title: Horizontal gene transfer and functional diversification of plant cell wall degrading polygalacturonases: Key events in the evolution of herbivory in beetles.
abstract: Plant cell walls are the largest reservoir of organic carbon on earth. To breach and utilize this carbohydrate-rich protective barrier, microbes secrete plant cell wall degrading enzymes (PCWDEs) targeting pectin, cellulose and hemicelluloses. There is a growing body of evidence that genomes of some herbivorous insects also encode PCWDEs, raising questions about their evolutionary origins and functions. Among herbivorous beetles, pectin-degrading polygalacturonases (PGs) are found in the diverse superfamilies Chrysomeloidea (leaf beetles, long-horn beetles) and Curculionoidea (weevils). Here our aim was to test whether these arose from a common ancestor of beetles or via horizontal gene transfer (HGT), and whether PGs kept their ancestral function in degrading pectin or evolved novel functions. Transcriptome data derived from 10 beetle species were screened for PG-encoding sequences and used for phylogenetic comparisons with their bacterial, fungal and plant counterparts. These analyses revealed a large family of PG-encoding genes of Chrysomeloidea and Curculionoidea sharing a common ancestor, most similar to PG genes of ascomycete fungi. In addition, 50 PGs from beetle digestive systems were heterologously expressed and functionally characterized, showing a set of lineage-specific consecutively pectin-degrading enzymes, as well as conserved but enzymatically inactive PG proteins. The evidence indicates that a PG gene was horizontally transferred ∼200 million years ago from an ascomycete fungus to a common ancestor of Chrysomeloidea and Curculionoidea. This has been followed by independent duplications in these two lineages, as well as independent replacement in two sublineages of Chrysomeloidea by two other subsequent HGTs. This origin, leading to subsequent functional diversification of the PG gene family within its new hosts, was a key event promoting the evolution of herbivory in these beetles.
authors: Department of Entomology, Max Planck Institute for Chemical Ecology, Hans-Knoell-Str. 8, 07745 Jena, Germany. Electronic address: rkirsch@ice.mpg.de.
authors: Roy
authors: R
authors: Kirsch
authors: Department of Genetics, Friedrich Schiller University Jena, Philosophenweg 12, 07743 Jena, Germany.
authors: Lydia
authors: L
authors: Gramzow
authors: Department of Genetics, Friedrich Schiller University Jena, Philosophenweg 12, 07743 Jena, Germany.
authors: Günter
authors: G
authors: Theißen
authors: Department of Entomology, University of Nebraska, 312A Entomology Hall, Lincoln, 68583-0816 NE, United States.
authors: Blair D
authors: BD
authors: Siegfried
authors: Biosciences, University of Exeter, Penryn TR10 9EZ, United Kingdom.
authors: Richard H
authors: RH
authors: Ffrench-Constant
authors: Department of Entomology, Max Planck Institute for Chemical Ecology, Hans-Knoell-Str. 8, 07745 Jena, Germany.
authors: David G
authors: DG
authors: Heckel
authors: Department of Entomology, Max Planck Institute for Chemical Ecology, Hans-Knoell-Str. 8, 07745 Jena, Germany. Electronic address: ypauchet@ice.mpg.de.
authors: Yannick
authors: Y
authors: Pauchet
mesh_terms: D000818:Animals; D001203:Ascomycota / Q000201:enzymology / Q000235:genetics; D001483:Base Sequence; D005075:Biological Evolution; D002473:Cell Wall; D001517:Coleoptera / Q000201:enzymology* / Q000235:genetics*; D022761:Gene Transfer, Horizontal; D060434:Herbivory / Q000235:genetics*; D008969:Molecular Sequence Data; D010368:Pectins / Q000378:metabolism; D010802:Phylogeny; D010944:Plants / Q000469:parasitology; D011096:Polygalacturonase / Q000235:genetics*; D059467:Transcriptome
chemical_list: D010368:Pectins; D011096:Polygalacturonase
keywords: Glycoside hydrolase; Horizontal gene transfer; Leaf beetles; Plant cell wall degradation; Weevils