Origin and evolution of glutamyl-prolyl tRNA synthetase WHEP domains reveal evolutionary relationships within Holozoa - PubMed (original) (raw)

Origin and evolution of glutamyl-prolyl tRNA synthetase WHEP domains reveal evolutionary relationships within Holozoa

Partho Sarothi Ray et al. PLoS One. 2014.

Abstract

Repeated domains in proteins that have undergone duplication or loss, and sequence divergence, are especially informative about phylogenetic relationships. We have exploited divergent repeats of the highly structured, 50-amino acid WHEP domains that join the catalytic subunits of bifunctional glutamyl-prolyl tRNA synthetase (EPRS) as a sequence-informed repeat (SIR) to trace the origin and evolution of EPRS in holozoa. EPRS is the only fused tRNA synthetase, with two distinct aminoacylation activities, and a non-canonical translation regulatory function mediated by the WHEP domains in the linker. Investigating the duplications, deletions and divergence of WHEP domains, we traced the bifunctional EPRS to choanozoans and identified the fusion event leading to its origin at the divergence of ichthyosporea and emergence of filozoa nearly a billion years ago. Distribution of WHEP domains from a single species in two or more distinct clades suggested common descent, allowing the identification of linking organisms. The discrete assortment of choanoflagellate WHEP domains with choanozoan domains as well as with those in metazoans supported the phylogenetic position of choanoflagellates as the closest sister group to metazoans. Analysis of clustering and assortment of WHEP domains provided unexpected insights into phylogenetic relationships amongst holozoan taxa. Furthermore, observed gaps in the transition between WHEP domain groupings in distant taxa allowed the prediction of undiscovered or extinct evolutionary intermediates. Analysis based on SIR domains can provide a phylogenetic counterpart to palaentological approaches of discovering "missing links" in the tree of life.

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Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Figure 1

Figure 1. WHEP domains in multiple deuterosome species.

(A) Domain model of human EPRS consisting of an ERS domain, 3 helix-turn-helix WHEP domains, and a PRS domain. (B) Phylogenetic analysis of WHEP domains in selected deuterostomes. 71 WHEP domain sequences from 14 vertebrate, one cephalochordate, two urochordate, one hemichordate, and one echino­derm species were used to construct a maximum-likelihood tree. Individual WHEP domains were identified by dot matrix analysis against Homo sapiens EPRS linker domain. The 50-amino acid sequences were multiple sequence-aligned and the alignment used for constructing the phylogenetic tree. The same taxa were also used to construct trees by neighbor-joining and Bayesian inference algorithms. Nodes supported by two or three tree-bulding algorithms are indicated by “*” and “**”, respectively. WHEP domains showing assortment in multiple clades are highlighted.

Figure 2

Figure 2. Phylogenetic analysis of WHEP domains in selected protostomes.

77 WHEP domain sequences from 18 protostomes that included 11 arthropod, two annelid, one mollusc, and four nematode species were used to construct a maximum-likelihood tree. Individual WHEP domains were identified by dot matrix analysis against Drosophila melanogaster EPRS linker domain. Phylogenetic trees were constructed and analyzed as in Figure 1.

Figure 3

Figure 3. Phylogenetic analysis of WHEP domains in selected basal metazoans, choanozoans, and representative bilateria.

Fifty WHEP domain sequences from the EPRS of two cnidarian, one placozoan, two poriferan, two choanoflagellate, one filastarean, and one icthyosporean species, together with 31 WHEP domain sequences from representative bilaterian species that included both protostomes and deuterostomes were used to construct a maximum-likelihood tree. Individual WHEP domains were identified by dot matrix analysis against Nematostella vectensis EPRS linker domain. Phylogenetic trees were constructed and analyzed as in Figure 1.

Figure 4

Figure 4. Species trees derived from WHEP domain analyses.

(A) Schematic representation of a putative species tree generated by collapsing WHEP domain groupings designated as “a”, “b” or “c” in Figure 3. Nodes (open circles) represent EPRS WHEP domain combinations of putative ancestral species whereas the terminal leaves represent known WHEP domain combinations of extant or predicted (filled circles) organisms. The putative genomic changes leading to various combinations of WHEP domains are indicated in parentheses. (B) Schematic representation of a putative species tree derived from the WHEP domain groupings “c′”, “u”, “v” and “f” indicated in Figure 1. The WHEP domain grouping “c” in Figure 3 and in (a) is indicated as the precursor of the deuterostome WHEP domains.

References

    1. Rokas A, King N, Finnerty J, Carroll SB (2003) Conflicting phylogenetic signals at the base of the metazoan tree. Evol Dev 5: 346–359. - PubMed
    1. Baldauf SL, Roger AJ, Wenk-Siefert I, Doolittle WF (2000) A kingdom-level phylogeny of eukaryotes based on combined protein data. Science 290: 972–977. - PubMed
    1. Wolf YI, Rogozin IB, Koonin EV (2004) Coelomata and not Ecdysozoa: evidence from genome-wide phylogenetic analysis. Genome Res 14: 29–36. - PMC - PubMed
    1. Salichos L, Rokas A (2013) Inferring ancient divergences requires genes with strong phylogenetic signals. Nature 497: 327–331. - PubMed
    1. Rokas A, Holland PW (2000) Rare genomic changes as a tool for phylogenetics. Trends Ecol Evol 15: 454–459. - PubMed

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