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Allopolyploidy and genomic differentiation in holocentric species of the Eleocharis montana complex (Cyperaceae)

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Abstract

Polyploidy and hybridization are key events in plant evolution. Due to these events, complexes of species can be formed. Dysploidy, a frequent chromosome change in holocentric organisms, may add some difficulties to species delimitation, especially in Cyperaceae. The Eleocharis montana complex is known for its members with overlapping morpho-anatomical features and unclear circumscription. To understand its biological history, several tools were used to investigate different American populations, including morpho-anatomical analysis, genome size estimates, cytogenomic analysis, molecular marker characterization, and genomic in situ hybridization (GISH). Despite overlapping morphological features, it was possible to separate two groups, the first containing E. parodii and E. subarticulata, presenting diploid and dysploid karyotypes, respectively, and small DNA C-values. The second contained E. elegans, E. contracta, and E. montana, with large genomes created by polyploidy. All analyses suggest that E. montana with 2n = 40 is a cytotype of E. contracta with 2n = 20, and both evolved from a natural hybridization involving E. parodii (2n = 10) and a second progenitor that is yet unknown. Furthermore, the GISH results indicated that E. parodii may be an ancestor of E. elegans. All species occur in the probable center of diversification in Austral South America, where the hybridization zone is identified. Fieldwork and information obtained from herbaria indicate that diploid and dysploid species (E. subarticulata and E. parodii) do not occur beyond the center of diversification. However, E. elegans and specially E. montana occur more widely, occupying different flooded environments and landscapes.

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Acknowledgements

The authors thank the Brazilian agencies FINEP, Fundação Araucária, CNPq, CAPES, and ProPPG-UEL for their financial support. We thank also the Department of Structural Biology, Molecular, and Genetics from Universidade Estadual de Ponta Grossa for technical support. The authors declare no conflict of interest within this article. A.L.L. Vanzela and R. Trevisan thank CNPq for the productivity scholarship (numbers 309902/2018-5 and 313306/2018-4, respectively).

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L. Johnen, T.B. de Souza, and D. M. Rocha performed all the experiments, wrote and corrected the manuscript. M. S. González-Elizondo and R. Trevisan were responsible for species identifications, support for morphological analyses and for manuscript corrections. S.R. Chaluvadi and J.L. Bennetzen performed the genomic sequencing, supported the bioinformatic analysis, and edited the manuscript. A.L.L. Vanzela designed the study, checked the data analyses, and organized, wrote, and corrected the manuscript.

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Correspondence to André L. L. Vanzela.

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Handling Editor: Martin A. Lysak.

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Information on Electronic Supplementary Material

Supplementary materials include list of species with samples localities and maps, images of achenes morphological analysis, anatomical sections of culms, dendrograms and DNA sequences, and comparative tables and graphs of composition of the repetitive DNA families. All these information complements the results presented in the main text.

Online Resource 1. Data for the Eleocharis montana complex sampled in this study.

Online Resource 2. Geographic localization of the collected populations of Eleocharis parodii, E. contracta, E. elegans, E. montana, and E. subarticulata from Brazilian regions.

Online Resource 3. Sequence alignment used in genetic relationship analysis.

Online Resource 4. Species differentiation using achene shapes and borders.

Online Resource 5. Comparison of morphological features using a distance matrix by the UPGMA method.

Online Resource 6. Measurements of diagnostic morphological structures of Eleocharis montana.

Online Resource 7. Culm anatomies of Eleocharis montana, E. elegans, E. contracta, E. subarticulata, and E. parodii, stained with 0.05% toluidine blue.

Online Resource 8. DNA C-value estimates for the Eleocharis montana complex.

Online Resource 9. Distribution of repetitive DNA elements on the assembled genomes of Eleocharis parodii (2n = 10), E. elegans (2n = 20) and E. montana (2n = 40).

Online Resource 10. In silico microsatellite scanning in three Eleocharis datasets.

Online Resource 11. Phylogeny based on Roalson et al. (2010), using the Brazilian Eleocharis montana complex species (Subgenus Eleocharis), plus E. acutangula (subg. Limnochloa) as an outgroup.

Online Resource 12. Comparison of trees using partial 35S rDNA and chloroplast (petN-psbM and trnC-ycf6) sequences.

Online Resource 13. Dendrogram concatenating data of partial 35S rDNA and chloroplast genes, molecular markers and morphological features using the Mesquite tool.

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Johnen, L., de Souza, T.B., Rocha, D.M. et al. Allopolyploidy and genomic differentiation in holocentric species of the Eleocharis montana complex (Cyperaceae). Plant Syst Evol 306, 39 (2020). https://doi.org/10.1007/s00606-020-01666-8

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  • DOI: https://doi.org/10.1007/s00606-020-01666-8

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