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Open Access Highly Accessed Research article

Distribution and evolution of glycoside hydrolase family 45 cellulases in nematodes and fungi

Juan E Palomares-Rius12, Yuuri Hirooka34, Isheng J Tsai1, Hayato Masuya3, Akina Hino1, Natsumi Kanzaki3, John T Jones56 and Taisei Kikuchi13*

Author Affiliations

1 Division of Parasitology, Faculty of Medicine, University of Miyazaki, Miyazaki 889-1692, Japan

2 Instituto de Agricultura Sostenible (IAS), Consejo Superior de Investigaciones Científicas (CSIC), Campus de Excelencia Internacional, Apdo. 4084, 14080 Córdoba, Spain

3 Forestry and Forest Products Research Institute, Tsukuba, Ibaraki 305-8687, Japan

4 Biodiversity (Mycology), Eastern Cereal and Oilseed Research Centre, Agriculture and Agri-Food Canada, Ottawa, ON K1A0C6, Canada

5 James Hutton Institute, Invergowrie, Dundee DD2 5DA, UK

6 Biology Department, Ghent University, K.L. Ledeganckstraat 35, 9000 Ghent, Belgium

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BMC Evolutionary Biology 2014, 14:69  doi:10.1186/1471-2148-14-69

Published: 1 April 2014

Abstract

Background

Horizontal gene transfer (HGT) has been suggested as the mechanism by which various plant parasitic nematode species have obtained genes important in parasitism. In particular, cellulase genes have been acquired by plant parasitic nematodes that allow them to digest plant cell walls. Unlike the typical glycoside hydrolase (GH) family 5 cellulase genes which are found in several nematode species from the order Tylenchida, members of the GH45 cellulase have only been identified in a cluster including the families Parasitaphelenchidae (with the pinewood nematode Bursaphelenchus xylophilus) and Aphelenchoididae, and their origins remain unknown.

Results

In order to investigate the distribution and evolution of GH45 cellulase genes in nematodes and fungi we performed a wide ranging screen for novel putative GH45 sequences. This revealed that the sequences are widespread mainly in Ascomycetous fungi and have so far been found in a single major nematode lineage. Close relationships between the sequences from nematodes and fungi were found through our phylogenetic analyses. An intron position is shared by sequences from Bursaphelenchus nematodes and several Ascomycetous fungal species.

Conclusions

The close phylogenetic relationships and conserved gene structure between the sequences from nematodes and fungi strongly supports the hypothesis that nematode GH45 cellulase genes were acquired via HGT from fungi. The rapid duplication and turnover of these genes within Bursaphelenchus genomes demonstrate that useful sequences acquired via HGT can become established in the genomes of recipient organisms and may open novel niches for these organisms to exploit.

Keywords:
Bursaphelenchus; Cellulases; Horizontal gene transfer; Ascomycota; Fungi