Plastome phylogenomics of Allaeanthus, Broussonetia and Malaisia (Dorstenieae, Moraceae) and the origin of B. × kazinoki

Kuo, Wen-Hsi; Liu, Shih-Hui; Chang, Chiung-Chih; Hsieh, Chia-Lun; Li, Yi-Hsuan; Ito, Takuro; Won, Hyosig; Kokubugata, Goro; Chung, Kuo-Fang

doi:10.1007/s10265-022-01369-w

Regular Paper – Taxonomy/Phylogenetics/Evolutionary Biology
Published: 26 January 2022

Plastome phylogenomics of Allaeanthus, Broussonetia and Malaisia (Dorstenieae, Moraceae) and the origin of B. × kazinoki

Journal of Plant Research volume 135, pages 203–220 (2022)Cite this article

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Abstract

Species of Broussonetia have been essential in the development of papermaking technology. In Japan and Korea, a hybrid between B. monoica and B. papyrifera (= B. × kazinoki) known as kōzo and daknamu is still the major source of raw materials for making traditional paper washi and hanji, respectively. Despite their cultural and practical significance, however, the origin and taxonomy of kōzo and daknamu remain controversial. Additionally, the long-held generic concept of Broussonetia s.l., which included Sect. Allaeanthus and Sect. Broussonetia, was challenged as phylogenetic analyses showed Malaisia is sister to the latter section. To re-examine the taxonomic proposition that recognizes Allaeanthus, Broussonetia, and Malaisia (i.e., Broussonetia alliance), plastome and nuclear ribosomal DNA (nrDNA) sequences of six species of the alliance were assembled. Characterized by the canonical quadripartite structure, genome alignments and contents of the six plastomes (160,121–162,594 bp) are highly conserved, except for the pseudogenization and/or loss of the rpl22 gene. Relationships of the Broussonetia alliance are identical between plastome and nrDNA trees, supporting the maintenance of Malaisia and the resurrection of Allaeanthus. The phylogenomic relationships also indicate that the monoecy in B. monoica is a derived state, possibly resulting from hybridization between the dioecious B. kaempferi (♀) and B. papyrifera (♂). Based on the hypervariable ndhF-rpl32 intergenic spacer selected by sliding window analysis, phylogeographic analysis indicates that B. monoica is the sole maternal parent of B. × kazinoki and that daknamu carries multiple haplotypes, while only one haplotype was detected in kōzo. Because hybridizations between B. monoica and B. papyrifera are unidirectional and have occurred rarely in nature, our data suggest that daknamu might have originated via deliberate hybrid breeding selected for making hanji in Korea. On the contrary, kōzo appears to have a single origin and the possibility of a Korean origin cannot be ruled out.

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12 March 2022
A Correction to this paper has been published: https://doi.org/10.1007/s10265-022-01382-z

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Acknowledgements

The authors thank Harvard University Herbaria (HUH) and Herbarium of Biodiversity Research Center, Academia Sinica (HAST) for permission to sample the herbarium specimens and curators of the Herbaria of National Museum of Nature and Science (TNS) and Tohoku University (TUS) for assistances during the visit. The hospitality of Shiroishi City government, Kurafuto Shiroishi, and Endo Tadao’s Family are deeply appreciated. K.-F. Chung’s travel to HUH was supported by 2016 Sargent Award for Visiting Scholar, Arnold Arboretum, Harvard University. We also thank two anonymous reviewers for constructive suggestions for the manuscript, Trevor Padgett for improving the writing, and Preecha Karaket, Danilo N. Tandang, and Pi-Fong Lu for permission to use their photographs. This study was supported by the Thematic Research Program grant of Academia Sinica (AS-TP-107-L18 AS-ASCDC-107-304) and a grant of the Minister of Science and Technology (MOST 109-2621-B-001-005-MY2) to K.-F. Chung.

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Research Museum and Herbarium (HAST), Biodiversity Research Center, Academia Sinica, Taipei, 115201, Taiwan
Wen-Hsi Kuo, Chiung-Chih Chang, Chia-Lun Hsieh, Yi-Hsuan Li & Kuo-Fang Chung
Department of Biology, Washington University, St. Louis, MO, USA
Wen-Hsi Kuo
Department of Biological Sciences, National Sun Yat- sen University, Kaohsiung, Taiwan
Shih-Hui Liu
The Center for Academic Resources and Archives/Botanical Gardens, Tohoku University, Sendai, Miyagi, Japan
Takuro Ito
Department of Biological Science and Institute of Natural Sciences, Daegu University, Gyungsan, Gyungbuk, South Korea
Hyosig Won
Department of Botany, National Museum of Nature and Science, Tsukuba, Ibaraki, Japan
Goro Kokubugata

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Chiung-Chih Chang
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Chia-Lun Hsieh
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Yi-Hsuan Li
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Takuro Ito
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Hyosig Won
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Goro Kokubugata
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Kuo-Fang Chung
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Correspondence to Kuo-Fang Chung.

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The original online version of this article is revised due to electronic supplementary files were incorrectly cross linked with different supplementary files and corrected in this version.

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Supplementary Material 1 Figs. S1–S4.

Supplementary Material 2 Tables S1–S4.

Supplementary Material 3 Alignment of unique haplotypes.

Supplementary Material 4 The R source code for haplotype, AMOVA, and G_ST analyses and visualization.

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Kuo, WH., Liu, SH., Chang, CC. et al. Plastome phylogenomics of Allaeanthus, Broussonetia and Malaisia (Dorstenieae, Moraceae) and the origin of B. × kazinoki. J Plant Res 135, 203–220 (2022). https://doi.org/10.1007/s10265-022-01369-w

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Received: 26 August 2021
Accepted: 11 January 2022
Published: 26 January 2022
Issue Date: March 2022
DOI: https://doi.org/10.1007/s10265-022-01369-w

Keywords

Asymmetrical hybridization
daknamu
Homoploid
kōzo
Phylogeography
Traditional papermaking