Adaptive evolution and co-evolution of chloroplast genomes in Pteridaceae species occupying different habitats: overlapping residues are always highly mutated

Abstract

Background: The evolution of protein residues depends on the mutation rates of their encoding nucleotides, but it may also be affected by co-evolution with other residues. Chloroplasts function as environmental sensors, transforming fluctuating environmental signals into different physiological responses. We reasoned that habitat diversity may affect their rate and mode of evolution, which might be evidenced in the chloroplast genome. The Pteridaceae family of ferns occupy an unusually broad range of ecological niches, which provides an ideal system for analysis.

Results: We conducted adaptive evolution and intra-molecular co-evolution analyses of Pteridaceae chloroplast DNAs (cpDNAs). The results indicate that the residues undergoing adaptive evolution and co-evolution were mostly independent, with only a few residues being simultaneously involved in both processes, and these overlapping residues tend to exhibit high mutations. Additionally, our data showed that Pteridaceae chloroplast genes are under purifying selection. Regardless of whether we grouped species by lineage (which corresponded with ecological niches), we determined that positively selected residues mainly target photosynthetic genes.

Conclusions: Our work provides evidence for the adaptive evolution of Pteridaceae cpDNAs, especially photosynthetic genes, to different habitats and sheds light on the adaptive evolution and co-evolution of proteins.

Keywords: Chloroplast; Intra-molecular co-evolution; Molecular evolution; Protein tertiary structure; Pteridaceae.

Fig. 1

Phylogenetic frame of 41 Pteridaceae species constructed for adaptive evolution and co-evolution analysis. Out.: Outgroup; Park.: Parkerioideae; Pter.: Pteridoideae; Cryp.: Cryptogrammoideae; Chei.: Cheilanthoideae; Vitt.: Vittarioideae. + represents newly added cpDNA samples

Fig. 2

The ω value of each retained protein-coding gene in different foreground clades under the branch model. Purple, blue, and green backgrounds represent genes related to the photosynthetic system, genetic system, and other functions respectively. * marked gene represents significance after p-value correction. Back.: Background clade; Ter.: Terrestrial clade; Aqu.: Aquatic clade; Epi.: Epiphytic clade

Fig. 3

Distribution of positively selected residues and co-evolved residues in the AtpA, AtpB, AtpH, MatK, NdhF, PetB, and RpoB proteins of Pteridaceae. All protein tertiary structures were predicted by homology based on P. arisanensis. Purple represents co-evolution residues, magenta represents adaptive evolution residues, and firebrick red represents both and is labeled accordingly

Fig. 4

The proportion of differential residues in multiple sequence alignment of co-evolved sites, positively selected sites, and overlapping sites between the two