Proposal of a Twin Aarginine Translocator System-Mediated Constraint against Loss of ATP Synthase Genes from Nonphotosynthetic Plastid Genomes

Kamikawa, Ryoma; Tanifuji, Goro; Ishikawa, Sohta A.; Ishii, Kenichiro; Matsuno, Yusei; Onodera, Naoko T.; Ishida, Koichi; Hashimoto, Takeji; Miyashita, Hideaki; Mayama, Shigeki; Inagaki, Yuji

doi:10.1093/molbev/msv134

Cited by 47 publications

(64 citation statements)

References 45 publications

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“…S4). The hypothesized turnover ratedependent rate shifts will be attenuated in genes that are required over longer periods, such as the ATP synthase (atp) genes or RuBisCO (rbcL), possibly because they take over or continue to carry out alternative functions (23,24). Therefore, nonphotosynthetic parasites such as M. californica, Orobanche (11), or some Cuscuta species (7,25), which all retain intact genes for the ATP synthase despite the loss of other photosynthesis genes, also have lower base-level evolutionary rates.…”

Section: Discussionmentioning

confidence: 99%

Mechanistic model of evolutionary rate variation en route to a nonphotosynthetic lifestyle in plants

Wicke

Müller²,

dePamphilis

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

174

285

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Because novel environmental conditions alter the selection pressure on genes or entire subgenomes, adaptive and nonadaptive changes will leave a measurable signature in the genomes, shaping their molecular evolution. We present herein a model of the trajectory of plastid genome evolution under progressively relaxed functional constraints during the transition from autotrophy to a nonphotosynthetic parasitic lifestyle. We show that relaxed purifying selection in all plastid genes is linked to obligate parasitism, characterized by the parasite's dependence on a host to fulfill its life cycle, rather than the loss of photosynthesis. Evolutionary rates and selection pressure coevolve with macrostructural and microstructural changes, the extent of functional reduction, and the establishment of the obligate parasitic lifestyle. Inferred bursts of gene losses coincide with periods of relaxed selection, which are followed by phases of intensified selection and rate deceleration in the retained functional complexes. Our findings suggest that the transition to obligate parasitism relaxes functional constraints on plastid genes in a stepwise manner. During the functional reduction process, the elevation of evolutionary rates reaches several new rate equilibria, possibly relating to the modified protein turnover rates in heterotrophic plastids.parasitism | relaxed selection | evolutionary rates | plastid genomes | Orobanchaceae L ineages change over time as they adapt to new environments. Novel conditions determine the selection in genes or cellular genomes and shape their functional and structural evolution. A system well suited to study the evolution of genomic traits in the context of altered selective regimes that is also tractable technically (due to its small size and high copy number) is the plastid genome (plastome). The prime function of plastids is photosynthesis, but this essential plant organelle also produces starch, lipids, amino acids, sulfur compounds, and pigments. As a result of the strong selective pressure on plastid gene function, plastid genomes have a conserved gene content (1; but see ref.2) and their genes functioning in photosynthesis (atp, ndh, pet, psa, psb, ccsA, cemA, ycf3/4, rbcL), transcription, transcript maturation or translation (rpo, matK, rpl, rps, infA), and other pathways (accD, clpP, ycf1, and ycf2) evolve at lower evolutionary rates than nuclear genes (3). However, in eukaryotic lineages such as Apicomplexan pathogens and nongreen plants that independently made the transition from an autotrophic to a parasitic way of life, plastomes have experienced convergent reductions and accelerations of evolutionary rates (4). Although there is a general understanding of the association of the nonphotosynthetic lifestyle with plastome degradation and rate acceleration, the precise trajectory of plastome evolution under progressively reduced function along the way from being a full autotroph to an obligate nonphotosynthetic parasite remains unknown.Parasitic plants are an excellent system for stu...

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Section: Discussionmentioning

confidence: 99%

Mechanistic model of evolutionary rate variation en route to a nonphotosynthetic lifestyle in plants

Wicke

Müller²,

dePamphilis

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

174

285

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“…In photosynthetic plants, this enzyme complex is associated with the thylakoid, and uses a proton gradient generated by light reactions to generate ATP. It has also been implicated in producing proton gradients (via ATP hydrolysis) to enable protein transport across thylakoid membranes of photosynthetic plants (Kohzuma et al, 2012;Kamikawa et al, 2015). Whether it functions in this way in full mycoheterotrophs that retain plastid ATP synthase is unknown; this would also presumably require retention of plastid internal membrane systems, present in some heterotrophs (e.g.…”

Section: Retention and Loss Of Photosynthesis Genes With Secondary Fumentioning

confidence: 99%

Plastomes on the edge: the evolutionary breakdown of mycoheterotroph plastid genomes

2017

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Contents 48I.48II.50III.5354References54 Summary We examine recent evidence for ratchet‐like genome degradation in mycoheterotrophs, plants that obtain nutrition from fungi. Initial loss of the NADH dehydrogenase‐like (NDH) complex may often set off an irreversible evolutionary cascade of photosynthetic gene losses. Genes for plastid‐encoded subunits of RNA polymerase and photosynthetic enzymes with secondary functions (Rubisco and ATP synthase) can persist initially, with nonsynchronous and quite broad windows in the relative timing of their loss. Delayed losses of five core nonbioenergetic genes (especially trnE and accD, which respectively code for glutamyl tRNA and a subunit of acetyl‐CoA carboxylase) probably explain long‐term persistence of heterotrophic plastomes. The observed range of changes of mycoheterotroph plastomes is similar to that of holoparasites, although greater diversity of both probably remains to be discovered. These patterns of gene loss/retention can inform research programs on plastome function.

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“…These characteristics are similar to those of E. gracilis transcriptomic data (Additional file 1: Figure S1; [7,9]) and suggest that our assembly covers the majority of genes in the E. longa genome. 31,742 E. longa transcript models (46%) possessed at least a partial spliced leader (SL) sequence as a sign of their 5'-end completeness. The percentage of transcripts with the SL sequence in E. gracilis was comparable (54%; [9]), even though SL absence was so far directly experimentally demonstrated only for mRNA of a single E. gracilis gene, the one encoding the nucleolar protein fibrillarin [26].…”

Section: Resultsmentioning

confidence: 99%

“…However, rps18 is missing from some other colourless plastid genomes, such as those of apicomplexans, the chlorophytes Helicosporidium sp., Prototheca stagnora, and Polytoma uvella, and the diatom Nitzschia sp. NIES-3581 [30][31][32].…”

Section: No Traces Of the Photosynthetic Machinery In The Transcriptomentioning

confidence: 99%

Peculiar features of the plastids of the colourless algaEuglena longaand photosynthetic euglenophytes unveiled by transcriptome analyses

Záhonová

Füssy

Birčák

et al. 2018

Preprint

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Background:Euglenophytes are an interesting algal group that emerged within the ancestrally plastid-lacking Euglenozoa phylum by acquiring a plastid from a green algal donor. However, the knowledge of euglenophyte plastid biology and evolution is highly incomplete, partly because euglenophytes have so far been little studied on a genome-and transcriptome-wide scale.Transcriptome data from only a single species, Euglena gracilis, have been exploited to functional insights, but aspects of the plastid biology have been largely neglected. Results:To expand the resources for studying euglenophyte biology and to improve our knowledge of the euglenophyte plastid function and evolution, we sequenced and analysed the transcriptome of the non-photosynthetic species Euglena longa. The transcriptomic data confirmed the absence of genes for the photosynthetic machinery in this species, but provided a number of candidate plastid-localized proteins bearing the same type of N-terminal bipartite topogenic signals (BTSs) as known from the photosynthetic species E. gracilis. Further comparative analyses using transcriptome assemblies available for E. gracilis and two additional photosynthetic euglenophytes of the genus Eutreptiella enabled us to unveil several salient aspects of the basic plastid infrastructure in euglenophytes. First, a number of plastidial proteins seem to reach the organelle as C-terminal translational fusions with other BTS-bearing proteins.Second, the conventional eubacteria-derived plastidial ribosomal protein L24 is missing and seems to have been replaced by very different homologs of the archaeo-eukaryotic origin. Third, no homologs of any key component of the TOC/TIC system (translocon of the outer/inner chloroplast membrane) and the plastid division apparatus are discernible in euglenophytes, and the machinery for intraplastidial protein targeting has been simplified by the loss of the cpSRP/cpFtsY system and the SEC2 translocon. Lastly, euglenophytes proved to encode a plastid-targeted homolog of the termination factor Rho horizontally acquired from a Lambdaproteobacteria-related donor, suggesting an unprecedented modification of the transcription mechanism in their plastid. Conclusions:Our study suggests that the euglenophyte plastid has been substantially remodelled comparted to its green algal progenitor by both loss of original and acquisition of novel molecular components, making it a particularly interesting subject for further studies. BackgroundEuglenophytes, exemplified by the highly studied mixotrophic alga Euglena gracilis, are a peculiar algal group constituting one of the many lineages of the phylum Euglenozoa [1].Euglenophytes and other euglenozoans share many unusual features, such as regulation of gene primarily at the post-transcriptional level [2][3][4]. Furthermore, euglenozoans employ trans-splicing to process mRNA molecules, whereby the 5'-end of pre-mRNA is replaced by the 5'-end of the specialized spliced leader (SL) RNA, resulting in the presence of the invariant SL sequence at th...

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Proposal of a Twin Aarginine Translocator System-Mediated Constraint against Loss of ATP Synthase Genes from Nonphotosynthetic Plastid Genomes

Cited by 47 publications

References 45 publications

Mechanistic model of evolutionary rate variation en route to a nonphotosynthetic lifestyle in plants

Mechanistic model of evolutionary rate variation en route to a nonphotosynthetic lifestyle in plants

Plastomes on the edge: the evolutionary breakdown of mycoheterotroph plastid genomes

Peculiar features of the plastids of the colourless algaEuglena longaand photosynthetic euglenophytes unveiled by transcriptome analyses

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