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The New Phytologist May 2021The transition from an engulfed autonomous unicellular photosynthetic bacterium to a semiautonomous endosymbiont plastid was accompanied by the transfer of genetic... (Review)
Review
The transition from an engulfed autonomous unicellular photosynthetic bacterium to a semiautonomous endosymbiont plastid was accompanied by the transfer of genetic material from the endosymbiont to the nuclear genome of the host, followed by the establishment of plastid-to-nucleus (retrograde) signaling. The retrograde coordinated activities of the two subcellular genomes ensure chloroplast biogenesis and function as the photosynthetic hub and sensing and signaling center that tailors growth-regulating and adaptive processes. This review specifically focuses on the current knowledge of selected stress-induced retrograde signals, genomes uncoupled 1 (GUN1), methylerythritol cyclodiphosphate (MEcPP), apocarotenoid and β-cyclocitral, and 3'-phosphoadenosine 5'-phosphate (PAP), which evolved to establish the photoautotrophic lifestyle and are instrumental in the integration of light and hormonal signaling networks to ultimately fashion adaptive responses in an ever-changing environment.
Topics: Arabidopsis; Arabidopsis Proteins; Chloroplasts; DNA-Binding Proteins; Gene Expression Regulation, Plant; Plastids; Signal Transduction
PubMed: 33452833
DOI: 10.1111/nph.17192 -
Independent Size Expansions and Intron Proliferation in Red Algal Plastid and Mitochondrial Genomes.Genome Biology and Evolution Apr 2022Proliferation of selfish genetic elements has led to significant genome size expansion in plastid and mitochondrial genomes of various eukaryotic lineages. Within the...
Proliferation of selfish genetic elements has led to significant genome size expansion in plastid and mitochondrial genomes of various eukaryotic lineages. Within the red algae, such expansion events are only known in the plastid genomes of the Proteorhodophytina, a highly diverse group of mesophilic microalgae. By contrast, they have never been described in the much understudied red algal mitochondrial genomes. Therefore, it remains unclear how widespread such organellar genome expansion events are in this eukaryotic phylum. Here, we describe new mitochondrial and plastid genomes from 25 red algal species, thereby substantially expanding the amount of organellar sequence data available, especially for Proteorhodophytina, and show that genome expansions are common in this group. We confirm that large plastid genomes are limited to the classes Rhodellophyceae and Porphyridiophyceae, which, in part, are caused by lineage-specific expansion events. Independently expanded mitochondrial genomes-up to three times larger than typical red algal mitogenomes-occur across Proteorhodophytina classes and a large shift toward high GC content occurred in the Stylonematophyceae. Although intron proliferation is the main cause of plastid and mitochondrial genome expansion in red algae, we do not observe recent intron transfer between different organelles. Phylogenomic analyses of mitochondrial and plastid genes from our expanded taxon sampling yielded well-resolved phylogenies of red algae with strong support for the monophyly of Proteorhodophytina. Our work shows that organellar genomes followed different evolutionary dynamics across red algal lineages.
Topics: Cell Proliferation; Evolution, Molecular; Genome, Mitochondrial; Genome, Plastid; Introns; Phylogeny; Plastids; Rhodophyta
PubMed: 35289373
DOI: 10.1093/gbe/evac037 -
Philosophical Transactions of the Royal... Jun 2020Plastid genes in higher plants are transcribed by at least two different RNA polymerases, the plastid-encoded RNA polymerase (PEP), a bacteria-like core enzyme whose... (Review)
Review
The plastid transcription machinery and its coordination with the expression of nuclear genome: Plastid-Encoded Polymerase, Nuclear-Encoded Polymerase and the Genomes Uncoupled 1-mediated retrograde communication.
Plastid genes in higher plants are transcribed by at least two different RNA polymerases, the plastid-encoded RNA polymerase (PEP), a bacteria-like core enzyme whose subunits are encoded by plastid genes (, , and ), and the nuclear-encoded plastid RNA polymerase (NEP), a monomeric bacteriophage-type RNA polymerase. Both PEP and NEP enzymes are active in non-green plastids and in chloroplasts at all developmental stages. Their transcriptional activity is affected by endogenous and exogenous factors and requires a strict coordination within the plastid and with the nuclear gene expression machinery. This review focuses on the different molecular mechanisms underlying chloroplast transcription regulation and its coordination with the photosynthesis-associated nuclear genes () expression. Particular attention is given to the link between NEP and PEP activity and the GUN1- (Genomes Uncoupled 1) mediated chloroplast-to-nucleus retrograde communication with respect to the adaptive response, i.e. the increased accumulation of NEP-dependent transcripts upon depletion of PEP activity, and the editing-level changes observed in NEP-dependent transcripts, including and , in cotyledons after norflurazon or lincomycin treatment. The role of cytosolic preproteins and HSP90 chaperone as components of the GUN1-retrograde signalling pathway, when chloroplast biogenesis is inhibited in cotyledons, is also discussed. This article is part of the theme issue 'Retrograde signalling from endosymbiotic organelles'.
Topics: Cell Nucleus; Chloroplasts; DNA-Directed RNA Polymerases; Gene Expression Regulation, Plant; Genome, Plant; Photosynthesis; Plant Proteins; Plants; Plastids; Signal Transduction; Transcription, Genetic
PubMed: 32362266
DOI: 10.1098/rstb.2019.0399 -
Scientific Reports Aug 2022Artemisia giraldii Pamp. is an herbaceous plant distributed only in some areas in China. To understand the evolutionary relationship between plastid and mitochondria in...
Artemisia giraldii Pamp. is an herbaceous plant distributed only in some areas in China. To understand the evolutionary relationship between plastid and mitochondria in A. giraldii, we sequenced and analysed the plastome and mitogenome of A. giraldii on the basis of Illumina and Nanopore DNA sequencing data. The mitogenome was 194,298 bp long, and the plastome was 151,072 bp long. The mitogenome encoded 56 genes, and the overall GC content was 45.66%. Phylogenetic analysis of the two organelle genomes revealed that A. giraldii is located in the same branching position. We found 13 pairs of homologous sequences between the plastome and mitogenome, and only one of them might have transferred from the plastid to the mitochondria. Gene selection pressure analysis in the mitogenome showed that ccmFc, nad1, nad6, atp9, atp1 and rps12 may undergo positive selection. According to the 18 available plastome sequences, we found 17 variant sites in two hypervariable regions that can be used in completely distinguishing 18 Artemisia species. The most interesting discovery was that the mitogenome of A. giraldii was only 43,226 bp larger than the plastome. To the best of our knowledge, this study represented one of the smallest differences between all sequenced mitogenomes and plastomes from vascular plants. The above results can provide a reference for future taxonomic and molecular evolution studies of Asteraceae species.
Topics: Artemisia; Evolution, Molecular; Genome, Mitochondrial; Genome, Plastid; Phylogeny; Plastids
PubMed: 35978085
DOI: 10.1038/s41598-022-18387-2 -
Genes Nov 2022Andr., a member of Paeoniaceae, is native to China. In its 1600 years' cultivation, more than 2000 cultivars for different purposes (ornamental, medicinal and oil use)...
Andr., a member of Paeoniaceae, is native to China. In its 1600 years' cultivation, more than 2000 cultivars for different purposes (ornamental, medicinal and oil use) have been inbred. However, there are still some controversies regarding the provenance of tree peony cultivars and the phylogenetic relationships between and within different cultivar groups. In this study, plastid genome sequencing was performed on 10 representative tree peony cultivars corresponding to 10 different flower types. Structure and comparative analyses of the plastid genomes showed that the total lengths of the chloroplast genome of the 10 cultivars ranged from 152,153 to 152,385 bp and encoded 84-88 protein-coding genes, 8 rRNAs and 31-40 tRNAs. The number of simple sequence repeats and interspersed repeat sequences of the 10 cultivars ranged from 65-68 and 40-42, respectively. Plastid phylogenetic relationships of species/cultivars were reconstructed incorporating data from our newly sequenced plastid genomes and 15 published species, and results showed that subsect. was the closest relative to the central plains cultivar group with robust support, and that it may be involved in the formation of the group. was recovered as a successive sister group to this lineage. Additionally, eleven morphological characteristics of flowers were mapped to the phylogenetic skeleton to reconstruct the evolutionary trajectory of flower architecture in Paeoniaceae.
Topics: Paeonia; Phylogeny; Flowers; Chromosome Mapping; Plastids
PubMed: 36553496
DOI: 10.3390/genes13122229 -
American Journal of Botany Jun 2022Chaetopeltidales is a poorly characterized order in the Chlorophyceae, with only two plastid and no mitochondrial genomes published. Here we describe a new taxon in...
PREMISE
Chaetopeltidales is a poorly characterized order in the Chlorophyceae, with only two plastid and no mitochondrial genomes published. Here we describe a new taxon in Chaetopeltidales, Gormaniella terricola gen. et sp. nov. and characterize both of its organellar genomes.
METHODS
Gormaniella terricola was inadvertently isolated from a surface-sterilized hornwort thallus. Light microscopy was used to characterize its vegetative morphology. Organellar genomes were assembled, annotated, and analyzed using a variety of software packages.
RESULTS
The mitochondrial genome (66,927 bp) represents the first complete mitochondrial genome published for Chaetopeltidales. The chloroplast genome, measuring 428,981 bp, is one of the largest plastid genomes published to date and shares this large size and an incredible number of short, dispersed repeats with the other sequenced chloroplast genomes in Chaetopeltidales. Despite these shared features, the chloroplast genomes of Chaetopeltidales appear to be highly rearranged when compared to one another, with numerous inversions, translocations, and duplications, suggesting a particularly dynamic chloroplast genome. Both the chloroplast and mitochondrial genomes of G. terricola contain a number of mobile group I and group II introns, which appear to have invaded separately. Three of the introns within the mitochondrial genome encode homing endonucleases that are phylogenetically nested within those found in fungi, rather than algae, suggesting a possible case of horizontal gene transfer.
CONCLUSIONS
These results help to shed light on a poorly understood group of algae and their unusual organellar genomes, raising additional questions about the unique patterns of genome evolution within Chaetopeltidales.
Topics: Chlorophyceae; Chloroplasts; Evolution, Molecular; Genome, Chloroplast; Genome, Mitochondrial; Genome, Plastid; Introns; Phylogeny
PubMed: 35678538
DOI: 10.1002/ajb2.16015 -
Proceedings of the National Academy of... Aug 2022The fate of new mitochondrial and plastid mutations depends on their ability to persist and spread among the numerous organellar genome copies within a cell...
The fate of new mitochondrial and plastid mutations depends on their ability to persist and spread among the numerous organellar genome copies within a cell (heteroplasmy). The extent to which heteroplasmies are transmitted across generations or eliminated through genetic bottlenecks is not well understood in plants, in part because their low mutation rates make these variants so infrequent. Disruption of (), a gene involved in plant organellar DNA repair, results in numerous de novo point mutations, which we used to quantitatively track the inheritance of single nucleotide variants in mitochondrial and plastid genomes in . We found that heteroplasmic sorting (the fixation or loss of a variant) was rapid for both organelles, greatly exceeding rates observed in animals. In mutants, plastid variants sorted faster than those in mitochondria and were typically fixed or lost within a single generation. Effective transmission bottleneck sizes () for plastids and mitochondria were ∼ 1 and 4, respectively. Restoring MSH1 function further increased the rate of heteroplasmic sorting in mitochondria ( ∼ 1.3), potentially because of its hypothesized role in promoting gene conversion as a mechanism of DNA repair, which is expected to homogenize genome copies within a cell. Heteroplasmic sorting also favored GC base pairs. Therefore, recombinational repair and gene conversion in plant organellar genomes can potentially accelerate the elimination of heteroplasmies and bias the outcome of this sorting process.
Topics: Arabidopsis; Arabidopsis Proteins; DNA, Mitochondrial; DNA, Plant; Genome, Plant; Heteroplasmy; Mitochondria; MutS DNA Mismatch-Binding Protein; Plastids
PubMed: 35969753
DOI: 10.1073/pnas.2206973119 -
Journal of Experimental Botany Oct 2022The N-terminus is a frequent site of protein modifications. Referring primarily to knowledge gained from land plants, here we review the modifications that change... (Review)
Review
The N-terminus is a frequent site of protein modifications. Referring primarily to knowledge gained from land plants, here we review the modifications that change protein N-terminal residues and provide updated information about the associated machinery, including that in Archaeplastida. These N-terminal modifications include many proteolytic events as well as small group additions such as acylation or arginylation and oxidation. Compared with that of the mitochondrion, the plastid-dedicated N-terminal modification landscape is far more complex. In parallel, we extend this review to plastid-containing Chromalveolata including Stramenopiles, Apicomplexa, and Rhizaria. We report a well-conserved machinery, especially in the plastid. Consideration of the two most abundant proteins on Earth-Rubisco and actin-reveals the complexity of N-terminal modification processes. The progressive gene transfer from the plastid to the nuclear genome during evolution is exemplified by the N-terminus modification machinery, which appears to be one of the latest to have been transferred to the nuclear genome together with crucial major photosynthetic landmarks. This is evidenced by the greater number of plastid genes in Paulinellidae and red algae, the most recent and fossil recipients of primary endosymbiosis.
Topics: Ribulose-Bisphosphate Carboxylase; Actins; Phylogeny; Plastids; Symbiosis; Evolution, Molecular
PubMed: 35768189
DOI: 10.1093/jxb/erac290 -
BMC Biology Mar 2022The 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...
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 the new genus Leontynka, with two species (L. pallida and L. elongata) distinguishable through both their 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, the carotenoid biosynthesis pathway, and a plastoquinone-based electron transport chain, the latter two modules having an obvious functional link to the eyespot present in Leontynka. Most strikingly, the ~362 kbp plastome of L. pallida is by far the largest among the non-photosynthetic eukaryotes investigated to date due to an extreme proliferation of sequence repeats. These repeats are also present in coding sequences, with one repeat type found in the exons of 11 out of 34 protein-coding genes, with up to 36 copies per gene, thus affecting 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 hitherto studied. It is also bloated with repeats, though entirely different from those in the L. pallida plastome, which contrasts with the situation in H. lacustris where both the 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 its unprecedented combination of plastid and mitochondrial genome characteristics, Leontynka pushes the frontiers of organellar genome diversity and is an interesting model for studying organellar genome evolution.
Topics: Chlorophyceae; Chlorophyta; Evolution, Molecular; Genome, Plastid; Photosynthesis; Phylogeny; Plastids
PubMed: 35296310
DOI: 10.1186/s12915-022-01263-w -
The New Phytologist Jun 2021Plants are able to adjust phenotype in response to changes in the environment. This system depends on an internal capacity to sense environmental conditions and to... (Review)
Review
Plants are able to adjust phenotype in response to changes in the environment. This system depends on an internal capacity to sense environmental conditions and to process this information to plant response. Recent studies have pointed to mitochondria and plastids as important environmental sensors, capable of perceiving stressful conditions and triggering gene expression, epigenomic, metabolic and phytohormone changes in the plant. These processes involve integrated gene networks that ultimately modulate the energy balance between growth and plant defense. This review attempts to link several unusual recent findings into a comprehensive hypothesis for the regulation of plant phenotypic plasticity.
Topics: Gene Expression Regulation, Plant; Mitochondria; Phenotype; Plants; Plastids
PubMed: 33704791
DOI: 10.1111/nph.17333