Comparative genomics and community curation further improve gene annotations in the nematode Pristionchus pacificus

Abstract

Background Nematode model organisms such as Caenorhabditis elegans and Pristionchus pacificus are powerful systems for studying the evolution of gene function at a mechanistic level. However, the identification of P. pacificus orthologs of candidate genes known from C. elegans is complicated by the discrepancy in the quality of gene annotations, a common problem in nematode and invertebrate genomics. Results Here, we combine comparative genomic screens for suspicious gene models with community-based curation to further improve the quality of gene annotations in P. pacificus. We extend previous curations of one-to-one orthologs to larger gene families and also orphan genes. Cross-species comparisons of protein lengths, screens for atypical domain combinations and species-specific orphan genes resulted in 4311 candidate genes that were subject to community-based curation. Corrections for 2946 gene models were implemented in a new version of the P. pacificus gene annotations. The new set of gene annotations contains 28,896 genes and has a single copy ortholog completeness level of 97.6%. Conclusions Our work demonstrates the effectiveness of comparative genomic screens to identify suspicious gene models and the scalability of community-based approaches to improve the quality of thousands of gene models. Similar community-based approaches can help to improve the quality of gene annotations in other invertebrate species, including parasitic nematodes.

The community-curated Pristionchus pacificus genome facilitates automated gene annotation improvement in related nematodes

“…Previously, comparative genomic screens were combined with community curation to improve the quality of gene annotations in P. pacificus [ 4 ]. Here, the objective is to demonstrate how community curation of a single genome can be used to automatically improve the quality of phylogenomic data from related species.…”

“…Previous studies of novel gene origin in P. pacificus pointed towards an inflated number of species-specific orphan genes that are most likely gene prediction artifacts recognizing spurious coding signals on the antisense strand of truly protein-coding genes [ 10 ]. Thus, to facilitate more conclusive studies of gene birth processes using purely evidence-based set of gene annotations, species-specific genes without RNA-seq support were removed from current annotations [ 4 ]. Furthermore, other types of gene prediction artifacts such as artificially fused gene models do not necessarily impact BUSCO completeness levels but impair the detection of orthologs [ 3 ].…”

“…These transcribed ORFs were aligned against the respective reference assembly with the help of the exonerate protein2genome program with the following parameter settings: --bestn 2, −-dnawordlen 20, and --maxintron 20,000 (version 2.2.0) [ 28 ]. The homology model data set was generated by aligning P. pacificus proteins (El Paco gene annotation, version 3) against the reference assemblies using exonerate with the same parameter settings [ 4 ]. The -bestn option was set to two in order to annotate potential duplicates.…”

“…Currently, multiple representative genomes of the highly diverse and rapidly evolving nematode phylum are still poorly annotated. To overcome this problem in the case of the nematode model organism Pristionchus pacificus , community-based curations have recently been initiated to improve the quality of gene annotations [ 3 , 4 ]. P. pacificus was initially established for comparative studies with the classical nematode model organism Caenorhabditis elegans [ 5 ], but more recently it gained importance as an independent model system for elucidating the genetic basis of phenotypic plasticity [ 6 – 8 ] and the emergence of novel genes [ 9 – 11 ].…”

“…This motivated a screen for suspicious gene models based on comparative genomic approaches and to propose corrections after manual inspection by community annotators. Two rounds of community curations improved the BUSCO completeness level from 86 to 98% (nematode odb9 data set) [ 2 – 4 ].…”