Genome-wide association study of berry-related traits in grape [Vitis vinifera L.] based on genotyping-by-sequencing markers

Abstract

Deciphering the genetic control of grape berry traits is crucial for optimizing yield, fruit quality, and consumer acceptability. In this study, an association panel of 179 grape genotypes comprising a mixture of ancient cultivars, landraces, and modern varieties collected worldwide were genotyped with genotyping-by-sequencing using a genome-wide association approach based on 32,311 single-nucleotide polymorphism (SNP) markers. Genome-wide efficient mixed-model association was selected as the optimal statistical model based on the results of known control loci of grape berry color traits. Many of the associated SNPs identified in this study were in accordance with the previous QTL analyses using biparental mapping. The grape skin color locus was found to be associated with a mybA transcription factor on chromosome 2. Two strong and distinct association signals associated with berry development periods were found on chromosome 16. Most candidate genes of the interval were highlighted as receptor-like protein kinase. For berry weight, significant association loci were identified on chromosome 18, as previously known, and on chromosome 19 and chromosome 17, as newly mapped. Berry flesh texture was newly located on chromosome 16; candidate genes in the interval were related to calcium. Berry flavor was determined on chromosome 5. Genomic regions were further investigated to reveal candidate genes. In this work, we identified interesting genetic determinants of grape berry-related traits. The identification of the markers closely associated with these berry traits may be useful for grape molecular breeding.

References

[1] Doligez, A. et al. Genetic mapping of grapevine (Vitis vinifera L.) applied to the detection of QTLs for seedlessness and berry weight . Theor. Appl. Genet. 105, 780-795 (2002).

[2] Fischer, B. M. et al. Quantitative trait locus analysis of fungal disease resistance factors on a molecular map of grapevine. Theor. Appl. Genet. 108, 501-515 (2004).

[3] Mejía, N. et al. Identification of QTLs for seedlessness, berry size, and ripening date in a seedless x seedless table grape progeny. Am. J. Enol. Vitic. 58, 499-507 (2007).

[4] Costantini, L., Battilana, J., Lamaj, F., Fanizza, G. & Grando, M. S. Berry and phenology-related traits in grapevine (Vitis vinifera L.): from quantitative trait loci to underlying genes . BMC Plant Biol. 8, 38 (2008).

[5] Ban, Y., Mitani, N., Sato, A., Kono, A. & Hayashi, T. Genetic dissection of quantitative trait loci for berry traits in interspecific hybrid grape (Vitis labruscana × Vitis vinifera) . Euphytica 211, 295-310 (2016).

[6] Correa, J. et al. New stable QTLs for berry firmness in table grapes. Am. J. Enol. Vitic. 67, 212-217 (2016).

[7] Dai, Z. W. et al. Ecophysiological, genetic, and molecular causes of variation in grape berry weight and composition: a review. Am. J. Enol. Vitic. 62, 413-425 (2011).

[8] Tello, J., Torres-Perez, R., Grimplet, J. & Ibanez, J . Association analysis of grapevine bunch traits using a comprehensive approach. Theor. Appl. Genet. 129, 227-242 (2016).

[9] Lipka, A. E. et al. From association to prediction: statistical methods for the dissection and selection of complex traits in plants. Curr. Opin. Plant Biol. 24, 110-118 (2015).

[10] Elshire, R. J. et al. A robust, simple genotyping-by-sequencing (GBS) approach for high diversity species. PLoS One 6, e19379 (2011).

[11] Sakiroglu, M. & Brummer, E. C. Identification of loci controlling forage yield and nutritive value in diploid alfalfa using GBS-GWAS. Theor. Appl. Genet. 130, 261-268 (2016).

[12] Myles, S. et al. Association mapping: critical considerations shift from genotyping to experimental design. Plant Cell 21, 2194-2202 (2009).

[13] Cao, K. et al. Genome-wide association study of 12 agronomic traits in peach. Nat. Commun. 7, 13246 (2016).

[14] Myles, S. et al. Genetic structure and domestication history of the grape. Proc. Natl. Acad. Sci. 108, 3530-3535 (2011).

[15] Chitwood, D. H. et al. A modern ampelography: a genetic basis for leaf shape and venation patterning in grape. Plant Physiol. 164, 259-272 (2014).

[16] Nicolas, S. D. et al. Genetic diversity, linkage disequilibrium and power of a large grapevine (Vitis vinifera L) diversity panel newly designed for association studies . BMC Plant Biol. 16, 74 (2016).

[17] Migicovsky, Z. et al. Patterns of genomic and phenomic diversity in wine and table grapes. Hortic. Res. 4, 17035 (2017).

[18] Yang, X. et al. Genetic diversity and association study of aromatics in grapevine. J. Am. Soc. Hortic. Sci. 142, 225-231 (2017).

[19] Emanuelli, F. et al. A candidate gene association study on muscat flavor in grapevine (Vitis vinifera L.) . BMC Plant Biol. 10, 241 (2010).

[20] Zhang, Z. et al. Mixed linear model approach adapted for genome-wide association studies. Nat. Genet. 42, 355-360 (2010).

[21] Kang, H. M. et al. Variance component model to account for sample structure in genome-wide association studies. Nat. Genet. 42, 348-354 (2010).

[22] Zhou, X. & Stephens, M. Genome-wide efficient mixed-model analysis for association studies. Nat. Genet. 44, 821-824 (2012).

[23] Liu, X. M. et al. Construction of primary core collection of grape genetic resources. J. Plant Genet Resour. 13, 72-76 (2012).

[24] Zyprian, E. et al. Quantitative trait loci affecting pathogen resistance and ripening of grapevines. Mol. Genet Genom. 291, 1573-1594 (2016).

[25] Purcell, S. et al. PLINK: a tool set for whole-genome association and population-based linkage analyses. Am. J. Hum. Genet. 81, 559-575 (2007).

[26] Li, M.-X., Yeung, J. M., Cherny, S. S. & Sham, P. C. Evaluating the effective numbers of independent tests and significant p-value thresholds in commercial genotyping arrays and public imputation reference datasets. Hum. Genet. 131, 747-756 (2012).

[27] Atwell, S. et al. Genome-wide association study of 107 phenotypes in Arabidopsis thaliana inbred lines . Nature 465, 627-631 (2010).

[28] Ogura, T. & Busch, W. From phenotypes to causal sequences: using genome wide association studies to dissect the sequence basis for variation of plant development. Curr. Opin. Plant Biol. 23, 98-108 (2015).

[29] Yano, K. et al. Genome-wide association study using whole-genome sequencing rapidly identifies new genes influencing agronomic traits in rice. Nat. Genet. 48, 927-934 (2016).

[30] Lijavetzky, D., Cabezas, J. A., Ibáñez, A., Rodríguez, V. & Martínez-Zapater, J. M. High throughput SNP discovery and genotyping in grapevine (Vitis vinifera L.) by combining a re-sequencing approach and SNPlex technology . BMC Genom. 8, 424 (2007).

[31] Marrano, A. et al. SNP-discovery by RAD-sequencing in a germplasm collection of wild and cultivated grapevines (V. vinifera L.) . PloS One 12, e0170655 (2017).

[32] Walker, A. R. et al. White grapes arose through the mutation of two similar and adjacent regulatory genes. Plant J. 49, 772-785 (2007).

[33] Matus, J. T. et al. A group of grapevine MYBA transcription factors located in chromosome 14 control anthocyanin synthesis in vegetative organs with different specificities compared with the berry color locus. Plant J. 91, 220-236 (2017).

[34] Wang, H. & Qin, F. Genome-wide association study reveals natural variations contributing to drought resistance in crops. Front. Plant Sci. 8, 1110 (2017).

[35] Yu, J. et al. A unified mixed-model method for association mapping that accounts for multiple levels of relatedness. Nat. Genet. 38, 203-208 (2006).

[36] Huang, X. et al. Genome-wide association studies of 14 agronomic traits in rice landraces. Nat. Genet. 42, 961-967 (2010).

[37] Azuma, A. et al. Color recovery in berries of grape (Vitis vinifera L.)‘Benitaka’, a bud sport of ‘Italia’, is caused by a novel allele at the VvmybA1 locus . Plant Sci. 176, 470-478 (2009).

[38] Jiao, J. et al. Study of the relationship between the cultivars of Vitis vinifera and the white-fruited and hermaphrodite Chinese wild grapes . Mol. Breed. 34, 1401-1411 (2014).

[39] Duchêne, E., Butterlin, G., Dumas, V. & Merdinoglu, D. Towards the adaptation of grapevine varieties to climate change: QTLs and candidate genes for developmental stages. Theor. Appl. Genet. 124, 623-635 (2012).

[40] Zhao, Y. H., Su, K., Guo, Y. H., Ma, H. F. & Guo, X. W. Molecular genetic map construction and QTL analysis of fruit maturation period in grapevine. Genet. Mol. Res. 15, 15028040 (2016).

[41] Zhang, Q. et al. Genome-wide identification and expression analysis of MRLK family genes associated with strawberry (Fragaria vesca) fruit ripening and abiotic stress responses . PLoS One 11, e0163647 (2016).

[42] Jia, M. et al. Two FERONIA-like receptor kinases regulate apple fruit ripening by modulating ethylene production. Front. Plant Sci. 8, 1406 (2017).

[43] Doligez, A. et al. New stable QTLs for berry weight do not colocalize with QTLs for seed traits in cultivated grapevine (Vitis vinifera L.) . BMC Plant Biol. 13, 217 (2013).

[44] Chialva, C. et al. Expression of grapevine AINTEGUMENTA-like genes is associated with variation in ovary and berry size. Plant Mol. Biol. 91, 67-80 (2016).

[45] Carreño, I. et al. Quantitative genetic analysis of berry firmness in table grape (Vitis vinifera L.) . Tree Genet. & Genomes 11, 818 (2015).

[46] White, P. J. & Broadley, M. R. Calcium in plants. Ann. Bot. 92, 487-511 (2003).

[47] Balic, I. et al. Biochemical and physiological study of the firmness of table grape berries. Postharvest Biol. Tec. 93, 15-23 (2014).

[48] Yang, X., et al. Associations between the 1-deoxy-d-xylulose-5-phosphate synthase gene and aroma in different grapevine varieties. Genes Genom. 39, 1059-1067 (2017).

[49] Doligez, A., Audiot, E., Baumes, R. & This, P. QTLs for muscat flavor and monoterpenic odorant content in grapevine (Vitis vinifera L.) . Mol. Breed. 18, 109-125 (2006).

[50] Battilana, J. et al. The 1-deoxy-d-xylulose 5-phosphate synthase gene co-localizes with a major QTL affecting monoterpene content in grapevine. Theor. Appl. Genet. 118, 653-669 (2009).