Abundant RNA editing sites of chloroplast protein-coding genes in Ginkgo biloba and an evolutionary pattern analysis

Abstract

BackgroundRNA editing is a posttranscriptional modification process that alters the RNA sequence so that it deviates from the genomic DNA sequence. RNA editing mainly occurs in chloroplasts and mitochondrial genomes, and the number of editing sites varies in terrestrial plants. Why and how RNA editing systems evolved remains a mystery. Ginkgo biloba is one of the oldest seed plants and has an important evolutionary position. Determining the patterns and distribution of RNA editing in the ancient plant provides insights into the evolutionary trend of RNA editing, and helping us to further understand their biological significance.ResultsIn this paper, we investigated 82 protein-coding genes in the chloroplast genome of G. biloba and identified 255 editing sites, which is the highest number of RNA editing events reported in a gymnosperm. All of the editing sites were C-to-U conversions, which mainly occurred in the second codon position, biased towards to the U_A context, and caused an increase in hydrophobic amino acids. RNA editing could change the secondary structures of 82 proteins, and create or eliminate a transmembrane region in five proteins as determined in silico. Finally, the evolutionary tendencies of RNA editing in different gene groups were estimated using the nonsynonymous-synonymous substitution rate selection mode.ConclusionsThe G. biloba chloroplast genome possesses the highest number of RNA editing events reported so far in a seed plant. Most of the RNA editing sites can restore amino acid conservation, increase hydrophobicity, and even influence protein structures. Similar purifying selections constitute the dominant evolutionary force at the editing sites of essential genes, such as the psa, some psb and pet groups, and a positive selection occurred in the editing sites of nonessential genes, such as most ndh and a few psb genes.Electronic supplementary materialThe online version of this article (doi:10.1186/s12870-016-0944-8) contains supplementary material, which is available to authorized users.

The complete plastome of macaw palm [Acrocomia aculeata (Jacq.) Lodd. ex Mart.] and extensive molecular analyses of the evolution of plastid genes in Arecaceae

“…From the total sites, 87 are shared among all species sampled in this study and 74 are completely or partially edited in C. nucifera (Huang et al, 2013), which suggest high conservation of the RNA editing mechanism within Arecoideae. Interestingly, most RNA editing sites predicted here change the encoded amino acid from polar to apolar, increasing the protein hydrophobicity which can affect structural features such as the creation of new transmembrane regions (He et al 2016;Chen et al 2017). Thereby, the general editing process is biased towards to increase the hydrophobicity of plastid proteins, which may be involved in protein-protein interactions and transmembrane domains present in the plastid protein complexes.…”

“…In this study, a total of 100 RNA editing sites were predicted to occur within the subfamily Arecoideae. Like most angiosperms, all editing sites identified are C-to-U conversions, at the first or second position of the codons (Takenaka et al 2013;He et al 2016). RNA editing sites at the third position of the codon are less common, generally resulting in synonymous substitutions and having low frequency (He et al 2016;Chen et al 2017).…”

“…Like most angiosperms, all editing sites identified are C-to-U conversions, at the first or second position of the codons (Takenaka et al 2013;He et al 2016). RNA editing sites at the third position of the codon are less common, generally resulting in synonymous substitutions and having low frequency (He et al 2016;Chen et al 2017). From the total sites, 87 are shared among all species sampled in this study and 74 are completely or partially edited in C. nucifera (Huang et al, 2013), which suggest high conservation of the RNA editing mechanism within Arecoideae.…”

“…The mechanism of RNA editing has a monophyletic origin beginning with the evolution of land plants, when hundreds of editing sites were created in basal lineages. Following the evolution of higher plants several RNA editing sites were lost maintaining a relative conserved number of editing sites in angiosperms (Tillich et al 2006;Takenaka et al 2013;He et al 2016). Plastid RNA editing sites have been identified in mRNA, introns, and untranslated regions, being implicated primordially as error correctors, but also acting in regulatory functions and producing variants of proteins to adapt to different physiological needs (Takenaka et al 2013;Tseng et al 2013;He et al 2016;Chen et al 2017).…”

“…Nevertheless, the diversification rate over time within palm genera seems to increase and a convergent evolution has been reported among palm species adapted to shaded areas (Ma et al 2015;Faurby et al 2016). Despite most plastid genes are conserved, several evolutionary events have been described such as new RNA editing sites, loss of introns, high divergence of genes, and positive signatures (Sen et al 2012;Williams et al 2015;He et al 2016;Chen et al 2017). In grasses, one-third of the plastid genes underwent positive selection, which shows a relationship between gene evolution and environmental conditions regarding the photosynthetic apparatus (Piot et al 2017).…”