Draft genome of the Native American cold hardy grapevine Vitis riparia Michx. ‘Manitoba 37’

Abstract

Vitis riparia, a critically important Native American grapevine species, is used globally in rootstock and scion breeding and contributed to the recovery of the French wine industry during the mid-19th century phylloxera epidemic. This species has abiotic and biotic stress tolerance and the largest natural geographic distribution of the North American grapevine species. Here we report an Illumina short-read 369X coverage, draft de novo heterozygous genome sequence of V. riparia Michx. ‘Manitoba 37’ with the size of ~495 Mb for 69,616 scaffolds and a N50 length of 518,740 bp. Using RNAseq data, 40,019 coding sequences were predicted and annotated. Benchmarking with Universal Single-Copy Orthologs (BUSCO) analysis of predicted gene models found 96% of the complete BUSCOs in this assembly. The assembly continuity and completeness were further validated using V. riparia ESTs, BACs, and three de novo transcriptome assemblies of three different V. riparia genotypes resulting in >98% of respective sequences/ transcripts mapping with this assembly. Alignment of the V. riparia assembly and predicted CDS with the latest V. vinifera ‘PN40024’ CDS and genome assembly showed 99% CDS alignment and a high degree of synteny. An analysis of plant transcription factors indicates a high degree of homology with the V. vinifera transcription factors. QTL mapping to V. riparia ‘Manitoba 37’ and V. vinifera PN40024 has identified genetic relationships to phenotypic variation between species. This assembly provides reference sequences, gene models for marker development and understanding V. riparia’s genetic contributions in grape breeding and research.

References

[1] Reisch, B. J. & Pratt, C. in Fruit Breeding, Vine and Small Fruits, (eds Janick, J. & More, J. N.) Ch. 4, Vol. 2 (John Wiley and Sons, Inc., 1996).

[2] Yang et al. Next generation mapping of enological traits in an F² interspecific grapevine hybrid family . PLoS ONE 11, e0149560 (2016).

[3] Zou, C. et al. Haplotyping the Vitis collinear core genome with rhAmpSeq improves marker transferability in a diverse genus. Nat. Commun. 11, 413 (2020).

[4] Gong, F., Karsai, I. & Liu, Y.-S. Vitis Seeds (Vitaceae) from the late Neogene Gray fossil site, Northeastern Tennessee, U.S.A. J. Rev. Palaeobot. Palyno. 162, 71-83 (2010).

[5] Graham, A. The role of land bridges, ancient environments, and migrations in the assembly of the North American flora. J. Sys. Evol. 56, 405-429 (2018).

[6] Manchester, S. R. Revisions to Rowland Brown’s North American Paleocene flora. Acta Musei Nationalis Pragae, Ser. B - Historia Naturalis 70, 153-210 (2014).

[7] Nie, Z. L. et al. Molecular phylogeny and biogeographic diversification of Parthenocissus (Vitaceae) disjunct between Asia and North America. Am. J. Bot. 97, 1342-1353 (2010).

[8] Wan, Y. Z. et al. A phylogenetic analysis of the grape genus (Vitis L.) reveals broad reticulation and concurrent diversification during Neogene and Quaternary climate change. BMC Evol. Biol. 13, 141 (2013).

[9] Zohary, D. & Hopf, M. Domestication of plants in the old world: The origin and spread of cultivated plants in West Asia, Europe and the Nile Valley. 3rd edn. (Oxford University, New York, 2000)

[10] Klein, L. L. et al. High-throughput sequencing data clarify evolutionary relationships among North American Vitis species and improve identification in USDA Vitis germplasm collection. Am. J. Bot. 105, 215-216 (2018).

[11] Hemstad, P. R. & Breeder, G. in Grapevine Breeding Programs for the Wine Industry (ed Reynolds, A.) 1st edn, Ch. 17 (Woodhead Publishing, 2015).

[12] Hemstad, P. R. & Luby, J. J. Utilization of Vitis riparia for the development of new wine varieties with resistance to disease and extreme cold. (eds Bouquet, A. & Boursiquot, M. J.) VII international symposium on grapevine genetics and breeding; Acta Horticulturae 528, 487-490 (2000).

[13] Luby, J. & Fennell, A. Fruit breeding for the northern great plains at the University of Minnesota and South Dakota State University. HortSci. 41, 25-26 (2006).

[14] Lowe, K. M. & Walker, M. A. Genetic linkage map of the interspecific grape rootstock cross Ramsey (Vitis champinii) x Riparia Gloire (Vitis riparia). Theor. Appl. Genet. 112, 1582-1592 (2006).

[15] Tuck, B., Gartner, W. & Appiah, G. Vineyards and grapes of the North. University of Minnesota. University of Minnesota Digital Conservancy, http://hdl.handle.net/11299/197814 (2016).

[16] Tuck, B., Gartner, W., Appiah, G. Wineries of the North. University of Minnesota. Retrieved from the University of Minnesota Digital Conservancy, http://hdl.handle.net/11299/197823 (2016).

[17] Fennell, A., Mathiason, K. & Luby, J. Genetic segregation for indicators of photoperiod control of dormancy induction in Vitis species. Acta Hort. 689, 533 (2005). 539.

[18] Garris, A. et al. Mapping of photoperiod-induced growth cessation in the wild grape Vitis riparia. J. Am. Soc. Hort. Sci. 134, 261-272 (2009).

[19] Fennell, A., Alahakoon, D., Luby, J. & Clark, M. Mapping the genetic architecture of grapevine bud growth-cycling quantitative traits. Acta Hort. 1248, 337-343 (2019).

[20] Fennell, A. & Line, M. J. Identifying differential tissue response in grape (Vitis riparia) during induction of endodormancy using nuclear magnetic resonance imaging. J. Am. Soc. Hort. Sci. 126, 681-688 (2001).

[21] Fennell, A. et al. Short day transcriptomic programming during induction of dormancy in grapevine. Front Plant Sci. 6, 834 (2015).

[22] George, I. S., Fennell, A. Y. & Haynes, P. A. Protein identification and quantification from riverbank grape, Vitis riparia: Comparing SDS-PAGE and FASP-GPF techniques for shotgun proteomic analysis. Proteomics 16, 3061-3065 (2015).

[23] Jaillon, O. et al. The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449, 463-467 (2007).

[24] Girollet, N. et al. De novo phased assembly of Vitis riparia grape genome. Sci. Data 6, 127 (2019).

[25] Canaguier, A. et al. A new version of the grapevine reference genome assembly (12X.v2) and of its annotation (VCost.v3). Genomics Data 14, 56-62 (2017).

[26] Chin, C.-S. et al. Phased diploid genome assembly with single-molecule real-time sequencing. Nat. Methods 13, 1050-1054 (2016).

[27] Minio, A. et al. Diploid genome assembly of the wine grape Carménère. G3 9, 1331-1337 (2019).

[28] Roach, M. J. et al. Population sequencing reveals clonal diversity and ancestral inbreeding in the grapevine cultivar Chardonnay. PLoS Genet. 14, e1007807 (2018).

[29] Di Genova, A. et al. Whole genome comparison between table and wine grapes reveals a comprehensive catalog of structural variants. BMC Plant Biol. 14, 7 (2014).

[30] Patel, S. et al. Comparison of three assembly strategies for a heterozygous seedless grapevine genome assembly. BMC Genomics 19, 57 (2018).

[31] Grimplet, J., Pimentel, D., Agudelo-Romero, P ., Martinez-Zapater, J. M. & Fortes, A. M. The lateral organ boundaries domain gene family in grapevine: genome-wide characterization and expresson analyses during developmental processes and stress responses. Sci. Rep. 7, 15968 (2017).

[32] Wang, M. et al. Genome and transcriptome analysis of the grapevine (Vitis vinifera L.) WRKY gene family. Hortic. Res. 1, 14016 (2014).

[33] Eulgem, T., Rushton, P. J., Robatzek, S. & Somssich, I. E. The WRKY superfamily of plant transcription factors. Trends Plant Sci. 5, 199-206 (2000).

[34] Licausi, F. et al. Genomic and transcriptomic analysis of the AP2/ERF superfamily in Vitis vinifera. BMC Genomics 11, 719 (2010).

[35] Jin, J. et al. PlantTFDB 4.0: toward a central hub for transcription factors and regulatory interactions in plants. Nucleic Acids Res. 45, D1040-D1045 (2017).

[36] Gonzalez, A., Zhao, M., Leavitt, J. M. & Loyd, A. M. Regulation of the anthocyanin pathway by the TTG1/bHLH/Myb transcriptional complex in Arabidopsis seedlings. Plant J. 53, 814-827 (2008).

[37] Li, Z., Pan, Q., Jin, Z., Mu, L. & Duan, C. Comparison on phenoloic compounds in Vitis vinifera cv. Cabernet Sauvignon wines from five wine-growing regions in China. Food Chem. 125, 77-83 (2011).

[38] Liang, Z. et al. Anthocyanin composition and content in grape berry skin in Vitis germplasm. Food Chem. 111, 837-844 (2008).

[39] Manns, D. C., Lenerz, C. T. M. C. & Mansfield, A. K. Impact of processing parameters on the phenolic profile of wines produced from hybrid red grapes Maréchal Foch, Corot noir, and Marquette. J. Food Sci. 78, 696-702 (2013).

[40] Sant’Ana, G. C. et al. Comparison of a retrotransposon-based marker with microsatellite markers for discriminating accessions of Vitis vinifera. Genet. Mol. Res. 11, 1507-1525 (2012).

[41] Danecek, P. et al. The variant call format and VCFtools. Bioinform 27, 2156-2158 (2011).

[42] Zheng, X. et al. A high-performance computing toolset for relatedness and principal component analysis of SNP data. Bioinformatics 28, 3326-3328 (2012).

[43] Wickham, H. ggplot2: Elegant Graphics for Data Analysis. (Springer-Verlag, New York, 2016).

[44] Kajitani, R. et al. Efficient de novo assembly of highly heterozygous genomes from whole-genome shotgun short reads. Genome Res. 24, 1384-1395 (2014).

[45] Ensembl Plants. Available at: http://plants.ensembl.org/index.html. (Accessed: 1st June 2019).

[46] Sook Jung et al. 15 years of GDR: new data and functionality in the Genome Database for Rosaceae. Nucleic Acids Res. 47, D1137-D1145 (2018).

[47] Index of /DATA. (2016). Available at: http://genomes.cribi.unipd.it/DATA/. (Accessed: 25th July 2019).

[48] Dubos et al. MYB transcription factors in Arabidopsis. Trends Plant Sci. 15, 573-581 (2010).

[49] Nakano, T., Suzuki, K., Fujimura, T. & Shinshi, H . Genome-wide analysis of the ERF gene family in Arabidopsis and Rice. Plant Physiol. 140, 411-432 (2006).