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

Published on Aug 25, 2017in PeerJ 2.35
· DOI :10.7717/peerj.3725
Nadja Dabbagh2
Estimated H-index: 2
,
Matthew S. Bennett11
Estimated H-index: 11
(MSU: Michigan State University)
+ 1 AuthorsAngelika Preisfeld2
Estimated H-index: 2
Cite
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.
  • References (61)
  • Citations (3)
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References61
Newest
Published on Jun 1, 2017in Journal of Phycology 2.83
Matthew S. Bennett11
Estimated H-index: 11
(MSU: Michigan State University),
Shin Han Shiu43
Estimated H-index: 43
(MSU: Michigan State University),
Richard E. Triemer25
Estimated H-index: 25
(MSU: Michigan State University)
4 Citations Source Cite
Published on Jan 1, 2017in Journal of Eukaryotic Microbiology 2.36
Nadja Dabbagh2
Estimated H-index: 2
,
Angelika Preisfeld2
Estimated H-index: 2
A comparative analysis of the chloroplast genome of Euglena mutabilis underlined a high diversity in the evolution of plastids in euglenids. Gene clusters in more derived Euglenales increased in complexity with only a few, but remarkable changes in the genus Euglena. Euglena mutabilis differed from other Euglena species in a mirror-inverted arrangement of 12 from 15 identified clusters, making it very likely that the emergence at the base of the genus Euglena, which has been considered a long br...
7 Citations Source Cite
Published on Oct 25, 2016in PeerJ 2.35
Jean-Simon Brouard6
Estimated H-index: 6
(Laval University),
Monique Turmel41
Estimated H-index: 41
(Laval University)
+ 1 AuthorsClaude Lemieux45
Estimated H-index: 45
(Laval University)
Background. The chloroplast genome sustained extensive changes in architecture during the evolution of the Chlorophyceae, a morphologically and ecologically diverse class of green algae belonging to the Chlorophyta; however, the forces driving these changes are poorly understood. The five orders recognized in the Chlorophyceae form two major clades: the CS clade consisting of the Chlamydomonadales and Sphaeropleales, and the OCC clade consisting of the Oedogoniales, Chaetophorales, and Chaetopel...
6 Citations Source Cite
Published on Sep 1, 2016in Genome Biology and Evolution 3.73
Monique Turmel41
Estimated H-index: 41
(Laval University),
Christian Otis34
Estimated H-index: 34
(Laval University),
Claude Lemieux45
Estimated H-index: 45
(Laval University)
To probe organelle genome evolution in the Ulvales/Ulotrichales clade, the newly sequenced chloroplast and mitochondrial genomes of Gloeotilopsis planctonica and Gloeotilopsis sarcinoidea (Ulotrichales) were compared with those of Pseudendoclonium akinetum (Ulotrichales) and of the few other green algae previously sampled in the Ulvophyceae. At 105,236 bp, the G. planctonica mitochondrial DNA (mtDNA) is the largest mitochondrial genome reported so far among chlorophytes, whereas the 221,431-bp G...
9 Citations Source Cite
Published on Jun 1, 2016in Journal of Phycology 2.83
Beth A. Kasiborski1
Estimated H-index: 1
(CMU: Central Michigan University),
Matthew S. Bennett11
Estimated H-index: 11
(MSU: Michigan State University),
Eric W. Linton10
Estimated H-index: 10
(CMU: Central Michigan University)
8 Citations Source Cite
Published on Nov 1, 2015in Journal of Eukaryotic Microbiology 2.36
Matthew S. Bennett11
Estimated H-index: 11
(MSU: Michigan State University),
Richard E. Triemer25
Estimated H-index: 25
(MSU: 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 Feb 16, 2015in Microbiology spectrum
Alan M. Lambowitz65
Estimated H-index: 65
(University of Texas at Austin),
Marlene Belfort55
Estimated H-index: 55
(SUNY: 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...
54 Citations Source Cite
Published on Jan 1, 2014in Phycologia 1.98
Matthew S. Bennett11
Estimated H-index: 11
(MSU: Michigan State University),
Krystle E. Wiegert5
Estimated H-index: 5
(MSU: Michigan State University),
Richard E. Triemer25
Estimated H-index: 25
(MSU: Michigan State University)
Euglena proxima is a common, globally dispersed, and easily identified photosynthetic euglenoid. Previous phylogenetic analyses using nuclear-encoded small subunit (SSU) and large subunit (LSU) rRNA genes revealed that this taxon was paraphyletic with other Euglena species and was positioned as sister to all Euglenaceae. Despite this, authors were reluctant to remove this taxon from Euglena until additional data, or taxa pairing with E. proxima, were obtained because it created a monotypic genus...
20 Citations Source Cite
Published on Mar 1, 2013in Journal of Eukaryotic Microbiology 2.36
Krystle E. Wiegert5
Estimated H-index: 5
(MSU: Michigan State University),
Matthew S. Bennett11
Estimated H-index: 11
(MSU: Michigan State University),
Richard E. Triemer25
Estimated H-index: 25
(MSU: Michigan State University)
The chloroplast genomes of two photosynthetic euglenoids, Colacium vesiculosum Ehrenberg (128,889 bp), and Strombomonas acuminata (Schmarda) Deflandre (144,167 bp) have been sequenced. These chloroplast genomes in combination with those of Euglena gracilis, Eutreptia viridis, and Eutreptiella gymnastica provide a snapshot of euglenoid chloroplast evolution allowing comparisons of gene content, arrangement, and expansion. The gene content of the five chloroplast genomes is very similar varying on...
18 Citations Source Cite
Published on Jan 1, 2013in Nucleic Acids Research 11.15
Sarah W. Burge4
Estimated H-index: 4
(HHMI: Howard Hughes Medical Institute),
Jennifer Daub21
Estimated H-index: 21
(HHMI: Howard Hughes Medical Institute)
+ 6 AuthorsAlex Bateman67
Estimated H-index: 67
(HHMI: Howard Hughes Medical Institute)
The Rfam database (available via the website at http://rfam.sanger.ac.uk and through our mirror at http://rfam.janelia.org) is a collection of non-coding RNA families, primarily RNAs with a conserved RNA secondary structure, including both RNA genes and mRNA cis-regulatory elements. Each family is represented by a multiple sequence alignment, predicted secondary structure and covariance model. Here we discuss updates to the database in the latest release, Rfam 11.0, including the introduction of...
505 Citations Source Cite
Cited By3
Newest
Published on Dec 1, 2018in Scientific Reports 4.01
Anna Karnkowska6
Estimated H-index: 6
(University of Warsaw),
Matthew S. Bennett11
Estimated H-index: 11
(MSU: Michigan State University),
Richard E. Triemer25
Estimated H-index: 25
(MSU: 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...
1 Citations Source Cite
Published on Dec 1, 2018in Scientific Reports 4.01
Abdullah Zubaer2
Estimated H-index: 2
(UM: University of Manitoba),
Alvan Wai3
Estimated H-index: 3
(UM: University of Manitoba),
Georg Hausner24
Estimated H-index: 24
(UM: 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