Gene-Specific Signatures of Elevated Non-Synonymous Substitution Rates Correlate Poorly across the Plasmodium Genus

Weedall, Gareth D.; Polley, Spencer D.; Conway, David J.

doi:10.1371/journal.pone.0002281

Cited by 14 publications

(11 citation statements)

References 78 publications

(24 reference statements)

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“…3 c). This is consistent with the previously constructed phylogenetic topology based on partial mitochondrial genomes ( Escalante et al, 1998 , Carlton et al, 2008b ) as well as genes encoding surface antigens ( Weedall et al, 2008 ). The sequence-based phylogenetic tree(s) are different from the transcriptional differences that is reflective of its mammalian host lineage (as mentioned above) ( Fig.…”

Section: Resultssupporting

confidence: 91%

Integrated analysis of the Plasmodium species transcriptome

et al. 2016

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The genome sequence available for different Plasmodium species is a valuable resource for understanding malaria parasite biology. However, comparative genomics on its own cannot fully explain all the species-specific differences which suggests that other genomic aspects such as regulation of gene expression play an important role in defining species-specific characteristics. Here, we developed a comprehensive approach to measure transcriptional changes of the evolutionary conserved syntenic orthologs during the intraerythrocytic developmental cycle across six Plasmodium species. We show significant transcriptional constraint at the mid-developmental stage of Plasmodium species while the earliest stages of parasite development display the greatest transcriptional variation associated with critical functional processes. Modeling of the evolutionary relationship based on changes in transcriptional profile reveal a phylogeny pattern of the Plasmodium species that strictly follows its mammalian hosts. In addition, the work shows that transcriptional conserved orthologs represent potential future targets for anti-malaria intervention as they would be expected to carry out key essential functions within the parasites. This work provides an integrated analysis of orthologous transcriptome, which aims to provide insights into the Plasmodium evolution thereby establishing a framework to explore complex pathways and drug discovery in Plasmodium species with broad host range.

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Section: Resultssupporting

confidence: 91%

Integrated analysis of the Plasmodium species transcriptome

et al. 2016

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“…As expected for genes evolving under diversifying selection, d AA for these genes is relatively high, with all values above the 50th percentile. The regression residual values associated with these genes are also relatively high (none is among the lowest 25th percentile), suggesting that patterns of positive selection are not necessarily constant across lineages, as previously observed ( Weedall et al 2008 ).…”

Section: Resultssupporting

confidence: 50%

“…Many Plasmodium genes evolving under strong diversifying selection will be absent from our data sets, because they will not satisfy the stringent homology criteria of our HQ data sets. In fact, of a set of 43 P. faciparum genes expected to evolve under positive selection ( Weedall et al 2008 ) only seven are captured in at least one of our four comparisons ( supplementary table S2 , Supplementary Material online). As expected for genes evolving under diversifying selection, d AA for these genes is relatively high, with all values above the 50th percentile.…”

Section: Resultsmentioning

confidence: 99%

A New Method for Estimating Species Age Supports the Coexistence of Malaria Parasites and Their Mammalian Hosts

Silva

Egan

Arze

et al. 2015

Molecular Biology and Evolution

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Species in the genus Plasmodium cause malaria in humans and infect a variety of mammals and other vertebrates. Currently, estimated ages for several mammalian Plasmodium parasites differ by as much as one order of magnitude, an inaccuracy that frustrates reliable estimation of evolutionary rates of disease-related traits. We developed a novel statistical approach to dating the relative age of evolutionary lineages, based on Total Least Squares regression. We validated this lineage dating approach by applying it to the genus Drosophila. Using data from the Drosophila 12 Genomes project, our approach accurately reconstructs the age of well-established Drosophila clades, including the speciation event that led to the subgenera Drosophila and Sophophora, and age of the melanogaster species subgroup. We applied this approach to hundreds of loci from seven mammalian Plasmodium species. We demonstrate the existence of a molecular clock specific to individual Plasmodium proteins, and estimate the relative age of mammalian-infecting Plasmodium. These analyses indicate that: 1) the split between the human parasite Plasmodium vivax and P. knowlesi, from Old World monkeys, occurred 6.1 times earlier than that between P. falciparum and P. reichenowi, parasites of humans and chimpanzees, respectively; and 2) mammalian Plasmodium parasites originated 22 times earlier than the split between P. falciparum and P. reichenowi. Calibrating the absolute divergence times for Plasmodium with eukaryotic substitution rates, we show that the split between P. falciparum and P. reichenowi occurred 3.0–5.5 Ma, and that mammalian Plasmodium parasites originated over 64 Ma. Our results indicate that mammalian-infecting Plasmodium evolved contemporaneously with their hosts, with little evidence for parasite host-switching on an evolutionary scale, and provide a solid timeframe within which to place the evolution of new Plasmodium species.

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“…In these studies, dN/dS was calculated from pairwise alignments resulting in ratios which are a composite of substitutions in both lineages compared since their divergence from their last common ancestor. Using an outgroup species allows the calculation of lineage-specific dN/dS (Arbiza et al 2006;Bakewell et al 2007;Kawahara & Imanishi 2007;Weedall et al 2008;Parmakelis et al 2010;Toll-Riera et al 2011) which could unmask further genes with species-specific signatures of positive selection and/or potentially stronger associations between certain genomic characteristics and the rate of sequence evolution. The model plant Arabidopsis thaliana is an ideal organism for investigating genomewide signatures of selection in the plant taxa as a sister species, Arabidopsis lyrata (with an estimated 13 mya divergence time from A. thaliana), has been sequenced (Hu et al 2011).…”

Section: Introductionmentioning

confidence: 99%

Lineage‐specific sequence evolution and exon edge conservation partially explain the relationship between evolutionary rate and expression level in A. thaliana

2015

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Rapidly evolving proteins can aid the identification of genes underlying phenotypic adaptation across taxa, but functional and structural elements of genes can also affect evolutionary rates. In plants, the ‘edges’ of exons, flanking intron junctions, are known to contain splice enhancers and to have a higher degree of conservation compared to the remainder of the coding region. However, the extent to which these regions may be masking indicators of positive selection or account for the relationship between dN/dS and other genomic parameters is unclear. We investigate the effects of exon edge conservation on the relationship of dN/dS to various sequence characteristics and gene expression parameters in the model plant Arabidopsis thaliana. We also obtain lineage-specific dN/dS estimates, making use of the recently sequenced genome of Thellungiella parvula, the second closest sequenced relative after the sister species Arabidopsis lyrata. Overall, we find that the effect of exon edge conservation, as well as the use of lineage-specific substitution estimates, upon dN/dS ratios partly explains the relationship between the rates of protein evolution and expression level. Furthermore, the removal of exon edges shifts dN/dS estimates upwards, increasing the proportion of genes potentially under adaptive selection. We conclude that lineage-specific substitutions and exon edge conservation have an important effect on dN/dS ratios and should be considered when assessing their relationship with other genomic parameters.

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Gene-Specific Signatures of Elevated Non-Synonymous Substitution Rates Correlate Poorly across the Plasmodium Genus

Cited by 14 publications

References 78 publications

Integrated analysis of the Plasmodium species transcriptome

Integrated analysis of the Plasmodium species transcriptome

A New Method for Estimating Species Age Supports the Coexistence of Malaria Parasites and Their Mammalian Hosts

Lineage‐specific sequence evolution and exon edge conservation partially explain the relationship between evolutionary rate and expression level in A. thaliana

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