Comparative organelle genome analysis of the sister genera Ceratocephala and Myosurus (Ranunculaceae) reveals fast evolutionary rates in arid and aquatic environments.

BACKGROUND: Longer branches in phylogenetic trees usually correspond to accelerated evolutionary rates. However, little is known about the potential correlation between accelerated evolution rates of organisms and their adapation to novel environments. Here, we sampled representative species of Ranunculeae in different habitats, including two xerophytic Ceratocephala species, two hydrophytic Myosurus species, and six mesophytic species from other four genera within the tribe. By an integration of phylogenomic, comparative genomic, and evolutionary rate analyses, we identified fast-evolving genes (FSGs) of organelle genomes in Ceratocephala and Myosurus and explored their relationships with adaptation to dry and aquatic habitats, respectively. RESULTS: The Ceratocephala-Myosurus clade originated at 33.01 Ma and began to diversify at 24.43 Ma. A total of nine plastid FSGs (ndhB, ndhD, rpoB, rpoC1, rps3, rps7, rps11, ycf1, ycf4) and two mitochondrial FSGs (ccmFC, nad6) were identified as shared by Ceratocephala and Myosurus. Ceratocephala has four unique plastid FSGs (rps4, petD, psbH, rpl22) and two unique mitochondrial FSGs (ccmB, nad4); Myosurus has three unique plastid FSGs (ndhA, psbC, rpl32) and one unique mitochondrial FSG (atp1). The predicted protein structure of ycf1 is obviously different among Ceratocephala, Myosurus, and Ranunculus. The predicted protein structures of rps4 and ccmFC in Ceratocephala markedly differ from those in Ranunculus. CONCLUSIONS: Plastid (rpo-, rps-, rpl-) and mitochondrial (nad-, ccm-) genes constitute the predominant functional categories within the FSGs, implying that they may play an important role in adaptation to specific habitats. The Ceratocephala-specific six FSGs and predicted protein structural changes of ycf1, rps4 and ccmFC may be related to the adaptation of this genus to dry habitats in the late Oligocene. The Myosurus-specific four FSGs and predicted protein structural change of ycf1 may be associated with the adaptation of this genus to aquatic habitats. These findings suggest that the increases in evolutionary rates and predicted protein structural changes of organelle genes may facilitate organisms to adapt specific habitats.