Radiation history of Asian Asarum (sect. Heterotropa, Aristolochiaceae) resolved using a phylogenomic approach based on double-digested RAD-seq data.

Asarum Heterotropa East Asia Japan archipelago Taiwan biogeographic history reconstruction double-digested RAD-seq phylogenetic resolution phylogenomics species radiation

Journal

Annals of botany
ISSN: 1095-8290
Titre abrégé: Ann Bot
Pays: England
ID NLM: 0372347

Informations de publication

Date de publication:
24 07 2020
Historique:
received: 20 01 2020
accepted: 11 04 2020
pubmed: 15 4 2020
medline: 3 10 2020
entrez: 15 4 2020
Statut: ppublish

Résumé

The genus Asarum sect. Heterotropa (Aristolochiaceae) probably experienced rapid diversification into 62 species centred on the Japanese Archipelago and Taiwan, providing an ideal model for studying island adaptive radiation. However, resolving the phylogeny of this plant group using Sanger sequencing-based approaches has been challenging. To uncover the radiation history of Heterotropa, we employed a phylogenomic approach using double-digested RAD-seq (ddRAD-seq) to yield a sufficient number of phylogenetic signals and compared its utility with that of the Sanger sequencing-based approach. We first compared the performance of phylogenetic analysis based on the plastid matK and trnL-F regions and nuclear ribosomal internal transcribed spacer (nrITS), and phylogenomic analysis based on ddRAD-seq using a reduced set of the plant materials (83 plant accessions consisting of 50 species, one subspecies and six varieties). We also conducted more thorough phylogenomic analyses including the reconstruction of biogeographic history using comprehensive samples of 135 plant accessions consisting of 54 species, one subspecies, nine varieties of Heterotropa and six outgroup species. Phylogenomic analyses of Heterotropa based on ddRAD-seq were superior to Sanger sequencing-based approaches and resulted in a fully resolved phylogenetic tree with strong support for 72.0-84.8 % (depending on the tree reconstruction methods) of the branches. We clarified the history of Heterotropa radiation and found that A. forbesii, the only deciduous Heterotropa species native to mainland China, is sister to the evergreen species (core Heterotropa) mostly distributed across the Japanese Archipelago and Taiwan. The core Heterotropa group was divided into nine subclades, each of which had a narrow geographic distribution. Moreover, most estimated dispersal events (22 out of 24) were between adjacent areas, indicating that the range expansion has been geographically restricted throughout the radiation history. The findings enhance our understanding of the remarkable diversification of plant lineages in the Japanese Archipelago and Taiwan.

Sections du résumé

BACKGROUND AND AIMS
The genus Asarum sect. Heterotropa (Aristolochiaceae) probably experienced rapid diversification into 62 species centred on the Japanese Archipelago and Taiwan, providing an ideal model for studying island adaptive radiation. However, resolving the phylogeny of this plant group using Sanger sequencing-based approaches has been challenging. To uncover the radiation history of Heterotropa, we employed a phylogenomic approach using double-digested RAD-seq (ddRAD-seq) to yield a sufficient number of phylogenetic signals and compared its utility with that of the Sanger sequencing-based approach.
METHODS
We first compared the performance of phylogenetic analysis based on the plastid matK and trnL-F regions and nuclear ribosomal internal transcribed spacer (nrITS), and phylogenomic analysis based on ddRAD-seq using a reduced set of the plant materials (83 plant accessions consisting of 50 species, one subspecies and six varieties). We also conducted more thorough phylogenomic analyses including the reconstruction of biogeographic history using comprehensive samples of 135 plant accessions consisting of 54 species, one subspecies, nine varieties of Heterotropa and six outgroup species.
KEY RESULTS
Phylogenomic analyses of Heterotropa based on ddRAD-seq were superior to Sanger sequencing-based approaches and resulted in a fully resolved phylogenetic tree with strong support for 72.0-84.8 % (depending on the tree reconstruction methods) of the branches. We clarified the history of Heterotropa radiation and found that A. forbesii, the only deciduous Heterotropa species native to mainland China, is sister to the evergreen species (core Heterotropa) mostly distributed across the Japanese Archipelago and Taiwan.
CONCLUSIONS
The core Heterotropa group was divided into nine subclades, each of which had a narrow geographic distribution. Moreover, most estimated dispersal events (22 out of 24) were between adjacent areas, indicating that the range expansion has been geographically restricted throughout the radiation history. The findings enhance our understanding of the remarkable diversification of plant lineages in the Japanese Archipelago and Taiwan.

Identifiants

pubmed: 32285123
pii: 5819776
doi: 10.1093/aob/mcaa072
pmc: PMC7380484
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

245-260

Informations de copyright

© The Author(s) 2020. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.

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Auteurs

Yudai Okuyama (Y)

Tsukuba Botanical Garden, National Museum of Nature and Science, Tsukuba, Ibaraki, Japan.

Nana Goto (N)

The Nature Conservation Society of Japan (NACS-J), Tokyo, Japan.
Makino Herbarium, Tokyo Metropolitan University, Hachioji, Tokyo, Japan.

Atsushi J Nagano (AJ)

Faculty of Agriculture, Department of Plant Life Sciences, Ryukoku University, Otsu, Shiga, Japan.

Masaki Yasugi (M)

Center for Ecological Research, Kyoto University, Otsu, Shiga, Japan.
Faculty of Engineering, Utsunomiya University, Utsunomiya, Tochigi, Japan.

Goro Kokubugata (G)

Tsukuba Botanical Garden, National Museum of Nature and Science, Tsukuba, Ibaraki, Japan.

Hiroshi Kudoh (H)

Center for Ecological Research, Kyoto University, Otsu, Shiga, Japan.

Zhechen Qi (Z)

College of Life Sciences and Medicine, Zhejiang Sci-Tech University, Hangzhou, Zhejiang, China.

Takuro Ito (T)

Tsukuba Botanical Garden, National Museum of Nature and Science, Tsukuba, Ibaraki, Japan.
Graduate School of Agriculture, Kyoto University, Kyoto, Japan.

Satoshi Kakishima (S)

Tsukuba Botanical Garden, National Museum of Nature and Science, Tsukuba, Ibaraki, Japan.

Takashi Sugawara (T)

Makino Herbarium, Tokyo Metropolitan University, Hachioji, Tokyo, Japan.

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Classifications MeSH