Reductive evolution of chloroplasts in non-photosynthetic plants, algae and protists

Hadariová, Lucia; Vesteg, Matej; Hampl, Vladimı́r; Krajčovič, Juraj

doi:10.1007/s00294-017-0761-0

Cited by 69 publications

(71 citation statements)

References 225 publications

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“…We have sequenced and assembled the transcriptome of an interesting organism and a useful model for studying plastid reduction accompanying the loss of photosynthesis -a widespread phenomenon among non-photosynthetic plants, algae and protists [71]. Our analyses suggest that our E. longa transcriptome assembly provides a good representation of nucleus-encoded plastidtargeted proteins in general.…”

Section: Discussionmentioning

confidence: 96%

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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Section: Discussionmentioning

confidence: 96%

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

Záhonová

Füssy

Birčák

et al. 2018

Preprint

Self Cite

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“…The importance of photosynthesis to the nature of plants can be seen by comparing parasitic plants with their more typical autotrophic relatives. The anatomy of parasitic plants is often reduced to only haustoria‐like structures and reproductive organs (Kokla and Melnyk, ), and frequently there is the loss of plastids and photosynthetic genes (Hadariová et al ., ; Vogel et al ., ).…”

Section: The Genomic Complexity Of Photosynthesismentioning

confidence: 98%

Converging phenomics and genomics to study natural variation in plant photosynthetic efficiency

et al. 2019

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SummaryIn recent years developments in plant phenomic approaches and facilities have gradually caught up with genomic approaches. An opportunity lies ahead to dissect complex, quantitative traits when both genotype and phenotype can be assessed at a high level of detail. This is especially true for the study of natural variation in photosynthetic efficiency, for which forward genetics studies have yielded only a little progress in our understanding of the genetic layout of the trait. High‐throughput phenotyping, primarily from chlorophyll fluorescence imaging, should help to dissect the genetics of photosynthesis at the different levels of both plant physiology and development. Specific emphasis should be directed towards understanding the acclimation of the photosynthetic machinery in fluctuating environments, which may be crucial for the identification of genetic variation for relevant traits in food crops. Facilities should preferably be designed to accommodate phenotyping of photosynthesis‐related traits in such environments. The use of forward genetics to study the genetic architecture of photosynthesis is likely to lead to the discovery of novel traits and/or genes that may be targeted in breeding or bio‐engineering approaches to improve crop photosynthetic efficiency. In the near future, big data approaches will play a pivotal role in data processing and streamlining the phenotype‐to‐gene identification pipeline.

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“…The increase in the AT content in the plastid genomes of heterotrophic plants, as well as the increase in their substitution rates, are known and many times discussed phenomena (Bromham et al, 2013;Wicke et al, 2016;Hadariová et al, 2018;Wicke and Naumann, 2018). However, their origin is still unknown.…”

Section: Known Sizes Of Nuclear Genomes Of Plants From Santalales Varmentioning

confidence: 99%

Rhopalocnemis phalloides has one of the most reduced and mutated plastid genomes known

Schelkunov

Nuraliev

Logacheva

2018

Preprint

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Although most plant species are photosynthetic, several hundred species have lost the ability to photosynthesize and instead obtain nutrients via various types of heterotrophic feeding. Their genomes, especially plastid genomes, markedly differ from the genomes of photosynthetic plants. In this work, we describe the sequenced plastid genome of the heterotrophic plant Rhopalocnemis phalloides, which belongs to the family Balanophoraceae and feeds by parasitizing on other plants. The genome is highly reduced (18 622 base pairs versus approximately 150 kilobase pairs in autotrophic plants) and possesses an outstanding AT content, 86.8%, the highest of all sequenced plant plastid genomes. The gene content of this genome is quite typical of heterotrophic plants, with all of the genes related to photosynthesis having been lost. The remaining genes are notably distorted by a high mutation rate and the aforementioned AT content. The high AT content has led to sequence convergence between some of the remaining genes and their homologues from AT-rich plastid genomes of protists. Overall, the plastid genome of R. phalloides is one of the most unusual plastid genomes known.

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Reductive evolution of chloroplasts in non-photosynthetic plants, algae and protists

Cited by 69 publications

References 225 publications

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

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

Converging phenomics and genomics to study natural variation in plant photosynthetic efficiency

Rhopalocnemis phalloides has one of the most reduced and mutated plastid genomes known

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