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Review
. 2013 Aug;41(4):881-6.
doi: 10.1042/BST20130086.

Functional diversification of Argonautes in nematodes: an expanding universe

Amy H Buck  1 , Mark Blaxter
Affiliations
Review

Functional diversification of Argonautes in nematodes: an expanding universe

Amy H Buck et al. Biochem Soc Trans. 2013 Aug.

Abstract

In the last decade, many diverse RNAi (RNA interference) pathways have been discovered that mediate gene silencing at epigenetic, transcriptional and post-transcriptional levels. The diversity of RNAi pathways is inherently linked to the evolution of Ago (Argonaute) proteins, the central protein component of RISCs (RNA-induced silencing complexes). An increasing number of diverse Agos have been identified in different species. The functions of most of these proteins are not yet known, but they are generally assumed to play roles in development, genome stability and/or protection against viruses. Recent research in the nematode Caenorhabditis elegans has expanded the breadth of RNAi functions to include transgenerational epigenetic memory and, possibly, environmental sensing. These functions are inherently linked to the production of secondary siRNAs (small interfering RNAs) that bind to members of a clade of WAGOs (worm-specific Agos). In the present article, we review briefly what is known about the evolution and function of Ago proteins in eukaryotes, including the expansion of WAGOs in nematodes. We postulate that the rapid evolution of WAGOs enables the exceptional functional plasticity of nematodes, including their capacity for parasitism.

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Figures

Figure 1
Figure 1. Phylogenetic analysis of Ago proteins from Nematoda
(A) Cartoon of the phylogenetic relationships of the nematode species analysed, based on analyses of the nuclear small subunit ribosomal RNA gene. The colours associated with each species are used to decorate the subtrees in (C)–(J). Coloured stars on the subtrees indicate species-specific ‘blooms’ of paralogues. (B) The global tree of nematode Ago represented as an unrooted phylogram. We assume that each subtree is effectively rooted by the other subtrees, although we note that extreme divergence results in the support for structure within some subtrees being marginal. (C) The ALG1/ALG2 subtree, which contains representatives from all the nematode clades surveyed. (D) The RDE1/ERGO1 (endogenous RNAi-deficient Ago 1)/PRG1/PRG2 subtree, which contains no members from the animal parasites of Clade III. (E) The WAGO10/WAGO11/NRDE (nuclear RNAi-defective) subtree, which has wide representation across the Nematoda. (F) A SAGO2 (synthetic secondary siRNA-deficient Ago mutant 2)/PPW (PAZ/PIWI domain-containing) WAGO subtree, which is restricted to Caenorhabditis and P. pacificus. (G) A subtree of WAGO proteins, which lacks any members from Caenorhabditis, Clade IV or Clade I species, but is present in P. pacificus and animal parasites in Clades III and V. (H) The WAGO1/WAGO2/WAGO4/WAGO5 subtree, restricted to Clade IV and V nematode species, with a remarkable bloom of paralogues in P. redivivus. (I) This component of Ago diversity includes C. elegans CSR and a subtree of WAGO proteins restricted to Clade III, IV and V species, with a second paralogue bloom in P. redivivus. (J) The ALG3/ALG4 subtree, in which T. spiralis has a remarkable bloom of 119 distinct Ago proteins. Over 550 distinct Ago proteins (containing PIWI and PAZ domains) were obtained by extensive similarity searching of the NCBI NR protein database, WormBase nematode genome data (http://www.wormbase.org) and NEMBASE4 (http://www.nematodes.org), and aligned using CLUSTAL Omega. The alignment was analysed in MrBayes 3.2.1 using a mixed prior on amino acid evolution model, and run for 1 million generations. After visual inspection in Tracer (http://tree.bio.ed.ac.uk/software/tracer/), the first 500000 generations were discarded as burnin. The input sequences, alignment, MrBayes command block, treefiles and summary phylograms are available on DataDryad (doi:10.5061/dryad.5qs11). For improved clarity, a full-size PDF version of this Figure can be found at http://www.biochemsoctrans.org/bst/041/bst0410881add.htm.
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