Abstract

BackgroundOver the last few years multiple studies have been published showing a great diversity in size of chloroplast genomes (cpGenomes), and in the arrangement of gene clusters, in the Euglenales. However, while these genomes provided important insights into the evolution of cpGenomes across the Euglenales and within their genera, only two genomes were analyzed in regard to genomic variability between and within Euglenales and Eutreptiales. To better understand the dynamics of chloroplast genome evolution in early evolving Eutreptiales, this study focused on the cpGenome of Eutreptiella pomquetensis, and the spread and peculiarities of introns.MethodsThe Etl. pomquetensis cpGenome was sequenced, annotated and afterwards examined in structure, size, gene order and intron content. These features were compared with other euglenoid cpGenomes as well as those of prasinophyte green algae, including Pyramimonas parkeae.Results and DiscussionWith about 130,561 bp the chloroplast genome of Etl. pomquetensis, a basal taxon in the phototrophic euglenoids, was considerably larger than the two other Eutreptiales cpGenomes sequenced so far. Although the detected quadripartite structure resembled most green algae and plant chloroplast genomes, the gene content of the single copy regions in Etl. pomquetensis was completely different from those observed in green algae and plants. The gene composition of Etl. pomquetensis was extensively changed and turned out to be almost identical to other Eutreptiales and Euglenales, and not to P. parkeae. Furthermore, the cpGenome of Etl. pomquetensis was unexpectedly permeated by a high number of introns, which led to a substantially larger genome. The 51 identified introns of Etl. pomquetensis showed two major unique features: (i) more than half of the introns displayed a high level of pairwise identities; (ii) no group III introns could be identified in the protein coding genes. These findings support the hypothesis that group III introns are degenerated group II introns and evolved later.

Highlights

  • Recent analyses of chloroplast genomes have been largely used to retrace evolutionary steps of phototrophic euglenoids

  • The genome was composed of a large single copy region (LSC 80,941 bp), a small single copy region (SSC 39,856 bp) and two inverted repeats (IR) containing the rRNA genes in a way similar to O. tauri, but different in gene content (Figs. 1A & 1B)

  • This can be seen by high pairwise identities in coding regions with the putative chloroplast ancestor P. parkeae and a typical green algae and land plant quadripartite genome structure

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Summary

Introduction

Recent analyses of chloroplast genomes (cpGenomes) have been largely used to retrace evolutionary steps of phototrophic euglenoids. Fitting into a scheme of increasing intron quantity and genome size, the invasion of introns in euglenoids was assumed to have started with very low intron numbers and as a consequence small cpGenomes in Eutreptiales, which both increased during diversification of photosynthetic euglenoids (Bennett & Triemer, 2015; Hrdá et al, 2012; Thompson et al, 1995; Wiegert, Bennett & Triemer, 2012) This hypothesis was initially corroborated by the fact that in Pyramimonas parkeae, as the closest living relative of the euglenoid plastid, only one intron was detected (Turmel et al, 2009). These findings support the hypothesis that group III introns are degenerated group II introns and evolved later

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