Phylogenetic analysis and divergence time estimation of Lycium species in China based on the chloroplast genomes.
Lycium
Comparative analysis
Divergence time
Phylogenetic relationship
Plastome structure
Journal
BMC genomics
ISSN: 1471-2164
Titre abrégé: BMC Genomics
Pays: England
ID NLM: 100965258
Informations de publication
Date de publication:
06 Jun 2024
06 Jun 2024
Historique:
received:
01
03
2024
accepted:
31
05
2024
medline:
7
6
2024
pubmed:
7
6
2024
entrez:
6
6
2024
Statut:
epublish
Résumé
Lycium is an economically and ecologically important genus of shrubs, consisting of approximately 70 species distributed worldwide, 15 of which are located in China. Despite the economic and ecological importance of Lycium, its phylogeny, interspecific relationships, and evolutionary history remain relatively unknown. In this study, we constructed a phylogeny and estimated divergence time based on the chloroplast genomes (CPGs) of 15 species, including subspecies, of the genus Lycium from China. We sequenced and annotated 15 CPGs in this study. Comparative analysis of these genomes from these Lycium species revealed a typical quadripartite structure, with a total sequence length ranging from 154,890 to 155,677 base pairs (bp). The CPGs was highly conserved and moderately differentiated. Through annotation, we identified a total of 128-132 genes. Analysis of the boundaries of inverted repeat (IR) regions showed consistent positioning: the junctions of the IRb/LSC region were located in rps19 in all Lycium species, IRb/SSC between the ycf1 and ndhF genes, and SSC/IRa within the ycf1 gene. Sequence variation in the SSC region exceeded that in the IR region. We did not detect major expansions or contractions in the IR region or rearrangements or insertions in the CPGs of the 15 Lycium species. Comparative analyses revealed five hotspot regions in the CPG: trnR(UCU), atpF-atpH, ycf3-trnS(GGA), trnS(GGA), and trnL-UAG, which could potentially serve as molecular markers. In addition, phylogenetic tree construction based on the CPG indicated that the 15 Lycium species formed a monophyletic group and were divided into two typical subbranches and three minor branches. Molecular dating suggested that Lycium diverged from its sister genus approximately 17.7 million years ago (Mya) and species diversification within the Lycium species of China primarily occurred during the recent Pliocene epoch. The divergence time estimation presented in this study will facilitate future research on Lycium, aid in species differentiation, and facilitate diverse investigations into this economically and ecologically important genus.
Sections du résumé
BACKGROUND
BACKGROUND
Lycium is an economically and ecologically important genus of shrubs, consisting of approximately 70 species distributed worldwide, 15 of which are located in China. Despite the economic and ecological importance of Lycium, its phylogeny, interspecific relationships, and evolutionary history remain relatively unknown. In this study, we constructed a phylogeny and estimated divergence time based on the chloroplast genomes (CPGs) of 15 species, including subspecies, of the genus Lycium from China.
RESULTS
RESULTS
We sequenced and annotated 15 CPGs in this study. Comparative analysis of these genomes from these Lycium species revealed a typical quadripartite structure, with a total sequence length ranging from 154,890 to 155,677 base pairs (bp). The CPGs was highly conserved and moderately differentiated. Through annotation, we identified a total of 128-132 genes. Analysis of the boundaries of inverted repeat (IR) regions showed consistent positioning: the junctions of the IRb/LSC region were located in rps19 in all Lycium species, IRb/SSC between the ycf1 and ndhF genes, and SSC/IRa within the ycf1 gene. Sequence variation in the SSC region exceeded that in the IR region. We did not detect major expansions or contractions in the IR region or rearrangements or insertions in the CPGs of the 15 Lycium species. Comparative analyses revealed five hotspot regions in the CPG: trnR(UCU), atpF-atpH, ycf3-trnS(GGA), trnS(GGA), and trnL-UAG, which could potentially serve as molecular markers. In addition, phylogenetic tree construction based on the CPG indicated that the 15 Lycium species formed a monophyletic group and were divided into two typical subbranches and three minor branches. Molecular dating suggested that Lycium diverged from its sister genus approximately 17.7 million years ago (Mya) and species diversification within the Lycium species of China primarily occurred during the recent Pliocene epoch.
CONCLUSION
CONCLUSIONS
The divergence time estimation presented in this study will facilitate future research on Lycium, aid in species differentiation, and facilitate diverse investigations into this economically and ecologically important genus.
Identifiants
pubmed: 38844874
doi: 10.1186/s12864-024-10487-9
pii: 10.1186/s12864-024-10487-9
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
569Subventions
Organisme : the Ningxia Natural Science Foundation
ID : 2022AAC05063
Organisme : the Ningxia Natural Science Foundation
ID : 2021AAC02005
Organisme : the National Natural Science Foundation of China
ID : 32260049
Informations de copyright
© 2024. The Author(s).
Références
Zhang JX, Guan SH, Feng RH, Wang Y, Wu ZY, Zhang YB, Chen XH, Bi KS, Guo DA. Neolignanamides, lignanamides, and other phenolic compounds from the root bark of Lycium chinense. J Nat Prod. 2013;76:51–8.
pubmed: 23282106
doi: 10.1021/np300655y
Turchetto C, Fagundes NJ, Segatto AL, Kuhlemeier C, Solis Neffa VG, Speranza PR, Bonatto SL, Freitas LB. Diversification in the South American Pampas: the genetic and morphological variation of the widespread Petunia axillaris complex (Solanaceae). Mol Ecol. 2014;23:374–89.
pubmed: 24372681
doi: 10.1111/mec.12632
Zhang ZY, Lu AM, Solanaceae. In: Wu Z, Raven P, editors. Flora of China. Volume 17. Beijing, China: Science; 1994.
Chen TY, Jiang XL, Li QS, Zhang ZY, Joongku LE. A new species and a new variety of Lycium (Solanaceae) from Ningxia, China. Guihaia. 2012;32:5–8.
Liao Q, Wang RJ. Lycium Ningxiaense, a replacement name for Lycium parvifolium. (Solanaceae) Pyhtotaxa. 2014;173(4):299–300. T.Y. Chen & Xu L. Jiang
doi: 10.11646/phytotaxa.173.4.5
Li JN, Jiang XL, Li ZG, Chen TY, Zhang ZY. Lycium qingshuiheense, a new species of Solanaceae from Ningxia, China. Guihaia. 2011;31(4):427–9.
Xie DM, Zhang XB, Qian D, Zha X, Huang LQ. Lycium amarum sp. nov. (Solanaceae) from Xizang, supported from morphological characters and phylogenetic analysis. Nord J Bot. 2016;34:538–44.
doi: 10.1111/njb.01071
Potterat O. Goji (Lycium barbarum and L. Chinense): Phytochemistry, pharmacology and safety in the perspective of traditional uses and recent popularity. Planta Med. 2010;76:7–19.
pubmed: 19844860
doi: 10.1055/s-0029-1186218
Kim MH, Kim EJ, Choi YY, Hong J, Yang WM. Lycium chinense improves post-menopausal obesityvia regulation of PPAR-gamma and estrogen receptor-alpha/beta expressions. Am J Chin Med. 2017;45:269–82.
pubmed: 28231739
doi: 10.1142/S0192415X17500173
Yao R, Heinrich M, Weckerle CS. The genus Lycium as food and medicine: a botanical, ethnobotanical and historical review. J Ethnopharmacology: Interdisciplinary J Devoted Bioscientific Res Indigenous Drugs. 2018;212:50–66.
doi: 10.1016/j.jep.2017.10.010
Qin X, Yamauchi R, Aizawa K, Inakuma T, Kato K. Structural features of arabinogalactan-proteins from the fruit of Lycium chinense. Carbohydr Res. 2001;333:79–85.
pubmed: 11423113
doi: 10.1016/S0008-6215(01)00118-5
Chen X, Zhou J, Cui Y, Wang Y, Duan B, Yao H. Identification of Ligularia herbs using the complete chloroplast genome as a super-barcode. Front Pharmacol. 2018;9:695.
pubmed: 30034337
pmcid: 6043804
doi: 10.3389/fphar.2018.00695
He L, Qian J, Li X, Sun Z, Xu X, Chen S. Complete chloroplast genome of medicinal plant lonicera japonica: genome rearrangement, intron gain and loss, and implications for phylogenetic studies. Molecules. 2017;22:249.
pubmed: 28178222
pmcid: 6155926
doi: 10.3390/molecules22020249
Zheng GQ, Wang ZZ, Wei JR, Zhao JH, Zhang C, Mi JJ, Zong Y, Liu GH, Wang Y, Xu X, Zeng SH. Fruit development and ripening orchestrating the biosynthesis and regulation of Lycium barbarum polysaccharides in goji berry. Int J Biol Macromol. 2024;254:127970.
pubmed: 37944729
doi: 10.1016/j.ijbiomac.2023.127970
Bao H, Zheng GQ, Qi GL, Su XL, Wang J. Cellular localization and levels of arabinogalactan proteins in Lycium barbarum’s fruit. Pak J Bot. 2016;48(5):1951–63.
Zhao JH, Xu YH, Li HX, An W, Yin Y, Wang B, Wang LP, Wang B, Duan LY, Ren YX, Liang XJ, Wang YJ, Wan R, Huang T, Zhang B, Li YL, Luo J, Cao YL. Metabolite-based genome-wide association studies enable the dissection of the genetic bases of flavonoids, betaine and spermidine in wolfberry (Lycium). Plant Biotechnol J. 2024, pp:1–18.
Zhao JH, Xu YH, Li HX, Zhu XL, Yin Y, Zhang XY, Qin XY, Zhou J, Duan LY, Liang XJ, Huang T, Zhang B, Wan R, Shi ZG, Cao YL, An W. ERF5.1 modulates carotenoid accumulation by interacting with CCD4.1 in Lycium. Hortic Res. 2023;10:1–14.
doi: 10.1093/hr/uhad230
Ni LL, Zhao ZL, Lu JN. DNA barcoding construction of medicinal plants in genus Lycium L. based on multiple genomic segments. Chin Traditional Herb Drugs. 2016;47:5.
Hebert PD, Cywinska A, Ball SL, de Waard JR. Biological identifications through DNA barcodes. Proceedings of the Royal Society B: Biological Sciences. 2003;270:313–321.
Sanchez-Puerta MV, Abbona CC. The chloroplast genome of Hyoscyamus niger and a phylogenetic study of the tribe Hyoscyameae (Solanaceae). PLoS ONE. 2014;9:e98353.
pubmed: 24851862
pmcid: 4031233
doi: 10.1371/journal.pone.0098353
Yang Y, Dang Y, Li Q, Lu J, Li X, Wang Y. Complete chloroplast genome sequence of poisonous and medicinal plant Datura stramonium: Organizations and implications for genetic engineering. PLoS ONE. 2014;9:e110656.
pubmed: 25365514
pmcid: 4217734
doi: 10.1371/journal.pone.0110656
Shaw J, Lickey EB, Schilling EE, Small RL. Comparison of whole chloroplast genome sequences to choose noncoding regions for phylogenetic studies in angiosperms: the tortoise and the hare III. Am J Bot. 2007;94:275–88.
pubmed: 21636401
doi: 10.3732/ajb.94.3.275
Shaw J, Lickey EB, Beck JT, Farmer SB, Liu W, Miller J, Siripun KC, Winder CT, Schilling EE, Small RL. The tortoise and the hare II: relative utility of 21 noncoding chloroplast DNA sequences for phylogenetic analysis. Am J Bot. 2005;92:142–66.
pubmed: 21652394
doi: 10.3732/ajb.92.1.142
Nielsen AZ, Ziersen B, Jensen K, Lassen LM, Olsen CE, Moller BL, Jensen PE. Redirecting photosynthetic reducing power toward bioactive natural product synthesis. ACS Chem Biol. 2013;2:308–15.
Yang ZR, Huang YY, An WL, Zheng XS, Huang S, Liang LL. Sequencing and structural analysis of the complete chloroplast genome of the medicinal plant lyciumchinense mill. Plants. 2019;8:87.
pubmed: 30987216
pmcid: 6524360
doi: 10.3390/plants8040087
Guo XY, Liu JQ, Hao GQ, Zhang L, Mao KS, Wang XJ, Zhang D, Ma T, Hu QJ, Al-Shehbaz IA, Koch MA. Plastome phylogeny and early diversification of Brassicaceae. BMC Genomics. 2017;18:176.
pubmed: 28209119
pmcid: 5312533
doi: 10.1186/s12864-017-3555-3
Xie HH, Zhang L, Zhang C, Chang H, Xi ZX, Xu XT. Comparative analysis of the complete chloroplast genomes of six threatened subgenus Gynopodium (Magnolia) species. BMC Genomics. 2022;23:716.
pubmed: 36261795
pmcid: 9583488
doi: 10.1186/s12864-022-08934-6
Hu H, Hu QJ, Al-Shehbaz IA, Luo X, Zeng TT, Guo XY, Liu JQ. Species delimitation and interspecific relationships of the genus Orychophragmus (Brassicaceae) inferred from whole chloroplast genomes. Front Plant Sci. 2016;7:1826.
pubmed: 27999584
pmcid: 5138468
doi: 10.3389/fpls.2016.01826
Palmer JD. Comparative organization of chloroplast genomes. Annu Rev Genet. 1985;19:325–54.
pubmed: 3936406
doi: 10.1146/annurev.ge.19.120185.001545
Daniell H, Lin CS, Yu M, Chang WJ. Chloroplast genomes: diversity, evolution, and applications in genetic engineering. Genome Biol. 2016;17:134.
pubmed: 27339192
pmcid: 4918201
doi: 10.1186/s13059-016-1004-2
Wicke S, Schneeweiss GM, dePamphilis CW, Muller KF, Quandt D. The evolution of the plastid chromosome in land plants: gene content, gene order, gene function. Plant Mol Biol. 2011;76(3–5):273–97.
pubmed: 21424877
pmcid: 3104136
doi: 10.1007/s11103-011-9762-4
Kim GB, Lim CE, Kim JS, Kim K, Lee JH, Yu HJ. Comparative chloroplast genome analysis of Artemisia (Asteraceae) in East Asia: insights into evolutionary divergence and phylogenomic implications. BMC Genomics. 2020;21(1):415.
pubmed: 32571207
pmcid: 7310033
doi: 10.1186/s12864-020-06812-7
Xiong Q, Hu YX, Lv WQ, Wang QH, Liu GX, Hu ZY. Chloroplast genomes of five Oedogonium species: genome structure, phylogenetic analysis and adaptive evolution. BMC Genomics. 2021;22(1):707.
pubmed: 34592920
pmcid: 8485540
doi: 10.1186/s12864-021-08006-1
Yang YX, Zhi LQ, Jia Y, Zhong QY, Liu ZL, Yue M. Nucleotide diversity and demographic history of Pinus bungeana, an endangered conifer species endemic in China. J Syst Evol. 2020;58(3):282–94.
doi: 10.1111/jse.12546
Zhang FJ, Wang T, Shu XC, Wang N, Zhuang WB, Wang Z. Complete chloroplast genomes and comparative analyses of L. Chinensis, L. Anhuiensis, and L. Aurea (Amaryllidaceae). Int J Mol Sci. 2020;21(16):5729.
pubmed: 32785156
pmcid: 7461117
doi: 10.3390/ijms21165729
Li HT, Yi TS, Gao LM, Ma PF, Zhang T, Yang JB. Origin of angiosperms and the puzzle of the jurassic gap. Nat Plants. 2019;5(5):461–70.
pubmed: 31061536
doi: 10.1038/s41477-019-0421-0
Cui YX, Zhou JG, Chen XL, Xu ZC, Wang Y, Sun W, Song JY, Yao H. Complete chloroplast genome and comparative analysis of three Lycium (Solanaceae) species with medicinal and edible properties. Gene Rep. 2019;17:100464.
doi: 10.1016/j.genrep.2019.100464
Yin XL, Fang KT, Liang YZ, Wong RN, Ha AWY. Assessing phylogenetic relationships of Lycium samples using RAPD and entropy theory. Acta Pharmacol Sin. 2005;26(10):1217–24.
pubmed: 16174438
doi: 10.1111/j.1745-7254.2005.00197.x
Xin T, Yao H, Gao H, Zhou X, Ma X, Xu C, Chen J, Han J, Pang X, Xu R. Super food Lycium barbarum (solanaceae) traceability via an internal transcribed spacer 2 barcode. Food Res Int. 2013;54:1699–704.
doi: 10.1016/j.foodres.2013.10.007
Ran ZH, Li Z, Xiao X, An MT, Yan C. Complete chloroplast genomes of 13 species of sect. Tuberculata Chang (Camellia L.): genomic features, comparative analysis, and phylogenetic relationships. BMC Genomics. 2024;25:108.
pubmed: 38267876
pmcid: 10809650
doi: 10.1186/s12864-024-09982-w
Yang Z, Ma WX, Yang XH, Wang LJ, Zhao TT, Liang LS, Wang GX, Ma QH. Plastome phylogenomics provide new perspective into the phylogeny and evolution of Betulaceae (Fagales). BMC Plant Biol. 2022;22:611.
pubmed: 36566190
pmcid: 9789603
doi: 10.1186/s12870-022-03991-1
Song Y, Wang SJ, Ding YM, Xu J, Li MF, Zhu SF. Chloroplast genomic resource of Paris for species discrimination. Sci Rep. 2017;7:3427.
pubmed: 28611359
pmcid: 5469780
doi: 10.1038/s41598-017-02083-7
Cheng H, Li JF, Zhang H, Cai BH, Gao ZH, Qiao YS. The complete chloroplast genome sequence of strawberry (Fragaria × ananassa Duch.) And comparison with related species of Rosaceae. PeerJ. 2017;5:e3919.
pubmed: 29038765
pmcid: 5641433
doi: 10.7717/peerj.3919
Clegg MT, Gaut BS, Learn GH, Morton BR. Rates and patterns of chloroplast DNA evolution. Proc Natl Acad Sci USA. 1994;91(15):6795–801.
pubmed: 8041699
pmcid: 44285
doi: 10.1073/pnas.91.15.6795
Tyagi S, Jung JA, Kim JS, Won SY. Comparative analysis of the complete chloroplast genome of mainland Aster Spathulifolius and other Aster species. Plants. 2020;9:568.
pubmed: 32365609
pmcid: 7285121
doi: 10.3390/plants9050568
Wu LL, Wei RX, Yang QW, Zhang ZY. A preliminary study on the hybrid origin of new taxa in Lycium (Solanaceae). Guihaia. 2011;31(3):304–11.
Firetti F, Zuntini AR, Gaiarsa JW, Oliveira RS, Lohmann LG, VanSluys MA. Complete chloroplast genome sequences contribute to plant species delimitation: a case study of the Anemopaegma species complex. Am J Bot. 2017;104(10):1493–509.
pubmed: 29885220
doi: 10.3732/ajb.1700302
Yu XQ, Drew BT, Yang JB, Gao LM, Li DZ. Comparative chloroplast genomes of eleven Schima (Theaceae) species: insights into DNA barcoding and phylogeny. PLoS ONE. 2017;12(6):e0178026.
pubmed: 28575004
pmcid: 5456055
doi: 10.1371/journal.pone.0178026
Allen GC, Floresvergara MA, Krasynanski S, Kumar S, Thompson WF. A modified protocol for rapid DNA isolation from plant tissues using cetyltrimethy lammonium bromide. Nat Protoc. 2006;1:2320–5.
pubmed: 17406474
doi: 10.1038/nprot.2006.384
Dierckxsens N, Mardulyn P, Smits G. NOVOPlasty: de novo assembly of organelle genomes from whole genome data. Nucleic Acids Res. 2017;45(4):e18.
pubmed: 28204566
Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S. Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics. 2012;28:1647–9.
pubmed: 22543367
pmcid: 3371832
doi: 10.1093/bioinformatics/bts199
Huang DI, Cronk QC, Plann. A command-line application for annotating plastome sequences. Appl Plant Sci. 2015;3:1500026.
doi: 10.3732/apps.1500026
Löytynoja A, Goldman N. Phylogeny-aware gap placement prevents errors in sequence alignment and evolutionary analysis. Science. 2008;320:1632–5.
pubmed: 18566285
doi: 10.1126/science.1158395
Castresana J. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol. 2000;17:540–52.
pubmed: 10742046
doi: 10.1093/oxfordjournals.molbev.a026334
Lohse M, Drechsel O, Kahlau S, Bock R. OrganellarGenomeDRAW-a suite of tools for generating physical maps of plastid and mitochondrial genomes and visualizing expression data sets. Nucleic Acids Res. 2013;41:W575–81.
pubmed: 23609545
pmcid: 3692101
doi: 10.1093/nar/gkt289
Sayers EW, Cavanaugh M, Clark K, Ostell J, Pruitt KD, Karsch-Mizrachi I. GenBank Nucleic Acids Res. 2020;48:D84–6.
pubmed: 31665464
doi: 10.1093/nar/gkaa500
Frazer KA, Pachter L, Poliakov A, Rubin EM, Dubchak I. VISTA: computational tools for comparative genomics. Nucleic Acids Res. 2004;32:W273–9.
pubmed: 15215394
pmcid: 441596
doi: 10.1093/nar/gkh458
Brudno M, Malde S, Poliakov A, Do CB, Couronne O, Dubchak I, Batzoglou S. Glocal alignment: finding rearrangements during alignment. Bioinformatics. 2003;19:i54–62.
pubmed: 12855437
doi: 10.1093/bioinformatics/btg1005
Amiryousefi A, Hyvönen J, Poczai P. IRscope: an online program to visualize the junction sites of chloroplast genomes. Bioinformatics. 2018;34:3030–1.
pubmed: 29659705
doi: 10.1093/bioinformatics/bty220
Rozas J, Ferrer-Mata A, Sánchez-Delbarrio JC, Guirao-Rico S, Librado P, Ramos-Onsins SE, Sánchez-Gracia A. DnaSP 6: DNA sequence polymorphism analysis of large data sets. Mol Biology Evol. 2017;34:3299–302.
doi: 10.1093/molbev/msx248
Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics. 2014;30:1312.
pubmed: 24451623
pmcid: 3998144
doi: 10.1093/bioinformatics/btu033
Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Hohna S, Larget Bret, Liu L, Suchard MA, Huelsenbeck JP, Notes A. MrBayes 3.2: efficient bayesian phylogenetic inference and model choice across a large model space. Syst Biol. 2012;61(3):539–42.
pubmed: 22357727
pmcid: 3329765
doi: 10.1093/sysbio/sys029
Rambaut A. FigTree v1. 4. University of Edinburgh, Edinburgh, UK. 2012. http://tree.bio.ed.ac.uk/software/figtree .
Yang ZH. PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol. 2007;24:1586–91.
pubmed: 17483113
doi: 10.1093/molbev/msm088
Rannala B, Yang Z. Inferring speciation times under an episodic molecular clock. Syst Biol. 2007;56:453–66.
pubmed: 17558967
doi: 10.1080/10635150701420643
Crepet WL, Nixon KC, Gandolfo MA. Fossil evidenceand phylogeny: the age of major angiosperm clades based on mesofossil and macrofossil evidence from cretaceous deposits. Am J Bot. 2004;91:1666–82.
pubmed: 21652316
doi: 10.3732/ajb.91.10.1666
Vander BJ. Miocene floras in the Lower Rhenish basin and their ecological interpretation. Rev Palaeobotany Playnology. 1987;52:299–366.
doi: 10.1016/0034-6667(87)90064-9
Särkinen T, Bohs L, Olmstead RG, Knapp S. A phylogenetic framework for evolutionary study of the nightshades (Solanaceae): a dated 1000-tip tree. BMC Ecol Evol. 2013;13:214.