scholarly journals A new lineage of non-photosynthetic green algae with extreme organellar genomes

2021 ◽  
Author(s):  
Tomáš Pánek ◽  
Dovilė Barcytė ◽  
Sebastian C. Treitli ◽  
Kristína Záhonová ◽  
Martin Sokol ◽  
...  
Keyword(s):  
Mitochondrial Genome ◽  
Genome Evolution ◽  
Transcriptome Assembly ◽  
Molecular Characteristics ◽  
Functional Link ◽  
Coding Regions ◽  
Organellar Genome ◽  
Organellar Genomes ◽  
Green Algal ◽  
Plastid Genomes

Background: The plastid genomes of the green algal order Chlamydomonadales tend to expand their non-coding regions, but this phenomenon is poorly understood. Here we shed new light on organellar genome evolution in Chlamydomonadales by studying a previously unknown non-photosynthetic lineage. We established cultures of two new Polytoma-like flagellates, defined their basic characteristics and phylogenetic position, and obtained complete organellar genome sequences and a transcriptome assembly for one of them. Results: We discovered a novel deeply diverged chlamydomonadalean lineage that has no close photosynthetic relatives and represents an independent case of photosynthesis loss. To accommodate these organisms, we establish a new genus, Leontynka, with two species L. pallida and L. elongata distinguished by both morphological and molecular characteristics. Notable features of the colourless plastid of L. pallida deduced from the plastid genome (plastome) sequence and transcriptome assembly include the retention of ATP synthase, thylakoid-associated proteins, carotenoid biosynthesis pathway, and plastoquinone-based electron transport chain, the latter two modules having an obvious functional link to the eyespot present in Leontynka. Most strikingly, the L. pallida plastome with its ~362 kbp is by far the largest among non-photosynthetic eukaryotes investigated to date. Instead of a high gene content, its size reflects extreme proliferation of sequence repeats. These are present also in coding sequences, with one repeat type found in exons of 11 out of 34 protein-coding genes and up to 36 copies per gene, affecting thus the encoded proteins. The mitochondrial genome of L. pallida is likewise exceptionally large, with its >104 kbp surpassed only by the mitogenome of Haematococcus lacustris among all members of Chlamydomonadales studied so far. It is also bloated with repeats, yet completely different from those in the L. pallida plastome, which contrasts with the situation in H. lacustris where both organellar genomes have accumulated related repeats. Furthermore, the L. pallida mitogenome exhibits an extremely high GC content in both coding and non-coding regions and, strikingly, a high number of predicted G-quadruplexes. Conclusions: With the unprecedented combination of plastid and mitochondrial genome characteristics, Leontynka pushes the frontiers of organellar genome diversity and becomes an interesting model for studying organellar genome evolution.

scholarly journals Maturyoshka: a maturase inside a maturase, and other peculiarities of the novel chloroplast genomes of marine euglenophytes

2021 ◽  
Author(s):  
Kacper Maciszewski ◽  
Nadja Dabbagh ◽  
Angelika Preisfeld ◽  
Anna Karnkowska
Keyword(s):  
Essential Gene ◽  
Functional Domains ◽  
The Novel ◽  
Patchy Distribution ◽  
Organellar Genomes ◽  
Green Algal ◽  
Plastid Genomes ◽  
Chloroplast Genomes ◽  
History Of ◽  
Eventual Loss

Organellar genomes often carry group II introns, which occasionally encode proteins called maturases that are important for splicing. The number of introns varies substantially among various organellar genomes, and bursts of introns have been observed in multiple eukaryotic lineages, including euglenophytes, with more than 100 introns in their plastid genomes. To examine the evolutionary diversity and history of maturases, an essential gene family among euglenophytes, we searched for their homologs in newly sequenced and published plastid genomes representing all major euglenophytes' lineages. We found that maturase content in plastid genomes has a patchy distribution, with a maximum of eight of them present in Eutreptiella eupharyngea. The most basal lineages of euglenophytes, Eutreptiales, share the highest number of maturases, but the lowest number of introns. We also identified a peculiar convoluted structure of a gene located in an intron, in a gene within an intron, within yet another gene, present in some Eutreptiales. Further investigation of functional domains of identified maturases shown that most of them lost at least one of the functional domains, which implies that the patchy maturase distribution is due to frequent inactivation and eventual loss over time. Finally, we identified the diversified evolutionary origin of analysed maturases, which were acquired along with the green algal plastid or horizontally transferred. These findings indicate that euglenophytes' plastid maturases have experienced a surprisingly dynamic history due to gains from diversified donors, their retention, and loss.

scholarly journals Intergenomic gene transfer in diploid and allopolyploid Gossypium

2019 ◽  
Vol 19 (1) ◽  
Author(s):  
Nan Zhao ◽  
Corrinne E. Grover ◽  
Zhiwen Chen ◽  
Jonathan F. Wendel ◽  
Jinping Hua
Keyword(s):  
Gene Transfer ◽  
Mitochondrial Genome ◽  
Chloroplast Dna ◽  
Nuclear Genome ◽  
Plant Evolution ◽  
Trna Genes ◽  
Organellar Genomes ◽  
Plastid Genomes ◽  
Cotton Species ◽  
Chloroplast Trna Genes

Abstract Background Intergenomic gene transfer (IGT) between nuclear and organellar genomes is a common phenomenon during plant evolution. Gossypium is a useful model to evaluate the genomic consequences of IGT for both diploid and polyploid species. Here, we explore IGT among nuclear, mitochondrial, and plastid genomes of four cotton species, including two allopolyploids and their model diploid progenitors (genome donors, G. arboreum: A2 and G. raimondii: D5). Results Extensive IGT events exist for both diploid and allotetraploid cotton (Gossypium) species, with the nuclear genome being the predominant recipient of transferred DNA followed by the mitochondrial genome. The nuclear genome has integrated 100 times more foreign sequences than the mitochondrial genome has in total length. In the nucleus, the integrated length of chloroplast DNA (cpDNA) was between 1.87 times (in diploids) to nearly four times (in allopolyploids) greater than that of mitochondrial DNA (mtDNA). In the mitochondrion, the length of nuclear DNA (nuDNA) was typically three times than that of cpDNA. Gossypium mitochondrial genomes integrated three nuclear retrotransposons and eight chloroplast tRNA genes, and incorporated chloroplast DNA prior to divergence between the diploids and allopolyploid formation. For mitochondrial chloroplast-tRNA genes, there were 2-6 bp conserved microhomologies flanking their insertion sites across distantly related genera, which increased to 10 bp microhomologies for the four cotton species studied. For organellar DNA sequences, there are source hotspots, e.g., the atp6-trnW intergenic region in the mitochondrion and the inverted repeat region in the chloroplast. Organellar DNAs in the nucleus were rarely expressed, and at low levels. Surprisingly, there was asymmetry in the survivorship of ancestral insertions following allopolyploidy, with most numts (nuclear mitochondrial insertions) decaying or being lost whereas most nupts (nuclear plastidial insertions) were retained. Conclusions This study characterized and compared intracellular transfer among nuclear and organellar genomes within two cultivated allopolyploids and their ancestral diploid cotton species. A striking asymmetry in the fate of IGTs in allopolyploid cotton was discovered, with numts being preferentially lost relative to nupts. Our results connect intergenomic gene transfer with allotetraploidy and provide new insight into intracellular genome evolution.

scholarly journals Mycoheterotrophic Epirixanthes (Polygalaceae) has a typical angiosperm mitogenome but unorthodox plastid genomes

2019 ◽  
Vol 124 (5) ◽  
pp. 791-807 ◽  
Author(s):  
G Petersen ◽  
H Darby ◽  
V K Y Lam ◽  
H Æ Pedersen ◽  
V S F T Merckx ◽  
...  
Keyword(s):  
Mitochondrial Genome ◽  
Housekeeping Genes ◽  
Structural Rearrangements ◽  
Substitution Rates ◽  
Organellar Genomes ◽  
Genome Data ◽  
Plastid Genomes ◽  
Plastome Evolution ◽  
Mycoheterotrophic Plants ◽  
Mitochondrial Genome Evolution

Abstract Background and Aims Fully mycoheterotrophic plants derive carbon and other nutrients from root-associated fungi and have lost the ability to photosynthesize. While mycoheterotroph plastomes are often degraded compared with green plants, the effect of this unusual symbiosis on mitochondrial genome evolution is unknown. By providing the first complete organelle genome data from Polygalaceae, one of only three eudicot families that developed mycoheterotrophy, we explore how both organellar genomes evolved after loss of photosynthesis. Methods We sequenced and assembled four complete plastid genomes and a mitochondrial genome from species of Polygalaceae, focusing on non-photosynthetic Epirixanthes. We compared these genomes with those of other mycoheterotroph and parasitic plant lineages, and assessed whether organelle genes in Epirixanthes experienced relaxed or intensified selection compared with autotrophic relatives. Key Results Plastomes of two species of Epirixanthes have become substantially degraded compared with that of autotrophic Polygala. Although the lack of photosynthesis is presumably homologous in the genus, the surveyed Epirixanthes species have marked differences in terms of plastome size, structural rearrangements, gene content and substitution rates. Remarkably, both apparently replaced a canonical plastid inverted repeat with large directly repeated sequences. The mitogenome of E. elongata incorporated a considerable number of fossilized plastid genes, by intracellular transfer from an ancestor with a less degraded plastome. Both plastid and mitochondrial genes in E. elongata have increased substitution rates, but the plastid genes of E. pallida do not. Despite this, both species have similar selection patterns operating on plastid housekeeping genes. Conclusions Plastome evolution largely fits with patterns of gene degradation seen in other heterotrophic plants, but includes highly unusual directly duplicated regions. The causes of rate elevation in the sequenced Epirixanthes mitogenome and of rate differences in plastomes of related mycoheterotrophic species are not currently understood.

scholarly journals OGDA: a comprehensive organelle genome database for algae

Database ◽  
2020 ◽  
Vol 2020 ◽  
Author(s):  
Tao Liu ◽  
Yutong Cui ◽  
Xuli Jia ◽  
Jing Zhang ◽  
Ruoran Li ◽  
...  
Keyword(s):  
Marine Organism ◽  
Structural Characteristics ◽  
Genome Structure ◽  
Evolutionary Relationship ◽  
Uniparental Inheritance ◽  
Genome Database ◽  
Organelle Genome ◽  
Organellar Genomes ◽  
Genome Data ◽  
Plastid Genomes

Abstract Algae are the oldest taxa on Earth, with an evolutionary relationship that spans prokaryotes (Cyanobacteria) and eukaryotes. A long evolutionary history has led to high algal diversity. Their organelle DNAs are characterized by uniparental inheritance and a compact genome structure compared with nuclear genomes; thus, they are efficient molecular tools for the analysis of gene structure, genome structure, organelle function and evolution. However, an integrated organelle genome database for algae, which could enable users to both examine and use relevant data, has not previously been developed. Therefore, to provide an organelle genome platform for algae, we have developed a user-friendly database named Organelle Genome Database for Algae (OGDA, http://ogda.ytu.edu.cn/). OGDA contains organelle genome data either retrieved from several public databases or sequenced in our laboratory (Laboratory of Genetics and Breeding of Marine Organism [MOGBL]), which are continuously updated. The first release of OGDA contains 1055 plastid genomes and 755 mitochondrial genomes. Additionally, a variety of applications have been integrated into this platform to analyze the structural characteristics, collinearity and phylogeny of organellar genomes for algae. This database represents a useful tool for users, enabling the rapid retrieval and analysis of information related to organellar genomes for biological discovery.

scholarly journals Mitochondrial Genome Evolution in a Single Protoploid Yeast Species

2012 ◽  
Vol 2 (9) ◽  
pp. 1103-1111 ◽  
Author(s):  
Paul P. Jung ◽  
Anne Friedrich ◽  
Cyrielle Reisser ◽  
Jing Hou ◽  
Joseph Schacherer
Keyword(s):  
Mitochondrial Genome ◽  
Genome Evolution ◽  
Yeast Species ◽  
Mitochondrial Genome Evolution

Gene fragmentation: a key to mitochondrial genome evolution in Euglenozoa?

2011 ◽  
Vol 57 (4) ◽  
pp. 225-232 ◽  
Author(s):  
Pavel Flegontov ◽  
Michael W. Gray ◽  
Gertraud Burger ◽  
Julius Lukeš
Keyword(s):  
Mitochondrial Genome ◽  
Genome Evolution ◽  
Mitochondrial Genome Evolution

scholarly journals Nuclear-cytoplasmic balance: whole genome duplications induce elevated organellar genome copy number

2021 ◽  
Author(s):  
Matheus Fernandes Gyorfy ◽  
Emma R Miller ◽  
Justin L Conover ◽  
Corrinne E Grover ◽  
Jonathan F Wendel ◽  
...  
Keyword(s):  
Copy Number ◽  
Nuclear Genome ◽  
Plant Genome ◽  
Whole Genome ◽  
Genome Copy ◽  
Relative Copy Number ◽  
Organellar Genome ◽  
Plastid Genomes ◽  
Copy Numbers ◽  
Genome Copy Number

The plant genome is partitioned across three distinct subcellular compartments: the nucleus, mitochondria, and plastids. Successful coordination of gene expression among these organellar genomes and the nuclear genome is critical for plant function and fitness. Whole genome duplication events (WGDs) in the nucleus have played a major role in the diversification of land plants and are expected to perturb the relative copy number (stoichiometry) of nuclear, mitochondrial, and plastid genomes. Thus, elucidating the mechanisms whereby plant cells respond to the cytonuclear stoichiometric imbalance that follow WGDs represents an important yet underexplored question in understanding the evolutionary consequences of genome doubling. We used droplet digital PCR (ddPCR) to investigate the relationship between nuclear and organellar genome copy numbers in allopolyploids and their diploid progenitors in both wheat and Arabidopsis. Polyploids exhibit elevated organellar genome copy numbers per cell, largely preserving the cytonuclear stoichiometry observed in diploids despite the change in nuclear genome copy number. To investigate the timescale over which cytonuclear stoichiometry may respond to WGD, we also estimated organellar genome copy number in Arabidopsis synthetic autopolyploids and in a haploid-induced diploid line. We observed corresponding changes in organellar genome copy number in these laboratory-generated lines, indicating that at least some of the cellular response to cytonuclear stoichiometric imbalance is immediate following WGD. We conclude that increases in organellar genome copy numbers represent a common response to polyploidization, suggesting that maintenance of cytonuclear stoichiometry is an important component in establishing polyploid lineages.

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