Chloroplast genome expansion by intron multiplication in the basal psychrophilic euglenoid Eutreptiella pomquetensis

Published on Aug 25, 2017in PeerJ 2.12
· DOI :10.7717/peerj.3725
Nadja Dabbagh2
Estimated H-index: 2
,
Matthew S. Bennett11
Estimated H-index: 11
(Michigan State University)
+ 1 AuthorsAngelika Preisfeld2
Estimated H-index: 2
Abstract
BACKGROUND:Over 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. METHODS:The 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 DISCUSSION:With 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.
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  • Citations (3)
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References61
Published on Dec 1, 1992in The EMBO Journal 10.56
D W Copertino1
Estimated H-index: 1
,
S Shigeoka1
Estimated H-index: 1
,
R B Hallick1
Estimated H-index: 1
The chloroplast genes of Euglena gracilis contain more than 60 group II and 47 group III introns. Some Euglena chloroplast genes also contain twintrons, introns-within-introns. Two types of twintrons have previously been described, a group II twintron and a mixed group II/group III twintron. We report that four introns, three within the RNA polymerase subunit gene rpoC1 and one within ribosomal protein gene rpl16, with mean lengths twice typical group III introns, are a new type of twintron. The...
17 Citations Source Cite
Published on Feb 16, 2015in Microbiology spectrum
Alan M. Lambowitz62
Estimated H-index: 62
(University of Texas at Austin),
Marlene Belfort53
Estimated H-index: 53
(State University of New York System)
This review focuses on recent developments in our understanding of group II intron function, the relationships of these introns to retrotransposons and spliceosomes, and how their common features have informed thinking about bacterial group II introns as key elements in eukaryotic evolution. Reverse transcriptase-mediated and host factor-aided intron retrohoming pathways are considered along with retrotransposition mechanisms to novel sites in bacteria, where group II introns are thought to have...
53 Citations Source Cite
Published on Feb 15, 2005in BMC Bioinformatics 2.21
Guy Slater9
Estimated H-index: 9
(European Bioinformatics Institute),
Ewan Birney94
Estimated H-index: 94
(European Bioinformatics Institute)
Background Exhaustive methods of sequence alignment are accurate but slow, whereas heuristic approaches run quickly, but their complexity makes them more difficult to implement. We introduce bounded sparse dynamic programming (BSDP) to allow rapid approximation to exhaustive alignment. This is used within a framework whereby the alignment algorithms are described in terms of their underlying model, to allow automated development of efficient heuristic implementations which may be applied to a ge...
919 Citations Source Cite
Published on Nov 1, 2015in Journal of Eukaryotic Microbiology 2.54
Matthew S. Bennett11
Estimated H-index: 11
(Michigan State University),
Richard E. Triemer25
Estimated H-index: 25
(Michigan State University)
Over the last few years multiple studies have been published outlining chloroplast genomes that represent many of the photosynthetic euglenid genera. However, these genomes were scattered throughout the euglenophyceaean phylogenetic tree, and focused on comparisons with Euglena gracilis. Here, we present a study exclusively on taxa within the Euglenaceae. Six new chloroplast genomes were characterized, those of Cryptoglena skujai, E. gracilis var. bacillaris, Euglena viridis, Euglenaria anabaena...
22 Citations Source Cite
Published on Mar 1, 2009in Molecular Biology and Evolution 10.22
Monique Turmel41
Estimated H-index: 41
(Laval University),
Marie-Christine Gagnon1
Estimated H-index: 1
(Laval University)
+ 2 AuthorsClaude Lemieux45
Estimated H-index: 45
(Laval University)
Because they represent the earliest divergences of the Chlorophyta and include the smallest known eukaryotes (e.g., the coccoid Ostreococcus), the morphologically diverse unicellular green algae making up the Prasinophyceae are central to our understanding of the evolutionary patterns that accompanied the radiation of chlorophytes and the reduction of cell size in some lineages. Seven prasinophyte lineages, four of which exhibit a coccoid cell organization (no flagella nor scales), were uncovere...
142 Citations Source Cite
Published on Mar 20, 2012in PLOS ONE 2.77
Štěpánka Hrdá4
Estimated H-index: 4
(Charles University in Prague),
Jan Fousek6
Estimated H-index: 6
(Academy of Sciences of the Czech Republic)
+ 2 AuthorsCestmir Vlcek30
Estimated H-index: 30
(Academy of Sciences of the Czech Republic)
Euglenids are a group of protists that comprises species with diverse feeding modes. One distinct and diversified clade of euglenids is photoautotrophic, and its members bear green secondary plastids. In this paper we present the plastid genome of the euglenid Eutreptiella, which we assembled from 454 sequencing of Eutreptiella gDNA. Comparison of this genome and the only other available plastid genomes of photosynthetic euglenid, Euglena gracilis, revealed that they contain a virtually identica...
36 Citations Source Cite
Published on Mar 1, 1999in Journal of Eukaryotic Microbiology 2.54
Eric W. Linton10
Estimated H-index: 10
(Rutgers University),
Dana Hittner1
Estimated H-index: 1
(Rutgers University)
+ 2 AuthorsRichard E. Triemer25
Estimated H-index: 25
(Rutgers University)
The euglenoids are an ancient and extremely diverse lineage of eukaryotic flagellates with unclear relationships among taxa. Synapomorphies for the euglenoids include a surface pellicle and a closed mitosis with a series of separate sub-spindles. The taxonomy currently in use is inconsistent with the available data and needs revision. Most euglenoid phylogenies are largely intuitive reconstructions based on a limited number of morphological characters. Therefore, we have added molecular characte...
54 Citations Source Cite
Published on Jan 1, 1995in Nucleic Acids Research 11.56
Michael D. Thompson2
Estimated H-index: 2
,
Donald W. Copertino6
Estimated H-index: 6
+ 2 AuthorsRichard B. Hallick23
Estimated H-index: 23
Abstract The origin of present day introns is a subject of spirited debate. Any intron evolution theory must account for not only nuclear spliceosomal introns but also their antecedents. The evolution of group II introns is fundamental to this debate, since group II introns are the proposed progenitors of nuclear spliceosomal introns and are found in ancient genes from modern organisms. We have studied the evolution of chloroplast introns and twintrons (introns within introns) in the genus Eugle...
40 Citations Source Cite
Published on Dec 1, 2000in Protist 2.70
Gaby Gockel2
Estimated H-index: 2
(University of Bonn),
Wolfgang Hachtel14
Estimated H-index: 14
(University of Bonn)
Summary Astasia longa is a colourless heterotrophic flagellate closely related to the photoautotrophic Euglena gracilis . A circular 73 kb plastid DNA (ptDNA) has been isolated from A. longa that is about half the size of the chloroplast DNA of E. gracilis (143 kb). We have determined the complete sequence of the ptDNA of A. longa and established a complete gene map. All chloroplast genes for photosynthesis-related proteins are completely absent from the A. longa plastid DNA except for rbc L, th...
92 Citations Source Cite
Cited By3
Published on Dec 1, 2018in Scientific Reports 4.12
Anna Karnkowska5
Estimated H-index: 5
(University of Warsaw),
Matthew S. Bennett11
Estimated H-index: 11
(Michigan State University),
Richard E. Triemer25
Estimated H-index: 25
(Michigan State University)
Photosynthetic euglenids (Euglenophyta) are a monophyletic group of unicellular eukaryotes characterized by the presence of plastids, which arose as the result of the secondary endosymbiosis. Many Euglenophyta plastid (pt) genomes have been characterized recently, but they represented mainly one family – Euglenaceae. Here, we report a comparative analysis of plastid genomes from eight representatives of the family Phacaceae. Newly sequenced plastid genomes share a number of features including sy...
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Published on Dec 1, 2018in Scientific Reports 4.12
Abdullah Zubaer2
Estimated H-index: 2
(University of Manitoba),
Alvan Wai3
Estimated H-index: 3
(University of Manitoba),
Georg Hausner24
Estimated H-index: 24
(University of Manitoba)
Endoconidiophora resinifera (=Ceratocystis resinifera) is a blue-stain fungus that occurs on conifers. The data showed that the Endoconidiophora resinifera mitochondrial genome is one of the largest mitochondrial genomes (>220 kb) so far reported among members of the Ascomycota. An exceptional large number of introns (81) were noted and differences among the four strains were restricted to minor variations in intron numbers and a few indels and single nucleotide polymorphisms. The major differen...
1 Citations Source Cite