Comparative analysis of 12 water lily plastid genomes reveals genomic divergence and evolutionary relationships in early flowering plants

Weicai Song, Wenbo Shi, Huan Wang, Zirui Zhang, Ruiqing Tao, Jin Liu, Shuo Wang, Michael S. Engel, Chao Shi

Marine Life Science & Technology ›› 2024, Vol. 6 ›› Issue (3) : 425-441. DOI: 10.1007/s42995-024-00242-0

Comparative analysis of 12 water lily plastid genomes reveals genomic divergence and evolutionary relationships in early flowering plants

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Abstract

The aquatic plant Nymphaea, a model genus of the early flowering plant lineage Nymphaeales and family Nymphaeaceae, has been extensively studied. However, the availability of chloroplast genome data for this genus is incomplete, and phylogenetic relationships within the order Nymphaeales remain controversial. In this study, 12 chloroplast genomes of Nymphaea were assembled and analyzed for the first time. These genomes were 158,290–160,042 bp in size and contained 113 non-repeat genes, including 79 protein-coding genes, 30 tRNA genes, and four rRNA genes. We also report on codon usage, RNA editing sites, microsatellite structures, and new repetitive sequences in this genus. Comparative genomics revealed that expansion and contraction of IR regions can lead to changes in the gene numbers. Additionally, it was observed that the highly variable regions of the chloroplast genome were mainly located in intergenic regions. Furthermore, the phylogenetic tree showed the order Nymphaeales was divided into three families, and the genus Nymphaea can be divided into five (or three) subgenera, with the subgenus Nymphaea being the oldest. The divergence times of nymphaealean taxa were analyzed, with origins of the order Nymphaeales and family Nymphaeaceae being about 194 and 131 million years, respectively. The results of the phylogenetic analysis and estimated divergence times will be useful for future evolutionary studies of basal angiosperm lineages.

Keywords

Aquatic plants / Nymphaea / Phylogenetic analysis / Plastid genomics / Structural variation

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Weicai Song, Wenbo Shi, Huan Wang, Zirui Zhang, Ruiqing Tao, Jin Liu, Shuo Wang, Michael S. Engel, Chao Shi. Comparative analysis of 12 water lily plastid genomes reveals genomic divergence and evolutionary relationships in early flowering plants. Marine Life Science & Technology, 2024, 6(3): 425‒441 https://doi.org/10.1007/s42995-024-00242-0

References

[]
Abdullah MF, Shahzadi I, Waseem S, Mirza B, Ahmed I, Waheed MT. Chloroplast genome of Hibiscus rosasinensis (Malvaceae): comparative analyses and identification of mutational hotspots. Genomics, 2020, 112: 581-591.
[]
Alfaro ME, Holder MT. The posterior and the prior in Bayesian phylogenetics. Annu Rev Ecol Evol Syst, 2006, 37:19-42.
[]
Amiryousefi A, Hyvönen J, Poczai P. IRscope: an online program to visualize the junction sites of chloroplast genomes. Bioinformatics, 2018, 34: 3030-3031.
[]
Andrews S (2014) FastQC—a quality control tool for high throughput sequence data. Babraham Bioinforma. http://www.bioinformatics.babraham.ac.uk/projects/fastqc/. Accessed 26 June 2013
[]
Asaf S, Khan AL, Khan AR, Waqas M, Kang SM, Khan MA, Lee SM, Lee IJ. Complete chloroplast genome of Nicotiana otophora and its comparison with related species. Front Plant Sci, 2016, 7:1-12.
[]
Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, Lesin VM, Nikolenko SI, Pham S, Prjibelski AD, Pyshkin AV, Sirotkin AV, Vyahhi N, Tesler G, Alekseyev MA, Pevzner PA. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol, 2012, 19: 455-477.
[]
Beier S, Thiel T, Münch T, Scholz U, Mascher M. MISA-web: a web server for microsatellite prediction. Bioinformatics, 2017, 33: 2583-2585.
[]
Bell CD, Soltis DE, Soltis PS. The age and diversification of the angiosperms re-revisited. Am J Bot, 2010, 97: 1296-1303.
[]
Bhandarkar MR, Khan A. Antihepatotoxic effect of Nymphaea stellata willd., against carbon tetrachloride-induced hepatic damage in albino rats. J Ethnopharmacol, 2004, 91: 61-64.
[]
Birky CW. Uniparental inheritance of mitochondrial and chloroplast genes: mechanisms and evolution. Proc Natl Acad Sci USA, 1995, 92: 11331-11338.
[]
Biswal DK, Debnath M, Kumar S, Tandon P. Phylogenetic reconstruction in the order Nymphaeales: ITS2 secondary structure analysis and in silico testing of maturase k (matK) as a potential marker for DNA bar coding. BMC Bioinform, 2012, 13:1-16.
[]
Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics, 2014, 30: 2114-2120.
[]
Borsch T, Hilu KW, Wiersema JH, Löhne C, Barthlott W, Wilde V. Phylogeny of Nymphaea (Nymphaeaceae): evidence from substitutions and microstructural changes in the chloroplast trnT-trnF region. Int J Plant Sci, 2007, 168:639-671.
[]
Bouckaert R, Heled J, Kühnert D, Vaughan T, Wu CH, Xie D, Suchard MA, Rambaut A, Drummond AJ. BEAST 2: a software platform for Bayesian evolutionary analysis. PLoS Comput Biol, 2014, 10: e1003537.
[]
Brudno M, Malde S, Poliakov A, Do CB, Couronne O, Dubchak I, Batzoglou S. Glocal alignment: finding rearrangements during alignment. Bioinformatics, 2003, 19: i54-i62.
[]
Brunkard JO, Runkel AM, Zambryski PC. Chloroplasts extend stromules independently and in response to internal redox signals. Proc Natl Acad Sci USA, 2015, 112: 10044-10049.
[]
Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, Madden TL. BLAST+: architecture and applications. BMC Bioinform, 2009, 10:1-9.
[]
Castresana J. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol, 2000, 17: 540-552.
[]
Chen H, Deng L, Jiang Y, Lu P, Yu J. RNA editing sites exist in protein-coding genes in the chloroplast genome of Cycas taitungensis. J Integr Plant Biol, 2011, 53: 961-970.
[]
Cheng Y, He X, Priyadarshani SVGN, Wang Y, Ye L, Shi C, Ye K, Zhou Q, Luo Z, Deng F, Cao L, Zheng P, Aslam M, Qin Y. Assembly and comparative analysis of the complete mitochondrial genome of Suaeda glauca. BMC Genom, 2021, 22:1-19.
[]
Chumley TW, Palmer JD, Mower JP, Fourcade HM, Calie PJ, Boore JL, Jansen RK. The complete chloroplast genome sequence of Pelargonium × hortorum: organization and evolution of the largest and most highly rearranged chloroplast genome of land plants. Mol Biol Evol, 2006, 23: 2175-2190.
[]
Clegg MT, Gaut BS, Learn GH, Morton BR. Rates and patterns of chloroplast DNA evolution. Proc Natl Acad Sci USA, 1994, 91: 6795-6801.
[]
Conard HS (1905) The waterlilies: a monograph of the genus Nymphaea, vol 4. Carnegie institution of Washington
[]
Dalziell EL, Lewandrowski W, Merritt DJ. Increased salinity reduces seed germination and impacts upon seedling development in Nymphaea L. (Nymphaeaceae) from northern Australia’s freshwater wetlands. Aquat Bot, 2020, 165:103235
[]
Dkhar J, Kumaria S, Rao SR, Tandon P. Sequence characteristics and phylogenetic implications of the nrDNA internal transcribed spacers (ITS) in the genus Nymphaea with focus on some Indian representatives. Plant Syst Evol, 2012, 298:93-108.
[]
Dong WP, Xu C, Cheng T, Lin K, Zhou SL. Sequencing angiosperm plastid genomes made easy: a complete set of universal primers and a case study on the phylogeny of Saxifragales. Genome Biol Evol, 2013, 5: 989-997.
[]
Doorduin L, Gravendeel B, Lammers Y, Ariyurek Y, Chin-A-Woeng T, Vrieling K. The complete chloroplast genome of 17 individuals of pest species Jacobaea vulgaris: SNPs, microsatellites and barcoding markers for population and phylogenetic studies. DNA Res, 2011, 18: 93-105.
[]
Ewels P, Magnusson M, Lundin S, Käller M. MultiQC: summarize analysis results for multiple tools and samples in a single report. Bioinformatics, 2016, 32: 3047-3048.
[]
Fay JC, Wu C-I. The neutral theory in the genomic era. Curr Opin Genet Dev, 2001, 11: 642-646.
[]
Fay JC, Wu CI. Sequence divergence, functional constraint, and selection in protein evolution. Annu Rev Genomics Hum Genet, 2003, 4: 213-235.
[]
Foster CSP, Ho SYW. Strategies for partitioning clockmodels in phylogenomic dating: application to the angiosperm evolutionary timescale. Genome Biol Evol, 2017, 9: 2752-2763.
[]
Frazer KA, Pachter L, Poliakov A, Rubin EM, Dubchak I. VISTA: computational tools for comparative genomics. Nucleic Acids Res, 2004, 32: W273-W279.
[]
Ge Y, Dong X, Wu B, Wang N, Chen D, Chen H, Zou M, Xu Z, Tan L, Zhan R. Evolutionary analysis of six chloroplast genomes from three Persea americana ecological races: insights into sequence divergences and phylogenetic relationships. PLoS ONE, 2019, 14: e0221827.
[]
Gruenstaeudl M, Nauheimer L, Borsch T. Plastid genome structure and phylogenomics of Nymphaeales: conserved gene order and new insights into relationships. Plant Syst Evol, 2017, 303:1251-1270.
[]
Han CY, Ding R, Zong XY, Zhang LJ, Chen XH, Qu B. Structural characterization of Platanthera ussuriensis chloroplast genome and comparative analyses with other species of Orchidaceae. BMC Genom, 2022, 23:1-13.
[]
He DX, Gichira AW, Li ZZ, Nzei JM, Guo YH, Wang QF, Chen JM. Intergeneric relationships within the early-diverging angiosperm family Nymphaeaceae based on chloroplast phylogenomics. Int J Mol Sci, 2018, 19:9-11.
[]
Heslop-Harrison Y. Nymphaea L. J Ecol, 1955, 43:719-734.
[]
Hu J, Pan L, Liu H, Wang S, Wu Z, Ke W, Ding Y. Comparative analysis of genetic diversity in sacred lotus (Nelumbo nucifera Gaertn.) using AFLP and SSR markers. Mol Biol Rep, 2012, 39: 3637-3647.
[]
Jian SG, Soltis PS, Gitzendanner MA, Moore MJ, Li RQ, Hendry TA, Qiu YL, Dhingra A, Bell CD, Soltis DE. Resolving an ancient, rapid radiation in Saxifragales. Syst Biol, 2008, 57: 38-57.
[]
Jin JJ, Yu WB, Yang JB, Song Y, Depamphilis CW, Yi TS, Li DZ. GetOrganelle: a fast and versatile toolkit for accurate de novo assembly of organelle genomes. Genome Biol, 2020, 21: 241.
[]
Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol, 2013, 30: 772-780.
[]
Kawabe A, Nukii H, Furihata HY. Exploring the history of chloroplast capture in Arabis using whole chloroplast genome sequencing. Int J Mol Sci, 2018, 19: 602.
[]
Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T, Ashton B, Meintjes P, Drummond A. Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics, 2012, 28: 1647-1649.
[]
Koga K, Kadono Y, Setoguchi H. The genetic structure of populations of the vulnerable aquatic macrophyte Ranunculus nipponicus (Ranunculaceae). J Plant Res, 2007, 120: 167-174.
[]
Kuang DY, Wu H, Wang YL, Gao LM, Zhang SZ, Lu L. Complete chloroplast genome sequence of Magnolia kwangsiensis (Magnoliaceae): implication for DNA barcoding and population genetics. Genome, 2011, 54: 663-673.
[]
Kumar S, Dhingra A, Daniell H. Stable transformation of the cotton plastid genome and maternal inheritance of transgenes. Plant Mol Biol, 2004, 56: 203-216.
[]
Kumar H, Priya P, Singh N, Kumar M, Choudhary BK, Kumar L, Singh IS, Kumar N. RAPD and ISSR marker-based comparative evaluation of genetic diversity among Indian germplasms of Euryale ferox: an aquatic food plant. Appl Biochem Biotechnol, 2016, 180: 1345-1360.
[]
Kumar S, Stecher G, Li M, Knyaz C, Tamura K. MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol, 2018, 35: 1547-1549.
[]
Kumar S, Stecher G, Suleski M, Blair Hedges S. TimeTree: a resource for timelines, timetrees, and divergence times. Mol Biol Evol, 2017, 34: 1812-1819.
[]
Kurtz S, Choudhuri JV, Ohlebusch E, Schleiermacher C, Stoye J, Giegerich R. REPuter: the manifold applications of repeat analysis on a genomic scale. Nucleic Acids Res, 2001, 29: 4633-4642.
[]
Lagesen K, Hallin P, Rødland EA, Stærfeldt HH, Rognes T, Ussery DW. RNAmmer: consistent and rapid annotation of ribosomal RNA genes. Nucleic Acids Res, 2007, 35: 3100-3108.
[]
Lavid N, Barkay Z, Tel-Or E. Accumulation of heavy metals in epidermal glands of the waterlily (Nymphaeaceae). Planta, 2001, 212: 313-322.
[]
Lehwark P, Greiner S. GB2sequin—a file converter preparing custom GenBank files for database submission. Genomics, 2019, 111: 759-761.
[]
Les DH, Garvin DK, Wimpee CF. Molecular evolutionary history of ancient aquatic angiosperms. Proc Natl Acad Sci USA, 1991, 88: 10119-10123.
[]
Li HT, Luo Y, Gan L, Ma PF, Gao LM, Yang JB, Cai J, Gitzendanner MA, Fritsch PW, Zhang T, Jin JJ, Zeng CX, Wang H, Yu WB, Zhang R, van der Bank M, Olmstead RG, Hollingsworth PM, Chase MW, Soltis DE, Soltis PS, Yi TS, Li DZ. Plastid phylogenomic insights into relationships of all flowering plant families. BMC Biol, 2021, 19: 232.
[]
Li HT, Yi TS, Gao LM, Ma PF, Zhang T, Yang JB, Gitzendanner MA, Fritsch PW, Cai J, Luo Y, Wang H, van der Bank M, Zhang SD, Wang QF, Wang J, Zhang ZR, Fu CN, Yang J, Hollingsworth PM, Chase MW, et al. Origin of angiosperms and the puzzle of the Jurassic gap. Nat Plants, 2019, 5: 461-470.
[]
Li J, Zhang Z, Vang S, Yu J, Wong GKS, Wang J. Correlation between Ka/Ks and Ks is related to substitution model and evolutionary lineage. J Mol Evol, 2009, 68: 414-423.
[]
Li YT, Dong Y, Liu YC, Yu XY, Yang MS, Huang YR. Comparative analyses of Euonymus chloroplast genomes: genetic structure, screening for loci with suitable polymorphism, positive selection genes, and phylogenetic relationships within Celastrineae. Front Plant Sci, 2021, 11: 593984.
[]
Li ZZ, Saina JK, Gichira AW, Kyalo CM, Wang QF, Chen JM. Comparative genomics of the Balsaminaceae sister genera Hydrocera triflora and Impatiens pinfanensis. Int J Mol Sci, 2018, 19:1-17.
[]
Liu QP, Xue QZ. Comparative studies on codon usage pattern of chloroplasts and their host nuclear genes in four plant species. J Genet, 2005, 84: 55-62.
[]
Liu X, Wang ZS, Shao WH, Ye ZY, Zhang JG. Phylogenetic and taxonomic status analyses of the abaso section from multiple nuclear genes and plastid fragments reveal new insights into the North America origin of Populus (Salicaceae). Front Plant Sci, 2017, 7: 2022.
[]
Löhne C, Borsch T, Wiersema JH. Phylogenetic analysis of Nymphaeales using fast-evolving and noncoding chloroplast markers. Bot J Linn Soc, 2007, 154:141-163.
[]
Lowe TM, Eddy SR. TRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res, 1996, 25:955-964.
[]
Lu XM, Lu PZ, Chen JJ. Nitrogen and phosphorus removal and morphological and physiological response in Nymphaea tetragona under various planting densities. Toxicol Environ Chem, 2012, 94:1319-1330.
[]
Magallón S. Using fossils to break long branches in molecular dating: a comparison of relaxed clocks applied to the origin of angiosperms. Syst Biol, 2010, 59: 384-399.
[]
Massoni J, Couvreur TLP, Sauquet H. Five major shifts of diversification through the long evolutionary history of Magnoliidae (angiosperms) phylogenetics and phylogeography. BMC Evol Biol, 2015, 15: 49.
[]
Mehmood F, Abdullah SI, Ahmed I, Waheed MT, Mirza B. Characterization of Withania somnifera chloroplast genome and its comparison with other selected species of Solanaceae. Genomics, 2020, 112: 1522-1530.
[]
Morris JL, Puttick MN, Clark JW, Edwards D, Kenrick P, Pressel S, Wellman CH, Yang Z, Schneider H, Donoghue PCJ. The timescale of early land plant evolution. Proc Natl Acad Sci USA, 2018, 115: E2274-E2283.
[]
Odintsova MS, Yurina NP. Plastid genomes of higher plants and algae: structure and functions. Mol Biol, 2003, 37:649-662.
[]
Olmstead RG, Palmer JD. Chloroplast DNA systematics: a review of methods and data analysis. Am J Bot, 1994, 81:1205-1224.
[]
Parveen S, Singh N, Adit A, Kumaria S, Tandon R, Agarwal M, Jagannath A, Goel S. Contrasting reproductive strategies of two Nymphaea species affect existing natural genetic diversity as assessed by microsatellite markers: implications for conservation and wetlands restoration. Front Plant Sci, 2022, 13: 773572.
[]
Posada D, Buckley TR. Model selection and model averaging in phylogenetics: advantages of Akaike information criterion and Bayesian approaches over likelihood ratio tests. Syst Biol, 2004, 53: 793-808.
[]
Posada D, Crandall KA. Modeltest: testing the model of DNA substitution. Bioinformatics, 1998, 14: 817-818.
[]
Puttick MN. MCMCtreeR: functions to prepare MCMCtree analyses and visualize posterior ages on trees. Bioinformatics, 2019, 35: 5321-5322.
[]
Qiu YL, Lee J, Bernasconi-Quadroni F, Soltis DE, Soltis PS, Zanis M, Zimmer EA, Chen Z, Savolainen V, Chase MW. The earliest angiosperms: evidence from mitochondrial, plastid and nuclear genomes. Nature, 1999, 402: 404-407.
[]
Qu XJ, Moore MJ, Li DZ, Yi TS. PGA: a software package for rapid, accurate, and flexible batch annotation of plastomes. Plant Methods, 2019, 15: 50.
[]
Rambaut A, Drummond AJ, Xie D, Baele G, Suchard MA. Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Syst Biol, 2018, 67: 901-904.
[]
Ran JH, Shen TT, Wang MM, Wang XQ. Phylogenomics resolves the deep phylogeny of seed plants and indicates partial convergent or homoplastic evolution between Gnetales and angiosperms. Proc R Soc, 2018, 285:20181012
[]
Ronquist F, Huelsenbeck JP. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 2003, 19: 1572-1574.
[]
Rozas J, Ferrer-Mata A, Sanchez-DelBarrio JC, Guirao-Rico S, Librado P, Ramos-Onsins SE, Sanchez-Gracia A. DnaSP 6: DNA sequence polymorphism analysis of large data sets. Mol Biol Evol, 2017, 34: 3299-3302.
[]
Ruhfel BR, Gitzendanner MA, Soltis PS, Soltis DE, Burleigh JG. From algae to angiosperms-inferring the phylogeny of green plants (Viridiplantae) from 360 plastid genomes. BMC Evol Biol, 2014, 14: 23.
[]
Saarela JM, Rai HS, Doyle JA, Endress PK, Mathews S, Marchant AD, Briggs BG, Graham SW. Hydatellaceae identified as a new branch near the base of the angiosperm phylogenetic tree. Nature, 2007, 446: 312-315.
[]
Sato S, Nakamura Y, Kaneko T, Asamizu E, Tabata S. Complete structure of the chloroplast genome of Arabidopsis thaliana. DNA Res, 1999, 290:283-290.
[]
Shi C, Wang S, Cai HH, Zhang HR, Long XX, Tihelka E, Song WC, Feng Q, Jiang RX, Cai CY, Lombard N, Li X, Yuan J, Zhu JP, Yang HY, Liu XF, Xiang QP, Zhao ZT, Long CL, Schneider H, et al. Fire-prone Rhamnaceae with South African affinities in Cretaceous Myanmar amber. Nat Plants, 2022, 8: 125-135.
[]
Singh R, Singh G. Association of aphids with plants belonging to order Nymphaeales, Austrobaileyales, Laurales, Magnoliales and Piperales (Angiosperms) in India. J Appl Entomol, 2022, 2:54-60.
[]
Smith DR. Mutation rates in plastid genomes: they are lower than you might think. Genome Biol Evol, 2015, 7: 1227-1234.
[]
Sokoloff DD, Macfarlane TD, Remizowa MV, Rudall PJ. Classification of the early-divergent angiosperm family Hydatellaceae: one genus instead of two, four new species and sexual dimorphism in dioecious taxa. Taxon, 2008, 57:179-200.
[]
Soltis PS, Soltis DE, Zanis MJ, Kim S. Basal lineages of angiosperms: relationships and implications for floral evolution. Int J Plant Sci, 2000, 161:96-107.
[]
Song WC, Chen ZM, He L, Feng Q, Zhang HR, Du GL, Shi C. Comparative chloroplast genome analysis of wax gourd (Benincasa hispida) with three Benincaseae species, revealing evolutionary dynamic patterns and phylogenetic implications. Genes, 2022, 13: 461.
[]
Song WC, Ji CX, Chen ZM, Cai HH, Wu XM, Shi C, Wang S. Comparative analysis the complete chloroplast genomes of nine Musa species: genomic features, comparative analysis, and phylogenetic implications. Front Plant Sci, 2022, 13:1-15.
[]
Sun C, Chen F, Teng N, Xu Y, Dai Z. Comparative analysis of the complete chloroplast genome of seven Nymphaea species. Aquat Bot, 2021, 170:103353
[]
Sun L, Fang L, Zhang Z, Chang X, Penny D, Zhong B. Chloroplast phylogenomic inference of green algae relationships. Sci Rep, 2016, 6: 20528.
[]
Tillich M, Lehwark P, Pellizzer T, Ulbricht-Jones ES, Fischer A, Bock R, Greiner S. GeSeq - Versatile and accurate annotation of organelle genomes. Nucleic Acids Res, 2017, 45: W6-W11.
[]
Wang RJ, Cheng CL, Chang CC, Wu CL, Su TM, Chaw SM. Dynamics and evolution of the inverted repeat-large single copy junctions in the chloroplast genomes of monocots. BMC Evol Biol, 2008, 8: 36.
[]
Widmer A, Baltisberger M. Extensive intraspecific chloroplast DNA (cpDNA) variation in the alpine Draba aizoides L. (Brassicaceae): haplotype relationships and population structure. Mol Ecol, 1999, 8: 1405-1415.
[]
Wu CS, Chaw SM. Evolutionary stasis in cycad plastomes and the first case of plastome GC-biased gene conversion. Genome Biol Evol, 2015, 7: 2000-2009.
[]
Wu Z, Gui S, Quan Z, Pan L, Wang S, Ke W, Liang D, Ding Y. A precise chloroplast genome of Nelumbo nucifera (Nelumbonaceae) evaluated with Sanger, Illumina MiSeq, and PacBio RS II sequencing platforms: insight into the plastid evolution of basal eudicots. BMC Plant Biol, 2014, 14: 289.
[]
Xi ZX, Liu L, Rest JS, Davis CC. Coalescent versus concatenation methods and the placement of Amborella as sister to water lilies. Syst Biol, 2014, 63: 919-932.
[]
Yamada T, Imaichi R, Kato M. Developmental morphology of ovules and seeds of Nymphaeales. Am J Bot, 2001, 88: 963-974.
[]
Yang J, Hu G, Hu G. Comparative genomics and phylogenetic relationships of two endemic and endangered species (Handeliodendron bodinieri and Eurycorymbus cavaleriei) of two monotypic genera within Sapindales. BMC Genom, 2022, 23:1-22.
[]
Yang X, Luo X, Cai X. Analysis of codon usage pattern in Taenia saginata based on a transcriptome dataset. Parasit Vectors, 2014, 7: 527.
[]
Yang YY, Qu XJ, Zhang R, Stull GW, Yi TS. Plastid phylogenomic analyses of Fagales reveal signatures of conflict and ancient chloroplast capture. Mol Phylogenet Evol, 2021, 163: 107232.
[]
Yang YZ, Sun PH, Lv LK, Wang DL, Ru DF, Li Y, Ma T, Zhang L, Shen XX, Meng FB, Jiao BB, Shan LX, Liu M, Wang QF, Qin ZJ, Xi ZX, Wang XY, Davis CC, Liu JQ. Prickly waterlily and rigid hornwort genomes shed light on early angiosperm evolution. Nat Plants, 2020, 6: 215-222.
[]
Yang Z. PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol, 2007, 24: 1586-1591.
[]
Ye WQ, Yap ZY, Li P, Comes HP, Qiu YX. Plastome organization, genome-based phylogeny and evolution of plastid genes in Podophylloideae (Berberidaceae). Mol Phylogenet Evol, 2018, 127: 978-987.
[]
Zanis MJ, Soltis DE, Soltis PS, Mathews S, Donoghue MJ. The root of the angiosperms revisited. Proc Natl Acad Sci USA, 2002, 99: 6848-6853.
[]
Zeng L, Zhang Q, Sun R, Kong H, Zhang N, Ma H. Resolution of deep angiosperm phylogeny using conserved nuclear genes and estimates of early divergence times. Nat Commun, 2014, 5: 4956.
[]
Zhang LS, Chen F, Zhang XT, Li Z, Zhao YY, Lohaus R, Chang XJ, Dong W, Ho SYW, Liu X, Song A, Chen JH, Guo WL, Wang ZJ, Zhuang YY, Wang HF, Chen XQ, Hu J, Liu YH, Qin Y, et al. The water lily genome and the early evolution of flowering plants. Nature, 2020, 577: 79-84.
[]
Zheng S, Poczai P, Hyvönen J, Tang J, Amiryousefi A. Chloroplot: an online program for the versatile plotting of organelle genomes. Front Genet, 2020, 11: 576124.
[]
Zhou M, Long W, Li X. Patterns of synonymous codon usage bias in chloroplast genomes of seed plants. For Stud China, 2008, 10:235-242.
[]
Zhou T, Ruhsam M, Wang J, Zhu H, Li W, Zhang X, Xu Y, Xu F, Wang X. The complete chloroplast genome of Euphrasia regelii, pseudogenization of ndhH genes and the phylogenetic relationships within Orobanchaceae. Front Genet, 2019, 10: 444.
[]
Zhu QH, Ge S. Phylogenetic relationships among A-genome species of the genus Oryza revealed by intron sequences of four nuclear genes. New Phytol, 2005, 167: 249-265.

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