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

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, hundreds of single-copy nuclear (SCN) genes (785) and complete plastomes (75) 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 involved in known and suspected hybridization and allopolyploidy events. The nuclear phylogeny recovered the monophyly of Malus s.l. (including Docynia); however, it was supported to be biphyletic in the plastid phylogeny. An ancient chloroplast capture event best explains the cytonuclear discordance that occurred in the Eocene in western North America. Our conflict analysis demonstrated that ILS, hybridization, and allopolyploidy could explain the widespread nuclear gene tree discordance. We detected one deep hybridization event (Malus doumeri) involving the ancestor of pome-bearing species and Docynia delavayi, and one recent hybridization event (Malus coronaria) between M. sieversii and a combined clade of M. ioensis and M. angustifolia. Furthermore, our historical biogeographic analysis combining living and fossil species supported a widespread East Asian-western North American origin of Malus s.l., followed by a series of extinction events in the Eocene in northern East Aisa and western North America. This study provides a valuable evolutionary framework for the breeding and crop improvement of apples and their close relatives.

Synthesis of Nuclear and Chloroplast Data Combined With Network Analyses Supports the Polyploid Origin of the Apple Tribe and the Hybrid Origin of the Maleae—Gillenieae Clade

“…Furthermore, within the Rosaceae, many relationships between tribes were inconsistent between the nuclear and chloroplast genomes, such as the placement of all tribes within the Rosoideae except for Ulmarieae ( Xiang et al, 2017 ; Zhang et al, 2017 ). Cytonuclear conflict also exists within the Rosaceae at shallower systematic scales (e.g., within the tribe Maleae; Liu et al, 2019 , 2020a , b , 2021 ).…”

“…The time is ripe to re-evaluate these hypotheses using analyses that consider phylogenomic data from both nuclear and chloroplast genomes, and methodologies that explicitly incorporate discordance and/or reticulation into phylogenies. As researchers obtain more DNA sequence data from both the nuclear and chloroplast genomes, it is becoming increasingly clear that cytonuclear conflict is prevalent in many plant lineages ( Huang et al, 2014 ; Bruun-Lund et al, 2017 ; Lee-Yaw et al, 2018 ; Hodel et al, 2021 ; Liu et al, 2021 ; Wang et al, 2021 ; Xu et al, 2021 ). Here, we limit our focus to studying and resolving cytonuclear conflict within the Amygdaloideae.…”

Phylogenomics and the flowering plant tree of life

“…Recent phylogenomic studies are refreshing our understanding of relationships at lower taxonomic scales, such as at subfamilial level of Pooideae (Poaceae; Zhang et al, 2022); at tribal level of Andropogoneae (Welker et al, 2020) and Arundinarieae Guo et al, 2021a) within Poaceae; at the subtribal level of Saussureinae (Asteraceae; Herrando-Moraira et al, 2020); at generic level of the Alchemilla (Rosaceae; Morales-Briones et al, 2022), the Bambusa-Dendrocalamus-Gigantochloa (BDG) complex (Poaceae; Liu et al, 2020a), Begonia (Begoniaceae; Li et al, 2022), Carex (Cyperaceae; Villaverde et al, 2020), Lachemilla (Rosaceae; Morales-Briones et al, 2018), Magnolia (Magnoliaceae; Dong et al, 2022a), Malus (Liu et al, 2022), Prunus (Hodel et al, 2021), and Rosa (Debray et al, 2022) within Rosaceae, and Rhododendron (Ericaceae; Xia et al, 2021); at sectional level of the Passiflora sect. Decaloba (Passifloraceae; Acha et al, 2021), Primula sect.…”