Plant phylogenomics based on genome-partitioning strategies: Progress and prospects

doi:10.1016/j.pld.2018.06.005

Abstract

Abstract:

The rapid expansion of next-generation sequencing (NGS) has generated a powerful array of approaches to address fundamental questions in biology. Several genome-partitioning strategies to sequence selected subsets of the genome have emerged in the fields of phylogenomics and evolutionary genomics. In this review, we summarize the applications, advantages and limitations of four NGS-based genomepartitioning approaches in plant phylogenomics:genome skimming, transcriptome sequencing (RNA-seq), restriction site associated DNA sequencing (RAD-Seq), and targeted capture (Hyb-seq). Of these four genome-partitioning approaches, targeted capture (especially Hyb-seq) shows the greatest promise for plant phylogenetics over the next few years. This review will aid researchers in their selection of appropriate genome-partitioning approaches to address questions of evolutionary scale, where we anticipate continued development and expansion of whole-genome sequencing strategies in the fields of plant phylogenomics and evolutionary biology research.

Key words: Plant phylogenomics, Next-generation sequencing, Whole-genome sequencing, Genome skimming, RAD-Seq, Targeted capture

Xiangqin Yu, Dan Yang, Cen Guo, Lianming Gao. Plant phylogenomics based on genome-partitioning strategies: Progress and prospects[J]. Plant Diversity, 2018, 40(04): 158-164.

References

Andrews, K.R., Good, J.M., Miller, M.R., et al., 2016. Harnessing the power of RADseq for ecological and evolutionary genomics. Nat. Rev. Genet. 17, 81.
Baird, N.A., Etter, P.D., Atwood, T.S., et al., 2008. Rapid SNP discovery and genetic mapping using sequenced RAD markers. PLoS One 3, e3376.
Bakker, F.T., Lei, D., Yu, J., et al., 2015. Herbarium genomics:plastome sequence assembly from a range of herbarium specimens using an Iterative Organelle Genome Assembly pipeline. Biol. J. Linn. Soc.
Barrett, C.F., Davis, J.I., Leebens-Mack, J., et al., 2013. Plastid genomes and deep relationships among the commelinid monocot angiosperms. Cladistics 29, 65-87.
Barrett, C.F., Baker, W.J., Comer, J.R., et al., 2016. Plastid genomes reveal support for deep phylogenetic relationships and extensive rate variation among palms and other commelinid monocots. New Phytol. 209, 855-870.
Baxter, S.W., Davey, J.W., Johnston, J.S., et al., 2011. Linkage mapping and comparative genomics using next-generation RAD sequencing of a non-model organism. PLoS One 6, e19315.
Bayley, H., 2015. Nanopore sequencing:from imagination to reality. Clin. Chem. 61, 25-31.
Bellot, S., Renner, S.S., 2015. The plastomes of two species in the endoparasite genus Pilostyles (Apodanthaceae) each retain just five or six possibly functional genes.Genome Biol. Evol. 8, 189-201.
Bi, K., Vanderpool, D., Singhal, S., et al., 2012. Transcriptome-based exon capture enables highly cost-effective comparative genomic data collection at moderate evolutionary scales. BMC Genom. 13.
Bi, K., Linderoth, T., Vanderpool, D., et al., 2013. Unlocking the vault:nextgeneration museum population genomics. Mol. Ecol. 22, 6018-6032.
Brandley, M.C., Bragg, J.G., Singhal, S., et al., 2015. Evaluating the performance of anchored hybrid enrichment at the tips of the tree of life:a phylogenetic analysis of Australian Eugongylus group scincid lizards. BMC Evol. Biol. 15.
Cariou, M., Duret, L., Charlat, S., 2013. Is RAD-seq suitable for phylogenetic inference? An in silico assessment and optimization. Ecol. Evol. 3, 846-852.
Cheng, S., Melkonian, M., Smith, S.A., et al., 2018. 10KP:a phylodiverse genome sequencing plan. GigaScience 7, 4880447.
Corriveau, J.L., Coleman, A.W., 1988. Rapid screening method to detect potential biparental inheritance of plastid DNA and results for over 200 Angiosperm species. Am. J. Bot. 75, 1443-1458.
Crawford, N.G., Parham, J.F., Sellas, A.B., et al., 2015. A phylogenomic analysis of turtles. Mol. Phylogenet. Evol. 83, 250-257.
Davis, C.C., Xi, Z., Mathews, S., 2014. Plastid phylogenomics and green plant phylogeny:almost full circle but not quite there. BMC Biol. 12, 11.
Deamer, D., Akeson, M., Branton, D., 2016. Three decades of nanopore sequencing.Nat. Biotechnol. 34, 518-524.
Delsuc, F., Brinkmann, H., Philippe, H., 2005. Phylogenomics and the reconstruction of the tree of life. Nature 6, 361-375.
Dodsworth, S., 2015. Genome skimming for next-generation biodiversity analysis.Trends Plant Sci. 20, 525-527.
Dodsworth, S., Chase, M.W., Sarkinen, T., et al., 2016. Using genomic repeats for phylogenomics:a case study in wild tomatoes (Solanum section Lycopersicon:solanaceae). Biol. J. Linn. Soc. 117, 96-105.
Duan, N., Bai,Y.,Sun, H., etal., 2017. Genomere-sequencing reveals the history ofapple and supports a two-stage model for fruit enlargement. Nat. Commun. 8, 249.
Duarte, J.M., Wall, P.K., Edger, P.P., et al., 2010. Identification of shared single copy nuclear genes in Arabidopsis, Populus, Vitis and Oryza and their phylogenetic utility across various taxonomic levels. BMC Evol. Biol. 10, 61.
Eaton, D.A., Ree, R.H., 2013. Inferring phylogeny and introgression using RADseq data:an example from flowering plants (Pedicularis:orobanchaceae). Syst. Biol. 62, 689-706.
Eaton, D.A., Spriggs, E.L., Park, B., et al., 2017. Misconceptions on missing data in RAD-seq phylogenetics with a deep-scale example from flowering plants. Syst.Biol. 66, 399-412.
Eid, J., Fehr, A., Gray, J., et al., 2009. Real-time DNA sequencing from single polymerase molecules. Science 323, 133-138.
Eisen, J.A., 1998. Phylogenomics:improving functional predictions for uncharacterized genes by evolutionary analysis. Genome Res. 8, 163-167.
Eisen, J.A., Fraser, C.M., 2003. Phylogenomics:intersection of evolution and genomics. Science 300, 1706-1707.
Elshire, R.J., Glaubitz, J.C., Sun, Q., et al., 2011. A robust, simple genotyping-bysequencing (GBS) approach for high diversity species. PLoS One 6, e19379.
Emerson, K.J., Merz, C.R., Catchen, J.M., et al., 2010. Resolving postglacial phylogeography using high-throughput sequencing. Proc. Natl. Acad. Sci. U.S.A. 107, 16196-16200.
Escudero, M., Eaton, D.A., Hahn, M., et al., 2014. Genotyping-by-sequencing as a tool to infer phylogeny and ancestral hybridization:a case study in Carex (Cyperaceae). Mol. Phylogenet. Evol. 79, 359-367.
Etter, P.D., Johnson, E., 2012. RAD paired-end sequencing for local de novo assembly and SNP discovery in non-model organisms. Data Production and Analysis in Population Genomics. Humana Press, Totowa, NJ, pp. 135-151.
Eytan, R.I., Evans, B.R., Dornburg, A., et al., 2015. Are 100 enough? Inferring acanthomorph teleost phylogeny using Anchored Hybrid Enrichment. BMC Evol.Biol. 15.
Faircloth, B.C., McCormack, J.E., Crawford, N.G., et al., 2012. Ultraconserved elements anchor thousands of genetic markers spanning multiple evolutionary timescales. Syst. Biol. 61, 717-726.
Fleischmann, R.D., Adams, M.D., White, O., et al., 1995. Whole-genome random sequencing and assembly of Haemophilus influenzae Rd. Science 269, 496-512.
Folk, R.A., Mandel, J.R., Freudenstein, J.V., 2017. Ancestral gene flow and parallel organellar genome capture result in extreme phylogenomic discord in a lineage of angiosperms. Syst. Biol. 66, 320-337.
Fragoso-Martínez, I., Salazar, G.A., Martinez-Gordillo, M., et al., 2017. A pilot study applying the plant anchored hybrid enrichment method to New World sages(Salvia subgenus Calosphace; Lamiaceae). Mol. Phylogenet. Evol. 117, 124-134.
Fu, C.N., Li, H.T., Milne, R., et al., 2017. Comparative analyses of plastid genomes from fourteen Cornales species:inferences for phylogenetic relationships and genome evolution. BMC Genom. 18, 956.
Gao, L., Su, Y.J., Wang, T., 2010. Plastid genome sequencing, comparative genomics, and phylogenomics:current status and prospects. J. Systemat. Evol. 48, 77-93.
Gitzendanner, M.A., Soltis, P.S., Wong, G.K.S., et al., 2018. Plastid phylogenomic analysis of green plants:a billion years of evolutionary history. Am. J. Bot. 105, 291-301.
Goffeau, A., Barrell, B.G., Bussey, H., et al., 1996. Life with 6000 genes. Science 274, 546-567.
Goremykin, V.V., Hirsch-Ernst, K.I., Wölfl, S., et al., 2003. Analysis of the Amborella trichopoda chloroplast genome sequence suggests that Amborella is not a basal angiosperm. Mol. Biol. Evol. 20, 1499-1505.
Goremykin, V.V., Hirsch-Ernst, K.I., Wölfl, S., et al., 2004. The chloroplast genome of Nymphaea alba:whole-genome analyses and the problem of identifying the most basal angiosperm. Mol. Biol. Evol. 21, 1445-1454.
Granados Mendoza, C., Naumann, J., Samain, M.S., et al., 2015. A genome-scale mining strategy for recovering novel rapidly-evolving nuclear single-copy genes for addressing shallow-scale phylogenetics in Hydrangea. BMC Evol. Biol. 15.
Guisinger, M.M., Kuehl, J.V., Boore, J.L., et al., 2010. Extreme reconfiguration of plastid genomes in the angiosperm family Geraniaceae:rearrangements, repeats, and codon usage. Mol. Biol. Evol. 28, 583-600.
Harrison, N., Kidner, C.A., 2011. Next-generation sequencing and systematics:what can a billion base pairs of DNA sequence data do for you? Taxon 60, 1552-1566.
Hart, M.L., Forrest, L.L., Nicholls, J.A., et al., 2016. Retrieval of hundreds of nuclear loci from herbarium specimens. Taxon 65, 1081-1092.
Hedtke, S.M., Morgan, M.J., Cannatella, D.C., et al., 2013. Targeted enrichment:maximizing orthologous gene comparisons across deep evolutionary time. PLoS One 8.
Henning, F., Lee, H.J., Franchini, P., et al., 2014. Genetic mapping of horizontal stripes in Lake Victoria cichlid fishes:benefits and pitfalls of using RAD markers for dense linkage mapping. Mol. Ecol. 23, 5224-5240.
Hipp, A.L., Eaton, D.A., Cavender-Bares, J., et al., 2014. A framework phylogeny of the American oak clade based on sequenced RAD data. PLoS One 9, e93975.
Hipp, A.L., Manos, P.S., Gonzalez-Rodríguez, A., et al., 2018. Sympatric parallel diversification of major oak clades in the Americas and the origins of Mexican species diversity. New Phytol. 217, 439-452.
Huang, H., Knowles, L.L., 2014. Unforeseen consequences of excluding missing data from next-generation sequences:simulation study of RAD sequences. Syst. Biol. 65, 357-365.
Huang, D.I., Hefer, C.A., Kolosova, N., et al., 2014. Whole plastome sequencing reveals deep plastid divergence and cytonuclear discordance between closely related balsam poplars, Populus balsamifera and P. trichocarpa (Salicaceae). New Phytol. 204, 693-703.
Huang, C.H., Sun, R., Hu, Y., et al., 2015. Resolution of Brassicaceae phylogeny using nuclear genes uncovers nested radiations and supports convergent morphological evolution. Mol. Biol. Evol. 33, 394-412.
Huang, C.H., Zhang, C.F., Liu, M., et al., 2016. Multiple polyploidization events across Asteraceae with two nested events in the early history revealed by nuclear phylogenomics. Mol. Biol. Evol. 33, 2820-2835.
Ilves, K.L., Lopez-Fernandez, H., 2014. A targeted next-generation sequencing toolkit for exon-based cichlid phylogenomics. Mol. Ecol. Resour. 14, 802-811.
International Human Genome Sequencing Consortium, 2004. Finishing the euchromatic sequence of the human genome. Nature 431, 931-945.
Jansen, R.K., Raubeson, L.A., Boore, J.L., et al., 2005. Methods for obtaining and analyzing whole chloroplast genome sequences. In:Zimmer, E.A., Roalson, E.H. (Eds.), Molecular Evolution:Producing the Biochemical Data, Part B, pp. 348-384.
Jansen, R.K., Cai, Z., Raubeson, L.A., et al., 2007. Analysis of 81 genes from 64 plastid genomes resolves relationships in angiosperms and identifies genome-scale evolutionary patterns. Proc. Natl. Acad. Sci. U.S.A. 104, 19369-19374.
Jarvis, E.D., Mirarab, S., Aberer, A.J., et al., 2014. Whole-genome analyses resolve early branches in the tree of life of modern birds. Science 346, 1320-1331.
Jones, M.R., Good, J.M., 2016. Targeted capture in evolutionary and ecological genomics. Mol. Ecol. 25, 185-202.
Leache, A.D., Banbury, B.L., Felsenstein, J., et al., 2015. Short tree, long tree, right tree, wrong tree:new acquisition bias corrections for inferring SNP phylogenies.Syst. Biol. 64, 1032-1047.
Lee, E.K., Cibrian-Jaramillo, A., Kolokotronis, S.O., et al., 2011. A functional phylogenomic view of the seed plants. PLoS Genet. 7.
Lemmon, E.M., Lemmon, A.R., 2013. High-throughput genomic data in systematics and phylogenetics. Annu. Rev. Ecol. Evol. Syst. 44, 99-121.
Liu, Y., Cox, C.J., Wang, W., et al., 2014. Mitochondrial phylogenomics of early land plants:mitigating the effects of saturation, compositional heterogeneity, and codon-usage bias. Syst. Biol. 63, 862-878.
Lonsdale, D.M., Brears, T., Hodge, T.P., et al., 1988. The plant mitochondrial genomehomologous recombination as a mechanism for generating heterogeneity.Philos. Trans. R. Soc. Lond. Ser. B Biol. Sci. 319, 149-163.
Ma, P.F., Zhang, Y.X., Zeng, C.X., et al., 2014. Chloroplast phylogenomic analyses resolve deep-level relationships of an intractable bamboo tribe Arundinarieae(poaceae). Syst. Biol. 63, 933-950.
Male, P.J.G., Bardon, L., Besnard, G., et al., 2014. Genome skimming by shotgun sequencing helps resolve the phylogeny of a pantropical tree family. Mol. Ecol.Resour. 14, 966-975.
Mandel, J.R., Dikow, R.B., Funk, V.A., et al., 2014. A target enrichment method for gathering phylogenetic information from hundreds of loci:an example from the Compositae. Appl. Plant Sci. 2.
Martin, W., Deusch, O., Stawski, N., et al., 2005. Chloroplast genome phylogenetics:why we need independent approaches to plant molecular evolution. Trends Plant Sci. 10, 203-209.
Massatti, R., Reznicek, A.A., Knowles, L.L., 2016. Utilizing RADseq data for phylogenetic analysis of challenging taxonomic groups:a case study in Carex sect.Racemosae. Am. J. Bot. 103, 337-347.
Matasci, N., Hung, L.H., Yan, Z.X., et al., 2014. Data access for the 1,000 Plants (1KP)project. GigaScience 3.
McCormack, J.E., Faircloth, B.C., Crawford, N.G., et al., 2012. Ultraconserved elements are novel phylogenomic markers that resolve placental mammal phylogeny when combined with species-tree analysis. Genome Res. 22, 746-754.
McCormack, J.E., Harvey, M.G., Faircloth, B.C., et al., 2013a. A phylogeny of birds based on over 1,500 loci collected by target enrichment and high-throughput sequencing. PLoS One 8.
McCormack, J.E., Hird, S.M., Zellmer, A.J., et al., 2013b. Applications of nextgeneration sequencing to phylogeography and phylogenetics. Mol. Phylogenet. Evol. 66, 526-538.
Mirarab, S., Bayzid, M.S., Boussau, B., et al., 2014. Statistical binning enables an accurate coalescent-based estimation of the avian tree. Science 346, 1250463.
Misof, B., Liu, S., Meusemann, K., et al., 2014. Phylogenomics resolves the timing and pattern of insect evolution. Science 346, 763-767.
Moore, M.J., Bell, C.D., Soltis, P.S., et al., 2007. Using plastid genome-scale data to resolve enigmatic relationships among basal angiosperms. Proc. Natl. Acad. Sci.U.S.A. 104, 19363-19368.
Moore, M.J., Soltis, P.S., Bell, C.D., et al., 2010. Phylogenetic analysis of 83 plastid genes further resolves the early diversification of eudicots. Proc. Natl. Acad. Sci.U.S.A. 107, 4623-4628.
Nater, A., Burri, R., Kawakami, T., et al., 2015. Resolving evolutionary relationships in closely related species with whole-genome sequencing data. Syst. Biol. 64, 1000-1017.
Nicholls, J.A., Pennington, R.T., Koenen, E.J.M., et al., 2015. Using targeted enrichment of nuclear genes to increase phylogenetic resolution in the neotropical rain forest genus Inga (Leguminosae:mimosoideae). Front. Plant Sci. 6.
Nock, C.J., Waters, D.L.E., Edwards, M.A., et al., 2011. Chloroplast genome sequences from total DNA for plant identification. J. Plant Biotechnol. 9, 328-333.
Ohyama, K., Fukuzawa, H., Kohchi, T., et al., 1986. Chloroplast gene organization deduced from complete sequence of liverwort Marchantia polymorpha chloroplast DNA. Nature 322, 572-574.
Olson, M., 2007. Enrichment of super-sized resequencing targets from the human genome. Nat. Methods 4, 891-892.
Palmer, J.D., Herbon, L.A., 1988. Plant mitochondrial-DNA evolves rapidly in structure, but slowly in sequence. J. Mol. Evol. 28, 87-97.
Peterson, B.K., Weber, J.N., Kay, E.H., et al., 2012. Double digest RADseq:an inexpensive method for de novo SNP discovery and genotyping in model and nonmodel species. PLoS One 7, e37135.
Pfender, W.F., Saha, M.C., Johnson, E.A., et al., 2011. Mapping with RAD (restrictionsite associated DNA) markers to rapidly identify QTL for stem rust resistance in Lolium perenne. Theor. Appl. Genet. 122, 1467-1480.
Philippe, H., Delsuc, F., Brinkmann, H., et al., 2005. Phylogenomics. Annu. Rev. Ecol.Evol. Systemat. 36, 541-562.
Philippe, H., Brinkmann, H., Lavrov, D.V., et al., 2011. Resolving difficult phylogenetic questions:why more sequences are not enough. PLoS Biol. 9.
Raubeson, L.A., Jansen, R.K., 2005. Chloroplast genomes of plants. In:Henry, R.J.(Ed.), Plant Diversity and Evolution:Genotypic and Phenotypic Variation in Higher Plants. CABI Publishing, Wallingford, pp. 45-68.
Ren, G., Mateo, R.G., Liu, J., et al., 2017. Genetic consequences of Quaternary climatic oscillations in the Himalayas:Primula tibetica as a case study based on restriction site-associated DNA sequencing. New Phytol. 213, 1500-1512.
Rokas, A., Holland, P.W., 2000. Rare genomic changes as a tool for phylogenetics.Trends Ecol. Evol. 15, 454-459.
Ross, T.G., Barrett, C.F., Soto Gomez, M., et al., 2015. Plastid phylogenomics and molecular evolution of Alismatales. Cladistics 32, 160-178.
Rubin, B.E.R., Ree, R.H., Moreau, C.S., 2012. Inferring phylogenies from RAD sequence data. PLoS One 7, e33394.
Sanger, F., Nicklen, S., Coulson, A.R., 1977. DNA sequencing with chain-terminating inhibitors. Proc. Natl. Acad. Sci. U.S.A. 74, 5463-5467.
Schmickl, R., Liston, A., Zeisek, V., et al., 2016. Phylogenetic marker development for target enrichment from transcriptome and genome skim data:the pipeline and its application in southern African Oxalis (Oxalidaceae). Mol. Ecol. Resour. 16, 1124-1135.
Schott, R.K., Panesar, B., Card, D.C., et al., 2017. Targeted capture of complete coding regions across divergent species. Genome Biol. Evol. 9, 398-414.
Senapathy, P., Bhasi, A., Mattox, J., et al., 2010. Targeted genome-wide enrichment of functional regions. PLoS One 5, e11138.
Shendure, J., Balasubramanian, S., Church, G.M., et al., 2017. DNA sequencing at 40:past, present and future. Nature 550, 345-353.
Shinozaki, K., Ohme, M., Tanaka, M., et al., 1986. The complete nucleotide sequence of the tobacco chloroplast genome:its gene organization and expression. EMBO J. 5, 2043-2049.
Sims, G.E., Jun, S.R., Wu, G.A., et al., 2009. Whole-genome phylogeny of mammals:evolutionary information in genic and nongenic regions. Proc. Natl. Acad. Sci.U.S.A. 106, 17077-17082.
Sollars, E.S., Harper, A.L., Kelly, L.J., et al., 2016. Genome sequence and genetic diversity of European ash trees. Nature 541, 212-216.
Soltis, D.E., Gitzendanner, M.A., Stull, G., et al., 2013. The potential of genomics in plant systematics. Taxon 62, 886-898.
Stamatakis, A., Aberer, A.J., Goll, C., et al., 2012. RAxML-Light:a tool for computing terabyte phylogenies. Bioinformatics 28, 2064-2066.
Stegemann, S., Keuthe, M., Greiner, S., et al., 2012. Horizontal transfer of chloroplast genomes between plant species. Proc. Natl. Acad. Sci. U.S.A. 109, 2434-2438.
Straub, S.C., Parks, M., Weitemier, K., et al., 2012. Navigating the tip of the genomic iceberg:next-generation sequencing for plant systematics. Am. J. Bot. 99, 349-364.
Sullivan, A.R., Schiffthaler, B., Thompson, S.L., et al., 2017. Interspecific plastome recombination reflects ancient reticulate evolution in Picea (pinaceae). Mol.Biol. Evol. 34, 1689-1701.
Teh, B.T., Lim, K., Yong, C.H., et al., 2017. The draft genome of tropical fruit durian(Durio zibethinus). Nat. Genet. 49, 1633-1641.
The C. elegans Sequencing Consortium, 1998. Genome sequence of the nematode C. elegans:a platform for investigating biology. Science 282, 2012-2018.
Tsitrone, A., Kirkpatrick, M., Levin, D.A., 2003. A model for chloroplast capture.Evolution 57, 1776-1782.
Valderrama, E., Richardson, J.E., Kidner, C.A., et al., 2018. Transcriptome mining for phylogenetic markers in a recently radiated genus of tropical plants (Renealmia L.f., Zingiberaceae). Mol. Phylogenet. Evol. 119, 13-24.
Vargas, O.M., Ortiz, E.M., Simpson, B.B., 2017. Conflicting phylogenomic signals reveal a pattern of reticulate evolution in a recent high-Andean diversification(Asteraceae:astereae:Diplostephium). New Phytol. 214, 1736-1750.
Wagner, C.E., Keller, I., Wittwer, S., et al., 2013. Genome-wide RAD sequence data provide unprecedented resolution of species boundaries and relationships in the Lake Victoria cichlid adaptive radiation. Mol. Ecol. 22, 787-798.
Wang, X., Ye, X., Zhao, L., et al., 2017. Genome-wide RAD sequencing data provide unprecedented resolution of the phylogeny of temperate bamboos (Poaceae:bambusoideae). Sci. Rep. 7, 11546.
Weitemier, K., Straub, S.C., Cronn, R.C., et al., 2014. Hyb-Seq:combining target enrichment and genome skimming for plant phylogenomics. Appl. Plant Sci. 2, 1400042.
Wickett, N.J., Mirarab, S., Nguyen, N., et al., 2014. Phylotranscriptomic analysis of the origin and early diversification of land plants. Proc. Natl. Acad. Sci. U. S. A. 111, E4859-E4868.
Wysocki, W.P., Clark, L.G., Attigala, L., et al., 2015. Evolution of the bamboos(Bambusoideae; Poaceae):a full plastome phylogenomic analysis. BMC Evol.Biol. 15.
Xiang, Y.Z., Huang, C.H., Hu, Y., et al., 2016. Evolution of Rosaceae fruit types based on nuclear phylogeny in the context of geological times and genome duplication. Mol. Biol. Evol. 34, 262-281.
Yang, J.B., Li, D.Z., Li, H.T., 2014. Highly effective sequencing whole chloroplast genomes of Angiosperms by nine novel universal primer pairs. Mol. Ecol. Resour. 14, 1024-1031.
Yang, Y., Moore, M.J., Brockington, S.F., et al., 2015. Dissecting molecular evolution in the highly diverse plant clade Caryophyllales using transcriptome sequencing.Mol. Biol. Evol. msv081.
Yang, G.Q., Chen, Y.M., Wang, J.P., et al., 2016. Development of a universal and simplified ddRAD library preparation approach for SNP discovery and genotyping in angiosperm plants. Plant Meth. 12, 39.
Yi, T.S., Jin, G.H., Wen, J., 2015. Chloroplast capture and intra-and inter-continental biogeographic diversification in the Asian-new World disjunct plant genus Osmorhiza (Apiaceae). Mol. Phylogenet. Evol. 85, 10-21.
Yu, X.Q., Gao, L.M., Soltis, D.E., et al., 2017. Insights into the historical assembly of East Asian subtropical evergreen broadleaved forests revealed by the temporal history of the tea family. New Phytol. 215, 1235-1248.
Zeng, L.P., Zhang, Q., Sun, R.R., et al., 2014. Resolution of deep Angiosperm phylogeny using conserved nuclear genes and estimates of early divergence times.Nat. Commun. 5, 4956.
Zeng, L., Ming, C., Li, Y., et al., 2017a. Out of southern East Asia of the brown rat revealed by large scale genome sequencing. Mol. Biol. Evol. 35, 149-158.
Zeng, L.P., Zhang, N., Zhang, Q., et al., 2017b. Resolution of deep eudicot phylogeny and their temporal diversification using nuclear genes from transcriptomic and genomic datasets. New Phytol. 214, 1338-1354.
Zhang, N., Zeng, L.P., Shan, H.Y., et al., 2012. Highly conserved low-copy nuclear genes as effective markers for phylogenetic analyses in angiosperms. New Phytol. 195, 923-937.
Zhang, T., Zeng, C.X., Yang, J.B., et al., 2016. Fifteen novel universal primer pairs for sequencing whole chloroplast genomes and a primer pair for nuclear ribosomal DNAs. J. Systemat. Evol. 54, 219-227.
Zhang, G.Q., Liu, K.W., Li, Z., et al., 2017a. The Apostasia genome and the evolution of orchids. Nature 549, 379-383.
Zhang, S.D., Jin, J.J., Chen, S.Y., et al., 2017b. Diversification of Rosaceae since the late cretaceous based on plastid phylogenomics. New Phytol. 214, 1355-1367.
Zimmer, E.A., 2013. Reprint of:using nuclear gene data for plant phylogenetics:progress and prospects. Mol. Phylogenet. Evol. 66, 539-550.

[1]	Yu-Juan Zhao, Gen-Shen Yin, Xun Gong. RAD-sequencing improves the genetic characterization of a threatened tree peony (Paeonia ludlowii) endemic to China: Implications for conservation [J]. Plant Diversity, 2023, 45(05): 513-522.
[2]	Na Su, Richard G.J. Hodel, Xi Wang, Jun-Ru Wang, Si-Yu Xie, Chao-Xia Gui, Ling Zhang, Zhao-Yang Chang, Liang Zhao, Daniel Potter, Jun Wen. Molecular phylogeny and inflorescence evolution of Prunus (Rosaceae) based on RAD-seq and genome skimming analyses [J]. Plant Diversity, 2023, 45(04): 397-408.
[3]	Gang Yao, Bine Xue, Kun Liu, Yuling Li, Jiuxiang Huang, Junwen Zhai. Phylogenetic estimation and morphological evolution of Alsineae (Caryophyllaceae) shed new insight into the taxonomic status of the genus Pseudocerastium [J]. Plant Diversity, 2021, 43(04): 299-307.
[4]	Yu-Hang Chang, Gang Yao, Jens Neilsen, De-Tuan Liu, Lu Zhang, Yong-Peng Ma. Rhododendron kuomeianum (Ericaceae), a new species from northeastern Yunnan (China), based on morphological and genomic data [J]. Plant Diversity, 2021, 43(04): 292-298.
[5]	Yu-Long Yu, Hui-Chun Wang, Zhi-Xiang Yu, Johann Schinnerl, Rong Tang, Yu-Peng Geng, Gao Chen. Genetic diversity and structure of the endemic and endangered species Aristolochia delavayi growing along the Jinsha River [J]. Plant Diversity, 2021, 43(03): 225-233.
[6]	Luxian Liu, Yonghua Zhang, Pan Li. Development of genomic resources for the genus Celtis (Cannabaceae) based on genome skimming data [J]. Plant Diversity, 2021, 43(01): 43-53.
[7]	Cen Guo, Zhen-Hua Guo, De-Zhu Li. Phylogenomic analyses reveal intractable evolutionary history of a temperate bamboo genus (Poaceae: Bambusoideae) [J]. Plant Diversity, 2019, 41(04): 213-219.
[8]	Ying Guo, Guo-Qian Yang, Yun-Mei Chen, De-Zhu Li, Zhen-Hua Guo. A comparison of different methods for preserving plant molecular materials and the effect of degraded DNA on ddRAD sequencing [J]. Plant Diversity, 2018, 40(03): 106-116.
[9]	Hantao Qin, Guoqian Yang, Jim Provan, Jie Liu, Lianming Gao. Using MiddRAD-seq data to develop polymorphic microsatellite markers for an endangered yew species [J]. Plant Diversity, 2017, 39(05): 294-299.
[10]	ZHANG Yun-Jie, LI De-Zhu. Advances in Phylogenomics Based on Complete Chloroplast Genomes [J]. Plant Diversity, 2011, 33(4): 365-375.