Abstract
Because of rapid diversification and frequent interspecific gene flow within the genus and inappropriate molecular markers used for phylogenetic studies, phylogeny and evolution of the economically significant crop genus Vitis are poorly resolved and understood, and species delimitation of Vitis remain disputable. In order to better understand of relationships within Vitis, phylogenomic analysis of chloroplast genomes were performed based on extensive sampling scheme. Well resolved phylogenetic tree and clear divergence pattern of Vitis were obtained in the present study. The results shows that subg. Vitis was constituted by three strongly supported monophyletic clades whose species are distributed in North America, Europe and Asia, respectively. Nine molecular markers are provided as potential markers for DNA barcoding and phylogenetic study of Vitis. Furthermore, taxonomic position of the critically endangered species endemic to Northern China, V. baihuashanensis, is investigated and suggested to be a separate species based on phylogenomic analysis and morphological comparisons, and effective conservation actions is badly needed. Molecular resources reported in this study could also be used for genetic engineering studies of Vitis, and will potentially promote genomic exploration of crop wild relatives and conservation of the germplasm.
References
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Huang, D.I. & Cronk, Q.C. (2015) Plann: A command-line application for annotating plastome sequences. Applications in Plant Sciences 3: 1500026.
https://doi.org/10.3732/apps.1500026
Huotari, T. & Korpelainen, H. (2013) Comparative analyses of plastid sequences between native and introduced populations of aquatic weeds Elodea canadensis and E. nuttallii. PLoS One 8: e580734.
https://doi.org/10.1371/journal.pone.0058073
Imazio, S., Maghradze, D., De Lorenzis, G., Bacilieri, R., Laucou, V., This, P., Scienza, A. & Failla, O. (2013) From the cradle of grapevine domestication: molecular overview and description of Georgian grapevine (Vitis vinifera L.) germplasm. Tree Genetics & Genomes 9: 641–658.
https://doi.org/10.1007/s11295-013-0597-9
IUCN (2012) IUCN Red List Categories and Criteria: Version 3.1. Second edition. IUCN, Gland, Switzerland and Cambridge, UK.
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https://doi.org/10.1038/nature06148
Kang, M.S. & Lu, D.Z. (1993) A new species of Vitis from Beijing. Acta Phytotaxonomica Sinica 31: 70–71.
Katoh, K., Rozewicki, J. & Yamada, K.D. (2017) MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Briefings in Bioinformatics. (in press)
https://doi.org/10.1093/bib/bbx108
Kearse, M., Moir, R., Wilson, A., Stones-Havas, S., Cheung, M., Sturrock, S., Buxton, S., Cooper, A., Markowitz, S., Duran, C., Thierer, T., Ashton, B., Meintjes, P. & Drummond, A. (2012) Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28: 1647–1649.
https://doi.org/10.1093/bioinformatics/bts199
Klein, L.L., Miller, A.J., Ciotir, C., Hyma, K., Uribe-Convers, S. & Londo, J. (2018) High-throughput sequencing data clarify evolutionary relationships among North American Vitis species and improve identification in USDA Vitis germplasm collections. American Journal of Botany 105: 215–226.
https://doi.org/10.1002/ajb2.1033
Kumar, S., Stecher, G. & Tamura, K. (2016) MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets. Molecular Biology and Evolution 33: 1870–1874.
https://doi.org/10.1093/molbev/msw054
Lam-Tung, N., Heiko, A.S., Arndt, von H. & Bui, Q.M. (2015) IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Molecular Biology and Evolution 32 (1): 268–274.
https://doi.org/10.1093/molbev/msu300
Linnaeus, C. von (1753) Species Plantarum 2. Impensis Laurentii Salvii, Holmiae [Stockholm], 202 pp.
Li, C.L., Cao, Y.L. & He, Y.H. (1996) A taxonomical study on Vitis L. in China. Chinese Journal of Applied and Environmental Biology 2 (3):234–253.
Li, C.L. (1998) Vitis. In: Editorial Committee of Flora Sinicae (Org.) Flora Reipublicae Popularis Sinicae vol. 48 (2). Science Press, Beijing, pp. 136–178.
Li, J.L., Wang, S., Yu, J., Wang, L. & Zhou, S.L. (2013) A modified CTAB protocol for plant DNA extraction. Chinese Bulletin of Botany 48: 72–78.
https://doi.org/10.3724/SP.J.1259.2013.00072
Liu, X.Q., Ickert-Bond, S.M., Nie, Z.L., Zhou, Z., Chen, L.Q. & Wen, J. (2016) Phylogeny of the Ampelocissus-Vitis clade in Vitaceae supports the New World origin of the grape genus. Molecular Phylogenetics and Evolution 95: 217–228.
https://doi.org/10.1016/j.ympev.2015.10.013
Logacheva, M.D., Penin, A.A., Valiejo-Roman, C.M. & Antonov, A.S. (2009) Structure and evolution of junctions between inverted repeat and small single copy regions of chloroplast genome in non-core Caryophyllales. Molecular Biology 43: 757–765.
https://doi.org/10.1134/S0026893309050070
Logacheva, M.D., Samigullin, T.H., Dhingra, A. & Penin, A.A. (2008) Comparative chloroplast genomics and phylogenetics of Fagopyrum esculentum ssp. ancestrale - A wild ancestor of cultivated buckwheat. BMC Plant Biology: 8.
https://doi.org/10.1186/1471-2229-8-59
Lohse, M., Drechsel, O., Kahlau, S. & Bock, R. (2013) OrganellarGenomeDRAW-a suite of tools for generating physical maps of plastid and mitochondrial genomes and visualizing expression data sets. Nucleic Acids Research 41: W575–W581.
https://doi.org/10.1093/nar/gkt289
Lu, D.Z. & Liang, H.P. (1994) A study on Vitis in Beijing. Journal of Beijing Agricultural College 9: 78–81.
Ma, Z., Wen, J., Ickert-Bond, S.M., Chen, L. & Liu, X. (2016) Morphology, Structure, and Ontogeny of Trichomes of the Grape Genus (Vitis, Vitaceae). Frontiers in Plant Science 7: 704.
https://doi.org/10.3389/fpls.2016.00704
Magallon, S. & Castillo, A. (2009) Angiosperm diversification through time. American Journal of Botany 96: 349–365.
https://doi.org/10.3732/ajb.0800060
McGovern, P.E. (2003) Ancient Wine: The Search for the Origins of Viniculture. Princeton University Press, Princeton.
Myles, S., Boyko, A.R., Owens, C.L., Brown, P.J., Grassi, F., Aradhya, M.K., Prins, B., Reynolds, A., Chia, J., Ware, D., Bustamante, C.D. & Buckler, E.S. (2011) Genetic structure and domestication history of the grape. Proceedings of the National Academy of Science, USA 108: 3530–3535.
https://doi.org/10.1073/pnas.1009363108
Nie, Z.L., Sun, H., Manchester, S.R., Meng, Y., Luke, Q. & Wen, J. (2012) Evolution of the intercontinental disjunctions in six continents in the Ampelopsis clade of the grape family (Vitaceae). BMC Evolutionary Biology 12: 17.
https://doi.org/10.1186/1471-2148-12-17
Ren, H. & Wen, J. (2007) Vitis. In: Wu, C.Y., Hong, D.Y. & Raven, P.H. (Eds.) Flora of China. Science Press & Missouri Botanical Garden Press, Beijing & St. Louis, pp. 173–222.
Rozas, J., Ferrer-Mata, A., Sánchez-DelBarrio, J.C., Guirao-Rico, S., Librado, P., Ramos-Onsins, S.E. & Sánchez-Gracia, A. (2017) DnaSP 6: DNA sequence polymorphism analysis of large datasets. Molecular Biology and Evolution. (in press)
https://doi.org/10.1093/molbev/msx248
Ruprecht, F.J. (1857) Die Ersten Botanichen Nachrichten Uber uas Amurland. Bulletin de la Class Physico-Mathematique de l’Academie Imperiale des Sciences de Saint-Pétersbourg. St. Petersburg 15: 266.
Shaw, J., Lickey, E.B., Beck, J.T., Farmer, S.B., Liu, W.S., Miller, J., Siripun, K.C., Winder, C.T., Schilling, E.E. & Small, R.L. (2005) The tortoise and the hare II: Relative utility of 21 noncoding chloroplast DNA sequences for phylogenetic analysis. American Journal of Botany 92: 142–166.
https://doi.org/10.3732/ajb.92.1.142
Shaw, J., Lickey, E.B., Schilling, E.E. & Small, R.L. (2007) Comparison of whole chloroplast genome sequences to choose noncoding regions for phylogenetic studies in angiosperms: The tortoise and the hare III. American Journal of Botany 94: 275–288.
https://doi.org/10.3732/ajb.94.3.275
Skvortzow, B.W. (1925) Notes on trees and shrubs of Northern Manchuria. The Chinese Journal 15 (4): 200–201.
Small, R.L., Ryburn, J.A., Cronn, R.C., Seelanan, T. & Wendel, J.F. (1998) The tortoise and the hare: choosing between noncoding plastome and nuclear Adh sequences for phylogeny reconstruction in a recently diverged plant group. American Journal of Botany 85: 1301–1315.
https://doi.org/10.2307/2446640
Tabidze, V., Pipia, I., Gogniashvili, M., Kunelauri, N., Ujmajuridze, L., Pirtskhalava, M., Vishnepolsky, B., Hernandez, A.G., Fields, C.J. & Beridze, T. (2017) Whole genome comparative analysis of four Georgian grape cultivars. Molecular Genetics and Genomics 292: 1377–1389.
https://doi.org/10.1007/s00438-017-1353-x
Tröndle, D., Schroder, S., Kassemeyer, H.H., Kiefer, C., Koch, M.A. & Nick, P. (2010) Molecular phylogeny of the genus Vitis (Vitaceae) based on plastid markers. American Journal of Botany 97: 1168–1178.
https://doi.org/10.3732/ajb.0900218
Wan, Y., Schwaninger, H.R., Baldo, A.M., Labate, J.A., Zhong, G.Y. & Simon, C.J. (2013) A phylogenetic analysis of the grape genus (Vitis L.) reveals broad reticulation and concurrent diversification during Neogene and Quaternary climate change. BMC Evolutionary Biology 13: 141.
https://doi.org/10.1186/1471-2148-13-141
Wen, J. (2007) Vitaceae. In: Kubitzki, K. (Ed.) The Families and Genera of Vascular Plants. Springer-Verlag, Berlinm, pp. 466–478.
https://doi.org/10.1007/978-3-540-32219-1_54
Wyman, S.K., Jansen, R.K. & Boore, J.L. (2004) Automatic annotation of organellar genomes with DOGMA. Bioinformatics 20: 3252–3255.
https://doi.org/10.1093/bioinformatics/bth352
Xie, H., Jiao, J., Fan, X., Zhang, Y., Jiang, J., Sun, H. & Liu, C. (2017) The complete chloroplast genome sequence of Chinese wild grape Vitis amurensis (Vitaceae: Vitis L.). Conservation Genetics Resources 9: 43–46.
https://doi.org/10.1007/s12686-016-0615-y
Zecca, G., Abbott, J.R., Sun, W., Spada, A., Sala, F. & Grassi, F. (2012) The timing and the mode of evolution of wild grapes (Vitis). Molecular Phylogenetics and Evolution 62: 736–747.
https://doi.org/10.1016/j.ympev.2011.11.015
Zhou, Y., Massonnet, M., Sanjak, J.S., Cantu, D. & Gaut, B.S. (2017) Evolutionary genomics of grape (Vitis vinifera ssp. vinifera) domestication. Proceedings of the National Academy of Science, USA 114: 11715–11720.
https://doi.org/10.1073/pnas.1709257114
https://doi.org/10.1089/cmb.2012.0021
Daniell, H., Lin, C., Yu, M. & Chang, W. (2016) Chloroplast genomes: diversity, evolution, and applications in genetic engineering. Genome Biology 17: 134.
https://doi.org/10.1186/s13059-016-1004-2
Diep, T., Olga, C., Arndt, von H., Bui, Q. & Le, S. (2018) UFBoot2: improving the Ultrafast bootstrap approximation. Molecular Biology and Evolution 35 (2): 518–522.
https://doi.org/10.1093/molbev/msx281
Dong, W., Liu, J., Yu, J., Wang, L. & Zhou, S. (2012) Highly variable chloroplast markers for evaluating plant phylogeny at low taxonomic levels and for DNA barcoding. PLoS One 7: e35071.
https://doi.org/10.1371/journal.pone.0035071
Ebert, D. & Peakall, R. (2009) A new set of universal de novo sequencing primers for extensive coverage of noncoding chloroplast DNA: new opportunities for phylogenetic studies and cpSSR discovery. Molecular Ecology Resources 9: 777–783.
https://doi.org/10.1111/j.1755-0998.2008.02320.x
Huang, D.I. & Cronk, Q.C. (2015) Plann: A command-line application for annotating plastome sequences. Applications in Plant Sciences 3: 1500026.
https://doi.org/10.3732/apps.1500026
Huotari, T. & Korpelainen, H. (2013) Comparative analyses of plastid sequences between native and introduced populations of aquatic weeds Elodea canadensis and E. nuttallii. PLoS One 8: e580734.
https://doi.org/10.1371/journal.pone.0058073
Imazio, S., Maghradze, D., De Lorenzis, G., Bacilieri, R., Laucou, V., This, P., Scienza, A. & Failla, O. (2013) From the cradle of grapevine domestication: molecular overview and description of Georgian grapevine (Vitis vinifera L.) germplasm. Tree Genetics & Genomes 9: 641–658.
https://doi.org/10.1007/s11295-013-0597-9
IUCN (2012) IUCN Red List Categories and Criteria: Version 3.1. Second edition. IUCN, Gland, Switzerland and Cambridge, UK.
Jaillon, O., Aury, J., Noel, B., Policriti, A., Clepet, C., Casagrande, A., Choisne, N., Aubourg, S., Vitulo, N., Jubin, C., Vezzi, A., Legeai, F., Hugueney, P., Dasilva, C., Horner, D., Mica, E., Jublot, D., Poulain, J., Bruyere, C., Billault, A., Segurens, B., Gouyvenoux, M., Ugarte, E., Cattonaro, F., Anthouard, V., Vico, V., Del Fabbro, C., Alaux, M., Di Gaspero, G., Dumas, V., Felice, N., Paillard, S., Juman, I., Moroldo, M., Scalabrin, S., Canaguier, A., Le Clainche, I., Malacrida, G., Durand, E., Pesole, G., Laucou, V., Chatelet, P., Merdinoglu, D., Delledonne, M., Pezzotti, M., Lecharny, A., Scarpelli, C., Artiguenave, F., Pe, M.E., Valle, G., Morgante, M., Caboche, M., Adam-Blondon, A., Weissenbach, J., Quetier, F. & Wincker, P. (2007) The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449: 463–467.
https://doi.org/10.1038/nature06148
Kang, M.S. & Lu, D.Z. (1993) A new species of Vitis from Beijing. Acta Phytotaxonomica Sinica 31: 70–71.
Katoh, K., Rozewicki, J. & Yamada, K.D. (2017) MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Briefings in Bioinformatics. (in press)
https://doi.org/10.1093/bib/bbx108
Kearse, M., Moir, R., Wilson, A., Stones-Havas, S., Cheung, M., Sturrock, S., Buxton, S., Cooper, A., Markowitz, S., Duran, C., Thierer, T., Ashton, B., Meintjes, P. & Drummond, A. (2012) Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28: 1647–1649.
https://doi.org/10.1093/bioinformatics/bts199
Klein, L.L., Miller, A.J., Ciotir, C., Hyma, K., Uribe-Convers, S. & Londo, J. (2018) High-throughput sequencing data clarify evolutionary relationships among North American Vitis species and improve identification in USDA Vitis germplasm collections. American Journal of Botany 105: 215–226.
https://doi.org/10.1002/ajb2.1033
Kumar, S., Stecher, G. & Tamura, K. (2016) MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets. Molecular Biology and Evolution 33: 1870–1874.
https://doi.org/10.1093/molbev/msw054
Lam-Tung, N., Heiko, A.S., Arndt, von H. & Bui, Q.M. (2015) IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Molecular Biology and Evolution 32 (1): 268–274.
https://doi.org/10.1093/molbev/msu300
Linnaeus, C. von (1753) Species Plantarum 2. Impensis Laurentii Salvii, Holmiae [Stockholm], 202 pp.
Li, C.L., Cao, Y.L. & He, Y.H. (1996) A taxonomical study on Vitis L. in China. Chinese Journal of Applied and Environmental Biology 2 (3):234–253.
Li, C.L. (1998) Vitis. In: Editorial Committee of Flora Sinicae (Org.) Flora Reipublicae Popularis Sinicae vol. 48 (2). Science Press, Beijing, pp. 136–178.
Li, J.L., Wang, S., Yu, J., Wang, L. & Zhou, S.L. (2013) A modified CTAB protocol for plant DNA extraction. Chinese Bulletin of Botany 48: 72–78.
https://doi.org/10.3724/SP.J.1259.2013.00072
Liu, X.Q., Ickert-Bond, S.M., Nie, Z.L., Zhou, Z., Chen, L.Q. & Wen, J. (2016) Phylogeny of the Ampelocissus-Vitis clade in Vitaceae supports the New World origin of the grape genus. Molecular Phylogenetics and Evolution 95: 217–228.
https://doi.org/10.1016/j.ympev.2015.10.013
Logacheva, M.D., Penin, A.A., Valiejo-Roman, C.M. & Antonov, A.S. (2009) Structure and evolution of junctions between inverted repeat and small single copy regions of chloroplast genome in non-core Caryophyllales. Molecular Biology 43: 757–765.
https://doi.org/10.1134/S0026893309050070
Logacheva, M.D., Samigullin, T.H., Dhingra, A. & Penin, A.A. (2008) Comparative chloroplast genomics and phylogenetics of Fagopyrum esculentum ssp. ancestrale - A wild ancestor of cultivated buckwheat. BMC Plant Biology: 8.
https://doi.org/10.1186/1471-2229-8-59
Lohse, M., Drechsel, O., Kahlau, S. & Bock, R. (2013) OrganellarGenomeDRAW-a suite of tools for generating physical maps of plastid and mitochondrial genomes and visualizing expression data sets. Nucleic Acids Research 41: W575–W581.
https://doi.org/10.1093/nar/gkt289
Lu, D.Z. & Liang, H.P. (1994) A study on Vitis in Beijing. Journal of Beijing Agricultural College 9: 78–81.
Ma, Z., Wen, J., Ickert-Bond, S.M., Chen, L. & Liu, X. (2016) Morphology, Structure, and Ontogeny of Trichomes of the Grape Genus (Vitis, Vitaceae). Frontiers in Plant Science 7: 704.
https://doi.org/10.3389/fpls.2016.00704
Magallon, S. & Castillo, A. (2009) Angiosperm diversification through time. American Journal of Botany 96: 349–365.
https://doi.org/10.3732/ajb.0800060
McGovern, P.E. (2003) Ancient Wine: The Search for the Origins of Viniculture. Princeton University Press, Princeton.
Myles, S., Boyko, A.R., Owens, C.L., Brown, P.J., Grassi, F., Aradhya, M.K., Prins, B., Reynolds, A., Chia, J., Ware, D., Bustamante, C.D. & Buckler, E.S. (2011) Genetic structure and domestication history of the grape. Proceedings of the National Academy of Science, USA 108: 3530–3535.
https://doi.org/10.1073/pnas.1009363108
Nie, Z.L., Sun, H., Manchester, S.R., Meng, Y., Luke, Q. & Wen, J. (2012) Evolution of the intercontinental disjunctions in six continents in the Ampelopsis clade of the grape family (Vitaceae). BMC Evolutionary Biology 12: 17.
https://doi.org/10.1186/1471-2148-12-17
Ren, H. & Wen, J. (2007) Vitis. In: Wu, C.Y., Hong, D.Y. & Raven, P.H. (Eds.) Flora of China. Science Press & Missouri Botanical Garden Press, Beijing & St. Louis, pp. 173–222.
Rozas, J., Ferrer-Mata, A., Sánchez-DelBarrio, J.C., Guirao-Rico, S., Librado, P., Ramos-Onsins, S.E. & Sánchez-Gracia, A. (2017) DnaSP 6: DNA sequence polymorphism analysis of large datasets. Molecular Biology and Evolution. (in press)
https://doi.org/10.1093/molbev/msx248
Ruprecht, F.J. (1857) Die Ersten Botanichen Nachrichten Uber uas Amurland. Bulletin de la Class Physico-Mathematique de l’Academie Imperiale des Sciences de Saint-Pétersbourg. St. Petersburg 15: 266.
Shaw, J., Lickey, E.B., Beck, J.T., Farmer, S.B., Liu, W.S., Miller, J., Siripun, K.C., Winder, C.T., Schilling, E.E. & Small, R.L. (2005) The tortoise and the hare II: Relative utility of 21 noncoding chloroplast DNA sequences for phylogenetic analysis. American Journal of Botany 92: 142–166.
https://doi.org/10.3732/ajb.92.1.142
Shaw, J., Lickey, E.B., Schilling, E.E. & Small, R.L. (2007) Comparison of whole chloroplast genome sequences to choose noncoding regions for phylogenetic studies in angiosperms: The tortoise and the hare III. American Journal of Botany 94: 275–288.
https://doi.org/10.3732/ajb.94.3.275
Skvortzow, B.W. (1925) Notes on trees and shrubs of Northern Manchuria. The Chinese Journal 15 (4): 200–201.
Small, R.L., Ryburn, J.A., Cronn, R.C., Seelanan, T. & Wendel, J.F. (1998) The tortoise and the hare: choosing between noncoding plastome and nuclear Adh sequences for phylogeny reconstruction in a recently diverged plant group. American Journal of Botany 85: 1301–1315.
https://doi.org/10.2307/2446640
Tabidze, V., Pipia, I., Gogniashvili, M., Kunelauri, N., Ujmajuridze, L., Pirtskhalava, M., Vishnepolsky, B., Hernandez, A.G., Fields, C.J. & Beridze, T. (2017) Whole genome comparative analysis of four Georgian grape cultivars. Molecular Genetics and Genomics 292: 1377–1389.
https://doi.org/10.1007/s00438-017-1353-x
Tröndle, D., Schroder, S., Kassemeyer, H.H., Kiefer, C., Koch, M.A. & Nick, P. (2010) Molecular phylogeny of the genus Vitis (Vitaceae) based on plastid markers. American Journal of Botany 97: 1168–1178.
https://doi.org/10.3732/ajb.0900218
Wan, Y., Schwaninger, H.R., Baldo, A.M., Labate, J.A., Zhong, G.Y. & Simon, C.J. (2013) A phylogenetic analysis of the grape genus (Vitis L.) reveals broad reticulation and concurrent diversification during Neogene and Quaternary climate change. BMC Evolutionary Biology 13: 141.
https://doi.org/10.1186/1471-2148-13-141
Wen, J. (2007) Vitaceae. In: Kubitzki, K. (Ed.) The Families and Genera of Vascular Plants. Springer-Verlag, Berlinm, pp. 466–478.
https://doi.org/10.1007/978-3-540-32219-1_54
Wyman, S.K., Jansen, R.K. & Boore, J.L. (2004) Automatic annotation of organellar genomes with DOGMA. Bioinformatics 20: 3252–3255.
https://doi.org/10.1093/bioinformatics/bth352
Xie, H., Jiao, J., Fan, X., Zhang, Y., Jiang, J., Sun, H. & Liu, C. (2017) The complete chloroplast genome sequence of Chinese wild grape Vitis amurensis (Vitaceae: Vitis L.). Conservation Genetics Resources 9: 43–46.
https://doi.org/10.1007/s12686-016-0615-y
Zecca, G., Abbott, J.R., Sun, W., Spada, A., Sala, F. & Grassi, F. (2012) The timing and the mode of evolution of wild grapes (Vitis). Molecular Phylogenetics and Evolution 62: 736–747.
https://doi.org/10.1016/j.ympev.2011.11.015
Zhou, Y., Massonnet, M., Sanjak, J.S., Cantu, D. & Gaut, B.S. (2017) Evolutionary genomics of grape (Vitis vinifera ssp. vinifera) domestication. Proceedings of the National Academy of Science, USA 114: 11715–11720.
https://doi.org/10.1073/pnas.1709257114