Dates and rates in grape’s plastomes: evolution in slow motion
- 4 Downloads
The family Vitaceae includes the domesticated grapevine (Vitis vinifera), one of the most economically important crops in the world. Despite the importance of Vitaceae, there is still considerable controversy surrounding their phylogenetic relationships and evolutionary timescales. Moreover, variation in rates of molecular evolution among Vitaceae remains mostly unexplored. The present research aims to fill these knowledge gaps through the analysis of plastome sequences. Thirteen newly sequenced grape plastomes are presented and their phylogenetic relationships examined. Divergence times and absolute substitution rates are inferred under different molecular clocks by the analysis of 95 non-coding plastid regions and 43 representative accessions of the major lineages of Vitaceae. Furthermore, the phylogenetic informativeness of non-coding plastid regions is investigated. We find strong evidence in favor of the random local clock model and rate heterogeneity within Vitaceae. Substitution rates decelerate in Ampelocissus, Ampelopsis, Nekemias, Parthenocissus, Rhoicissus, and Vitis, with genus Vitis showing the lowest values up to a minimum of ~ 4.65 × 10−11 s/s/y. We suggest that liana-like species of Vitaceae evolve slower than erect growth habit plants and we invoke the “rate of mitosis hypothesis” to explain the observed pattern of the substitution rates. We identify a reduced set of 20 non-coding regions able to accurately reconstruct the phylogeny of Vitaceae and we provide a detailed description of all 152 non-coding regions identified in the plastomes of subg. Vitis. These polymorphic regions will find their applications in phylogenetics, phylogeography, and population genetics as well in grapes identification through DNA barcoding techniques.
KeywordsDivergence time estimation Grapevine Rate of mitosis hypothesis Substitution rate Vitaceae Vitis
Georgian part of research was funded by Mr. Kakha Bendukidze (1956–2014) via his Knowledge Fund, a funding organization of the Free University of Tbilisi and Agricultural University of Georgia. We thank Penelope Barrington for insightful discussion and English revision. We acknowledge the anonymous reviewers for providing useful suggestions to improve this manuscript.
GZ and FG participated in study design, did phylogenetic and statistical analyses, did figures and supplementary material, interpreted the results, and wrote the manuscript. VT did most of the lab experiments, obtaining plant materials, DNA isolation and assembly of plastid DNA reads. IP participated in plastid DNA isolation and construction of DNA libraries. AK and NK provided construction of shotgun genomic DNA libraries and Illumina sequencing. TB participated in design and coordination of the study, interpretation of results, and critical revision of manuscript. All authors read and approved the final manuscript.
- Beridze T, Pipia I, Beck J, Hsu SC, Gamkrelidze M, Gogniashvili M, Tabidze V, This P, Bacilieri R, Gotsiridze V, Glonti M, Schaal B (2011) Plastid DNA sequence diversity in a worldwide set of grapevine cultivars (Vitis vinifera L. subsp. vinifera). Bull Georgian Natl Acad Sci 5:91–96Google Scholar
- Chandler MEJ (1962) The lower tertiary floras of Southern England. II. Flora of the pipe-clay series of dorset (Lower Bagshot). British Museum (Natural History), London, UK, pp 100–110Google Scholar
- Chen I (2009) History of Vitaceae inferred from morphology-based phylogeny and the fossil record of seeds (Ph.D. Dissertation). University of Florida, Gainesville, USAGoogle Scholar
- Grassi F, Labra M, Scienza A, Imazio I (2002) Chloroplast SSR markers to assess DNA diversity in wild and cultivated grapevines. Vitis 41:157–158Google Scholar
- Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41:95–98Google Scholar
- Heibl C (2013) PHYLOCH: interfaces and graphic tools for phylogenetic data in R. http://www.christophheibl.de/Rpackages.html. Accessed 18 June 2018
- Jansen RK, Kaittanis C, Saski C, Lee SB, Tomkins J, Alverson AJ, Daniell H (2006) Phylogenetic analyses of Vitis (Vitaceae) based on complete chloroplast genome sequences: effects of taxon sampling and phylogenetic methods on resolving relationships among rosids. BMC Evol Biol 6:32CrossRefPubMedPubMedCentralGoogle Scholar
- Lekshmi RK, Rajesh R, Mini S (2015) Ethyl acetate fraction of Cissus quadrangularis stem ameliorates hyperglycaemia-mediated oxidative stress and suppresses inflammatory response in nicotinamide/streptozotocin induced type 2 diabetic rats. Phytomedicine 22:952–960. https://doi.org/10.1016/j.phymed.2015.06.014 CrossRefPubMedGoogle Scholar
- Miller MA, Pfeiffer W, Schwartz T (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In: Proceedings of the Gateway Computing Environments Workshop (GCE), 14 November 2010, New Orleans, LA pp 1–8Google Scholar
- Moore MO (1991) Classification and systematics of eastern North American Vitis L. (Vitaceae) north of Mexico. SIDA 14:339–367Google Scholar
- Moore MO, Wen J (2016) Vitaceae. In: Flora of North America Editorial Committee (ed), Flora of North America, North of Mexico, vol. 12. Oxford University Press, New York, OxfordGoogle Scholar
- Pipia I, Gogniashvili M, Tabidze V, Beridze T, Gamkrelidze M, Gotsiridze V, Melyan G, Musayev M, Salimov V, Beck JB, Schaal B (2012) Plastid DNA sequence diversity in wild grapevine samples (Vitis vinifera subsp. sylvestris) from the Caucasus region. Vitis 51:119–124Google Scholar
- R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. (https://www.R-project.org/)
- Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542. https://doi.org/10.1093/sysbio/sys029 CrossRefPubMedPubMedCentralGoogle Scholar
- Swofford DL (2003) PAUP*. Phylogenetic analysis using parsimony (*and Other Methods). Version 4. Sinauer Associates, Sunderland, MassachusettsGoogle Scholar
- Tabidze V, Baramidze G, Pipia I, Gogniashvili M, Ujmajuridze L, Beridze T, Hernandez AG, Schaal B (2014) The complete chloroplast DNA sequence of eleven grape cultivars. Simultaneous resequencing methodology. J Int Sci Vigne Vin 48:99–109Google Scholar
- Wang Y, Jiang W, Comes HP, Hu FS, Qiu Y, Fu C (2015) Molecular phylogeography and ecological niche modelling of a widespread herbaceous climber, Tetrastigma hemsleyanum (Vitaceae): insights into Plio-Pleistocene range dynamics of evergreen forest in subtropical China. New Phytol 206:852–867. https://doi.org/10.1111/nph.13261 CrossRefPubMedGoogle Scholar
- Wen J, Lu LM, Boggan JK (2013) Diversity and evolution of Vitaceae in the Philippines. Philipp J Sci 142:223–244Google Scholar