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

Richard G J Hodel; Elizabeth A Zimmer; Bin-Bin Liu; Jun Wen

doi:10.3389/fpls.2021.820997

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

Front Plant Sci. 2022 Jan 25:12:820997. doi: 10.3389/fpls.2021.820997. eCollection 2021.

Authors

Richard G J Hodel¹, Elizabeth A Zimmer¹, Bin-Bin Liu^{1

2}, Jun Wen¹

Affiliations

¹ Department of Botany, National Museum of Natural History, Smithsonian Institution, Washington, DC, United States.
² State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences, Beijing, China.

Abstract

Plant biologists have debated the evolutionary origin of the apple tribe (Maleae; Rosaceae) for over a century. The "wide-hybridization hypothesis" posits that the pome-bearing members of Maleae (base chromosome number x = 17) resulted from a hybridization and/or allopolyploid event between progenitors of other tribes in the subfamily Amygdaloideae with x = 8 and x = 9, respectively. An alternative "spiraeoid hypothesis" proposed that the x = 17 of Maleae arose via the genome doubling of x = 9 ancestors to x = 18, and subsequent aneuploidy resulting in x = 17. We use publicly available genomic data-448 nuclear genes and complete plastomes-from 27 species representing all major tribes within the Amygdaloideae to investigate evolutionary relationships within the subfamily containing the apple tribe. Specifically, we use network analyses and multi-labeled trees to test the competing wide-hybridization and spiraeoid hypotheses. Hybridization occurred between an ancestor of the tribe Spiraeeae (x = 9) and an ancestor of the clade Sorbarieae (x = 9) + Exochordeae (x = 8) + Kerrieae (x = 9), giving rise to the clade Gillenieae (x = 9) + Maleae (x = 17). The ancestor of the Maleae + Gillenieae arose via hybridization between distantly related tribes in the Amygdaloideae (i.e., supporting the wide hybridization hypothesis). However, some evidence supports an aspect of the spiraeoid hypothesis-the ancestors involved in the hybridization event were likely both x = 9, so genome doubling was followed by aneuploidy to result in x = 17 observed in Maleae. By synthesizing existing genomic data with novel analyses, we resolve the nearly century-old mystery regarding the origin of the apple tribe. Our results also indicate that nuclear gene tree-species tree conflict and/or cytonuclear conflict are pervasive at several other nodes in subfamily Amygdaloideae of Rosaceae.

Keywords: allopolyploidy; ancient hybridization; cytonuclear conflict; genome doubling; phylogenetic networks; phylogenomics; reticulate evolution.