An official website of the United States government
Abstract The complete chloroplast and mitochondrial genomes of Charophyta have shed new light on land plant terrestrialization. Here, we report the organellar genomes of the Zygnema circumcarinatum strain UTEX 1559, and a comparative genomics investigation of 33 plastomes and 18 mitogenomes of Chlorophyta, Charophyta (including UTEX 1559 and its conspecific relative SAG 698-1a), and Embryophyta. Gene presence/absence was determined across these plastomes and mitogenomes. A comparison between the plastomes of UTEX 1559 (157 548 bp) and SAG 698-1a (165 372 bp) revealed very similar gene contents, but substantial genome rearrangements. Surprisingly, the two plastomes share only 85.69% nucleotide sequence identity. The UTEX 1559 mitogenome size is 215 954 bp, the largest among all sequenced Charophyta. Interestingly, this large mitogenome contains a 50 kb region without homology to any other organellar genomes, which is flanked by two 86 bp direct repeats and contains 15 ORFs. These ORFs have significant homology to proteins from bacteria and plants with functions such as primase, RNA polymerase, and DNA polymerase. We conclude that (i) the previously published SAG 698-1a plastome is probably from a different Zygnema species, and (ii) the 50 kb region in the UTEX 1559 mitogenome might be recently acquired as a mobile element.
more »
« less
Rapid turnover of mitogenomic repeats and congruent phylogenomic signal among Digitalideae genomes
Digitalideae (Plantaginaceae) comprises ~25 species of foxgloves in two genera (Digitalis and the monotypic Erinus). Several species are notable as garden ornamentals or for their medical benefits and toxic side-effects, yet their genomic resources are limited to plastid genomes from two species. We assembled sequencing data from six Digitalideae species to evaluate the structural and functional evolution of their organellar genomes and to evaluate the phylogenetic signal of these organellar genomes and nuclear rDNA. Digitalideae plastomes are virtually identical among species, exhibiting invariant gene and intron content, a collinear gene order, and very similar sizes and repeat structures. The mitochondrial genomes are nearly identical in terms of gene and intron content but exhibit variation in size, substantial structural rearrangements, and extensive turnover of large repeat content. Comparison of large mitogenomic repeats is consistent with a turnover model, whereas plastomic inverted repeat content is consistent with a retention model, demonstrating distinctly different rates of repeat turnover between the organellar genomes. Phylogenetic trees constructed from entire plastomes, mitochondrial genes and introns, or nuclear rDNA are fully congruent among Digitalideae and other Plantaginaceae, and the results reveal some taxonomic uncertainties regarding Digitalideae systematics and possible species misidentifications in the existing data.
more »
« less
- Award ID(s):
- 2212075
- PAR ID:
- 10675145
- Publisher / Repository:
- Maximum Academic Press
- Date Published:
- Journal Name:
- Genomics Communications
- Volume:
- 3
- Issue:
- 1
- ISSN:
- 3066-3857
- Page Range / eLocation ID:
- 0 to 0
- Subject(s) / Keyword(s):
- Digitalideae Mitochondrial genome Plastid genome Repeat evolution Phylogenetics
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
IntroductionEukaryotic life depends on the functional elements encoded by both the nuclear genome and organellar genomes, such as those contained within the mitochondria. The content, size, and structure of the mitochondrial genome varies across organisms with potentially large implications for phenotypic variance and resulting evolutionary trajectories. Among yeasts in the subphylum Saccharomycotina, extensive differences have been observed in various species relative to the model yeastSaccharomyces cerevisiae, but mitochondrial genome sampling across many groups has been scarce, even as hundreds of nuclear genomes have become available. MethodsBy extracting mitochondrial assemblies from existing short-read genome sequence datasets, we have greatly expanded both the number of available genomes and the coverage across sparsely sampled clades. ResultsComparison of 353 yeast mitochondrial genomes revealed that, while size and GC content were fairly consistent across species, those in the generaMetschnikowiaandSaccharomycestrended larger, while several species in the order Saccharomycetales, which includesS. cerevisiae, exhibited lower GC content. Extreme examples for both size and GC content were scattered throughout the subphylum. All mitochondrial genomes shared a core set of protein-coding genes for Complexes III, IV, and V, but they varied in the presence or absence of mitochondrially-encoded canonical Complex I genes. We traced the loss of Complex I genes to a major event in the ancestor of the orders Saccharomycetales and Saccharomycodales, but we also observed several independent losses in the orders Phaffomycetales, Pichiales, and Dipodascales. In contrast to prior hypotheses based on smaller-scale datasets, comparison of evolutionary rates in protein-coding genes showed no bias towards elevated rates among aerobically fermenting (Crabtree/Warburg-positive) yeasts. Mitochondrial introns were widely distributed, but they were highly enriched in some groups. The majority of mitochondrial introns were poorly conserved within groups, but several were shared within groups, between groups, and even across taxonomic orders, which is consistent with horizontal gene transfer, likely involving homing endonucleases acting as selfish elements. DiscussionAs the number of available fungal nuclear genomes continues to expand, the methods described here to retrieve mitochondrial genome sequences from these datasets will prove invaluable to ensuring that studies of fungal mitochondrial genomes keep pace with their nuclear counterparts.more » « less
-
Abstract We have reported the first mitochondrial (GenBank accession PV035080) and chloroplast (GenBank accession PV035081) genomes for a representative of the gigartinalean family Dumontiaceae (Gibsmithia punonomaewa). High‐throughput sequencing yielded both organellar genomes for the holotype specimen ofGibsmithia punonomaewa, a recently described species that is also a putative endemic to the mesophotic zone of the Hawaiian Islands. Gene content and order of the 26,428‐bp mitochondrial genome are conserved relative to other available genomes of the Gigartinales. The genome contains 52 genes, including 25 protein‐coding sequences (CDSs), 3 rRNAs, and 24 tRNAs, as well as one group II intron in atrnI‐GAU tRNA. The chloroplast genome is 185,316 bp in length and contains 236 genes, including 203 CDSs, three rRNAs, and 30 tRNAs, and one group II intron in atrnM‐CAU tRNA. Both organellar genomes displayed high synteny compared to close relatives in the order Gigartinales, with unique features restricted to several open reading frames. Phylogenomic analyses of the mitochondrial and chloroplast genomes with other gigartinalean representatives yielded well‐resolved phylogenies that supported an early diverging position of the Dumontiaceae within the order Gigartinales.more » « less
-
The genus Trifolium is the largest of the tribe Trifolieae in the subfamily Papilionoideae (Fabaceae). The paucity of mitochondrial genome (mitogenome) sequences has hindered comparative analyses among the three genomic compartments of the plant cell (nucleus, mitochondrion and plastid). We assembled four mitogenomes from the two subgenera (Chronosemium and Trifolium) of the genus. The four Trifolium mitogenomes were compact (294,911–348,724 bp in length) and contained limited repetitive (6.6–8.6%) DNA. Comparison of organelle repeat content highlighted the distinct evolutionary trajectory of plastid genomes in a subset of Trifolium species. Intracellular gene transfer (IGT) was analyzed among the three genomic compartments revealing functional transfer of mitochondrial rps1 to nuclear genome along with other IGT events. Phylogenetic analysis based on mitochondrial and nuclear rps1 sequences revealed that the functional transfer in Trifolieae was independent from the event that occurred in robinioid clade that includes genus Lotus. A novel, independent fission event of ccmFn in Trifolium was identified, caused by a 59 bp deletion. Fissions of this gene reported previously in land plants were reassessed and compared with Trifolium.more » « less
-
Mitochondrial and plastid functions depend on coordinated expression of proteins encoded by genomic compartments that have radical differences in copy number of organellar and nuclear genomes. In polyploids, doubling of the nuclear genome may add challenges to maintaining balanced expression of proteins involved in cytonuclear interactions. Here, we use ribo-depleted RNA sequencing (RNA-seq) to analyze transcript abundance for nuclear and organellar genomes in leaf tissue from four different polyploid angiosperms and their close diploid relatives. We find that even though plastid genomes contain <1% of the number of genes in the nuclear genome, they generate the majority (69.9 to 82.3%) of messenger RNA (mRNA) transcripts in the cell. Mitochondrial genes are responsible for a much smaller percentage (1.3 to 3.7%) of the leaf mRNA pool but still produce much higher transcript abundances per gene compared to nuclear genome. Nuclear genes encoding proteins that functionally interact with mitochondrial or plastid gene products exhibit mRNA expression levels that are consistently more than 10-fold lower than their organellar counterparts, indicating an extreme cytonuclear imbalance at the RNA level despite the predominance of equimolar interactions at the protein level. Nevertheless, interacting nuclear and organellar genes show strongly correlated transcript abundances across functional categories, suggesting that the observed mRNA stoichiometric imbalance does not preclude coordination of cytonuclear expression. Finally, we show that nuclear genome doubling does not alter the cytonuclear expression ratios observed in diploid relatives in consistent or systematic ways, indicating that successful polyploid plants are able to compensate for cytonuclear perturbations associated with nuclear genome doubling.more » « less
- Free Publicly Accessible Full Text
-
Accepted Manuscript
- Journal Article:
- https://doi.org/10.48130/gcomm-0026-0003
