scholarly journals Gene fragmentation and RNA editing without borders: eccentric mitochondrial genomes of diplonemids

2020 ◽  
Vol 48 (5) ◽  
pp. 2694-2708 ◽  
Author(s):  
Binnypreet Kaur ◽  
Kristína Záhonová ◽  
Matus Valach ◽  
Drahomíra Faktorová ◽  
Galina Prokopchuk ◽  
...  

Abstract Diplonemids are highly abundant heterotrophic marine protists. Previous studies showed that their strikingly bloated mitochondrial genome is unique because of systematic gene fragmentation and manifold RNA editing. Here we report a comparative study of mitochondrial genome architecture, gene structure and RNA editing of six recently isolated, phylogenetically diverse diplonemid species. Mitochondrial gene fragmentation and modes of RNA editing, which include cytidine-to-uridine (C-to-U) and adenosine-to-inosine (A-to-I) substitutions and 3′ uridine additions (U-appendage), are conserved across diplonemids. Yet as we show here, all these features have been pushed to their extremes in the Hemistasiidae lineage. For example, Namystynia karyoxenos has its genes fragmented into more than twice as many modules than other diplonemids, with modules as short as four nucleotides. Furthermore, we detected in this group multiple A-appendage and guanosine-to-adenosine (G-to-A) substitution editing events not observed before in diplonemids and found very rarely elsewhere. With >1,000 sites, C-to-U and A-to-I editing in Namystynia is nearly 10 times more frequent than in other diplonemids. The editing density of 12% in coding regions makes Namystynia’s the most extensively edited transcriptome described so far. Diplonemid mitochondrial genome architecture, gene structure and post-transcriptional processes display such high complexity that they challenge all other currently known systems.

PeerJ ◽  
2020 ◽  
Vol 8 ◽  
pp. e9309
Author(s):  
Viktoria Yu Shtratnikova ◽  
Mikhail I. Schelkunov ◽  
Aleksey A. Penin ◽  
Maria D. Logacheva

Heterotrophic plants—plants that have lost the ability to photosynthesize—are characterized by a number of changes at all levels of organization. Heterotrophic plants are divided into two large categories—parasitic and mycoheterotrophic (MHT). The question of to what extent such changes are similar in these two categories is still open. The plastid genomes of nonphotosynthetic plants are well characterized, and they exhibit similar patterns of reduction in the two groups. In contrast, little is known about the mitochondrial genomes of MHT plants. We report the structure of the mitochondrial genome of Hypopitys monotropa, a MHT member of Ericaceae, and the expression of its genes. In contrast to its highly reduced plastid genome, the mitochondrial genome of H. monotropa is larger than that of its photosynthetic relative Vaccinium macrocarpon, and its complete size is ~810 Kb. We observed an unusually long repeat-rich structure of the genome that suggests the existence of linear fragments. Despite this unique feature, the gene content of the H. monotropa mitogenome is typical of flowering plants. No acceleration of substitution rates is observed in mitochondrial genes, in contrast to previous observations in parasitic non-photosynthetic plants. Transcriptome sequencing revealed the trans-splicing of several genes and RNA editing in 33 of 38 genes. Notably, we did not find any traces of horizontal gene transfer from fungi, in contrast to plant parasites, which extensively integrate genetic material from their hosts.


2019 ◽  
Vol 374 (1786) ◽  
pp. 20190100 ◽  
Author(s):  
Jeremy G. Wideman ◽  
Gordon Lax ◽  
Guy Leonard ◽  
David S. Milner ◽  
Raquel Rodríguez-Martínez ◽  
...  

Euglenozoa comprises euglenids, kinetoplastids, and diplonemids, with each group exhibiting different and highly unusual mitochondrial genome organizations. Although they are sister groups, kinetoplastids and diplonemids have very distinct mitochondrial genome architectures, requiring widespread insertion/deletion RNA editing and extensive trans -splicing, respectively, in order to generate functional transcripts. The evolutionary history by which these differing processes arose remains unclear. Using single-cell genomics, followed by small sub unit ribosomal DNA and multigene phylogenies, we identified an isolated marine cell that branches on phylogenetic trees as a sister to known kinetoplastids. Analysis of single-cell amplified genomic material identified multiple mitochondrial genome contigs. These revealed a gene architecture resembling that of diplonemid mitochondria, with small fragments of genes encoded out of order and or on different contigs, indicating that these genes require extensive trans -splicing. Conversely, no requirement for kinetoplastid-like insertion/deletion RNA-editing was detected. Additionally, while we identified some proteins so far only found in kinetoplastids, we could not unequivocally identify mitochondrial RNA editing proteins. These data invite the hypothesis that extensive genome fragmentation and trans -splicing were the ancestral states for the kinetoplastid-diplonemid clade but were lost during the kinetoplastid radiation. This study demonstrates that single-cell approaches can successfully retrieve lineages that represent important new branches on the tree of life, and thus can illuminate major evolutionary and functional transitions in eukaryotes. This article is part of a discussion meeting issue ‘Single cell ecology’.


2018 ◽  
Author(s):  
Ji Haishuo ◽  
Xu Xiaofeng ◽  
Jin Xiufeng ◽  
Cheng Zhi ◽  
jin Hong ◽  
...  

In this study, we used a small RNA sequencing (sRNA-seq) based method to annotate the mitochondrial genome of the insect Erthesina fullo Thunberg at 1 bp resolution. Most of the new annotations were consistent with the previous annotations which were obtained using PacBio full-length transcripts. Two important findings are that animals transcribe both entire strands of mitochondrial genomes and the tandem repeat in the control region of the E. fullo mitochondrial genome contains the repeated Transcription Initiation Sites (TISs) of the H-strand. In addition, we found that the copy numbers of tandem repeats showed a great diversity within an individual, enriching the fundamental knowledge of mitochondrial biology. This sRNA-seq based method uses 5′ and 3′ end small RNAs to annotate nuclear non-coding and mitochondrial genes at 1 bp resolution and can also be used to identify new steady-state RNAs, particularly long non-coding RNAs (lncRNAs). Animal mitochondrial genomes containing one control region only encode two steady-state lncRNAs, which are the Mitochondrial D-loop 1 (MDL1) and its antisense gene (MDL1AS), while all other reported mitochondrial lncRNAs could be degraded fragments of transient RNAs or random breaks during experimental processing. The high-resolution annotations of mitochondrial genomes can be used to study the phylogenetics and molecular evolution of animals or to investigate mitochondrial gene transcription, RNA processing, RNA maturation and several other related topics.


Genome ◽  
2009 ◽  
Vol 52 (4) ◽  
pp. 299-307 ◽  
Author(s):  
Grzegorz Bartoszewski ◽  
Piotr Gawronski ◽  
Marek Szklarczyk ◽  
Henk Verbakel ◽  
Michael J. Havey

Cucumber ( Cucumis sativus ) has one of the largest mitochondrial genomes known among all eukaryotes, due in part to the accumulation of short 20 to 60 bp repetitive DNA motifs. Recombination among these repetitive DNAs produces rearrangements affecting organization and expression of mitochondrial genes. To more efficiently identify rearrangements in the cucumber mitochondrial DNA, we built two nonoverlapping 800 and 220 kb BAC contigs and assigned major mitochondrial genes to these BACs. Polymorphism carried on the largest BAC contig was used to confirm paternal transmission. Mitochondrial genes were distributed across BACs and physically distant, although occasional clustering was observed. Introns in the nad1, nad4, and nad7 genes were larger than those reported in other plants, due in part to accumulation of short repetitive DNAs and indicating that increased intron sizes contributed to mitochondrial genome expansion in cucumber. Mitochondrial genes atp6 and atp9 are physically close to each other and cotranscribed. These physical contigs will be useful for eventual sequencing of the cucumber mitochondrial DNA, which can be exploited to more efficiently screen for unique rearrangements affecting mitochondrial gene expression.


2018 ◽  
Author(s):  
Helena Štorchová ◽  
James D. Stone ◽  
Daniel B. Sloan ◽  
Oushadee Abeyawardana ◽  
Karel Müller ◽  
...  

AbstractBackgroundSilene vulgaris (bladder campion) is a gynodioecious species existing as two genders – male-sterile females and hermaphrodites. Cytoplasmic male sterility (CMS) is generally encoded by mitochondrial genes, which interact with nuclear fertility restorer genes. Mitochondrial genomes of this species vary in DNA sequence, gene order and gene content. Multiple CMS genes are expected to exist in S. vulgaris, but little is known about their molecular identity.ResultsWe assembled the complete mitochondrial genome from the haplotype KRA of S. vulgaris. It consists of five chromosomes, two of which recombine with each other. Two small non-recombining chromosomes exist in linear, supercoiled and relaxed circle forms. We compared the mitochondrial transcriptomes from females and hermaphrodites and confirmed the differentially expressed chimeric gene bobt as the strongest CMS candidate gene in S. vulgaris KRA. The chimeric gene bobt is co-transcribed with the Cytochrome b (cob) gene in some genomic configurations. The co-transcription of a CMS factor with an essential gene may constrain transcription inhibition as a mechanism for fertility restoration because of the need to maintain appropriate production of the necessary protein. Homologous recombination places the gene cob outside the control of bobt, which allows for the suppression the CMS gene by the fertility restorer genes. In addition, by analyzing RNA editing, we found the loss of three editing sites in the KRA mitochondrial genome and identified four sites with highly distinct editing rates between KRA and another S. vulgaris haplotypes (KOV). Three of these highly differentially edited sites were located in the transport membrane protein B (mttB) gene. They resulted in differences in MttB protein sequences between haplotypes despite completely identical gene sequences.ConclusionsFrequent homologous recombination events that are widespread in plant mitochondrial genomes may change chromosomal configurations and also the control of gene transcription including CMS gene expression. Posttranscriptional processes, e.g RNA editing shall be evaluated in evolutionary and co-evolutionary studies of mitochondrial genes, because they may change protein composition despite the sequence identity of the respective genes. The investigation of natural populations of wild species such as S. vulgaris are necessary to reveal important aspects of CMS missed in domesticated crops, the traditional focus of the CMS studies.


2018 ◽  
Author(s):  
Sergio N Stampar ◽  
Michael B Broe ◽  
Jason Macrander ◽  
Adam M Reitzel ◽  
Marymegan Daly

Sequences and structural attributes of mitochondrial genomes have played a key role in the clarification of relationships among Cnidaria, a key phylum of early-diverging animals. Among the major lineages of Cnidaria, Ceriantharia ("tube anemones") remains one of the most enigmatic groups in terms of its phylogenetic position. We sequenced the mitochondrial genomes of two ceriantharians to see whether the complete organellar genome would provide more support for the phylogenetic placement of Ceriantharia. For both ceriantharian species studied, the mitochondrial gene sequences could not be assembled into a circular genome. Instead, our analyses suggest both species have fragmented mitochondrial genomes consisting of multiple linear fragments. Linear mitogenomes are characteristic of members of Medusozoa, one of the major lineages of Cnidaria, but are unreported for Anthozoa, which includes the Ceriantharia. The number of fragments and the variation in gene order between species is much greater in Ceriantharia than among Medusozoa. The novelty of the mitogenomic structure in Ceriantharia highlights the distinctiveness of this lineage but, because it appears to be both unique to and diverse within Ceriantharia, it is uninformative about the phylogenetic position of Ceriantharia relative to other anthozoan groups.


2019 ◽  
Author(s):  
Viktoria Y. Shtratnikova ◽  
Mikhail I. Schelkunov ◽  
Aleksey A. Penin ◽  
Maria D. Logacheva

AbstractHeterotrophic plants – the plants that lost the ability to photosynthesis – are characterized by a number of changes at all levels of organization. Heterotrophic plants divide into two large categories – parasitic and mycoheterotrophic. The question of to what extent these changes are similar in these two categories is still open. Plastid genomes of non-photosynthetic plants are well characterized and they demonstrate similar patterns of reduction in both groups. In contrast, little is known about mitochondrial genomes of mycoheterotrophic plants. We report the structure of the mitochondrial genome of Hypopitys monotropa, a mycoheterotrophic member of Ericaceae, and the expression of mitochondrial genes. In contrast to its highly reduced plastid genome, the mitochondrial genome of H. monotropa is larger than that of its photosynthetic relative Vaccinium macrocarpon, its complete size is ~810 Kbp. We found an unusually long repeat-rich structure of the genome that suggests the existence of linear fragments. Despite this unique feature, the gene content of the H. monotropa mitogenome is typical of flowering plants. No acceleration of substitution rates is observed in mitochondrial genes, in contrast to previous observations on parasitic non-photosynthetic plants. Transcriptome sequencing revealed trans-splicing of several genes and RNA editing in 33 genes of 38. Notably, we did not find any traces of horizontal gene transfer from fungi, in contrast to plant parasites which extensively integrate genetic material from their hosts.


2002 ◽  
Vol 16 (3) ◽  
pp. 345 ◽  
Author(s):  
M. Dowton ◽  
L. R. Castro ◽  
A. D. Austin

Mitochondrial gene rearrangements are the latest tool in the arsenal of phylogeneticists for investigating historical relationships. They are complex molecular characters that may provide more reliable evidence of ancestry than comparative molecular data. Here we review the phylogenetic utility of mitochondrial gene rearrangements, and find that despite isolated incidences of convergence, derived gene order appears highly congruent with phylogenies produced from other sources of data. We calculate that the chance of two mitochondrial genomes sharing the same derived genome organisation is only 1/2664, but caution that this ignores the possibility that the (as yet uncharacterised) gene rearrangement mechanism may greatly increase the chance of convergence. Broader taxonomic surveys of mitochondrial genome organisation will lead to a more realistic indication of the historical incidence of convergence in genome organisation.


2008 ◽  
Vol 83 (4) ◽  
pp. 301-320 ◽  
Author(s):  
Koichiro Tsunewaki ◽  
Yoshihiro Matsuoka ◽  
Yukiko Yamazaki ◽  
Yasunari Ogihara

2020 ◽  
Vol 20 (5) ◽  
Author(s):  
Jungmo Lee ◽  
Jonghyun Park ◽  
Hong Xi ◽  
Jongsun Park

Abstract Figulus binodulus Waterhouse is a small stag beetle distributed in East Asia. We determined the first mitochondrial genome of F. binodulus of which is 16,261-bp long including 13 protein-coding genes, two ribosomal RNA genes, 22 transfer RNAs, and a single large noncoding region of 1,717 bp. Gene order of F. binodulus is identical to the ancestral insect mitochondrial gene order as in most other stag beetle species. All of 22 tRNAs could be shaped into typical clover-leaf structure except trnSer1. Comparative analyses of 21 Lucanidae mitochondrial genomes was conducted in aspect of their length and AT-GC ratio. Nucleotide diversities analyses provide that cox1 and cox2 in Lucanidae are less diverse than those of Scarabaeoidea. Fifty simple sequence repeats (SSRs) were identified on F. binodulus mitochondrial genome. Comparative analysis of SSRs among five mitochondrial genomes displayed similar trend along with SSR types. Figulus binodulus was sister to all other available family Lucanidae species in the phylogenetic tree.


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