Evolution of Chloroplast Transcript Processing in Plasmodium and Its Chromerid Algal Relatives

Abstract

It is well understood that apicomplexan parasites, such as the malaria pathogen Plasmodium, are descended from free-living algae, and maintain a vestigial chloroplast that has secondarily lost all genes of photosynthetic function. Recently, two fully photosynthetic relatives of parasitic apicomplexans have been identified, the ‘chromerid’ algae Chromera velia and Vitrella brassicaformis, which retain photosynthesis genes within their chloroplasts. Elucidating the processes governing gene expression in chromerid chloroplasts might provide valuable insights into the origins of parasitism in the apicomplexans. We have characterised chloroplast transcript processing pathways in C. velia, V. brassicaformis and P. falciparum with a focus on the addition of an unusual, 3′ poly(U) tail. We demonstrate that poly(U) tails in chromerids are preferentially added to transcripts that encode proteins that are directly involved in photosynthetic electron transfer, over transcripts for proteins that are not involved in photosynthesis. To our knowledge, this represents the first chloroplast transcript processing pathway to be associated with a particular functional category of genes. In contrast, Plasmodium chloroplast transcripts are not polyuridylylated. We additionally present evidence that poly(U) tail addition in chromerids is involved in the alternative processing of polycistronic precursors covering multiple photosynthesis genes, and appears to be associated with high levels of transcript abundance. We propose that changes to the chloroplast transcript processing machinery were an important step in the loss of photosynthesis in ancestors of parasitic apicomplexans.

Author Summary

Chloroplasts contain their own genomes, containing two broad functional types of gene: genes encoding proteins directly involved in photosynthesis, and genes with a non-photosynthesis function, such as cofactor biosynthesis, assembly of protein complexes, or expression of the chloroplast genome. Thus far, to our knowledge, no chloroplast gene expression pathways in any lineage have been found to target one functional category of gene specifically. Here, we show that a chloroplast RNA processing pathway – the addition of a 3′ poly(U) tail – is specifically associated with photosynthesis genes in two species of algae, the ‘chromerids’ Chromera and Vitrella. The addition of the poly(U) tail enables the precise processing of mature photosynthesis gene transcripts from precursor RNA, and is likely to be essential for expression of the chromerid photosynthesis machinery. The chromerid algae are the closest photosynthetic relatives of a parasitic group of eukaryotes, the apicomplexans, which include the malaria pathogen Plasmodium. Apicomplexans are descended from algae, and retain a reduced chloroplast, which contains genes only of non-photosynthesis function. We have confirmed that 3′ poly(U) tails are not added to Plasmodium chloroplast transcripts. The expression pathways associated with photosynthesis genes have therefore been lost in the evolution of the apicomplexan chloroplast, and this loss could potentially have driven the transition from photosynthesis to parasitism.