Integrating genomic sequencing resources: an innovative perspective on recycling with universal Angiosperms353 probe sets

Abstract

Sequencing strategies have continually advanced, with high-throughput sequencing (HTS) technologies emerging as pivotal tools in plant phylogenomics. As a standard form of target capture sequencing, hybridization target enrichment sequencing (Hyb-seq) is innovative and flexible, and then HTS strategy is widely adopted in phylogenomics. The universal Angiosperms353 probe sets (Angiosperms353) are instrumental in Hyb-seq and have been witnessed increased application in recent years. This review integrates numerous publications and empirical datasets to comprehensively assess the potential applications of Angiosperms353. Through evaluations using 18-taxa and 343-taxa genomic datasets, this review explores potential factors influencing Angiosperms353 gene capture. The RNA-seq strategy yielded the highest number of Angiosperms353 genes, followed by whole-genome sequencing and genome skimming. Increased sequencing depth enhanced gene capture yields, and no evident bias was observed across all tested angiosperm groups. In the genomics era with extensive HTS data, this review provides comprehensive guidelines for the practical application of Angiosperms353, promoting resource recycling and maximizing genomic data sharing and utilization.

Keywords

High-throughput sequencing strategies / Phylogenomics / Angiosperms353 / HybPiper / Easy353 / Hyb-Seq

References

[1]	Acha S, Majure LC. A new approach using targeted sequence capture for phylogenomic studies across Cactaceae. Genes. 2022;13:350. https://doi.org/10.3390/genes13020350.
[2]	Andrews KR, Good JM, Miller MR, Luikart G, Hohenlohe PA. Harnessing the power of RADseq for ecological and evolutionary genomics. Nat Rev Genet. 2016;17:81–92. https://doi.org/10.1038/nrg.2015.28.
[3]	Antonelli A, Clarkson JJ, Kainulainen K, Maurin O, Brewer GE, Davis AP, et al. Settling a family feud: a high-level phylogenomic framework for the Gentianales based on 353 nuclear genes and partial plastomes. Am J Bot. 2021;108:1143–65. https://doi.org/10.1002/ajb2.1697.
[4]	APG IV. An updated of the angiosperm phylogeny group classifications for orders and families of flowering plants: APG IV. Bot J Linnean Soc. 2016;181:1–20. https://doi.org/10.1111/boj.12385.
[5]	Baker WJ, Dodsworth S, Forest F, Graham SW, Johnson MG, McDonnell A, et al. Exploring Angiosperms353: an open, community toolkit for collaborative phylogenomic research on flowering plants. Am J Bot. 2021;108:1059–65. https://doi.org/10.1002/ajb2.1703.
[6]	Baker WJ, Bailey P, Barber V, Barker A, Bellot S, Bishop D, et al. A comprehensive phylogenomic platform for exploring the angiosperm tree of life. Syst Biol. 2022;71:301–19. https://doi.org/10.1093/sysbio/syab035.
[7]	Bakker FT, Lei D, Yu J, Mohammadin S, Wei Z, van de Kerke S, et al. Herbarium genomics: plastome sequence assembly from a range of herbarium specimens using an iterative organelle genome assembly pipeline. Biol J Linnean Soc. 2016;117:33–43. https://doi.org/10.1111/bij.12642.
[8]	Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol. 2012;19:455–77. https://doi.org/10.1089/cmb.2012.0021.
[9]	Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30:2114–20. https://doi.org/10.1093/bioinformatics/btu170.
[10]	Bragg JG, Potter S, Bi K, Moritz C. Exon capture phylogenomics: efficacy across scales of divergence. Mol Ecol Resour. 2015;16:1059–68. https://doi.org/10.1111/1755-0998.12449.
[11]	Breinholt JW, Carey SB, Tiley GP, Davis EC, Endara L, McDaniel SF, et al. A target enrichment probe set for resolving the flagellate land plant tree of life. Appl Plant Sci. 2021;9:e11406. https://doi.org/10.1002/aps3.11406.
[12]	Brewer GE, Clarkson JJ, Maurin O, Zuntini AR, Barber V, Bellot S, et al. Factors affecting targeted sequencing of 353 nuclear genes from herbarium specimens spanning the diversity of angiosperms. Front Plant Sci. 2019;10:1102. https://doi.org/10.3389/fpls.2019.01102.
[13]	Cai L, Zhang H, Davis CC. PhyloHerb: a high-throughput phylogenomic pipeline for processing genome skimming data. Appl Plant Sci. 2022;10:e11475. https://doi.org/10.1002/aps3.11475.
[14]	Chamala S, García N, Godden GT, Krishnakumar V, Jordon-Thaden IE, De Smet R, et al. MarkerMiner 1.0: a new application for phylogenetic marker development using angiosperm transcriptomes. Appl Plant Sci. 2015;3:apps.1400115. https://doi.org/10.3732/apps.1400115.
[15]	Chau J, Rahfeldt WA, Olmstead RG. Comparison of taxon-specific versus general locus sets for targeted sequence capture in plant phylogenomics. Appl Plant Sci. 2018;6:e1032. https://doi.org/10.1002/aps3.1032.
[16]	Chen JT, Lidén M, Huang XH, Zhang L, Zhang XJ, Kuang TH, et al. An updated classification for the hyper-diverse genus Corydalis (Papaveraceae: Fumarioideae) based on phylogenomic and morphological evidence. J Integr Plant Biol. 2023;65:2138–56. https://doi.org/10.1111/jipb.13499.
[17]	Cheng CY, Krishnakumar V, Chan AP, Thibaud-Nissen F, Schobel S, Town CD. Araport11: a complete reannotation of the Arabidopsis thaliana reference genome. Plant J. 2017;89:789–804. https://doi.org/10.1111/tpj.13415.
[18]	Clarkson JJ, Zuntini AR, Maurin O, Downie SR, Plunkett GM, Nicolas AN, et al. A higher-level nuclear phylogenomic study of the carrot family (Apiaceae). Am J Bot. 2021;108:1252–69. https://doi.org/10.1002/ajb2.1701.
[19]	Coissac E, Hollingsworth PM, Lavergne S, Taberlet P. From barcodes to genomes: extending the concept of DNA barcoding. Mol Ecol. 2016;25:1423–8. https://doi.org/10.1111/mec.13549.
[20]	Compeau PEC, Pevzner PA, Tesler G. How to apply de Bruijn graphs to genome assembly. Nat Biotechnol. 2011;29:987–91. https://doi.org/10.1038/nbt.2023.
[21]	Cronn R, Knaus BJ, Liston A, Maughan PJ, Parks M, Syring JV, et al. Targeted enrichment strategies for next-generation plant biology. Am J Bot. 2012;99:291–311. https://doi.org/10.3732/ajb.1100356.
[22]	Crowl AA, Fritsch PW, Tiley GP, Lynch NP, Ranney TG, Ashrafi H, et al. A first complete phylogenomic hypothesis for diploid blueberries (Vaccinium section Cyanococcus). Am J Bot. 2022;109:1596–606. https://doi.org/10.1002/ajb2.16065.
[23]	Dodsworth S. Genome skimming for next-generation biodiversity analysis. Trends Plant Sci. 2015;20:525–7. https://doi.org/10.1016/j.tplants.2015.06.012.
[24]	Dodsworth S, Pokorny L, Johnson MG, Kim JT, Maurin O, Wickett NJ, et al. Hyb-seq for flowering plant systematics. Trends Plant Sci. 2019;24:887–91. https://doi.org/10.1016/j.tplants.2019.07.011.
[25]	Dornburg A, Su Z, Townsend JP, Mueller R. Optimal rates for phylogenetic inference and experimental design in the era of genome-scale data sets. Syst Biol. 2019;68:145–56. https://doi.org/10.1093/sysbio/syy047.
[26]	Edwards D. Methods in molecular biology. In: Edwards D, editor. Plant bioinformatics: methods and protocols. New York: Humana; 2022. p. 1374.
[27]	Chapter
[28]	Eserman LA, Thomas SK, Coffey EED, Leebens-Mack JH. Target sequence capture in orchids: developing a kit to sequence hundreds of single-copy loci. Appl Plant Sci. 2021;9:e11416. https://doi.org/10.1002/aps3.11416.
[29]	Faircloth BC. PHYLUCE is a software package for the analysis of conserved genomic loci. Bioinformatics. 2016;32:786–8. https://doi.org/10.1093/bioinformatics/btv646.
[30]	Folk RA, Mandel JR, Freudenstein JV. A protocol for targeted enrichment of intron-containing sequence markers for recent radiations: a phylogenomic example from Heuchera (Saxifragaceae). Appl Plant Sci. 2015;3:apps.1500039. https://doi.org/10.3732/apps.1500039.
[31]	Folk RA, Kates HR, LaFrance R, Soltis DE, Soltis PS, Guralnick RP. High-throughput methods for efficiently building massive phylogenies from natural history collections. Appl Plant Sci. 2021;9:e11410. https://doi.org/10.1002/aps3.11410.
[32]	Forrest LL, Hart ML, Hughes M, Wilson HP, Chung KF, Tseng YH, et al. The limits of Hyb-seq for herbarium specimens: impact of preservation techniques. Front Ecol Evol. 2019;7:439. https://doi.org/10.3389/fevo.2019.00439.
[33]	Frost L, Santamaría-Aguilar DA, Singletary D, Lagomarsino LP. Niche evolution of the neotropical tree genus Otoba in the context of global biogeography of the nutmeg family, Myristicaceae. bioRxiv. 2021;10. https://doi.org/10.1101/2020.10.02.324368.
[34]	Gagnon E, Hilgenhof R, Orejuela A, McDonnell A, Sablok G, Aubriot X, et al. Phylogenomic discordance suggests polytomies along the backbone of the large genus Solanum. Am J Bot. 2022;109:580–601. https://doi.org/10.1002/ajb2.1827.
[35]	Gitzendanner MA, Soltis PS, Wong GKS, Ruhfel BR, Soltis DE. Plastid phylogenomic analysis of green plants: a billion years of evolutionary history. Am J Bot. 2018;105:291–301. https://doi.org/10.1002/ajb2.1048.
[36]	Gomez SM, Pokorny L, Kantar MB, Forest F, Leitch IJ, Gravendeel B, et al. A customized nuclear target enrichment approach for developing a phylogenomic baseline for Dioscorea yams (Dioscoreaceae). Appl Plant Sci. 2019;7:e11254. https://doi.org/10.1002/aps3.11254.
[37]	Guo C, Luo Y, Gao LM, Yi TS, Li HT, Yang JB, et al. Phylogenomics and the flowering plant tree of life. J Integr Plant Biol. 2022;65:299–323. https://doi.org/10.1111/jipb.13415.
[38]	Haigh AL, Gibernau M, Maurin O, Bailey P, Carlsen MM, Hay A, et al. Target sequence data shed new light on the infrafamilial classification of Araceae. Am J Bot. 2023;110:e16117. https://doi.org/10.1002/ajb2.16117.
[39]	Heckenhauer J, Samuel R, Ashton PS, Abu Salim K, Paun O. Phylogenomics resolves evolutionary relationships and provides insights into floral evolution in the tribe Shoreeae (Dipterocarpaceae). Mol Phylogenet Evol. 2018;127:1–13. https://doi.org/10.1016/j.ympev.2018.05.010.
[40]	Hendriks KP, Mandáková T, Hay NM, Ly E, Hooft van Huysduynen A, Tamrakar R, et al. The best of both worlds: combining lineage-specific and universal bait sets in target-enrichment hybridization reactions. Appl Plant Sci. 2021;9:aps3.11438. https://doi.org/10.1002/aps3.11438.
[41]	Hendriks KP, Kiefer C, Al-Shehbaz IA, Bailey CD, Hooft van Huysduynen A, Nikolov LA, et al. Global Brassicaceae phylogeny based on filtering of 1,000-gene dataset. Curr Biol. 2023;33:4052-4068.e6. https://doi.org/10.1016/j.cub.2023.08.026.
[42]	Hollingsworth PM, Li DZ, van der Bank M, Twyford AD. Telling plant species apart with DNA: from barcodes to genomes. Philos Trans R Soc Lond B Biol Sci. 2016;371:20150338. https://doi.org/10.1098/rstb.2015.0338.
[43]	Howard CC, Crowl AA, Harvey TS, Cellinese N. Peeling back the layers: first phylogenomic insights into the Ledebouriinae (Scilloideae, Asparagaceae). Mol Phylogenet Evol. 2022;169:107430. https://doi.org/10.1016/j.ympev.2022.107430.
[44]	Huang Y, He J, Xu Y, Zheng W, Wang S, Chen P, et al. Pangenome analysis provides insight into the evolution of the orange subfamily and a key gene for citric acid accumulation in citrus fruits. Nat Genet. 2023;55(11):1964–75. https://doi.org/10.1038/s41588-023-01516-6.
[45]	Johnson MG, Gardner EM, Liu Y, Medina R, Goffinet B, Shaw AJ, et al. HybPiper: extracting coding sequence and introns for phylogenetics from high-throughput sequencing reads using target enrichment. Appl Plant Sci. 2016;4:1600016. https://doi.org/10.3732/apps.1600016.
[46]	Johnson MG, Pokorny L, Dodsworth S, Botigue LR, Cowan RS, Devault A, et al. A universal probe set for targeted sequencing of 353 nuclear genes from any flowering plant designed using k-medoids clustering. Syst Biol. 2019;68:594–606. https://doi.org/10.1101/361618.
[47]	Jones MR, Good JM. Targeted capture in evolutionary and ecological genomics. Mol Ecol. 2015;25:185–202. https://doi.org/10.1111/mec.13304.
[48]	Joyce EM, Appelhans MS, Buerki S, Cheek M, de Vos JM, Pirani JR, et al. Phylogenomic analyses of Sapindales support new family relationships, rapid mid-Cretaceous hothouse diversification, and heterogeneous histories of gene duplication. Front Plant Sci. 2023;14:1063174. https://doi.org/10.3389/fpls.2023.1063174.
[49]	Kumar R, Ichihashi Y, Kimura S, Chitwood DH, Headland LR, Peng J, et al. A high-throughput method for Illumina RNA-seq library preparation. Front Plant Sci. 2012;202:3. https://doi.org/10.3389/fpls.2012.00202.
[50]	Lamesch P, Berardini TZ, Li D, Swarbreck D, Wilks C, Sasidharan R, et al. The Arabidopsis Information Resource (TAIR): improved gene annotation and new tools. Nucleic Acids Res. 2012;40:D1202–10. https://doi.org/10.1093/nar/gkr1090.
[51]	Larridon I, Villaverde T, Zuntini AR, Pokorny L, Brewer GE, Epitawalage N, et al. Tackling rapid radiations with targeted sequencing. Front Plant Sci. 2020;10:1655. https://doi.org/10.3389/fpls.2019.01655.
[52]	Larridon I, Zuntini AR, Léveillé-Bourret é, Barrett RL, Starr JR, Muasya AM, et al. A new classification of Cyperaceae (Poales) supported by phylogenomic data. J Syst Evol. 2021;59:852–95. https://doi.org/10.1111/jse.12757.
[53]	Larson DA, Chanderbali AS, Maurin O, Gon?alves DJP, Dick CW, Soltis DE, et al. The phylogeny and global biogeography of Primulaceae based on high-throughput DNA sequence data. Mol Phylogenet Evol. 2023;182:107702. https://doi.org/10.1016/j.ympev.2023.107702.
[54]	Leebens-Mack JH, Barker MS, Carpenter EJ, Deyholos MK, Gitzendanner MA, Graham SW, et al. One thousand plant transcriptomes and the phylogenomics of green plants. Nature. 2019;574:679–85. https://doi.org/10.1038/s41586-019-1693-2.
[55]	Lewin HA, Robinson GE, Kress WJ, Baker WJ, Coddington J, Crandall KA, et al. Earth BioGenome Project: sequencing life for the future of life. Proc Natl Acad Sci USA. 2018;115:4325–33. https://doi.org/10.1073/pnas.1720115115.
[56]	Li H, Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics. 2009;25:1754–60. https://doi.org/10.1093/bioinformatics/btp324.
[57]	Li HT, Yi TS, Gao LM, Ma PF, Zhang T, Yang JB, et al. Origin of angiosperms and the puzzle of the Jurassic gap. Nat Plants. 2019;5:461–70. https://doi.org/10.1038/s41477-019-0421-0.
[58]	Liao M, Shepherd LD, Zhang JY, Feng Y, Mattapha S, Zhang LB, et al. Phylogeny, biogeography, and character evolution of the genus Sophora s.l. (Fabaceae, Papilionoideae). Mol Phylogenet Evol. 2023;181:107713. https://doi.org/10.1016/j.ympev.2023.107713.
[59]	Liu L, Wu S, Yu L. Coalescent methods for estimating species trees from phylogenomic data. J Syst Evol. 2015;53:380–90. https://doi.org/10.1111/jse.12160.
[60]	Mamanova L, Coffey AJ, Scott CE, Kozarewa I, Turner EH, Kumar A, et al. Target-enrichment strategies for next-generation sequencing. Nat Methods. 2010;7:111–8. https://doi.org/10.1038/nmeth.1419.
[61]	Mandel JR. What’s all the hype about HybSeq? A brief history and introduction to target enrichment in Compositae. Capitulum. 2021;1:44–7. https://doi.org/10.53875/capitulum.01.1.04.
[62]	Masters LE, Tomaszewska P, Schwarzacher T, Zuntini AR, Heslop-Harrison P, Vorontsova MS. Phylogenomic analysis reveals the evolutionary origins of five independent clades of forage grasses within the African genus Urochloa. bioRxiv. 2023. https://doi.org/10.1101/2023.07.03.547487.
[63]	Maurin O, Anest A, Bellot S, Biffin E, Brewer G, Charles-Dominique T, et al. A nuclear phylogenomic study of the angiosperm order Myrtales, exploring the potential and limitations of the universal Angiosperms353 probe set. Am J Bot. 2021;108:1087–111. https://doi.org/10.1002/ajb2.1699.
[64]	McDonnell AJ, Baker WJ, Dodsworth S, Forest F, Graham SW, Johnson MG, et al. Exploring Angiosperms353: developing and applying a universal toolkit for flowering plant phylogenomics. Appl Plant Sci. 2021;9:aps3.11443. https://doi.org/10.1002/aps3.11443.
[65]	McKain MR, Johnson MG, Uribe-Convers S, Eaton D, Yang Y. Practical considerations for plant phylogenomics. Appl Plant Sci. 2018;6:e1038. https://doi.org/10.1002/aps3.1038.
[66]	McVay J, Carstens B. Phylogenetic model choice: justifying a species tree or concatenation analysis. J Phylogen Evolution Biol. 2013;1:1000114. https://doi.org/10.4172/jpgeb.1000114.
[67]	Mendiburu Fd. Agricolae: statistical procedures for agricultural research. 2023. https://CRAN.R-project.org/package=agricolae.
[68]	Nauheimer L, Weigner N, Joyce E, Crayn D, Clarke C, Nargar K. HybPhaser: a workflow for the detection and phasing of hybrids in target capture data sets. Appl Plant Sci. 2021;9:aps3.11441. https://doi.org/10.1002/aps3.11441.
[69]	Ng P, Kirkness E. Whole genome sequencing. In: Barnes M, Breen G, editors. Genetic variation: methods and protocols. Totowa: Humana Press; 2010. p. 215–26.
[70]	Ogutcen E, Christe C, Nishii K, Salamin N, M?ller M, Perret M. Phylogenomics of Gesneriaceae using targeted capture of nuclear genes. Mol Phylogenet Evol. 2021;157:107068. https://doi.org/10.1016/j.ympev.2021.107068.
[71]	Phang A, Pezzini FF, Burslem DFRP, Khew GS, Middleton DJ, Ruhsam M, et al. Target capture sequencing for phylogenomic and population studies in the southeast Asian genus Palaquium (Sapotaceae). Bot J Linnean Soc. 2023;203:134–47. https://doi.org/10.1093/botlinnean/boad022.
[72]	Pillon Y, Hopkins HCF, Maurin O, Epitawalage N, Bradford J, Rogers ZS, et al. Phylogenomics and biogeography of Cunoniaceae (Oxalidales) with complete generic sampling and taxonomic realignments. Am J Bot. 2021;108:1181–200. https://doi.org/10.1002/ajb2.1688.
[73]	R Core Team. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. 2023. https://www.R-project.org.
[74]	Robillard T, Strijk JS, Binh HT, Ngoc NV, Pereira JT, Slik JWF, et al. Museomics for reconstructing historical floristic exchanges: divergence of stone oaks across Wallacea. PLoS One. 2020;15:e0232936. https://doi.org/10.1371/journal.pone.0232936.
[75]	Romeiro-Brito M, Telhe MC, Amaral DT, Franco FF, Moraes EM. A target capture probe set useful for deep- and shallow-level phylogenetic studies in Cactaceae. Genes. 2022;13:707. https://doi.org/10.3390/genes13040707.
[76]	Schbath S, Martin V, Zytnicki M, Fayolle J, Loux V, Gibrat JF. Mapping reads on a genomic sequence: an algorithmic overview and a practical comparative analysis. J Comput Biol. 2012;19:796–813. https://doi.org/10.1089/cmb.2012.0022.
[77]	Shafer ABA, Peart CR, Tusso S, Maayan I, Brelsford A, Wheat CW, et al. Bioinformatic processing of RAD-seq data dramatically impacts downstream population genetic inference. Methods Ecol Evol. 2016;8:907–17. https://doi.org/10.1111/2041-210x.12700.
[78]	Shi S, Li J, Sun J, Yu J, Zhou S. Phylogeny and Classification of Prunus sensu lato (Rosaceae). J Integr Plant Biol. 2013;55:1069–79. https://doi.org/10.1111/jipb.12095.
[79]	Sim?es ARG, Eserman LA, Zuntini AR, Chatrou LW, Utteridge TMA, Maurin O, et al. A bird’s eye view of the systematics of Convolvulaceae: novel insights from nuclear genomic data. Front Plant Sci. 2022;13:889988. https://doi.org/10.3389/fpls.2022.889988.
[80]	Siniscalchi CM, Hidalgo O, Palazzesi L, Pellicer J, Pokorny L, Maurin O, et al. Lineage-specific vs. universal: a comparison of the Compositae1061 and Angiosperms353 enrichment panels in the sunflower family. Appl Plant Sci. 2021;9:aps3.11422. https://doi.org/10.1002/aps3.11422.
[81]	Slimp M, Williams LD, Hale H, Johnson MG. On the potential of Angiosperms353 for population genomic studies. Appl Plant Sci. 2021;9:aps3.11419. https://doi.org/10.1002/aps3.11419.
[82]	Sun QH, Morales-Briones DF, Wang HX, Landis JB, Wen J, Wang HF. Phylogenomic analyses of the East Asian endemic Abelia (Caprifoliaceae) shed insights into the temporal and spatial diversification history with widespread hybridization. Ann Bot. 2022;129:201–16. https://doi.org/10.1093/aob/mcab139.
[83]	Sundararaman B, Sylvester MD, Kozyreva VK, Berrada ZL, Corbett-Detig RB, Green RE. A hybridization target enrichment approach for pathogen genomics. Mbio. 2023:e01889–01823. https://doi.org/10.1128/mbio.01889-23.
[84]	Supple MA, Shapiro B. Conservation of biodiversity in the genomics era. Genome Biol. 2018;19:131. https://doi.org/10.1186/s13059-018-1520-3.
[85]	Thomas SK, Liu X, Du ZY, Dong Y, Cummings A, Pokorny L, et al. Comprehending Cornales: phylogenetic reconstruction of the order using the Angiosperms353 probe set. Am J Bot. 2021;108:1112–21. https://doi.org/10.1002/ajb2.1696.
[86]	Thureborn O, Razafimandimbison SG, Wikstr?m N, Rydin C. Target capture data resolve recalcitrant relationships in the coffee family (Rubioideae, Rubiaceae). Front Plant Sci. 2022;13:967456. https://doi.org/10.3389/fpls.2022.967456.
[87]	Turner B, Paun O, Munzinger J, Chase MW, Samuel R. Sequencing of whole plastid genomes and nuclear ribosomal DNA of Diospyros species (Ebenaceae) endemic to New Caledonia: many species, little divergence. Ann Bot. 2016;117:1175–85. https://doi.org/10.1093/aob/mcw060.
[88]	Ufimov R, Zeisek V, Pí?ová S, Baker WJ, Fér T, van Loo M, et al. Relative performance of customized and universal probe sets in target enrichment: a case study in subtribe Malinae. Appl Plant Sci. 2021;9:e11442. https://doi.org/10.1002/aps3.11442.
[89]	Wang HX, Morales-Briones DF, Moore MJ, Wen J, Wang HF. A phylogenomic perspective on gene tree conflict and character evolution in Caprifoliaceae using target enrichment data, with Zabelioideae recognized as a new subfamily. J Syst Evol. 2021;59:897–914. https://doi.org/10.1111/jse.12745.
[90]	Weitemier K, Straub SCK, Cronn RC, Fishbein M, Schmickl R, McDonnell A, et al. Hyb-seq: combining target enrichment and genome skimming for plant phylogenomics. Appl Plant Sci. 2014;2:apps.1400042. https://doi.org/10.3732/apps.1400042.
[91]	Wickham H. Elegant graphics for data analysis. In: Wickham H, editor. ggplot2. New York: Springer Cham; 2016. p. 1–260.
[92]	Wickham H, Averick M, Bryan J, Chang W, McGowan L, Fran?ois R, et al. Welcome to the Tidyverse. J Open Source Softw. 2019;4:1686. https://doi.org/10.21105/joss.01686.
[93]	Wilkinson MJ, Szabo C, Ford CS, Yarom Y, Croxford AE, Camp A, et al. Replacing Sanger with next generation sequencing to improve coverage and quality of reference DNA barcodes for plants. Sci Rep. 2017;7:46040. https://doi.org/10.1038/srep46040.
[94]	Winter DJ. rentrez: an R package for the NCBI eUtils API. Peer J Preprints 5:e3179v2 [Preprint]. 2017:8. https://doi.org/10.7287/peerj.preprints.3179v2. Cited 2017 Aug 25.
[95]	Wolf PG, Robison TA, Johnson MG, Sundue MA, Testo WL, Rothfels CJ. Target sequence capture of nuclear-encoded genes for phylogenetic analysis in ferns. Appl Plant Sci. 2018;6:e01148. https://doi.org/10.1002/aps3.1148.
[96]	Xie P, Guo Y, Zhou W, Zhang Z, Yu Y. GeneMiner: a tool for extracting phylogenetic markers from next-generation sequencing data. 2023. https://doi.org/10.22541/au.168172406.69677221/v1.
[97]	Yardeni G, Viruel J, Paris M, Hess J, Groot Crego C, de La Harpe M, et al. Taxon-specific or universal? Using target capture to study the evolutionary history of rapid radiations. Mol Ecol Resour. 2021;22:927–45. https://doi.org/10.1111/1755-0998.13523.
[98]	Zhang C, Rabiee M, Sayyari E, Mirarab S. ASTRAL-III: polynomial time species tree reconstruction from partially resolved gene trees. BMC Bioinformatics. 2018;19:153. https://doi.org/10.1186/s12859-018-2129-y.
[99]	Zhang Z, Xie P, Guo Y, Zhou W, Liu E, Yu Y, et al. Easy353: a tool to get Angiosperms353 genes for phylogenomic research. Mol Biol Evol. 2022;39:msac261. https://doi.org/10.1093/molbev/msac261.
[100]	Zhao L, Jiang XW, Zuo YJ, Liu XL, Chin SW, Haberle R, Potter D, Chang ZY, Wen J. Multiple events of allopolyploidy in the evolution of the racemose lineages in Prunus (Rosaceae) based on integrated evidence from nuclear and plastid data. PLoS One. 2016;11(6):e0157123. https://doi.org/10.1371/journal.pone.0157123.
[101]	Zhao Y, Chen YP, Yuan JC, Paton AJ, Nuraliev MS, Zhao F et al. Museomics in Lamiaceae: resolving the taxonomic mystery of Pseudomarrubium. Curr Plant Biol. 2023;35–6. https://doi.org/10.1016/j.cpb.2023.100300.
[102]	Zhou W, Soghigian J, Xiang QY, Eaton D. A new pipeline for removing paralogs in target enrichment data. Syst Biol. 2022;71:410–25. https://doi.org/10.1093/sysbio/syab044.
[103]	Zuntini AR, Frankel LP, Pokorny L, Forest F, Baker WJ. A comprehensive phylogenomic study of the monocot order Commelinales, with a new classification of Commelinaceae. Am J Bot. 2021;108:1066–86. https://doi.org/10.1002/ajb2.1698.

Funding

National Natural Science Foundation of China(No. 32270222)