Patterns of genomic and phenomic diversity in wine and table grapes

Zoë Migicovsky , Jason Sawler , Kyle M Gardner , Mallikarjuna K Aradhya , Bernard H Prins , Heidi R Schwaninger , Carlos D Bustamante , Edward S Buckler , Gan-Yuan Zhong , Patrick J Brown , Sean Myles

Horticulture Research ›› 2017, Vol. 4 ›› Issue (1) : 17035

PDF (2679KB)
Horticulture Research ›› 2017, Vol. 4 ›› Issue (1) :17035 DOI: 10.1038/hortres.2017.35
ARTICLE
research-article
Patterns of genomic and phenomic diversity in wine and table grapes
Author information +
History +
PDF (2679KB)

Abstract

Grapes are one of the most economically and culturally important crops worldwide, and they have been bred for both winemaking and fresh consumption. Here we evaluate patterns of diversity across 33 phenotypes collected over a 17-year period from 580 table and wine grape accessions that belong to one of the world’s largest grape gene banks, the grape germplasm collection of the United States Department of Agriculture. We find that phenological events throughout the growing season are correlated, and quantify the marked difference in size between table and wine grapes. By pairing publicly available historical phenotype data with genome-wide polymorphism data, we identify large effect loci controlling traits that have been targeted during domestication and breeding, including hermaphroditism, lighter skin pigmentation and muscat aroma. Breeding for larger berries in table grapes was traditionally concentrated in geographic regions where Islam predominates and alcohol was prohibited, whereas wine grapes retained the ancestral smaller size that is more desirable for winemaking in predominantly Christian regions. We uncover a novel locus with a suggestive association with berry size that harbors a signature of positive selection for larger berries. Our results suggest that religious rules concerning alcohol consumption have had a marked impact on patterns of phenomic and genomic diversity in grapes.

Cite this article

Download citation ▾
Zoë Migicovsky, Jason Sawler, Kyle M Gardner, Mallikarjuna K Aradhya, Bernard H Prins, Heidi R Schwaninger, Carlos D Bustamante, Edward S Buckler, Gan-Yuan Zhong, Patrick J Brown, Sean Myles. Patterns of genomic and phenomic diversity in wine and table grapes. Horticulture Research, 2017, 4 (1) : 17035 DOI:10.1038/hortres.2017.35

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

McGovern PE . Ancient wine: the search for the origins of viniculture. Princeton University Press.Chapter 1 Stone Age Wine, Pages 1-15, 2003.

[2]

OIV. OIV report on the world vitivinicultural situation. Available from http://www.oiv.int/public/medias/4906/press-release-2016-bilan-en.pdf (Accessed 25 November 2016).

[3]

Bacilieri R, Lacombe T, Le Cunff L, et al. Genetic structure in cultivated grapevines is linked to geography and human selection. BMC Plant Biol 2013; 13: 25.

[4]

This P, Lacombe T, Thomas MR . Historical origins and genetic diversity of wine grapes. Trends Genet 2006; 22: 511-519.

[5]

Fournier-Level A, Lacombe T, Le Cunff L, Boursiquot JM, This P . Evolution of the VvMybA gene family, the major determinant of berry colour in cultivated grapevine (Vitis vinifera L.) . Heredity 2010; 104: 351-362.

[6]

Bouquet A . Grapevines and viticulture. In: Adam-Blondon A-F, Martínez-Zapater JM, Kole C (eds). Genetics, Genomics and Breeding of Grapes. CRC Press: Boca Raton, FL, 2011, pp 1-29.

[7]

Myles S. Improving fruit and wine: what does genomics have to offer? Trends Genet 2013; 29: 190-196.

[8]

Töpfer R, Hausmann L, Eibach R . Molecular breeding. In: Adam-Blondon A-F, Martínez-Zapater JM, Kole C (eds). Genetics, Genomics and Breeding of Grapes. CRC Press: Boca Raton, FL, 2011, pp 160-185.

[9]

Edge-Garza DA, Luby JJ, Peace C . Decision support for cost-efficient and logistically feasible marker-assisted seedling selection in fruit breeding. Mol Breed 2015; 35: 223.

[10]

McClure KA, Sawler J, Gardner KM, Money D, Myles S . Genomics: a potential panacea for the perennial problem. Am J Bot 2014; 101: 1780-1790.

[11]

Migicovsky Z, Sawler J, Money D et al. Genomic ancestry estimation quantifies use of wild species in grape breeding. BMC Genomics 2016; 17: 478.

[12]

Migicovsky Z, Myles S . Exploiting wild relatives for genomics-assisted breeding of perennial crops. Front Plant Sci 2017; 8: 460.

[13]

Riaz S, Tenscher AC, Graziani R, Krivanek AF, Ramming DW, Walker MA . Using marker-assisted selection to breed Pierce’s disease-resistant grapes. Am J Enol Vitic 2009; 60: 199-207.

[14]

Eibach R, Zyprian E, Welter L, Töpfer R . The use of molecular markers for pyramiding resistance genes in grapevine breeding. VITIS 2007; 46: 120-124.

[15]

Kobayashi S, Goto-Yamamoto N, Hirochika H . Retrotransposon-induced mutations in grape skin color. Science 2004; 304: 982- 982.

[16]

Fournier-Level A, Le Cunff L, Gomez C et al. Quantitative genetic bases of anthocyanin variation in grape (Vitis vinifera L. ssp. sativa) berry: a quantitative trait locus to quantitative trait nucleotide integrated study . Genetics 2009; 183: 1127-1139.

[17]

Marguerit E, Boury C, Manicki A et al. Genetic dissection of sex determinism, inflorescence morphology and downy mildew resistance in grapevine. Theor Appl Genet 2009; 118: 1261-1278.

[18]

Mejía N, Soto B, Guerrero M et al. Molecular, genetic and transcriptional evidence for a role of VvAGL11 in stenospermocarpic seedlessness in grapevine. BMC Plant Biol 2011; 11: 57.

[19]

Emanuelli F, Battilana J, Costantini L et al. A candidate gene association study on muscat flavor in grapevine (Vitis vinifera L.) . BMC Plant Biol 2010; 10: 241.

[20]

Luby JJ, Shaw DV . Does marker-assisted selection make dollars and sense in a fruit breeding program? HortScience 2001; 36: 872-879.

[21]

Houle D, Govindaraju DR, Omholt S . Phenomics: the next challenge. Nat Rev Genet 2010; 11: 855-866.

[22]

Baldwin SJ, Dodds KG, Auvray B, Genet RA, Macknight RC, Jacobs JME . Association mapping of cold-induced sweetening in potato using historical phenotypic data. Ann Appl Biol 2011; 158: 248-256.

[23]

Matthies IE, Malosetti M, Roder MS, van Eeuwijk F . Genome-wide association mapping for kernel and malting quality traits using historical European barley records. PLoS ONE 2014; 9: e110046.

[24]

Migicovsky Z, Gardner KM, Money D et al. Genome to phenome mapping in apple using historical data. Plant Genome 2016; 9: 2.

[25]

Adam-Blondon AF, Alaux M, Pommier C et al. Towards an open grapevine information system. Hort Res 2016; 3: 16056.

[26]

Myles S, Boyko AR, Owens CL et al. Genetic structure and domestication history of the grape. Proc Natl Acad Sci USA 2011; 108: 3530-3535.

[27]

Myles S, Chia J-M, Hurwitz B et al. Rapid genomic characterization of the genus Vitis . PLoS ONE 2010; 5: e8219.

[28]

Purcell S, Neale B, Todd-Brown K et al. PLINK: a tool set for whole-genome association and population-based linkage analyses. The Am J Hum Genet 2007; 81: 559-575.

[29]

R Core Team . R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing: Vienna, Austria, 2015.

[30]

Price AL, Patterson NJ, Plenge RM, Weinblatt ME, Shadick NA, Reich D . Principal components analysis corrects for stratification in genome-wide association studies. Nat Genet 2006; 38: 904-909.

[31]

Patterson N, Price AL, Reich D . Population structure and eigenanalysis. PLoS Genet 2006; 2: e190.

[32]

Jackman S. pscl: Classes and Methods for R Developed in the Political Science Computational Laboratory. Stanford University: Stanford, CA, 2012. R package version 1.04.4.

[33]

Money D, Gardner K, Migicovsky Z, Schwaninger H, Zhong GY, Myles S . LinkImpute: fast and accurate genotype imputation for non-model organisms. G3 2015; 5: 23383-22390.

[34]

Mohammadi M, Tiede T, Smith KP . PopVar: a genome-wide procedure for predicting genetic variance and correlated response in biparental breeding populations. Crop Sci 2015; 55: 2068.

[35]

Kang HM, Sul JH, Service SK et al. Variance component model to account for sample structure in genome-wide association studies. Nat Genet 2010; 42: 348-354.

[36]

Scheet P, Stephens M . A fast and flexible statistical model for large-scale population genotype data: applications to inferring missing genotypes and haplotypic phase. Am J Hum Genet 2006; 78: 629-644.

[37]

Szpiech ZA, Hernandez RD . selscan: an efficient multithreaded program to perform EHH-based scans for positive selection. Mol Biol Evol 2014; 31: 2824-2827.

[38]

Winkler AJ, Cook JA, Kliewer WM, Lider LA . General Viticulture. University of California Press: Berkeley, CA, 1974.

[39]

Keller M. Chapter 6-developmental physiology. In: Keller M (ed). The Science of Grapevines. Academic Press: San Diego, 2010, pp 169-225.

[40]

Roby G, Harbertson JF, Adams DA, Matthews MA . Berry size and vine water deficits as factors in winegrape composition: anthocyanins and tannins. Aust J Grape Wine Res 2004; 10: 100-107.

[41]

Singleton V. Effects on red wine quality of removing juice before fermentation to simulate variation in berry size. Am J Enol Vitic 1972; 23: 106-113.

[42]

Muñoz-Robredo P, Robledo P, Manríquez D, Molina R, Defilippi BG . Characterization of sugars and organic acids in commercial varieties of table grapes. Chilean J Of Agric Res 2011; 71: 452-458.

[43]

Conde C, Silva P, Fontes N et al. Biochemical Changes Throughout Grape Berry Development and Fruit and Wine Quality Food 2007; 1: 1-22.

[44]

Kliewer WM, Howarth L, Omori M . Concentrations of tartaric acid and malic acids and their salts in Vitis vinifera grapes . Am J Enol Vitic 1967; 18: 42-54.

[45]

Liu H-F, Wu B-H, Fan P-G, Li S-H, Li L-S . Sugar and acid concentrations in 98 grape cultivars analyzed by principal component analysis. J Sci Food Agric 2006; 86: 1526-1536.

[46]

Reisch BI, Owens CL, Cousins PS . Grape. In: Badenes ML, Byrne DH (eds). Fruit Breeding vol. 8. Springer: USA, 2012, pp 225-262.

[47]

Vargas AM, de Andrés MT, Borrego J, Ibáñez J . Pedigrees of fifty table-grape cultivars. Am J Enol Vitic 2009; 60: 525-532.

[48]

Ibáñez J, Vargas AM, Palancar M, Borrego J, de Andrés MT . Genetic relationships among table-grape varieties. Am J Enol Vitic 2009; 60: 35-42.

[49]

Heffner EL, Sorrells ME, Jannink J-L . Genomic selection for crop Improvement. Crop Science 2009; 49: 1-12.

[50]

Spindel J, Begum H, Akdemir D et al. Genomic selection and association mapping in rice (Oryza sativa): effect of trait genetic architecture, training population composition, marker number and statistical model on accuracy of rice genomic selection in elite, tropical rice breeding lines . PLoS Genet 2015; 11: e1004982.

[51]

Kumar S, Bink MCAM, Volz RK, Bus VGM, Chagné D . Towards genomic selection in apple (Malus × domestica Borkh.) breeding programmes: prospects, challenges and strategies . Tree Genet Genomes 2012; 8: 1-14.

[52]

Marrano A, Birolo G, Prazzoli ML, Lorenzi S, Valle G, Grando MS . SNP-discovery by RAD-sequencing in a germplasm collection of wild and cultivated grapevines (V. vinifera L.) . PLoS ONE 2017; 12: e0170655.

[53]

Owens CL . Grapes. In JF Hancock (eds). Temperate Fruit Crop Breeding. Springer, 2008, pp 197-233.

[54]

Lowe K, Walker M . Genetic linkage map of the interspecific grape rootstock cross Ramsey (Vitis champinii) × Riparia Gloire (Vitis riparia) . Theor Appl Genet 2006; 112: 1582-1592.

[55]

Dalbó M, Ye G, Weeden N, Steinkellner H, Sefc K, Reisch B . A gene controlling sex in grapevines placed on a molecular marker-based genetic map. Genome 2000; 43: 333-340.

[56]

Fechter I, Hausmann L, Daum M et al. Candidate genes within a 143 kb region of the flower sex locus in Vitis . Mol Genet Genomics 2012; 287: 247-259.

[57]

Myles S, Mahanil S, Harriman J et al. Genetic mapping in grapevine using SNP microarray intensity values. Mol Breed 2015; 35: 88.

[58]

Hyma KE, Barba P, Wang M et al. Heterozygous mapping strategy (HetMappS) for high resolution genotyping-by-sequencing markers: a case study in grapevine. PLoS ONE 2015; 10: e0134880.

[59]

Matus JT, Aquea F, Arce-Johnson P . Analysis of the grape MYB R2R3 subfamily reveals expanded wine quality-related clades and conserved gene structure organization across Vitis and Arabidopsis genomes . BMC Plant Biol 2008; 8: 83.

[60]

This P, Lacombe T, Cadle-Davidson M, Owens C . Wine grape (Vitis vinifera L.) color associates with allelic variation in the domestication gene VvmybA1 . Theor Appl Genet 2007; 114: 723-730.

[61]

Huang X, Wei X, Sang T et al. Genome-wide association studies of 14 agronomic traits in rice landraces. Nat Genet 2010; 42: 961-967.

[62]

Atwell S, Huang YS, Vilhjálmsson BJ et al. Genome-wide association study of 107 phenotypes in Arabidopsis thaliana inbred lines . Nature 2010; 465: 627-631.

[63]

Battilana J, Costantini L, Emanuelli F 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 2009; 118: 653-669.

[64]

Emanuelli F, Sordo M, Lorenzi S, Battilana J, Grando MS . Development of user-friendly functional molecular markers for gene conferring muscat flavor in grapevine. Mol Breed 2014; 33: 235-241.

[65]

Battilana J, Emanuelli F, Gambino G et al. Functional effect of grapevine 1-deoxy-D-xylulose 5-phosphate synthase substitution K284N on Muscat flavour formation. J Exp Bot 2011; 62: 5497-5508.

[66]

Kwan E, Friendly M . tableplot: Represents tables as semi-graphic displays. R package version 03-5, 2012; https://CRAN.R-project.org/package=tableplo.

PDF (2679KB)

0

Accesses

0

Citation

Detail

Sections
Recommended

/