carey E, Ball A (2017) Tackling vitamin A deficiency with biofortified sweetpotato in sub-Saharan Africa. Glob Food Secur 14:23–30
Lu S et al (2006) The cauliflower Or gene encodes a DnaJ cysteine-rich domain-containing protein that mediates high levels of β-carotene accumulation. Plant Cell 18:3594–3605
pubmed: 1785402
pmcid: 1785402
Lu PJ et al (2017) Cytological and molecular characterization of carotenoid accumulation in normal and high-lycopene mutant oranges. Sci Rep 7:761
pubmed: 28396598
pmcid: 5429694
Mollinari M, Garcia AAF (2019) Linkage analysis and haplotype phasing in experimental autopolyploid populations with high ploidy level using hidden Markov models. BioRxiv https://www.biorxiv.org/content/10.1101/415232v2
Mollinari M, Olokulu B, Pereira GDS, Khan A, Gemenet DC, Yencho C, Zeng Z-B (2019) Unraveling the hexaploid sweetpotato inheritance using ultra-dense multilocus mapping. BioRxiv Preprint. https://doi.org/10.1101/689638
Mortimer CL et al (2016) Product stability and sequestration mechanisms in solanum tuberosum engineered to biosynthesize high value ketocarotenoids. Plant Biotechnol J 14:140–152
pubmed: 25845905
Muñoz FJ, Baroja-Fernández E, Morán-Zorzano MT, Viale AM, Etxeberria E, Alonso-Casajús N, Pozueta-Romero J (2005) Sucrose synthase controls both intracellular ADP glucose levels and transitory starch biosynthesis in source leaves. Plant Cell Physiol 46(8):1366–1376
pubmed: 15951568
Mwanga ROM, Ghislain M, Kreuze J, Ssemakula GN, Yencho GC (2011) Exploiting the use of biotechnology in sweetpotato for improved nutrition and food security: progress and future outlook. In: Nampala P, Makara MA (eds) Proceedings of the international conference on agro-biotechnology, biosafety and seed systems in developing countries. Science Foundation for Livelihoods and Development, Kampala, Uganda, pp 25–31
Naeem M, Tetlow IJ, Emes MJ (1997) Starch synthesis in amyloplasts purified from developing potato tubers. Plant J 11(5):1095–1103
Ohdan T, Francisco PB Jr, Sawada T, Hirose T, Terao T, Satoh H, Nakamura Y (2005) Expression profiling of genes involved in starch synthesis in sink and source organs of rice. J Exp Bot 56(422):3229–3344
pubmed: 16275672
Pereira GS, Garcia AAF, Margarido GRA (2018) A fully automated pipeline for quantitative genotype calling from next generation sequencing data in autopolyploids. BMC Bioinform 19(1):398
Pereira GDS, Gemenet DC, Mollinari M, Olukolu BA, Diaz F, Mosquera V, Gruneberg WJ, Khan A, Yencho GC, Zeng Z-B (2019) Multiple QTL mapping in autopolyploids: a random-effect model approach with application in a hexaploid sweetpotato full-sib population. BioRxiv Preprint https://doi.org/10.1101/622951
Qu L, Guennel T, Marshall SL (2013) Linear score tests for variance components in linear mixed models and applications to genetic association studies. Biometrics 69(4):883–892
pubmed: 24328714
Rabbi IY et al (2017) Genome-wide association mapping of correlated traits in cassava: dry matter and total carotenoid content. Plant Genome. https://doi.org/10.3835/plantgenome2016.09.0094
doi: 10.3835/plantgenome2016.09.0094
pubmed: 29293815
Reeve RM (1967) A review of cellular structure, starch and texture qualities of processed potatoes. Econ Bot 21(4):294–308
Serang O, Mollinari M, Garcia AAF (2012) Efficient exact maximum a posteriori computation for bayesian SNP genotyping in polyploids. PLoS ONE 7(2):e30906
pubmed: 22363513
pmcid: 3281906
Shiotani I, Kawase T (1989) Genomic structure of the sweet- potato and hexaploids in Ipomoea trifida (HBK) DON. Jpn J Breed 39:57–66
Stein O, Ganot D (2019) An overview of sucrose synthases in plants. Front Plant Sci 10:95
pubmed: 30800137
pmcid: 6375876
Sun T, Yuan H, Cao H, Yazdani M, Tadmor Y, Li L (2018) Carotenoid metabolism in plants: the role of plastids. Mol Plant 11:58–74
pubmed: 28958604
Tetlow IJ, Blissett KJ, Emes MJ (1994) Starch synthesis and carbohydrate oxidation in amyloplasts from developing wheat endosperm. Planta 194:454–460
Tumwegamire S et al (2011) Evaluation of dry-matter, protein, starch, sucrose, beta-carotene, iron, zinc, calcium and magnesium in east African sweetpotato. Hort Sci 46(3):348–357
Tzuri G et al (2015) A ‘golden’ SNP in CmOr governs the fruit flesh color of melon (Cucumis melo). Plant J 82:267–279
Wadl PA et al (2018) Genetic diversity and population structure of the USDA sweetpotato (Ipomoea batatas) germplasm collections using GBSpoly. Front Plant Sci 9:1–13
Wu S et al (2018) Genome sequences of two diploid wild relatives of cultivated sweetpotato reveal targets for genetic improvement. Nat Commun 9:4580
pubmed: 30389915
pmcid: 6214957
Wurtzel E, Cuttriss A, Vallabhaneni R (2012) Maize provitamin A carotenoids, current resources, and future metabolic engineering challenges. Front Plant Sci 3:29
pubmed: 22645578
pmcid: 3355804
Xiao-xia Y et al (2014) Identification of QTLs for starch content in sweetpotato (Ipomoea batatas (L.) Lam.). J Integrative Agric 13(2):310–315
Yada B et al (2017) Genetic analysis and association of simple sequence repeat markers with storage root yield, dry matter starch and beta-carotene content in sweetpotato. Breed Sci 67(2):140–150
pubmed: 28588391
pmcid: 5445964
Yang J et al (2017) Haplotype-resolved sweet potato genome traces back its hexaploidization history. Nat Plants 3:696–703
pubmed: 28827752
Yuan H, Zhang J, Nageswaran D, Li L (2015) Carotenoid metabolism and regulation in horticultural crops. Hortic Res 2:15036
pubmed: 26504578
pmcid: 4591682
Zhang MK, Zhang MP, Mazourek M, Tadmor Y, Li L (2014) Regulatory control of carotenoid accumulation in winter squash during storage. Planta 240:1063–1074
pubmed: 25139277
Zhang K et al (2016) Development an identification of SSR markers associated with starch properties and β-Carotene content in the storage root of sweet potato (Ipomoea batatas L.). Front Plant Sci 7:223
pubmed: 26973669
pmcid: 4773602
Zhao N et al (2013) A genetic linkage map based on AFLP and SSR markers and mapping of QTL for dry-matter content in sweetpotato. Mol Breed 32:807–820
Zhou X, Welsch R, Yang Y, Álvarez D, Riediger M, Yuan H, Fish T, Liu J, Thannhauser TW, Li L (2015) Arabidopsis OR proteins are the major posttranscriptional regulators of phytoene synthase in controlling carotenoid biosynthesis. PNAS 112(11):3558–3563
pubmed: 25675505