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Although Pentapetalae (comprising all core eudicots except Gunnerales) include [almost equal to]70% of all angiosperms, the origin of and relationships among the major lineages of this clade have remained largely unresolved. Phylogenetic analyses of 83 protein-coding and rRNA genes from the plastid genome for 86 species of seed plants, including new sequences from 25 eudicots, indicate that soon after its origin, Pentapetalae diverged into three clades: (i) a \"superrosid\" clade consisting of Rosidae, Vitaceae, and Saxifragales; (ii) a \"superasterid\" clade consisting of Berberidopsidales, Santalales, Caryophyllales, and Asteridae; and (iii) Dilleniaceae. Maximum-likelihood analyses support the position of Dilleniaceae as sister to superrosids, but topology tests did not reject alternative positions of Dilleniaceae as sister to Asteridae or all remaining Pentapetalae. Molecular dating analyses suggest that the major lineages within both superrosids and superasterids arose in as little as 5 million years. This phylogenetic hypothesis provides a crucial historical framework for future studies aimed at elucidating the underlying causes of the morphological and species diversity in Pentapetalae.

Background Plastome-scale data have been prevalent in reconstructing the plant Tree of Life. However, phylogenomic studies currently based on plastomes rely primarily on maximum likelihood inference of concatenated alignments of plastid genes, and thus phylogenetic discordance produced by individual plastid genes has generally been ignored. Moreover, structural and functional characteristics of plastomes indicate that plastid genes may not evolve as a single locus and are experiencing different evolutionary forces, yet the genetic characteristics of plastid genes within a lineage remain poorly studied. Results We sequenced and annotated 10 plastome sequences of Gentianeae. Phylogenomic analyses yielded robust relationships among genera within Gentianeae. We detected great variation of gene tree topologies and revealed that more than half of the genes, including one ( atpB ) of the three widely used plastid markers ( rbcL , atpB and matK ) in phylogenetic inference of Gentianeae, are likely contributing to phylogenetic ambiguity of Gentianeae. Estimation of nucleotide substitution rates showed extensive rate heterogeneity among different plastid genes and among different functional groups of genes. Comparative analysis suggested that the ribosomal protein (RPL and RPS) genes and the RNA polymerase (RPO) genes have higher substitution rates and genetic variations among plastid genes in Gentianeae. Our study revealed that just one ( matK ) of the three ( matK, ndhB and rbcL ) widely used markers show high phylogenetic informativeness (PI) value. Due to the high PI and lowest gene-tree discordance, rpoC2 is advocated as a promising plastid DNA barcode for taxonomic studies of Gentianeae. Furthermore, our analyses revealed a positive correlation of evolutionary rates with genetic variation of plastid genes, but a negative correlation with gene-tree discordance under purifying selection. Conclusions Overall, our results demonstrate the heterogeneity of nucleotide substitution rates and genetic characteristics among plastid genes providing new insights into plastome evolution, while highlighting the necessity of considering gene-tree discordance into phylogenomic studies based on plastome-scale data.

Plastid genomes have been widely used to infer phylogenetic relationships among plants, but the selective pressures driving their evolution have not been systematically investigated. In our study, we analyse all protein-coding plastid genes from 113 species of PACMAD grasses (Poaceae) to evaluate the selective pressures driving their evolution. Our analyses confirm that the gene encoding the large subunit of RubisCO (rbcL) evolved under strong positive selection after C₃–C₄ photosynthetic transitions. We highlight new codons in rbcL that underwent parallel changes, in particular those encoding the C-terminal part of the protein. C₃–C₄ photosynthetic shifts did not significantly affect the evolutionary dynamics of other plastid genes. Instead, while two-third of the plastid genes evolved under purifying selection or neutrality, 25 evolved under positive selection across the PAC-MAD clade. This set of genes encode for proteins involved in diverse functions, including self-replication of plastids and photosynthesis. Our results suggest that plastid genes widely adapt to changing ecological conditions, but factors driving this evolution largely remain to be identified.

Polytomella spp. are free-living, nonphotosynthetic green algae closely related to the model organism Chlamydomonas reinhardtii. Although colorless, Polytomella spp. have a plastid, but it is still unknown whether they harbor a plastid genome. We took a next generation sequencing approach, along with transcriptome sequencing, to search for a plastid genome and an associated gene expression system in Polytomella spp. Illumina sequencing of total DNA from four Polytomella spp. did not produce any recognizable plastid-derived reads but did generate a large number of mitochondrial DNA sequences. Transcriptomic analysis of Polytomella parva uncovered hundreds of putative nuclear-encoded, plastid-targeted proteins, which support the presence of plastid-based metabolic functions, similar to those observed in the plastids of other nonphotosynthetic algae. Conspicuously absent, however, were any plastid-targeted proteins involved in the expression, replication, or repair of plastid DNA. Based on these findings and earlier findings, we argue that the Polytomella genus represents the first wellsupported example, to our knowledge, of a primary plastid-bearing lineage without a plastid genome.

PREMISE OF THE STUDY: Land-plant plastid genomes have only rarely undergone significant changes in gene content and order. Thus, discovery of additional examples adds power to tests for causes of such genome-scale structural changes. METHODS: Using next-generation sequence data, we assembled the plastid genome of saguaro cactus and probed the nuclear genome for transferred plastid genes and functionally related nuclear genes. We combined these results with available data across Cactaceae and seed plants more broadly to infer the history of gene loss and to assess the strength of phylogenetic association between gene loss and loss of the inverted repeat (IR). KEY RESULTS: The saguaro plastid genome is the smallest known for an obligately photosynthetic angiosperm (~113 kb), having lost the IR and plastid ndh genes. This loss supports a statistically strong association across seed plants between the loss of ndh genes and the loss of the IR. Many nonplastid copies of plastid ndh genes were found in the nuclear genome, but none had intact reading frames; nor did three related nuclear-encoded subunits. However, nuclear pgr5, which functions in a partially redundant pathway, was intact. CONCLUSIONS: The existence of an alternative pathway redundant with the function of the plastid NADH dehydrogenase-like complex (NDH) compex may permit loss of the plastid ndh gene suite in photoautotrophs like saguaro. Loss of these genes may be a recurring mechanism for overall plastid genome size reduction, especially in combination with loss of the IR.

PREMISE OF THE STUDY: We explored the phylogenetic utility of entire plastid DNA sequences in Daucus and compared the results with prior phylogenetic results using plastid and nuclear DNA sequences. METHODS: We used Illumina sequencing to obtain full plastid sequences of 37 accessions of 20 Daucus taxa and outgroups, analyzed the data with phylogenetic methods, and examined evidence for mitochondrial DNA transfer to the plastid (DcMP). KEY RESULTS: Our phylogenetic trees of the entire data set were highly resolved, with 100% bootstrap support for most of the external and many of the internal clades, except for the clade of D. carota and its most closely related species D. syrticus. Subsets of the data, including regions traditionally used as phylogenetically informative regions, provide various degrees of soft congruence with the entire data set. There are areas of hard incongruence, however, with phylogenies using nuclear data. We extended knowledge of a mitochondrial to plastid DNA insertion sequence previously named DcMP and identified the first instance in flowering plants of a sequence of potential nuclear genome origin inserted into the plastid genome. There is a relationship of inverted repeat junction classes and repeat DNA to phylogeny, but no such relationship with nonsynonymous mutations. CONCLUSIONS: Our data have allowed us to (1) produce a well‐resolved plastid phylogeny of Daucus, (2) evaluate subsets of the entire plastid data for phylogeny, (3) examine evidence for plastid and nuclear DNA phylogenetic incongruence, and (4) examine mitochondrial and nuclear DNA insertion into the plastid.

The emergence of photosynthetic eukaryotes has played a crucial role in evolution and has strongly modified earth's ecology. Several phylogenetic analyses have established that primary plastids arose from a cyanobacterium through endosymbiosis. However, the question of which present-day cyanobacterial lineage is most closely related to primary plastids has been unclear. Here, we have performed an extensive phylogenomic investigation on the origin of primary plastids based on the analysis of up to 191 protein markers and over 30,000 aligned amino acid sites from 22 primary photosynthetic eukaryotes and 61 cyanobacteria representing a wide taxonomic sampling of this phylum. By using a number of solutions to circumvent a large range of systematic errors, we have reconstructed a robust global phylogeny of cyanobacteria and studied the placement of primary plastids within it. Our results strongly support an early emergence of primary plastids within cyanobacteria, prior to the diversification of most present-day cyanobacterial lineages for which genomic data are available.

Plant mitochondrial and plastid genomes have exceptionally slow rates of sequence evolution, and recent work has identified an unusual member of the MutS gene family (“plant MSH1 ”) as being instrumental in preventing point mutations in these genomes. However, the effects of disrupting MSH1 -mediated DNA repair on “germline” mutation rates have not been quantified. Here, we used Arabidopsis thaliana mutation accumulation (MA) lines to measure mutation rates in msh1 mutants and matched wild type (WT) controls. We detected 124 single nucleotide variants (SNVs: 49 mitochondrial and 75 plastid) and 668 small insertions and deletions (indels: 258 mitochondrial and 410 plastid) in msh1 MA lines at a heteroplasmic frequency of ≥ 20%. In striking contrast, we did not find any organelle mutations in the WT MA lines above this threshold, and reanalysis of data from a much larger WT MA experiment also failed to detect any variants. The observed number of SNVs in the msh1 MA lines corresponds to estimated mutation rates of 6.1 × 10 -7 and 3.2 × 10 -6 per bp per generation in mitochondrial and plastid genomes, respectively. These rates exceed those of species known to have very high mitochondrial mutation rates (e.g., nematodes and fruit flies) by an order of magnitude or more and are on par with estimated rates in humans despite the generation times of A. thaliana being nearly 100-fold shorter. Therefore, disruption of a single plant-specific genetic factor in A. thaliana is sufficient to erase or even reverse the enormous difference in organelle mutation rates between plants and animals.

Why have some plants lost the organizational stability in plastid genomes (plastomes) that evolved in their algal ancestors? During the endosymbiotic transformation of a cyanobacterium into the eukaryotic plastid, most cyanobacterial genes were transferred to the nucleus or otherwise lost from the plastome, and the resulting plastome architecture in land plants confers organizational stability, as evidenced by the conserved gene order among bryophytes and lycophytes, whereas ferns, gymnosperms, and angiosperms share a single, 30-kb inversion. Although some additional gene losses have occurred, gene additions to angiosperm plastomes were previously unknown. Plastomes in the Campanulaceae sensu lato have incorporated dozens of large ORFs (putative protein-coding genes). These insertions apparently caused many of the 125+ large inversions now known in this small eudicot clade. This phylogenetically restricted phenomenon is not biogeographically localized, which indicates that these ORFs came from the nucleus or (less likely) a cryptic endosymbiont.

The plastid genome is highly conserved among plant species, suggesting that alterations of its structure would have dramatic impacts on plant fitness. Nevertheless, little is known about the direct consequences of plastid genome instability. Recently, it was reported that the plastid Whirly proteins WHY1 and WHY3 and a specialized type-I polymerase, POLIB< act as safeguards against plastid genome instability in Arabidopsis (Arabidopsis thaliana). In this study, we use ciprofloxacin, an organelle doublestrand break-inducing agent, and the why1why3polIb-1 variegated mutant to evaluate the impact of generalized plastid DNA instability. First, we show that in why1why3polIb-1 and ciprofloxacin-treated plants, plastid genome instability is associated with increased reactive oxygen species production. Then, using different light regimens, we show that the elevated reactive oxygen species production correlates with the appearance of a yellow-variegated phenotype in the why1why3polIb-1 population. This redox imbalance also correlates to modifications of nuclear gene expression patterns, which in turn leads to acclimation to high light. Taken together, these results indicate that plastid genome instability induces an oxidative burst that favors, through nuclear genetic reprogramming, adaptation to subsequent oxidative stresses.