Complete plastome sequence of (Ranunculaceae) and transfer of the gene to the nucleus in the ancestor of the subfamily Thalictroideae

Abstract

Background: Plastids originated from cyanobacteria and the majority of the ancestral genes were lost or functionally transferred to the nucleus after endosymbiosis. Comparative genomic investigations have shown that gene transfer from plastids to the nucleus is an ongoing evolutionary process but molecular evidence for recent functional gene transfers among seed plants have only been documented for the four genes, accD, infA, rpl22 and rpl32. Results: The complete plastid genome of , the first from the subfamily Thalictroideae (Ranunculaceae), was sequenced and revealed the losses of two genes, and . The functional transfer of these two genes to the nucleus in was verified by examination of nuclear transcriptomes. A survey of the phylogenetic distribution of the loss was performed using 17 species of and representatives of related genera in the subfamily Thalictroideae. The plastid-encoded gene is likely nonfunctional in members of the subfamily Thalictroideae (Aquilegia, Enemion, Isopyrum, Leptopyrum, Paraquilegia, and Semiaquilegia) including 17 species due to the presence of indels that disrupt the reading frame. A nuclear-encoded with high sequence identity was identified in both and The phylogenetic distribution of this gene loss/transfer and the high level of sequence similarity in transit peptides suggest a single transfer of the plastid-encoded to the nucleus in the ancestor of the subfamily Thalictroideae approximately 20-32 Mya. Conclusions: The genome sequence of provides valuable information for improving the understanding of the evolution of plastid genomes within Ranunculaceae and across angiosperms. is unusual among the three sequenced Ranunculaceae plastid genomes in the loss of two genes and , which have been functionally transferred to the nucleus. In the case of this represents the third documented independent transfer from the plastid to the nucleus with the other two transfers occurring in the unrelated angiosperm families Rhizophoraceae and Salicaceae. Furthermore, the transfer of provides additional molecular evidence for the monophyly of the subfamily Thalictroideae.