Ancient hybridization and repetitive element proliferation in the evolutionary history of the monocot genus Amomum (Zingiberaceae)

. 2024 ; 15 () : 1324358. [epub] 20240419

Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid38708400

Genome size variation is a crucial aspect of plant evolution, influenced by a complex interplay of factors. Repetitive elements, which are fundamental components of genomic architecture, often play a role in genome expansion by selectively amplifying specific repeat motifs. This study focuses on Amomum, a genus in the ginger family (Zingiberaceae), known for its 4.4-fold variation in genome size. Using a robust methodology involving PhyloNet reconstruction, RepeatExplorer clustering, and repeat similarity-based phylogenetic network construction, we investigated the repeatome composition, analyzed repeat dynamics, and identified potential hybridization events within the genus. Our analysis confirmed the presence of four major infrageneric clades (A-D) within Amomum, with clades A-C exclusively comprising diploid species (2n = 48) and clade D encompassing both diploid and tetraploid species (2n = 48 and 96). We observed an increase in the repeat content within the genus, ranging from 84% to 89%, compared to outgroup species with 75% of the repeatome. The SIRE lineage of the Ty1-Copia repeat superfamily was prevalent in most analyzed ingroup genomes. We identified significant difference in repeatome structure between the basal Amomum clades (A, B, C) and the most diverged clade D. Our investigation revealed evidence of ancient hybridization events within Amomum, coinciding with a substantial proliferation of multiple repeat groups. This finding supports the hypothesis that ancient hybridization is a driving force in the genomic evolution of Amomum. Furthermore, we contextualize our findings within the broader context of genome size variations and repeatome dynamics observed across major monocot lineages. This study enhances our understanding of evolutionary processes within monocots by highlighting the crucial roles of repetitive elements in shaping genome size and suggesting the mechanisms that drive these changes.

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Afgan E., Baker D., Batut B., van den Beek M., Bouvier D., Cech M., et al. . (2018). The Galaxy platform for accessible, reproducible and collaborative biomedical analyses: 2018 update. Nucleic Acids Res. 46, W537–W544. doi: 10.1093/nar/gky379 PubMed DOI PMC

Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J. (1990). Basic local alignment search tool. J. Mol. Biol. 215, 403–410. doi: 10.1016/S0022-2836(05)80360-2 PubMed DOI

Beaulieu J. M., Leitch I. J., Patel S., Pendharkar A., Knight C. A. (2008). Genome size is a strong predictor of cell size and stomatal density in angiosperms. New Phytol. 179, 975986. doi: 10.1111/j.1469-8137.2008.02528.x PubMed DOI

Bennetzen J. L., MA J., Devos K. M. (2005). Mechanisms of recent genome size variation in flowering plants. Ann. Bot. 95, 127–132. doi: 10.1093/aob/mci008 PubMed DOI PMC

Bennetzen J. L., Wang H. (2014). The contributions of transposable elements to the structure, function, and evolution of plant genomes. Annu. Rev. Plant Biol. 65, 505–530. doi: 10.1146/annurev-arplant-050213-035811 PubMed DOI

Cao Z., Zhu J., Nakhleh L. (2019). Empirical performance of tree-based inference of phylogenetic networks. 19th Int. Workshop Algorithms Bioinformatics (WABI 2019). Schloss Dagstuhl-Leibniz-Zentrum fuer Informatik. doi: 10.1101/693986 DOI

Carta A., Peruzzi L. (2016). Testing the large genome constraint hypothesis: plant traits, habitat and climate seasonality in liliaceae. New Phytol. 210, 709716. doi: 10.1111/nph.13769 PubMed DOI

Cheng F., Wu J., Wang X. (2014). Genome triplication drove the diversification of Brassica plants. Hortic. Res. 1, 14024. doi: 10.1038/hortres.2014.24 PubMed DOI PMC

D'Hont A., Denoeud F., Aury J. M., et al. . (2012). The banana (Musa acuminata) genome and the evolution of monocotyledonous plants. Nature 488, 213217. doi: 10.1038/nature11241 PubMed DOI

de Boer H., Newman M. F., Poulsen A. D., Fér T., Hien L., Hlavatá K., et al. . (2018). Convergent morphology in Alpinieae (Zingiberaceae): Recircumscribing Amomum as a monophyletic genus. Taxon 67, 6–36. doi: 10.12705/671.2 DOI

de Tomás C., Vicient C. M. (2024). The genomic shock hypothesis: genetic and epigenetic alterations of transposable elements after interspecific hybridization in plants. Epigenomes 8, 2. doi: 10.3390/epigenomes8010002 PubMed DOI PMC

Dodsworth S., Jang T. S., Struebig M., Chase M. W., Weiss-Schneeweiss H., Leitch A. R. (2017). Genome-wide repeat dynamics reflect phylogenetic distance in closely related allotetraploid Nicotiana (Solanaceae). Plant Syst. Evol. 303, 1013–1020. PubMed PMC

Faizullah L., Morton J. A., Hersch-Green E. I., Walczyk A. M., Leitch A. R., Leitch I. J. (2021). Exploring environmental selection on genome size in angiosperms. Trends Plant Sci. 26, 1039–1049. doi: 10.1016/j.tplants.2021.06.001 PubMed DOI

Fér T., Schmickl R. (2018). HybPhyloMaker: target enrichment data analysis from raw reads to species trees. Evol. Bioinform. 14, 1176934317742613. doi: 10.1177/1176934317742613 PubMed DOI PMC

Gaiero P., Vaio M., Peters S. A., Schranz M. E., de Jong H., Speranza P. R. (2019). Comparative analysis of repetitive sequences among species from the potato and the tomato clades. Ann. Bot. 123, 521–532. doi: 10.1093/aob/mcy186 PubMed DOI PMC

Garcia S., Wendel J. F., Borowska-Zuchowska N., Aïnouche M., Kuderova A., Kovarik A. (2020). The utility of graph clustering of 5S ribosomal DNA homoeologs in plant allopolyploids, homoploid hybrids, and cryptic introgressants. Front. Plant Sci. 11. doi: 10.3389/fpls.2020.00041 PubMed DOI PMC

Garrido-Ramos M. A. (Ed.) (2012). Repetitive DNA (Basel; New York: Karger; ).

Ghosh Dasgupta M., Dev S. A., Muneera Parveen A. B., Sarath P., Sreekumar V. B. (2021). Draft genome of Korthalsia laciniosa (Griff.) Mart., a climbing rattan elucidates its phylogenetic position. Genomics 113, 2010–2022. doi: 10.1016/j.ygeno.2021.04.023 PubMed DOI

Giraud D., Lima O., Huteau V., Coriton O., Boutte J., Kovarik A., et al. . (2021). Evolutionary dynamics of transposable elements and satellite DNAs in polyploid Spartina species. Plant Sci. Int. J. Exp. Plant Biol. 302, 110671. doi: 10.1016/j.plantsci.2020.110671 PubMed DOI

Hawkins J. S., Proulx S. R., Rapp R. A., Wendel J. F. (2009). Rapid DNA loss as a counterbalance to genome expansion through retrotransposon proliferation in plants. Proc. Natl. Acad. Sci. U.S.A. 106, 17811–17816. doi: 10.1073/pnas.0904339106 PubMed DOI PMC

Heslop-Harrison J. S., Brandes A., Taketa S., Schmidt T., Vershinin A. V., Alkhimova E. G., et al. . (1997). The chromosomal distributions of Ty1-copia group retrotransposable elements in higher plants and their implications for genome evolution. Genetica 100, 197–204. doi: 10.1023/A:1018337831039 PubMed DOI

Heyduk K., McAssey E. V., Grimwood J., Shu S., Schmutz J., McKain M. R., et al. . (2021). Hybridization history and repetitive element content in the genome of a homoploid hybrid, Yucca gloriosa (Asparagaceae). Front. Plant Sci. 11. doi: 10.3389/fpls.2020.573767 PubMed DOI PMC

Hlavatá K., Leong-Škorničková J., Záveská E., Šída O., Newman M., Mandáková T., et al. . (2023). Phylogenomics and genome size evolution in Amomum s.s. (Zingiberaceae): Comparison of traditional and modern sequencing methods. Mol. Phylogenet. Evol. 178, 107666. doi: 10.1016/j.ympev.2022.107666 PubMed DOI

Hloušková P., Mandáková T., Pouch M., Trávníček P., Lysak M. A. (2019). The large genome size variation in the Hesperis clade was shaped by the prevalent proliferation of DNA repeats and rarer genome downsizing. Ann. Bot. 124, 103–120. doi: 10.1093/aob/mcz036 PubMed DOI PMC

Hodgson J. G., Sharafi M., Jalili A., Díaz S., Montserrat-Martí G., Palmer C., et al. . (2010). Stomatal vs. genome size in angiosperms: the somatic tail wagging the genomic dog? Ann. Bot. 105, 573–584. doi: 10.1093/aob/mcq011 PubMed DOI PMC

Holland B., Moulton V. (2003). “Consensus networks: A method for visualising incompatibilities in collections of trees,” in Algorithms in Bioinformatics. Eds. Benson G., Page R. D. M. (Springer Berlin Heidelberg, Berlin, Heidelberg: ), 165–176.

Hsu C.-C., Chen S.-Y., Lai P.-H., Hsiao Y.-Y., Tsai W.-C., Liu Z.-J., et al. . (2020). Identification of high-copy number long terminal repeat retrotransposons and their expansion in Phalaenopsis orchids. BMC Genomics 21, 807. doi: 10.1186/s12864-020-07221-6 PubMed DOI PMC

Huson D. H., Bryant D. (2006). Application of phylogenetic networks in evolutionary studies. Mol. Biol. Evol. 23, 254–267. doi: 10.1093/molbev/msj030 PubMed DOI

Jansz N. (2019). DNA methylation dynamics at transposable elements in mammals. Essays Biochem. 63, 677–689. doi: 10.1042/EBC20190039 PubMed DOI

Junier T., Zdobnov E. M. (2010). The Newick utilities: high-throughput phylogenetic tree processing in the Unix shell. Bioinformatics 26, 1669–1670. doi: 10.1093/bioinformatics/btq243 PubMed DOI PMC

Keuler R., Garretson A., Saunders T., Erickson R. J., St. Andre N., Grewe F., et al. . (2020). Genome-scale data reveal the role of hybridization in lichen-forming fungi. Sci. Rep. 10, 1497. doi: 10.1038/s41598-020-58279-x PubMed DOI PMC

King D. G., Soller M., Kashi Y. (1997). Evolutionary tuning knobs. Endeavour 21, 36–40. doi: 10.1016/S0160-9327(97)01005-3 DOI

Knight C. A., Molinari N. A., Petrov D. A. (2005). The large genome constraint hypothesis: evolution, ecology and phenotype. Ann. Bot. 95, 177–190. doi: 10.1093/aob/mci011 PubMed DOI PMC

Kumar S., Mohapatra T. (2021). Dynamics of DNA methylation and its functions in plant growth and development. Front. Plant Sci. 12. doi: 10.3389/fpls.2021.596236 PubMed DOI PMC

Lee S.-I., Kim N.-S. (2014). Transposable elements and genome size variations in plants. Genomics Inform. 12, 87–97. doi: 10.5808/GI.2014.12.3.87 PubMed DOI PMC

Li H.-L., Wu L., Dong Z., Jiang Y., Jiang S., Xing H., et al. . (2021). Haplotype-resolved genome of diploid ginger (Zingiber officinale) and its unique gingerol biosynthetic pathway. Hortic. Res. 8, 189. doi: 10.1038/s41438-021-00627-7 PubMed DOI PMC

Liao X., Hu K., Salhi A., Zou Y., Wang J., Gao X. (2022). msRepDB: a comprehensive repetitive sequence database of over 80 000 species. Nucleic Acids Res. 50, D236–D245. doi: 10.1093/nar/gkab1089 PubMed DOI PMC

Liu P., Cuerda-Gil D., Shahid S., Slotkin R. K. (2022). The epigenetic control of the transposable element life cycle in plant genomes and beyond. Annu. Rev. Genet. 56, 63–87. doi: 10.1146/annurev-genet-072920-015534 PubMed DOI

Luo X., Chen S., Zhang Y. (2022). PlantRep: a database of plant repetitive elements. Plant Cell Rep. 41, 1163–1166. doi: 10.1007/s00299-021-02817-y PubMed DOI PMC

Mallet J. (2005). Hybridization as an invasion of the genome. Trends Ecol. Evol. 20, 229–237. doi: 10.1016/j.tree.2005.02.010 PubMed DOI

Mandáková T., Lysák M.A. (2016. a). “Chromosome preparation for cytogenetic analyses in Arabidopsis,” in Current Protocols in Plant Biology. Eds. Stacey G., Birchler J., Ecker J., Martin C. R., Stitt M., Zhou J.-M. (John Wiley & Sons, Inc, Hoboken, NJ, USA: ), 43–51. doi: 10.1002/cppb.20009 PubMed DOI

Mandáková T., Lysák M. A. (2016. b). “Painting of arabidopsis chromosomes with chromosome-specific BAC clones,” in Current Protocols in Plant Biology. Eds. Stacey G., Birchler J., Ecker J., Martin C. R., Stitt M., Zhou J.-M. (John Wiley & Sons, Inc, Hoboken, NJ, USA: ), 359–371. doi: 10.1002/cppb.20022 PubMed DOI

Mehrotra S., Goyal V. (2014). Repetitive sequences in plant nuclear DNA: types, distribution, evolution and function. Genomics Proteomics Bioinf. 12, 164–171. doi: 10.1016/j.gpb.2014.07.003 PubMed DOI PMC

Meudt H. M., Rojas-Andrés B. M., Prebble J. M., Low E., Garnock-Jones P. J., Albach D. C. (2015). Is genome downsizing associated with diversification in polyploid lineages of Veronica ? Bot. J. Linn. Soc 178, 243–266. doi: 10.1111/boj.2015.178.issue-2 DOI

Michalak P. (2009). Epigenetic, transposon and small RNA determinants of hybrid dysfunctions. Heredity 102, 45–50. doi: 10.1038/hdy.2008.48 PubMed DOI

Microsoft Corporation (2018). Microsoft Excel 365. Available at: https://office.microsoft.com/excel.

Moreno-Aguilar M. F., Inda L. A., Sánchez-Rodríguez A., Arnelas I., Catalán P. (2022). Evolutionary dynamics of the repeatome explains contrasting differences in genome sizes and hybrid and polyploid origins of grass loliinae lineages. Front. Plant Sci. 13. doi: 10.3389/fpls.2022.901733 PubMed DOI PMC

Neumann P., Novák P., Hoštáková N., Macas J. (2019). Systematic survey of plant LTR-retrotransposons elucidates phylogenetic relationships of their polyprotein domains and provides a reference for element classification. Mob DNA 10, 1. doi: 10.1186/s13100-018-0144-1 PubMed DOI PMC

Novák P., Ávila Robledillo L., Koblížková A., Vrbová I., Neumann P., Macas J. (2017). TAREAN: a computational tool for identification and characterization of satellite DNA from unassembled short reads. Nucleic Acids Res. 45, e111–e111. doi: 10.1093/nar/gkx257 PubMed DOI PMC

Novák P., Hřibová E., Neumann P., Koblížková A., Doležel J., Macas J. (2014). Genome-wide analysis of repeat diversity across the family musaceae. PloS One 9, e98918. doi: 10.1371/journal.pone.0098918 PubMed DOI PMC

Novák P., Neumann P., Macas J. (2020). Global analysis of repetitive DNA from unassembled sequence reads using RepeatExplorer2. Nat. Protoc. 15, 3745–3776. doi: 10.1038/s41596-020-0400-y PubMed DOI

O’Neill R. J. W., O’Neill M. J., Graves J. A. M. (1998). Undermethylation associated with retroelement activation and chromosome remodelling in an interspecific mammalian hybrid. Nature 393, 68–72. doi: 10.1038/29985 PubMed DOI

Orme D., Freckleton R., Thomas G., Petzoldt T., Fritz S., Isaac N., et al. . (2018) caper: Comparative Analyses of Phylogenetics and Evolution in R. Available at: https://CRAN.R-project.org/package=caper.

Pagel M. (1997). Inferring evolutionary processes from phylogenies. Zool. Scr. 26, 331–348. doi: 10.1111/j.1463-6409.1997.tb00423.x DOI

Pagel M. (1999). Inferring the historical patterns of biological evolution. Nature 401, 877. doi: 10.1038/44766 PubMed DOI

Paradis E., Schliep K. (2019). ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics 35, 526–528. doi: 10.1093/bioinformatics/bty633 PubMed DOI

Pellicer J., Fernández P., Fay M. F., Michálková E., Leitch I. J. (2021). Genome size doubling arises from the differential repetitive DNA dynamics in the genus heloniopsis (Melanthiaceae). Front. Genet. 12. doi: 10.3389/fgene.2021.726211 PubMed DOI PMC

Pellicer J., Hidalgo O., Dodsworth S., Leitch I. J. (2018). Genome size diversity and its impact on the evolution of land plants. Genes 9, 88. doi: 10.3390/genes9020088 PubMed DOI PMC

Pennell M. W., Eastman J. M., Slater G. J., Brown J. W., Uyeda J. C., FitzJohn R. G., et al. . (2014). geiger v2.0: an expanded suite of methods for fitting macroevolutionary models to phylogenetic trees. Bioinformatics 30, 22162218. doi: 10.1093/bioinformatics/btu181 PubMed DOI

Pulido M., Casacuberta J. M. (2023). Transposable element evolution in plant genome ecosystems. Curr. Opin. Plant Biol. 75, 102418. doi: 10.1016/j.pbi.2023.102418 PubMed DOI

Qiao X., Zhang S., Paterson A. H. (2022). Pervasive genome duplications across the plant tree of life and their links to major evolutionary innovations and transitions. Comput. Struct. Biotechnol. J. 20, 3248–3256. doi: 10.1016/j.csbj.2022.06.026 PubMed DOI PMC

R Core Team . (2022). R: A language and environment for statistical computing. Available at: https://www.R-project.org/.

Rebollo R., Horard B., Hubert B., Vieira C. (2010). Jumping genes and epigenetics: Towards new species. Gene 454, 1–7. doi: 10.1016/j.gene.2010.01.003 PubMed DOI

Renny-Byfield S., Kovarik A., Kelly L. J., Macas J., Novak P., Chase M. W., et al. . (2013). Diploidization and genome size change in allopolyploids is associated with differential dynamics of low- and high-copy sequences. Plant J. 74, 829–839. doi: 10.1111/tpj.12168 PubMed DOI

Revell L. J. (2012). phytools: An R package for phylogenetic comparative biology (and other things). Methods Ecol. Evol. 3, 217–233. doi: 10.1111/j.2041-210X.2011.00169.x DOI

Sader M., Vaio M., Cauz dos Santos L., Dornelas M., Vieira M.-L., Melo N., et al. . (2021). Large vs small genomes in Passiflora: the influence of the mobilome and the satellitome. Planta 253. doi: 10.1007/s00425-021-03598-0 PubMed DOI

Schley R. J., Pellicer J., Ge X.-J., Barrett C., Bellot S., Guignard M. S., et al. . (2022). The ecology of palm genomes: repeat-associated genome size expansion is constrained by aridity. New Phytol. 236, 433–446. doi: 10.1111/nph.18323 PubMed DOI PMC

Schrader L., Schmitz J. (2019). The impact of transposable elements in adaptive evolution. Mol. Ecol. 28, 1537–1549. doi: 10.1111/mec.14794 PubMed DOI

Shan X., Liu Z., Dong Z., Wang Y., Chen Y., Lin X., et al. . (2005). Mobilization of the Active MITE Transposons mPing and Pong in Rice by Introgression from Wild Rice (Zizania latifolia Griseb.). Mol. Biol. Evol. 22, 976–990. doi: 10.1093/molbev/msi082 PubMed DOI

Simonin K. A., Roddy A. B. (2018). Genome downsizing, physiological novelty, and the global dominance of flowering plants. PloS Biol. 16, e2003706. doi: 10.1371/journal.pbio.2003706 PubMed DOI PMC

Skopalíková J., Leong-Škorničková J., Šída O., Newman M., Chumová Z., Zeisek V., et al. . (2023). Ancient hybridization in Curcuma (Zingiberaceae)—Accelerator or brake in lineage diversifications? Plant J. 116, 773785. doi: 10.1111/tpj.16408 PubMed DOI

Smit A., Hubley R., Green P. (2013) RepeatMasker open-4.0. Available online at: http://www.repeatmasker.org.

Stamatakis A. (2014). RAxML version 8: A tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 13121313. doi: 10.1093/bioinformatics/btu033 PubMed DOI PMC

Staton S. E., Bakken B. H., Blackman B. K., Chapman M. A., Kane N. C., Tang S., et al. . (2012). The sunflower (Helianthus annuus L.) genome reflects a recent history of biased accumulation of transposable elements. Plant J. 72, 142–153. doi: 10.1111/j.1365-313X.2012.05072.x PubMed DOI

Stull G. W., Pham K. K., Soltis P. S., Soltis D. E. (2023). Deep reticulation: the long legacy of hybridization in vascular plant evolution. Plant J. 114, 743–766. doi: 10.1111/tpj.16142 PubMed DOI

Suguiyama V., Vasconcelos L., Rossi M., Biondo C., Setta N. (2019). The population genetic structure approach adds new insights into the evolution of plant LTR retrotransposon lineages. PloS One 14, e0214542. doi: 10.1371/journal.pone.0214542 PubMed DOI PMC

Sun X., Zhu S., Li N., Cheng Y., Zhao J., Qiao X., et al. . (2020). A Chromosome-Level Genome Assembly of Garlic (Allium sativum) Provides Insights into Genome Evolution and Allicin Biosynthesis. Mol. Plant 13, 1328–1339. doi: 10.1016/j.molp.2020.07.019 PubMed DOI

Than C., Ruths D., Nakhleh L. (2008). PhyloNet: a software package for analyzing and reconstructing reticulate evolutionary relationships. BMC Bioinf. 9, 322. doi: 10.1186/1471-2105-9-322 PubMed DOI PMC

Trávníček P., Čertner M., Ponert J., Chumová Z., Jersáková J., Suda J. (2019). Diversity in genome size and GC content shows adaptive potential in orchids and is closely linked to partial endoreplication, plant life-history traits and climatic conditions. New Phytol. 224, 1642–1656. doi: 10.1111/nph.15996 PubMed DOI

Ungerer M. C., Strakosh S. C., Zhen Y. (2006). Genome expansion in three hybrid sunflower species is associated with retrotransposon proliferation. Curr. Biol. CB 16, R872–R873. doi: 10.1016/j.cub.2006.09.020 PubMed DOI

Venner S., Feschotte C., Biémont C. (2009). Dynamics of transposable elements: towards a community ecology of the genome. Trends Genet. 25, 317–323. doi: 10.1016/j.tig.2009.05.003 PubMed DOI PMC

Vitales D., Garcia S., Dodsworth S. (2020). Reconstructing phylogenetic relationships based on repeat sequence similarities. Mol. Phylogenet. Evol. 147, 106766. doi: 10.1016/j.ympev.2020.106766 PubMed DOI

Wei G., Li X., Fang Y. (2021). Sympatric genome size variation and hybridization of four oak species as determined by flow cytometry genome size variation and hybridization. Ecol. Evol. 11, 1729–1740. doi: 10.1002/ece3.7163 PubMed DOI PMC

Yang Y., Huang L., Xu C., Qi L., Wu Z., Li J., et al. . (2021). Chromosome-scale genome assembly of areca palm (Areca catechu). Mol. Ecol. Resour. 21, 2504–2519. doi: 10.1111/1755-0998.13446 PubMed DOI

Yang P., Zhao H.-Y., Wei J.-S., Zhao Y.-Y., Lin X.-J., Su J., et al. . (2022). Chromosome-level genome assembly and functional characterization of terpene synthases provide insights into the volatile terpenoid biosynthesis of Wurfbainia villosa . Plant J. 112, 630–645. doi: 10.1111/tpj.15968 PubMed DOI

Yin Y., Xie X., Zhou L., Yin X., Guo S., Zhou X., et al. . (2022). A chromosome-scale genome assembly of turmeric provides insights into curcumin biosynthesis and tuber formation mechanism. Front. Plant Sci. 13. doi: 10.3389/fpls.2022.1003835 PubMed DOI PMC

Yu Y., Nakhleh L. (2015). “A distance-based method for inferring phylogenetic networks in the presence of incomplete lineage sorting,” in Harrison R., Li Y., Mãndoiu I. eds. Bioinformatics Research and Applications. ISBRA 2015. . Lecture Notes in Computer Science. (Springer, Cham: ) 9096, 378–389. doi: 10.1007/978-3-319-19048-8_32 DOI

Záveská E., Šída O., Leong-Škorničková J., Chumová Z., Trávníček P., Newman M. F., et al. . (2024). Testing the large genome constraint hypothesis in tropical rhizomatous herbs: life strategies, plant traits and habitat preferences in gingers. Plant J. 117, 12231238. doi: 10.1111/tpj.16559 PubMed DOI

Zhang L., Cao B., Bai C. (2013). New reports of nuclear DNA content for 66 traditional Chinese medicinal plant taxa in China. Caryologia 66, 375–383. doi: 10.1080/00087114.2013.859443 DOI

Zonneveld B., Grimshaw J., Davis A. (2003). The systematic value of nuclear DNA content in galanthus. Plant Syst. Evol. 241, 89102. doi: 10.1007/s00606-003-0016-z DOI

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