Highly syntenic and yet divergent: A tale of two Theilerias

Abstract

The published genomic sequences of the two major host-transforming Theileria species of cattle represent a rich resource of information, which has allowed novel bioinformatic and experimental studies into these important apicomplexan parasites. Since their publication in 2005, the genomes of T. annulata and T. parva have been utilised for a diverse range of applications, ranging from candidate antigen discovery to the identification of genetic markers for population analysis. This has led to advancements in the quest for a sub-unit vaccine, while providing a greater understanding of variation among parasite populations in the field. The unique ability of these Theileria species to induce host cell transformation is the subject of considerable scientific interest and the availability of full genomic sequences has also provided new insights into this area of research. This article reviews data underlying published comparative analyses, focussing on the general features of gene expression, the major Tpr/Tar multi-copy gene family and a reexamination of the predicted macroschizont secretome. Codon usage between the Theileria species is reviewed in detail, as this underpins ongoing comparative studies investigating selection at the intra-and inter-species level. The TashAT/TpshAT family of genes, conserved between T. annulata and T. parva, encodes products targeted to the host nucleus and has been implicated in contributing to the transformed bovine phenotype. Species-specific expansion and diversification at this critical locus is discussed, with reference to the availability, in the near future, of genomic datasets which are based on non-transforming Theileria species.

Evolution and diversity of secretome genes in the apicomplexan parasite Theileria annulata

“…The TashAT family is a 17-member family which is present in T. annulata with an orthologous family of genes in T. parva (TpHN) that show a significant level of synteny [13-15]. The majority of TashAT-encoded proteins are either predicted to be or have been demonstrated to locate to the host nucleus [1,13,14].…”

“…Representative examples of PEST and FAINT domain distribution for TashAT and SVSP sequences can be viewed in [7] and in Additional file 1. Significant divergence has occurred between the TashAT and TpHN gene families [1,15], and this is most easily detected by the specific absence of AT-hook DNA binding/nuclear localisation motifs in T. parva . However, the majority of the orthologous pairs encode the same basic putative functional motifs, which occur in the same general order and are frequently located in an identical or similar position [1].…”

“…However, the majority of the orthologous pairs encode the same basic putative functional motifs, which occur in the same general order and are frequently located in an identical or similar position [1]. Together with phylogenetic analysis [15] this strongly indicates that expansion and divergence of TashAT and TpHN genes have occurred to allow functions specific for each species to evolve, a postulation which predicts that functional motifs specific to orthologues of one species would be conserved within that species. To investigate this hypothesis, members of the TashAT gene family were selected for analysis of sequence diversity across different parasite isolates.…”

Jumbled Genomes: Missing Apicomplexan Synteny

“…The long-term conservation of synteny generally observed in chordates is also observed in some protists, for example, the kinetoplastids. In fact, one major difference between “model” chordates and parasitic protists is that rates of recombination and rearrangement are reported to be generally lower in protists (Kooij et al 2005), with considerable conservation present over great evolutionary distances in some lineages (El-Sayed et al 2005; Kooij et al 2005; Pain et al 2005; Peacock et al 2007; Weir et al 2009). In contrast, the Apicomplexa display an unprecedented degree of genome rearrangement with the near complete removal of synteny between major lineages within the phylum.…”

“…Despite the expansion of multicopy gene families and the generation of novel species-specific genes (Pain et al 2005, 2008; Kuo and Kissinger 2008; Weir et al 2009), the Apicomplexa have extremely small eukaryotic genomes characterized by gene loss. Overall, the removal of genetic material has outpaced the generation of novel DNA, resulting in small genome sizes.…”