Molecular evolution of glycoside hydrolase genes in the Western corn rootworm (Diabrotica virgifera virgifera)

PLoS One. 2014 Apr 9;9(4):e94052. doi: 10.1371/journal.pone.0094052. eCollection 2014.

Abstract

Cellulose is an important nutritional resource for a number of insect herbivores. Digestion of cellulose and other polysaccharides in plant-based diets requires several types of enzymes including a number of glycoside hydrolase (GH) families. In a previous study, we showed that a single GH45 gene is present in the midgut tissue of the western corn rootworm, Diabrotica virgifera virgifera (Coleoptera: Chrysomelidae). However, the presence of multiple enzymes was also suggested by the lack of a significant biological response when the expression of the gene was silenced by RNA interference. In order to clarify the repertoire of cellulose-degrading enzymes and related GH family proteins in D. v. virgifera, we performed next-generation sequencing and assembled transcriptomes from the tissue of three different developmental stages (eggs, neonates, and third instar larvae). Results of this study revealed the presence of seventy-eight genes that potentially encode GH enzymes belonging to eight families (GH45, GH48, GH28, GH16, GH31, GH27, GH5, and GH1). The numbers of GH45 and GH28 genes identified in D. v. virgifera are among the largest in insects where these genes have been identified. Three GH family genes (GH45, GH48, and GH28) are found almost exclusively in two coleopteran superfamilies (Chrysomeloidea and Curculionoidea) among insects, indicating the possibility of their acquisitions by horizontal gene transfer rather than simple vertical transmission from ancestral lineages of insects. Acquisition of GH genes by horizontal gene transfers and subsequent lineage-specific GH gene expansion appear to have played important roles for phytophagous beetles in specializing on particular groups of host plants and in the case of D. v. virgifera, its close association with maize.

Publication types

  • Comparative Study
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Sequence
  • Animals
  • Coleoptera / genetics*
  • Evolution, Molecular
  • Gene Expression Regulation, Developmental
  • Genes, Insect*
  • Glycoside Hydrolases / biosynthesis
  • Glycoside Hydrolases / classification
  • Glycoside Hydrolases / genetics*
  • Insect Proteins / biosynthesis
  • Insect Proteins / classification
  • Insect Proteins / genetics*
  • Larva / enzymology
  • Molecular Sequence Data
  • Ovum / enzymology
  • Phylogeny
  • RNA Interference
  • Sequence Alignment
  • Sequence Analysis, RNA
  • Sequence Homology, Amino Acid
  • Transcriptome

Substances

  • Insect Proteins
  • Glycoside Hydrolases

Grants and funding

This work was supported by the Consortium for Plant Biotechnology Research (CPBR Agreement GO12026-333) and Pioneer Hi-Bred International. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.