Genome sequencing and phylogenetic analysis of allotetraploid Salix matsudana Koidz

Abstract

Polyploidy is a common phenomenon among willow species. In this study, genome sequencing was conducted for Salix matsudana Koidz (also named Chinese willow), an important greening and arbor tree species, and the genome of this species was compared with those of four other tree species in Salicaceae. The total genome sequence of S. matsudana was 655.72 Mb in size, with repeated sequences accounting for 45.97% of the total length. In total, 531.43 Mb of the genome sequence could be mapped onto 38 chromosomes using the published genetic map as a reference. The genome of S. matsudana could be divided into two groups, the A and B genomes, through homology analysis with the genome of Populus trichocarpa, and the A and B genomes contained 23,985 and 25,107 genes, respectively. 4DTv combined transposon analysis predicted that allotetraploidy in S. matsudana appeared ~4 million years ago. The results from this study will help reveal the evolutionary history of S. matsudana and lay a genetic basis for its breeding.

References

[1] Gullberg, U. Towards making willows pilot species for coppicing production. For. Chron. 69, 721-726 (1993).

[2] Lindegaard, K. N. & Barker, J. Breeding willows for biomass. Asp. Appl Biol. 49, 155-162 (1997).

[3] Zhang, J. et al. The genetic architecture of growth traits in Salix matsudana under salt stress. Hortic. Res. 4, 17024 (2017).

[4] Polt, P., Sjödin, P., Weih, M., Rönnberg-Wästljung, A. C. & Berlin, S. Genome-wide transcriptional and physiological responses to drought stress in leaves and roots of two willow genotypes. BMC Plant Biol. 15, 244 (2015).

[5] Hangs, R. D., Schoenau, J. J., Van Rees, K. & Steppuhn, H. Examining the salt tolerance of willow (Salix spp.) bioenergy species for use on salt-affected agricultural lands. Can. J. Plant Sci. 91, 509-517 (2011).

[6] Yanitch, A. et al. Transcriptomic response of purple willow (Salix purpurea) to arsenic stress. Front. Plant Sci. 8, 1115 (2017).

[7] Aronsson, P., Dahlin, T. & Dimitriou, I. Treatment of landfill leachate by irrigation of willow coppice-plant response and treatment efficiency. Environ. Pollut. 158, 795-804 (2010).

[8] Suda, Y. & Argus, G. W. Chromosome numbers of some North American Salix. Brittonia 20, 191-197 (1968).

[9] Macalpine, W. J., Shield, I. F., Trybush, S. O., Hayes, C. M. & Karp, A. Overcoming barriers to crossing in willow (Salix spp.) breeding. Asp. Appl. Biol. 90, 173-180 (2008).

[10] Argus, G. W. Infrageneric classification of Salix (Salicaceae) in the new world. Syst. Bot. Monogr. 52, 1-121 (1997).

[11] Barcaccia, G., Meneghetti, S., Albertini, E., Triest, L. & Lucchin, M. Linkage mapping in tetraploid willows: segregation of molecular markers and estimation of linkage phases support an allotetraploid structure for Salix alba× Salix fragilis interspecific hybrids. Heredity 90, 169-180 (2003).

[12] Barcaccia, G., Meneghetti, S., Lucchin, M. & De Jong, H. Genetic segregation and genomic hybridization patterns support an allotetraploid structure and disomic inheritance for Salix species. Diversity 6, 633-651 (2014).

[13] Dai, X. et al. The willow genome and divergent evolution from poplar after the common genome duplication. Cell Res. 24, 1274-1277 (2014).

[14] Qiao, G. et al. Comparative proteomic analysis of responses to salt stress in Chinese willow (Salix matsudana Koidz). Plant Mol. Biol. Rep. 32, 814-827 (2014).

[15] Tuskan, G. A. et al. The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313, 1596-1604 (2006).

[16] Ma, T. et al. Genomic insights into salt adaptation in a desert poplar. Nat. Commun. 4, 1-9 (2013).

[17] Koren, S. et al. Canu: scalable and accurate long-read assembly via adaptive k-mer weighting and repeat separation. Genome Res. 27, 722-736 (2017).

[18] Chakraborty, M. et al. Contiguous and accurate de novo assembly of metazoan genomes with modest long read coverage. Nucleic Acids Res. 44, e147 (2016).

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

[20] Jennifer, S. & NicHerndon. Irys-Scaffolding: Irys-scaffolding Tools Version 1.0.0 https://doi.org/10.5281/zenodo.18591 (2015).

[21] Zhang, J. et al. A high-density genetic map of tetraploid Salix matsudana using specific length amplified fragment sequencing (SLAF-seq). PLoS ONE 11, e0157777 (2016).

[22] Hou, J. et al. Major chromosomal rearrangements distinguish willow and poplar after the ancestral “Salicoid” genome duplication. Genome Biol. Evol. 8, 1868-1875 (2016).

[23] Hou, J., Wei, S., Pan, H., Zhuge, Q. & Yin, T. Uneven selection pressure accelerating divergence of Populus and Salix. Hortic. Res. 6, 37 (2019).

[24] Qamar, M. T. et al. ppsPCP: a plant presence/absence variants scanner and pan-genome construction pipeline. Bioinformatics 35, 4156-4158 (2019).

[25] Thibault, J . Nuclear DNA amount in pure species and hybrid willows (Salix): a flow cytometric investigation. Can. J. Bot. 76, 157-165 (1998).

[26] Serapiglia, M. J., Gouker, F. E. & Smart, L. B. Early selection of novel triploid hybrids of shrub willow with improved biomass yield relative to diploids. BMC Plant Biol. 14, 74 (2014).

[27] Horjales, M. Cantidades de DNA nuclear en árboles y arbustos. Nova Acta Cient. Compostel. (Bioloxía) 13, 23-33 (2003).

[28] Zhang, M. L. A preliminary cladistic study on the multistaminal willows (Salix) in China. Bull. Bot. Res. 3, 299-305 (1994).

[29] Zhang, J. et al. Determination of chromosome ploidy and genome size of Salix matsudana based on flow cytometry. Jiangsu Agr. Sci. 46, 40-43 (2018).

[30] Ramsey, J. & Schemske, D. W. Pathways, mechanisms, and rates of polyploid formation in flowering plants. Annu. Rev. Ecol. Syst. 29, 467-501 (1998).

[31] Doyle, J. J. & Egan, A. N. Dating the origins of polyploidy events. N. Phytol. 186, 73-85 (2010).

[32] Haider, N. The origin of the B-genome of bread wheat (Triticum aestivum L.). Russ. J. Genet. 49, 263-274 (2013).

[33] Sattler, M. C., Carvalho, C. R. & Clarindo, W. R. The polyploidy and its key role in plant breeding. Planta 243, 281-296 (2016).

[34] Tu, Z. Y. Willow Breeding And Cultivation (Jiangsu Science & Technology Press, Nanjing, 1982).

[35] Branco, R. & Masle, J. Systemic signalling through translationally controlled tumour protein controls lateral root formation in Arabidopsis. J. Exp. Bot. 70, 3927-3940 (2019).

[36] Toscano-Morales, R., Xoconostle-Cázares, B., Martínez-Navarro, A. C. & Ruiz-Medrano, R. AtTCTP2 mRNA and protein movement correlates with formation of adventitious roots in tobacco. Plant Signal Behav. 11, e1071003 (2016).

[37] Li, H. et al. A WD40 domain cyclophilin interacts with histone H3 and functions in gene repression and organogenesis in Arabidopsis. Plant Cell. 19, 2403-2416 (2007).

[38] Yang, H. M. GENOMICS (China Science Press, 2016).

[39] Boucher, L. D., Manchester, S. R. & Judd, W. S. An extinct genus of Salicaceae based on twigs with attached flowers, fruits, and foliage from the Eocene Green River Formation of Utah and Colorado, USA. Am. J. Bot. 90, 1389-1399 (2003).

[40] Manchester, S. R., Judd, W. S. & Handley, B. Foliage and fruits of early poplars (Salicaceae: Populus) from the Eocene of Utah, Colorado, and Wyoming. Int. J. Plant Sci. 167, 897-908 (2006).

[41] Wu, J. et al. Phylogeny of Salix subgenus Salix sl (Salicaceae): delimitation, biogeography, and reticulate evolution. BMC Evol. Biol. 15, 31 (2015).

[42] Hohmann, N., Wolf, E. M., Lysak, M. A. & Koch, M. A. A time-calibrated road map of Brassicaceae species radiation and evolutionary history. Plant Cell. 27, 2770-2784 (2015).

[43] Xu, Z. & Wang, H. LTR_FINDER: an efficient tool for the prediction of full-length LTR retrotransposons. Nucleic Acids Res. 35, W265-W268 (2007).

[44] Han, Y. & Wessler, S. R. MITE-Hunter: a program for discovering miniature inverted-repeat transposable elements from genomic sequences. Nucleic Acids Res. 38, e199 (2010).

[45] Price, A. L., Jones, N. C. & Pevzner, P. A. De novo identification of repeat families in large genomes. Bioinformatics 21, i351-i358 (2005).

[46] Edgar, R. C. & Myers, E. W. PILER: identification and classification of genomic repeats. Bioinformatics 21, i152-i158 (2005).

[47] Wicker, T. et al. A unified classification system for eukaryotic transposable elements. Nat. Rev. Genet. 8, 973-982 (2007).

[48] Jurka, J. et al. Repbase update, a database of eukaryotic repetitive elements. Cytogenet. Genome Res. 110, 462-467 (2005).

[49] Tarailo Graovac, M. & Chen, N. Using RepeatMasker to identify repetitive elements in genomic sequences. Curr. Prot. Bioinformatics. 25, 4-10 (2009).

[50] Haas, B. J. et al. Automated eukaryotic gene structure annotation using EVidenceModeler and the Program to Assemble Spliced Alignments. Genome Biol. 9, R7 (2008).

[51] Burge, C. & Karlin, S. Prediction of complete gene structures in human genomic DNA. J. Mol. Biol. 268, 78-94 (1997).

[52] Stanke, M. & Waack, S. Gene prediction with a hidden Markov model and a new intron submodel. Bioinformatics 19, i215-i225 (2003).

[53] Majoros, W. H., Pertea, M. & Salzberg, S. L. TigrScan and GlimmerHMM: two open source ab initio eukaryotic gene-finders. Bioinformatics 20, 2878-2879 (2004).

[54] Blanco, E., Parra, G. & Guigó, R. Using geneid to identify genes. Curr. Prot. Bioinformatics. 18, 3-4 (2007).

[55] Korf, I. Gene finding in novel genomes. BMC Bioinformatics 5, 59 (2004).

[56] Keilwagen, J. et al. Using intron position conservation for homology-based gene prediction. Nucleic Acids Res. 44, e89 (2016).

[57] Campbell, M. A., Haas, B. J., Hamilton, J. P., Mount, S. M. & Buell, C. R. Comprehensive analysis of alternative splicing in rice and comparative analyses with Arabidopsis. BMC Genomics. 7, 327 (2006).

[58] Altschul, S. F., Gish, W., Miller, W., Myers, E. W. & Lipman, D. J. Basic local alignment search tool. J. Mol. Biol. 215, 403-410 (1990).

[59] Marchler-Bauer, A. et al. CDD: a Conserved Domain Database for the functional annotation of proteins. Nucleic Acids Res. 39, D225-D229 (2010).

[60] Tatusov, R. L. et al. The COG database: new developments in phylogenetic classification of proteins from complete genomes. Nucleic Acids Res. 29, 22-28 (2001).

[61] Kanehisa, M. & Goto, S. KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Res. 28, 27-30 (2000).

[62] Dimmer, E. C. et al. The UniProt-GO annotation database in 2011. Nucleic Acids Res. 40, D565-D570 (2012).

[63] Conesa, A. et al. Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21, 3674-3676 (2005).

[64] Li, L., Stoeckert, C. J. & Roos, D. S. OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res. 13, 2178-2189 (2003).

[65] Dan, S. P. SIGNAL SCAN: a computer program that scans DNA sequences for eukaryotic transcriptional elements. Comput. Appl. Bio. 7, 203 (1991).

[66] Edgar, R. C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792-1797 (2004).