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Punctuated plastome reduction and host-parasite horizontal gene transfer in the holoparasitic plant genus Aphyllon.

ABSTRACT: Foundational studies of chloroplast genome (plastome) evolution in parasitic plants have focused on broad trends across large clades, particularly among the Orobanchaceae, a species-rich and ecologically diverse family of root parasites. However, the extent to which such patterns and processes of plastome evolution, such as stepwise gene loss following the complete loss of photosynthesis (shift to holoparasitism), are detectable at shallow evolutionary time scale is largely unknown. We used genome skimming to assemble eight chloroplast genomes representing complete taxonomic sampling of Aphyllon sect. Aphyllon, a small clade within the Orobanchaceae that evolved approximately 6 Ma, long after the origin of holoparasitism. We show substantial plastome reduction occurred in the stem lineage, but subsequent change in plastome size, gene content, and structure has been relatively minimal, albeit detectable. This lends additional fine-grained support to existing models of stepwise plastome reduction in holoparasitic plants. Additionally, we report phylogenetic evidence based on an rbcL gene tree and assembled 60+ kb fragments of the Aphyllon epigalium mitochondrial genome indicating host-to-parasite horizontal gene transfers (hpHGT) of several genes originating from the plastome of an ancient Galium host into the mitochondrial genome of a recent common ancestor of A. epigalium Ecologically, this evidence of hpHGT suggests that the host-parasite associations between Galium and A. epigalium have been stable at least since its subspecies diverged hundreds of thousands of years ago.

SUBMITTER: Schneider AC

PROVIDER: S-EPMC6170807 | biostudies-literature | 2018 Sep

REPOSITORIES: biostudies-literature

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Publications

Punctuated plastome reduction and host-parasite horizontal gene transfer in the holoparasitic plant genus <i>Aphyllon</i>.

Schneider Adam C AC Chun Harold H Stefanović Saša S Baldwin Bruce G BG

Proceedings. Biological sciences 20180919 1887

Foundational studies of chloroplast genome (plastome) evolution in parasitic plants have focused on broad trends across large clades, particularly among the Orobanchaceae, a species-rich and ecologically diverse family of root parasites. However, the extent to which such patterns and processes of plastome evolution, such as stepwise gene loss following the complete loss of photosynthesis (shift to holoparasitism), are detectable at shallow evolutionary time scale is largely unknown. We used geno ...[more]

PMID: 30232155

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Project description:UNLABELLED:Microsporidia are a group of obligate intracellular parasites that are best known for their unique infection mechanism and their unparalleled levels of genomic reduction and compaction. We sequenced the genome of Ordospora colligata, a gut parasite of the microcrustacean Daphnia sp. and the closest known relative to the microsporidia characterized by the most extreme genomic reduction, the model genus Encephalitozoon. We found that the O. colligata genome is as compact as those of Encephalitozoon spp., featuring few introns and a similar complement of about 2,000 genes, altogether showing that the extreme reduction took place before the origin of Encephalitozoon spp. and their adaptation to vertebrate hosts. We also found that the O. colligata genome has acquired by horizontal transfer from its animal host a septin that is structurally analogous to septin 7, a protein that plays a major role in the endocytosis-based invasion mechanism of the fungal pathogen Candida albicans. Microsporidian invasion is most often characterized by injection through a projectile tube, but microsporidia are also known to invade cells by inducing endocytosis. Given the function of septins in other systems, we hypothesize that the acquired septin could help O. colligata induce its uptake by mimicking host receptors. IMPORTANCE:The smallest known eukaryotic genomes are found in members of the Encephalitozoon genus of microsporidian parasites. Their extreme compaction, however, is not characteristic of the group, whose genomes can differ by an order of magnitude. The processes and evolutionary forces that led the Encephalitozoon genomes to shed so much of their ancestral baggage are unclear. We sequenced the genome of Ordospora colligata, a parasite of the water flea Daphnia sp. and the closest known relative of Encephalitozoon species, and show that this extreme reduction predated the split between the two lineages. We also found that O. colligata has acquired a septin gene by host-to-parasite horizontal transfer and predicted that the encoded protein folds like a septin 7, which plays a major role in endocytosis. We hypothesize that this acquisition could help O. colligata parasitize its hosts by facilitating endocytic infection, a mechanism that occurs in microsporidia but that is not yet well understood.

Dataset Information

Punctuated plastome reduction and host-parasite horizontal gene transfer in the holoparasitic plant genus Aphyllon.

Publications

Punctuated plastome reduction and host-parasite horizontal gene transfer in the holoparasitic plant genus <i>Aphyllon</i>.

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