J Integr Plant Biol ›› 2022, Vol. 64 ›› Issue (5): 1020-1043.DOI: 10.1111/jipb.13246

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  • 收稿日期:2021-12-02 接受日期:2022-03-08 出版日期:2022-05-01 发布日期:2022-05-19

Phylogenomic conflict analyses in the apple genus Malus s.l. reveal widespread hybridization and allopolyploidy driving diversification, with insights into the complex biogeographic history in the Northern Hemisphere

Bin‐Bin Liu1,2, Chen Ren3,4, Myounghai Kwak5, Richard G.J. Hodel2, Chao Xu1, Jian He6, Wen‐Bin Zhou7, Chien‐Hsun Huang8, Hong Ma9, Guan‐Ze Qian10, De‐Yuan Hong1* and Jun Wen2*   

  1. 1 State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, the Chinese Academy of Sciences, Beijing 100093, China
    2 Department of Botany, National Museum of Natural History, Smithsonian Institution, PO Box 37012, Washington 20013–7012, DC, USA
    3 Key Laboratory of Plant Resources Conservation and Sustainable Utilization, South China Botanical Garden, The Chinese Academy of Sciences, Guangzhou 510650, China
    4 Guangdong Provincial Key Laboratory of Applied Botany, South China Botanical Garden, The Chinese Academy of Sciences, Guangzhou 510650, China
    5 National Institute of Biological Resources, Incheon 22689, South Korea
    6 School of Ecology and Nature Conservation, Beijing Forestry University, Beijing 100083, China
    7 Department of Plant and Microbial Biology, North Carolina State University, Raleigh 27965, NC, USA
    8 State Key Laboratory of Genetic Engineering and Collaborative Innovation Center of Genetics and Development, Ministry of Education Key Laboratory of Biodiversity and Ecological Engineering, Institute of Plant Biology, Center of Evolutionary Biology, School of Life Sciences, Fudan University, Shanghai 200433, China
    9 Department of Biology, Huck Institutes of the Life Sciences, Pennsylvania State University, 510D Mueller Laboratory, University Park, Pennsylvania 16802, USA
    10 College of Life Sciences, Liaocheng University, Liaocheng 252059, China

    *    Correspondence: Jun Wen (wenj@si.edu, Dr. Wen is fully responsible for the distribution of the materials associated with this article); De-Yuan Hong (hongdy@ibcas.ac.cn)
  • Received:2021-12-02 Accepted:2022-03-08 Online:2022-05-01 Published:2022-05-19

Abstract:

Phylogenomic evidence from an increasing number of studies has demonstrated that different data sets and analytical approaches often reconstruct strongly supported but conflicting relationships. In this study, 785 single-copy nuclear genes and 75 complete plastomes were used to infer the phylogenetic relationships and estimate the historical biogeography of the apple genus Malus sensu lato, an economically important lineage disjunctly distributed in the Northern Hemisphere and involved in known and suspected hybridization and allopolyploidy events. The nuclear phylogeny recovered the monophyly of Malus s.l. (including Docynia); however, the genus was supported to be biphyletic in the plastid phylogeny. An ancient chloroplast capture event in the Eocene in western North America best explains the cytonuclear discordance. Our conflict analysis demonstrated that ILS, hybridization, and allopolyploidy could explain the widespread nuclear gene tree discordance. One deep hybridization event (Malus doumeri) and one recent event (Malus coronaria) were detected in Malus s.l. Furthermore, our historical biogeographic analysis integrating living and fossil data supported a widespread East Asian-western North American origin of Malus s.l. in the Eocene, followed by several extinction and dispersal events in the Northern Hemisphere. We also propose a general workflow for assessing phylogenomic discordance and biogeographic analysis using deep genome skimming data sets.

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