Highly Diverse Shrub Willows (Salix L.) Share Highly Similar Plastomes
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection
Typ dokumentu časopisecké články
PubMed
34539686
PubMed Central
PMC8448165
DOI
10.3389/fpls.2021.662715
Knihovny.cz E-zdroje
- Klíčová slova
- Chamaetia/Vetrix clade, Eurasia, North America, genome skimming, phylogenomics, plastome evolution,
- Publikační typ
- časopisecké články MeSH
Plastome phylogenomics is used in a broad range of studies where single markers do not bear enough information. Phylogenetic reconstruction in the genus Salix is difficult due to the lack of informative characters and reticulate evolution. Here, we use a genome skimming approach to reconstruct 41 complete plastomes of 32 Eurasian and North American Salix species representing different lineages, different ploidy levels, and separate geographic regions. We combined our plastomes with published data from Genbank to build a comprehensive phylogeny of 61 samples (50 species) using RAxML (Randomized Axelerated Maximum Likelihood). Additionally, haplotype networks for two observed subclades were calculated, and 72 genes were tested to be under selection. The results revealed a highly conserved structure of the observed plastomes. Within the genus, we observed a variation of 1.68%, most of which separated subg. Salix from the subgeneric Chamaetia/Vetrix clade. Our data generally confirm previous plastid phylogenies, however, within Chamaetia/Vetrix phylogenetic results represented neither taxonomical classifications nor geographical regions. Non-coding DNA regions were responsible for most of the observed variation within subclades and 5.6% of the analyzed genes showed signals of diversifying selection. A comparison of nuclear restriction site associated DNA (RAD) sequencing and plastome data on a subset of 10 species showed discrepancies in topology and resolution. We assume that a combination of (i) a very low mutation rate due to efficient mechanisms preventing mutagenesis, (ii) reticulate evolution, including ancient and ongoing hybridization, and (iii) homoplasy has shaped plastome evolution in willows.
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Andrews S. (2010). FastQC: A Quality Control Tool for High Throughput Sequence Data. Available online at: http://www.bioinformatics.babraham.ac.uk/projects/fastqc
Argus G. W. (2010). Salix, in Flora of North America, Vol. 7 Magnoliophyta: Salicaceae to Brassicaceae, ed Flora of North America Editorial Committee E. (New York, NY: Oxford University Press; ), 23–51.
Azuma T., Kajita T., Yokoyama J., Ohashi H. (2000). Phylogenetic relationships of Salix (Salicaceae) based on rbcL sequence data. Am. J. Bot. 87, 67–75. 10.2307/2656686 PubMed DOI
Barcaccia G., Meneghetti S., Lucchin M., de Jong H. (2014). Genetic segregation and genomic hybridization patterns support an allotetraploid structure and disomic inheritance for Salix species. Diversity 6, 633–651. 10.3390/d6040633 DOI
Barrett C. F., Specht C. D., Leebens-Mack J., Stevenson D. W., Zomlefer W. B., Davis J. I. (2014). Resolving ancient radiations: can complete plastid gene sets elucidate deep relationships among the tropical gingers (Zingiberales)? Ann. Bot. 113, 119–133. 10.1093/aob/mct264 PubMed DOI PMC
Besnard G., Hernández P., Khadari B., Dorado G., Savolainen V. (2011). Genomic profiling of plastid DNA variation in the Mediterranean olive tree. BMC Plant Biol. 11:80. 10.1186/1471-2229-11-80 PubMed DOI PMC
Bock D. G., Andrew R. L., Rieseberg L. H. (2014). On the adaptive value of cytoplasmic genomes in plants. Mol. Ecol. 23, 4899–4911. 10.1111/mec.12920 PubMed DOI
Bock R., Timmis J. N. (2008). Reconstructing evolution: gene transfer from plastids to the nucleus. BioEssays 30, 556–566. 10.1002/bies.20761 PubMed DOI
Castresana J. (2000). Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol. Biol. Evol. 17, 540–552. 10.1093/oxfordjournals.molbev.a026334 PubMed DOI
Charlesworth B., Morgan M. T., Charlesworth D. (1993). The effect of deleterious mutations on neutral molecular variation. Genetics 134, 1289–1303. 10.1093/genetics/134.4.1289 PubMed DOI PMC
Chen A. J., Sun H., Wen J., Yang Y., Chen J., Sun H., et al. (2010). Molecular Phylogeny of Salix L. (Salicaceae) Inferred From Three Chloroplast Datasets and Its Systematic Implications. International Association for Plant Taxonomy (IAPT) Stable, 29–37. Available online at: http://www.jstor.org/stable/27757048
Chen J. (2020). Characterization of the complete chloroplast genome of Salix variegata (Salicaceae). Mitochondrial DNA Part B Resour. 5, 196–197. 10.1080/23802359.2019.1698989 PubMed DOI PMC
Clement M., Posada D., Crandall K. A. (2000). TCS: a computer program to estimate gene genealogies. Mol. Ecol. 9, 1657–1659. 10.1046/j.1365-294x.2000.01020.x PubMed DOI
Dong W., Liu J., Yu J., Wang L., Zhou S. (2012). Highly variable chloroplast markers for evaluating plant phylogeny at low taxonomic levels and for DNA barcoding. PLoS ONE 7:e35071. 10.1371/journal.pone.0035071 PubMed DOI PMC
Dong W., Xu C., Li C., Sun J., Zuo Y., Shi S., et al. . (2015). ycf 1, the most promising plastid DNA barcode of land plants. Sci. Rep. 5:8348. 10.1038/srep08348 PubMed DOI PMC
Duvall M. R., Burke S. V., Clark D. C. (2020). Plastome phylogenomics of Poaceae: alternate topologies depend on alignment gaps. Bot. J. Linn. Soc. 192, 9–20. 10.1093/botlinnean/boz060 DOI
Eaton D. A. R., Overcast I. (2016). iPYRAD: Interactive Assembly and Analysis of RADseq Data Sets. Available online at: available: http://ipyrad.readthedocs.io/ PubMed
Fang C., Zhao S., Skvortsov A. (1999). Salicaceae, in Flora of China, Vol. 4, eds Wu Z. Y. , Raven P. H. (St. Louis, MI: Science Press, Beijing and Missouri Botanical Garden Press; ), 139–274.
Flot J. F., Hespeels B., Li X., Noel B., Arkhipova I., Danchin E. G. J., et al. . (2013). Genomic evidence for ameiotic evolution in the bdelloid rotifer Adineta vaga. Nature 500, 453–457. 10.1038/nature12326 PubMed DOI
Friedberg E. C., Meira L. B. (2006). Database of mouse strains carrying targeted mutations in genes affecting biological responses to DNA damage Version 7. DNA Repair 5, 189–209. 10.1016/j.dnarep.2005.09.009 PubMed DOI
Gaut B., Yang L., Takuno S., Eguiarte L. E. (2011). The patterns and causes of variation in plant nucleotide substitution rates. Annu. Rev. Ecol. Evol. Syst. 42, 245–266. 10.1146/annurev-ecolsys-102710-145119 PubMed DOI
Gitzendanner M. A., Soltis P. S., Wong G. K. S., Ruhfel B. R., Soltis D. E. (2018). Plastid phylogenomic analysis of green plants: a billion years of evolutionary history. Am. J. Bot. 105, 291–301. 10.1002/ajb2.1048 PubMed DOI
Givnish T. J., Spalink D., Ames M., Lyon S. P., Hunter S. J., Zuluaga A., et al. . (2015). Orchid phylogenomics and multiple drivers of their extraordinary diversification. Proc. R. Soc. B Biol. Sci. 282, 171–180. 10.1098/rspb.2015.1553 PubMed DOI PMC
Gramlich S., Wagner N. D., Hörandl E. (2018). RAD-seq reveals genetic structure of the F2-generation of natural willow hybrids (Salix L.) and a great potential for interspecific introgression. BMC Plant Biol. 18:317. 10.1186/s12870-018-1552-6 PubMed DOI PMC
He L., Jia K. H., Zhang R. G., Wang Y., Shi T., Le L.i, Z. C., et al. . (2021a). Chromosome-scale assembly of the genome of Salix dunnii reveals a male-heterogametic sex determination system on chromosome 7. Mol. Ecol. Resour. 21, 1966–1982. 10.1101/2020.10.09.333229 PubMed DOI PMC
He L., Wagner N. D., Hörandl E. (2021b). Restriction-site associated DNA sequencing data reveal a radiation of willow species (Salix L., Salicaceae) in the Hengduan Mountains and adjacent areas. J. Syst. Evol. 59, 44–57. 10.1111/jse.12593 DOI
Hörandl E. (1992). Die Gattung Salix in Österreich (mit Berücksichtigung angrenzender Gebiete). Abh. Zool.-Bot. Ges. Österreich 27, 1–170.
Hörandl E., Florineth F., Hadacek F. (2012). Weiden in Österreich und Angrenzenden Gebieten (Willows in Austria and Adjacent Regions), 2nd ed. Vienna: University of Agriculture.
Huang D. I., Hefer C. A., Kolosova N., Douglas C. J., Cronk Q. C. B. (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. 10.1111/nph.12956 PubMed DOI
Huang Y., Wang J., Yang Y., Fan C., Chen J. (2017). Phylogenomic analysis and dynamic evolution of chloroplast genomes in Salicaceae. Front. Plant Sci. 8, 1–13. 10.3389/fpls.2017.01050 PubMed DOI PMC
Jia H., Wang L., Li J., Sun P., Lu M., Hu J. (2020). Physiological and metabolic responses of Salix sinopurpurea and Salix suchowensis to drought stress. Trees Struct. Funct. 34, 563–577. 10.1007/s00468-019-01937-z DOI
Karp A., Hanley S. J., Trybush S. O., Macalpine W., Pei M., Shield I. (2011). Genetic improvement of willow for bioenergy and biofuels. J. Integr. Plant Biol. 53, 151–165. 10.1111/j.1744-7909.2010.01015.x PubMed DOI
Kearse M., Moir R., Wilson A., Stones-Havas S., Cheung M., Sturrock S., et al. . (2012). Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics. 28, 1647–1649. 10.1093/bioinformatics/bts199 PubMed DOI PMC
Khakhlova O., Bock R. (2006). Elimination of deleterious mutations in plastid genomes by gene conversion. Plant J. 46, 85–94. 10.1111/j.1365-313X.2006.02673.x PubMed DOI
Kikuchi S., Bédard J., Hirano M., Hirabayashi Y., Oishi M., Imai M., et al. . (2013). Uncovering the protein translocon at the chloroplast inner envelope membrane. Science 339, 571–574. 10.1126/science.1229262 PubMed DOI
Lauron-Moreau A., Pitre F. E., Argus G. W., Labrecque M., Brouillet L. (2015). Phylogenetic relationships of American willows (Salix L., Salicaceae). PLoS ONE 10:e0121965. 10.1371/journal.pone.0121965 PubMed DOI PMC
Leskinen E., Alström-Rapaport C. (1999). Molecular phylogeny of Salicaceae and closely related Flacourtiaceae: evidence from 5.8 S, ITS 1 and ITS 2 of the rDNA. Plant Syst. Evol. 215, 209–227. 10.1007/BF00984656 DOI
Li M. M., Wang D. Y., Zhang L., Kang M. H., Lu Z. Q., Zhu R., et al. . (2019). Intergeneric relationships within the family Salicaceae s.l. based on plastid phylogenomics. Int. J. Mol. Sci. 20:3788. 10.3390/ijms20153788 PubMed DOI PMC
Lu D., Hao L., Huang H., Zhang G. (2019). The complete chloroplast genome of Salix psamaphila, a desert shrub in northwest China. Mitochondrial DNA Part B Resour. 4, 3432–3433. 10.1080/23802359.2019.1675485 PubMed DOI PMC
McKain M. R., Wilson M. (2017). Fast-Plast: Rapid de novo assembly and finishing for whole chloroplast genomes. Available online at: https://github.com/mrmckain/Fast-Plast
Mower J. P., Stefanovi,ć S., Hao W., Gummow J. S., Jain K., Ahmed D., et al. . (2010). Horizontal acquisition of multiple mitochondrial genes from a parasitic plant followed by gene conversion with host mitochondrial genes. BMC Biol. 8:150. 10.1186/1741-7007-8-150 PubMed DOI PMC
Mu X. Y., Tong L., Sun M., Zhu Y. X., Wen J., Lin Q. W., et al. . (2020). Phylogeny and divergence time estimation of the walnut family (Juglandaceae) based on nuclear RAD-Seq and chloroplast genome data. Mol. Phylogenet. Evol. 147:106802. 10.1016/j.ympev.2020.106802 PubMed DOI
Narango D. L., Tallamy D. W., Shropshire K. J. (2020). Few keystone plant genera support the majority of Lepidoptera species. Nat. Commun. 11, 1–8. 10.1038/s41467-020-19565-4 PubMed DOI PMC
Nargar K., Molina S., Wagner N., Nauheimer L., Micheneau C., Clements M. A. (2018). Australasian orchid diversification in time and space: molecular phylogenetic insights from the beard orchids (Calochilus, Diurideae). Aust. Syst. Bot. 31, 389–408. 10.1071/SB18027 DOI
Oksanen J., Blanchet F. G., Friendly M., Kindt R., Legendre R., McGlinn D., et al. (2019). Vegan: Community Ecology Package. R package version 2.5-6. Available online at: https://CRAN.Rproject.org/package=vegan
Palo R. T. (1984). Distribution of birch (Betula SPP.), willow (Salix SPP.), and poplar (Populus SPP.) secondary metabolites and their potential role as chemical defense against herbivores. J. Chem. Ecol. 10, 499–520. 10.1007/BF00988096 PubMed DOI
Paradis E., Schliep K. (2019). Ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics 35, 526–528. 10.1093/bioinformatics/bty633 PubMed DOI
Parks M., Cronn R., Liston A. (2012). Separating the wheat from the chaff: mitigating the effects of noise in a plastome phylogenomic data set from Pinus L. (Pinaceae). BMC Evol. Biol. 12:100. 10.1186/1471-2148-12-100 PubMed DOI PMC
Percy D. M., Argus G. W., Cronk Q. C., Fazekas A. J., Kesanakurti P. R., Burgess K. S., et al. . (2014). Understanding the spectacular failure of DNA barcoding in willows (Salix): does this result from a trans-specific selective sweep? Mol. Ecol. 23, 4737–4756. 10.1111/mec.12837 PubMed DOI
Pham K. K., Hipp A. L., Manos P. S., Cronn R. C. (2017). A time and a place for everything: phylogenetic history and geography as joint predictors of oak plastome phylogeny. Genome 60, 720–732. 10.1139/gen-2016-0191 PubMed DOI
Piatczak E., Dybowska M., Płuciennik E., Kośla K., Kolniak-ostek J., Kalinowska-lis U. (2020). Identification and accumulation of phenolic compounds in the leaves and bark of Salix alba (L.) and their biological potential. Biomolecules 10, 1–17. 10.3390/biom10101391 PubMed DOI PMC
R Core Team. (2019). R: A Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing. Available online at: https://www.R-project.org/
Rambaut A. (2014). Figtree, A Graphical Viewer of Phylogenetic Trees. Available online at: http://tree.bio.ed.ac.uk/software/figtree
Rieseberg L. H., Soltis D. E. (1991). Phylogenetic consequences of cytoplasmic geneflow in plants. Evol. Trends Plants 5, 65–84.
Ripma L. A., Simpson M. G., Hasenstab-Lehman K. (2014). Geneious! Simplified genome skimming methods for phylogenetic systematic studies: a case study in Oreocarya (Boraginaceae). Appl. Plant Sci. 2:1400062. 10.3732/apps.1400062 PubMed DOI PMC
Savage J. A., Cavender-Bares J. (2012). Habitat specialization and the role of trait lability in structuring diverse willow (genus Salix) communities. Ecology 93, 138–150. 10.1890/11-0406.1 DOI
Shaw J., Lickey E. B., Beck J. T., Farmer S. B., Liu W., Miller J., et al. . (2005). The tortoise and the hare II: relative utility of 21 noncoding chloroplast DNA sequences for phylogenetic analysis. Am. J. Bot. 92, 142–166. 10.3732/ajb.92.1.142 PubMed DOI
Shaw J., Lickey E. B., Schilling E. E., Small R. L. (2007). Comparison of whole chloroplast genome sequences to choose noncoding regions for phylogenetic studies in angiosperms: the Tortoise and the hare III. Am. J. Bot. 94, 275–288. 10.3732/ajb.94.3.275 PubMed DOI
Shi L., Chen H., Jiang M., Wang L., Wu X., Huang L., et al. . (2019). CPGAVAS2, an integrated plastome sequence annotator and analyzer. Nucleic Acids Res. 47, W65–W73. 10.1093/nar/gkz345 PubMed DOI PMC
Skvortsov A. K. (1999). Willows of Russia and adjacent countries, in Taxonomical and Geographical Revision, eds Zinovjev A. G. , Argus G. W. , Tahvanainen J. , Roininen H. (Finland: Joensuu; ).
Smart L. B., Volk T. A., Lin J., Kopp R. F., Phillips I. S., Cameron K. D., et al. . (2005). Genetic improvement of shrub willow (Salix spp.) crops for bioenergy and environmental applications in the United States. Unasylva 56, 51–55.
Stamatakis A. (2014). RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312–1313. 10.1093/bioinformatics/btu033 PubMed DOI PMC
Straub S. C. K., Moore M. J., Soltis P. S., Soltis D. E., Liston A., Livshultz T. (2014). Phylogenetic signal detection from an ancient rapid radiation: effects of noise reduction, long-branch attraction, and model selection in crown clade Apocynaceae. Mol. Phylogenet. Evol. 80, 169–185. 10.1016/j.ympev.2014.07.020 PubMed DOI
Straub S. C. K., Parks M., Weitemier K., Fishbein M., Cronn R. C., Liston A. (2012). Navigating the tip of the genomic iceberg: next-generation sequencing for plant systematics. Am. J. Bot. 99, 349–364. 10.3732/ajb.1100335 PubMed DOI
Suda Y., Argus G. W. (1968). Chromosome numbers of some North American Salix. Brittonia 20, 191–197. 10.2307/2805440 DOI
Taberlet P., Gielly L., Pautou G., Bouvet J. (1991). Universal primers for amplification of three non-coding regions of chloroplast DNA. Plant Mol. Biol. 17, 1105–1109. 10.1007/BF00037152 PubMed DOI
Tuskan G. A., DiFazio S., Jansson S., Bohlmann J., Grigoriev I., Hellsten U., et al. . (2006). The genome of black cottonwood, Populus trichocarpa (Torr. and Gray). Science 313, 1596–604. 10.1126/science.1128691 PubMed DOI
Wagner N. D., Gramlich S., Hörandl E. (2018). RAD sequencing resolved phylogenetic relationships in European shrub willows (Salix L. subg. Chamaetia and subg. Vetrix) and revealed multiple evolution of dwarf shrubs. Ecol. Evol. 8, 8243–8255. 10.1002/ece3.4360 PubMed DOI PMC
Wagner N. D., He L., Hörandl E. (2020). Phylogenomic relationships and evolution of polyploid Salix species revealed by RAD sequencing data. Front. Plant Sci. 11, 1–38. 10.3389/fpls.2020.01077 PubMed DOI PMC
Wagner N. D., He L., Hörandl E. (2021). The evolutionary history, diversity, and ecology of willows (Salix l.) in the European alps. Diversity 13, 1–16. 10.3390/d13040146 DOI
Wicke S., Schneeweiss G. M. (2015). Next-generation organellar genomics: potentials and pitfalls of highthroughput technologies for molecular evolutionary studies and plant systematics, in Next Generation Sequencing in Plant Systematics. Regnum; Vegetabile Book Series of the IAPT (International Association of Plant Taxonomy), eds Hörandl E. , Appelhans M. (Königstein: Koeltz Scientific Books; ). 10.14630/000002 DOI
Wolfe A. D., Randle C. P. (2004). Recombination, heteroplasmy, haplotype polymorphism, and paralogy in plastid genes: implications for plant molecular systematics. Syst. Bot. 29, 1011–1020. 10.1600/0363644042451008 DOI
Wolfe K. H., Li W. H., Sharp P. M. (1987). Rates of nucleotide substitution vary greatly among plant mitochondrial, chloroplast, and nuclear DNAs. Proc. Natl. Acad. Sci. U.S.A. 84, 9054–9058. 10.1073/pnas.84.24.9054 PubMed DOI PMC
Wu D., Wang Y., Zhang L. (2019). The complete chloroplast genome sequence of an economic plant Salix wilsonii. Mitochondrial DNA Part B 4, 3560–3562. 10.1080/23802359.2019.1668311 PubMed DOI PMC
Wu J., Nyman T., Wang D.-C., Argus G. W., Yang Y.-P., Chen J.-H. (2015). Phylogeny of Salix subgenus Salix s.l. (Salicaceae): delimitation, biogeography, and reticulate evolution. BMC Evol. Biol. 15:31. 10.1186/s12862-015-0311-7 PubMed DOI PMC
Yang Z. (2007). PAML 4: phylogenetic analysis by maximum likelihood. Mol. Biol. Evol. 24, 1586–1591. 10.1093/molbev/msm088 PubMed DOI
Zhang L., Xi Z., Wang M., Guo X., Ma T. (2018). Plastome phylogeny and lineage diversification of Salicaceae with focus on poplars and willows. Int. J. Bus. Innov. Res. 17, 7817–7823. 10.1002/ece3.4261 PubMed DOI PMC