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Plastid genomes of two brown algae, Ectocarpus siliculosus and Fucus vesiculosus: further insights on the evolution of red-algal derived plastids.

ABSTRACT: BACKGROUND:Heterokont algae, together with cryptophytes, haptophytes and some alveolates, possess red-algal derived plastids. The chromalveolate hypothesis proposes that the red-algal derived plastids of all four groups have a monophyletic origin resulting from a single secondary endosymbiotic event. However, due to incongruence between nuclear and plastid phylogenies, this controversial hypothesis remains under debate. Large-scale genomic analyses have shown to be a powerful tool for phylogenetic reconstruction but insufficient sequence data have been available for red-algal derived plastid genomes. RESULTS:The chloroplast genomes of two brown algae, Ectocarpus siliculosus and Fucus vesiculosus, have been fully sequenced. These species represent two distinct orders of the Phaeophyceae, which is a major group within the heterokont lineage. The sizes of the circular plastid genomes are 139,954 and 124,986 base pairs, respectively, the size difference being due principally to the presence of longer inverted repeat and intergenic regions in E. siliculosus. Gene contents of the two plastids are similar with 139-148 protein-coding genes, 28-31 tRNA genes, and 3 ribosomal RNA genes. The two genomes also exhibit very similar rearrangements compared to other sequenced plastid genomes. The tRNA-Leu gene of E. siliculosus lacks an intron, in contrast to the F. vesiculosus and other heterokont plastid homologues, suggesting its recent loss in the Ectocarpales. Most of the brown algal plastid genes are shared with other red-algal derived plastid genomes, but a few are absent from raphidophyte or diatom plastid genomes. One of these regions is most similar to an apicomplexan nuclear sequence. The phylogenetic relationship between heterokonts, cryptophytes and haptophytes (collectively referred to as chromists) plastids was investigated using several datasets of concatenated proteins from two cyanobacterial genomes and 18 plastid genomes, including most of the available red algal and chromist plastid genomes. CONCLUSION:The phylogenetic studies using concatenated plastid proteins still do not resolve the question of the monophyly of all chromist plastids. However, these results support both the monophyly of heterokont plastids and that of cryptophyte and haptophyte plastids, in agreement with nuclear phylogenies.

SUBMITTER: Le Corguille G

PROVIDER: S-EPMC2765969 | biostudies-literature | 2009 Oct

REPOSITORIES: biostudies-literature

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Plastid genomes of two brown algae, Ectocarpus siliculosus and Fucus vesiculosus: further insights on the evolution of red-algal derived plastids.

Le Corguillé Gildas G Pearson Gareth G Valente Marta M Viegas Carla C Gschloessl Bernhard B Corre Erwan E Bailly Xavier X Peters Akira F AF Jubin Claire C Vacherie Benoit B Cock J Mark JM Leblanc Catherine C

BMC evolutionary biology 20091016

<h4>Background</h4>Heterokont algae, together with cryptophytes, haptophytes and some alveolates, possess red-algal derived plastids. The chromalveolate hypothesis proposes that the red-algal derived plastids of all four groups have a monophyletic origin resulting from a single secondary endosymbiotic event. However, due to incongruence between nuclear and plastid phylogenies, this controversial hypothesis remains under debate. Large-scale genomic analyses have shown to be a powerful tool for ph ...[more]

PMID: 19835607

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Project description:BACKGROUND: Brown algae are sessile macro-organisms of great ecological relevance in coastal ecosystems. They evolved independently from land plants and other multicellular lineages, and therefore hold several original ontogenic and metabolic features. Most brown algae grow along the coastal zone where they face frequent environmental changes, including exposure to toxic levels of heavy metals such as copper (Cu). RESULTS: We carried out large-scale transcriptomic and metabolomic analyses to decipher the short-term acclimation of the brown algal model E. siliculosus to Cu stress, and compared these data to results known for other abiotic stressors. This comparison demonstrates that Cu induces oxidative stress in E. siliculosus as illustrated by the transcriptomic overlap between Cu and H2O2 treatments. The common response to Cu and H2O2 consisted in the activation of the oxylipin and the repression of inositol signaling pathways, together with the regulation of genes coding for several transcription-associated proteins. Concomitantly, Cu stress specifically activated a set of genes coding for orthologs of ABC transporters, a P1B-type ATPase, ROS detoxification systems such as a vanadium-dependent bromoperoxidase, and induced an increase of free fatty acid contents. Finally we observed, as a common abiotic stress mechanism, the activation of autophagic processes on one hand and the repression of genes involved in nitrogen assimilation on the other hand. CONCLUSIONS: Comparisons with data from green plants indicate that some processes involved in Cu and oxidative stress response are conserved across these two distant lineages. At the same time the high number of yet uncharacterized brown alga-specific genes induced in response to copper stress underlines the potential to discover new components and molecular interactions unique to these organisms. Of particular interest for future research is the potential cross-talk between reactive oxygen species (ROS)-, myo-inositol-, and oxylipin signaling.

Project description:BackgroundThe fucoid brown algae (Heterokontophyta, Phaeophyceae) are increasingly the focus of ecological genetics, biodiversity, biogeography and speciation research. The molecular genetics underlying mating system variation, where repeated dioecious - hermaphrodite switches during evolution are recognized, and the molecular evolution of sex-related genes are key questions currently hampered by a lack of genomic information. We therefore undertook a comparative analysis of male and female reproductive tissue transcriptomes against a vegetative background during natural reproductive cycles in Fucus vesiculosus.ResultsOver 300 k reads were assembled and annotated against public protein databases including a brown alga. Compared with the vegetative tissue, photosynthetic and carbohydrate metabolism pathways were under-expressed, particularly in male tissue, while several pathways involved in genetic information processing and replication were over-expressed. Estimates of sex-biased gene (SBG) expression were higher for male (14% of annotated orthologues) than female tissue (9%) relative to the vegetative background. Mean expression levels and variance were also greater in male- than female-biased genes. Major female-biased genes were carbohydrate-modifying enzymes with likely roles in zygote cell wall biogenesis and/or modification. Male-biased genes reflected distinct sperm development and function, and orthologues for signal perception (a phototropin), transduction (several kinases), and putatively flagella-localized proteins (including candidate gamete-recognition proteins) were uniquely expressed in males. Overall, the results suggest constraint on female-biased genes (possible pleiotropy), and less constrained male-biased genes, mostly associated with sperm-specific functions.ConclusionsOur results support the growing contention that males possess a large array of genes regulating male fitness, broadly supporting findings in evolutionarily distant heterogametic animal models. This work identifies an annotated set of F. vesiculosus gene products that potentially regulate sexual reproduction and may contribute to prezygotic isolation, one essential step towards developing tools for a functional understanding of species isolation and differentiation.

Dataset Information

Plastid genomes of two brown algae, Ectocarpus siliculosus and Fucus vesiculosus: further insights on the evolution of red-algal derived plastids.

Publications

Plastid genomes of two brown algae, Ectocarpus siliculosus and Fucus vesiculosus: further insights on the evolution of red-algal derived plastids.

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