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Background Longer branches in phylogenetic trees usually correspond to accelerated evolutionary rates. However, little is known about the potential correlation between accelerated evolution rates of organisms and their adapation to novel environments. Here, we sampled representative species of Ranunculeae in different habitats, including two xerophytic Ceratocephala species, two hydrophytic Myosurus species, and six mesophytic species from other four genera within the tribe. By an integration of phylogenomic, comparative genomic, and evolutionary rate analyses, we identified fast-evolving genes (FSGs) of organelle genomes in Ceratocephala and Myosurus and explored their relationships with adaptation to dry and aquatic habitats, respectively. Results The Ceratocephala - Myosurus clade originated at 33.01 Ma and began to diversify at 24.43 Ma. A total of nine plastid FSGs ( ndhB , ndhD , rpoB , rpoC1 , rps3 , rps7 , rps11 , ycf1 , ycf4 ) and two mitochondrial FSGs ( ccmFC , nad6 ) were identified as shared by Ceratocephala and Myosurus . Ceratocephala has four unique plastid FSGs ( rps4 , petD , psbH , rpl22 ) and two unique mitochondrial FSGs ( ccmB , nad4 ); Myosurus has three unique plastid FSGs ( ndhA , psbC , rpl32 ) and one unique mitochondrial FSG ( atp1 ). The predicted protein structure of ycf1 is obviously different among Ceratocephala , Myosurus , and Ranunculus . The predicted protein structures of rps4 and ccmFC in Ceratocephala markedly differ from those in Ranunculus . Conclusions Plastid ( rpo -, rps -, rpl -) and mitochondrial ( nad -, ccm -) genes constitute the predominant functional categories within the FSGs, implying that they may play an important role in adaptation to specific habitats. The Ceratocephala -specific six FSGs and predicted protein structural changes of ycf1 , rps4 and ccmFC may be related to the adaptation of this genus to dry habitats in the late Oligocene. The Myosurus -specific four FSGs and predicted protein structural change of ycf1 may be associated with the adaptation of this genus to aquatic habitats. These findings suggest that the increases in evolutionary rates and predicted protein structural changes of organelle genes may facilitate organisms to adapt specific habitats.

GetOrganelle is a state-of-the-art toolkit to accurately assemble organelle genomes from whole genome sequencing data. It recruits organelle-associated reads using a modified “baiting and iterative mapping” approach, conducts de novo assembly, filters and disentangles the assembly graph, and produces all possible configurations of circular organelle genomes. For 50 published plant datasets, we are able to reassemble the circular plastomes from 47 datasets using GetOrganelle. GetOrganelle assemblies are more accurate than published and/or NOVOPlasty-reassembled plastomes as assessed by mapping. We also assemble complete mitochondrial genomes using GetOrganelle. GetOrganelle is freely released under a GPL-3 license ( https://github.com/Kinggerm/GetOrganelle ).

Plant organelle genomes, particularly large mitochondrial genomes with complex repeats, present significant challenges for assembly. The advent of long-read sequencing enables the assembly of complete genomes, but problems of resolving alternative structures remain. Here we introduce a novel tool that employs a syncmer-based assembler for rapid assembly graph construction, integrates a profile-HMM database for robust organelle identification, and leverages a new search method to find the best supported path through the assembly graph. We describe high-quality organelle assemblies for 195 plant species, demonstrating improvements over other methods, and providing multiple insights into structural complexity, heteroplasmy, and DNA exchange between organelles.

Plant mitochondrial genomes have excessive size relative to coding capacity, a low mutation rate in genes and a high rearrangement rate. They also have abundant non-tandem repeats often including pairs of large repeats which cause isomerization of the genome by recombination, and numerous repeats of up to several hundred base pairs that recombine only when the genome is stressed by DNA damaging agents or mutations in DNA repair pathway genes. Early work on mitochondrial genomes led to the suggestion that repeats in the size range from several hundred to a few thousand base pair are underrepresented. The repeats themselves are not well-conserved between species, and are not always annotated in mitochondrial sequence assemblies. We systematically identified and compared these repeats, which are important clues to mechanisms of DNA maintenance in mitochondria. We developed a tool to find and curate non-tandem repeats larger than 50bp and analyzed the complete mitochondrial sequences from 157 plant species. We observed an interesting difference between taxa: the repeats are larger and more frequent in the vascular plants. Analysis of closely related species also shows that plant mitochondrial genomes evolve in dramatic bursts of breakage and rejoining, complete with DNA sequence gain and loss. We suggest an adaptive explanation for the existence of the repeats and their evolution.

Background Okra ( Abelmoschus esculentus L. Moench) is an economically important crop and is known for its slimy juice, which has significant scientific research value. The A. esculentus chloroplast genome has been reported; however, the sequence of its mitochondrial genome is still lacking. Results We sequenced the plastid and mitochondrial genomes of okra based on Illumina short reads and Nanopore long reads and conducted a comparative study between the two organelle genomes. The plastid genome of okra is highly structurally conserved, but the mitochondrial genome of okra has been confirmed to have abundant subgenomic configurations. The assembly results showed that okra’s mitochondrial genome existed mainly in the form of two independent molecules, which could be divided into four independent molecules through two pairs of long repeats. In addition, we found that four pairs of short repeats could mediate the integration of the two independent molecules into one complete molecule at a low frequency. Subsequently, we also found extensive sequence transfer between the two organelles of okra, where three plastid-derived genes ( psaA , rps7 and psbJ ) remained intact in the mitochondrial genome. Furthermore, psbJ , psbF , psbE and psbL were integrated into the mitochondrial genome as a conserved gene cluster and underwent pseudogenization as nonfunctional genes. Only psbJ retained a relatively complete sequence, but its expression was not detected in the transcriptome data, and we speculate that it is still nonfunctional. Finally, we characterized the RNA editing events of protein-coding genes located in the organelle genomes of okra. Conclusions In the current study, our results not only provide high-quality organelle genomes for okra but also advance our understanding of the gene dialogue between organelle genomes and provide information to breed okra cultivars efficiently.

Main conclusionThe first complete mitochondrial genome of Carex (C. breviculmis) was sequenced and assembled, and its genomic signature was analyzed and the possible conformations of its mitochondrial genome were validated.Carex breviculmis is a very adaptable grass that is highly resistant to environmental stresses such as drought and low light. It is also admired as a landscape plant with high development prospects and scientific research value. In this study, the mitochondrial genome of C. breviculmis was assembled using Pacbio and Illumina sequencing data. We detected 267 pairs of repeats and found that three pairs of repeats could mediate the recombination of its mitochondrial genome and formed four possible conformations, of which we verified the two conformations mediated by the shortest pair of repeats using PCR amplification and Sanger sequencing. The major conformation of the C. breviculmis mitochondrial genome is a 1,414,795 bp long circular molecule with 33 annotated protein-coding genes, 15 tRNA genes, and three rRNA genes. We detected a total of 25 homologous sequences between the chloroplast and mitochondrial genomes, corresponding to 0.40% of the mitochondrial genome. Combined with the low GC content (41.24%), we conclude that the reduction in RNA editing sites in the C. breviculmis mitochondrial genome may be due to an accumulation of point mutations in C-to-T or retroprocessing events within the genome. The relatively low number of RNA editing sites in its mitochondrial genome could serve as important material for subsequent studies on the selection pressure of RNA editing in angiosperms. A maximum likelihood analysis based on 23 conserved mitochondrial genes from 28 species reflects an accurate evolutionary and taxonomic position of C. breviculmis. This research provided us with a comprehensive understanding of the mitochondrial genome of Carex and also provided important information for its molecular breeding.

Mitochondrial and plastid genomes in land plants exhibit some of the slowest rates of sequence evolution observed in any eukaryotic genome, suggesting an exceptional ability to prevent or correct mutations. However, the mechanisms responsible for this extreme fidelity remain unclear. We tested seven candidate genes involved in cytoplasmic DNA replication, recombination, and repair (POLIA, POLIB, MSH1, RECA3, UNG, FPG, and OGG1) for effects on mutation rates in the model angiosperm Arabidopsis thaliana by applying a highly accurate DNA sequencing technique (duplex sequencing) that can detect newly arisenmitochondrial and plastidmutations even at low heteroplasmic frequencies. We find that disrupting MSH1 (but not the other candidate genes) leads to massive increases in the frequency of point mutations and small indels and changes to the mutation spectrum in mitochondrial and plastid DNA. We also used droplet digital PCR to show transmission of de novo heteroplasmies across generations in msh1 mutants, confirming a contribution to heritable mutation rates. This dual-targeted gene is part of an enigmatic lineagewithin the mutS mismatch repair family thatwe find is also present outside of green plants in multiple eukaryotic groups (stramenopiles, alveolates, haptophytes, and cryptomonads), as well as certain bacteria and viruses. MSH1 has previously been shown to limit ectopic recombination in plant cytoplasmic genomes. Our results point to a broader role in recognition and correction of errors in plant mitochondrial and plastid DNA sequence, leading to greatly suppressed mutation rates perhaps via initiation of doublestranded breaks and repair pathways based on faithful homologous recombination.

Background The genomes within organelles are crucial for physiological functions such as respiration and photosynthesis and may also contribute to environmental adaptation. However, the limited availability of genetic resources, particularly mitochondrial genomes, poses significant challenges for in-depth investigations. Results Here, we explored various assembly methodologies and successfully reconstructed the complex organelle genomes of two Rhododendron species: Rhododendron nivale subsp. boreale and Rhododendron vialii . The mitogenomes of these species exhibit various conformations, as evidenced by long-reads mapping. Notably, only the mitogenome of R. vialii can be depicted as a singular circular molecule. The plastomes of both species conform to the typical quadripartite structure but exhibit elongated inverted repeat (IR) regions. Compared to the high similarity between plastomes, the mitogenomes display more obvious differences in structure, repeat sequences, and codon usage. Based on the analysis of 58 organelle genomes from angiosperms inhabiting various altitudes, we inferred the genetic adaptations associated with high-altitude environments. Phylogenetic analysis revealed partial inconsistencies between plastome- and mitogenome-derived phylogenies. Additionally, evolutionary lineage was determined to exert a greater influence on codon usage than altitude. Importantly, genes such as atp4 , atp9 , mttB , and clpP exhibited signs of positive selection in several high-altitude species, suggesting a potential link to alpine adaptation. Conclusions We tested the effectiveness of different organelle assembly methods for dealing with complex genomes, while also providing and validating high-quality organelle genomes of two Rhododendron species. Additionally, we hypothesized potential strategies for high-altitude adaptation of organelles. These findings offer a reference for the assembly of complex organelle genomes, while also providing new insights and valuable resources for understanding their adaptive evolution patterns.

The mystery of genomic alternations in heterotrophic plants is among the most intriguing in evolutionary biology. Compared to plastid genomes (plastomes) with parallel size reduction and gene loss, mitochondrial genome (mitogenome) variation in heterotrophic plants remains underexplored in many aspects. To further unravel the evolutionary outcomes of heterotrophy, we present a comparative mitogenomic study with 13 de novo assemblies of Gastrodia (Orchidaceae), one of the largest fully mycoheterotrophic plant genera, and its relatives. Analyzed Gastrodia mitogenomes range from 0.56 to 2.1 Mb, each consisting of numerous, unequally abundant chromosomes or contigs. Size variation might have evolved through chromosome rearrangements followed by stochastic loss of “dispensable” chromosomes, with deletion-biased mutations. The discovery of a hyper-abundant (∼15 times intragenomic average) chromosome in two assemblies represents the hitherto most extreme copy number variation in any mitogenomes, with similar architectures discovered in two metazoan lineages. Transferred sequence contents highlight asymmetric evolutionary consequences of heterotrophy: despite drastically reduced intracellular plastome transfers convergent across heterotrophic plants, their rarity of horizontally acquired sequences sharply contrasts parasitic plants, where massive transfers from their hosts prevail. Rates of sequence evolution are markedly elevated but not explained by copy number variation, extending prior findings of accelerated molecular evolution from parasitic to heterotrophic plants. Putative evolutionary scenarios for these mitogenomic convergence and divergence fit well with the common (e.g. plastome contraction) and specific (e.g. host identity) aspects of the two heterotrophic types. These idiosyncratic mycoheterotrophs expand known architectural variability of plant mitogenomes and provide mechanistic insights into their content and size variation.