Rapid structural evolution of Dendrobium mitogenomes and mito‐nuclear phylogeny discordances in Dendrobium (Orchidaceae)

• Published in: Journal of systematics and evolution : JSE 2023-09, Vol.61 (5), p.790-805
• Main Authors: Wang, Meng‐Ting, Hou, Zhen‐Yu, Li, Chao, Yang, Jia‐Peng, Niu, Zhi‐Tao, Xue, Qing‐Yun, Liu, Wei, Ding, Xiao‐Yu
• Format: Article
• Language: English
• Subjects: Angiosperms; Bats; Biological evolution; Chromosomes; Dendrobium; Deoxyribonucleic acid; Discordance; DNA; Evolution; Evolutionary genetics; Gene mapping; Genes; Genomes; Hybridization; Isoforms; Mitochondrial DNA; mitochondrial genome; Network analysis; phylogenetic discordance; Phylogeny; Species; structural evolution; Variation
• ISSN: 1674-4918; 1759-6831
• DOI: 10.1111/jse.12912

Reconstructing mitochondrial genomes of angiosperms is extremely intricate due to frequent recombinations which give rise to varied sized in Dendrobium mitogenomes and their structural variations, even in most orchid species. In this study, we first sequenced two complete and five draft mitochondrial genomes of Dendrobium using next‐generation and third‐generation sequencing technologies. The mitochondrial genomes were 420 538–689 048 bp long, showing multipartite (multichromosomal) structures that consisted of variably sized circular or linear‐mapping isoforms (chromosomes). The comparison of mitochondrial genomes showed frequent gene losses in Dendrobium species. To explore structure variations of mitochondrial genomes in vivo, we quantified copy numbers of five mitochondrial genes and DNA contents per mitochondrion. The gene copy numbers and the DNA contents showed extreme differences during Dendrobium development, suggesting dynamic structures of mitochondrial genomes. Furthermore, phylogenetic relationships of 97 accessions from 39 Dendrobium species were constructed based on 12 nuclear single‐copy genes and 15 mitochondrial genes. We discovered obvious discordance between the nuclear and mitochondrial trees. Reticulate evolution was inferred from the species network analysis in Dendrobium. Our findings revealed the rapid structural evolution of Dendrobium mitochondrial genomes and the existence of hybridization events in Dendrobium species, which provided new insights into in vivo structural variations of plant mitochondrial genomes and the strong potential of mitochondrial genes in deciphering plant evolution history. Mitochondrial genomes of Dendrobium showed multichromosomal structures with variably sized circular or linear isoforms. Mitochondrial protein‐coding genes underwent frequent lost events in Dendrobium species. The structures of mitochondrial genomes were dynamic during Dendrobium development. The mitochondrial tree and the nuclear tree displayed obvious phylogenetic discordances in Dendrobium.