Abstract

Bursaphelenchus xylophilus is the nematode responsible for a devastating epidemic of pine wilt disease in Asia and Europe, and represents a recent, independent origin of plant parasitism in nematodes, ecologically and taxonomically distinct from other nematodes for which genomic data is available. As well as being an important pathogen, the B. xylophilus genome thus provides a unique opportunity to study the evolution and mechanism of plant parasitism. Here, we present a high-quality draft genome sequence from an inbred line of B. xylophilus, and use this to investigate the biological basis of its complex ecology which combines fungal feeding, plant parasitic and insect-associated stages. We focus particularly on putative parasitism genes as well as those linked to other key biological processes and demonstrate that B. xylophilus is well endowed with RNA interference effectors, peptidergic neurotransmitters (including the first description of ins genes in a parasite) stress response and developmental genes and has a contracted set of chemosensory receptors. B. xylophilus has the largest number of digestive proteases known for any nematode and displays expanded families of lysosome pathway genes, ABC transporters and cytochrome P450 pathway genes. This expansion in digestive and detoxification proteins may reflect the unusual diversity in foods it exploits and environments it encounters during its life cycle. In addition, B. xylophilus possesses a unique complement of plant cell wall modifying proteins acquired by horizontal gene transfer, underscoring the impact of this process on the evolution of plant parasitism by nematodes. Together with the lack of proteins homologous to effectors from other plant parasitic nematodes, this confirms the distinctive molecular basis of plant parasitism in the Bursaphelenchus lineage. The genome sequence of B. xylophilus adds to the diversity of genomic data for nematodes, and will be an important resource in understanding the biology of this unusual parasite.

Highlights

  • The nematode Caenorhabditis elegans was the first multicellular organism for which a complete genome sequence was available, and subsequent genomics research on a wider range of nematodes has provided information on many important biological processes and is underpinned by the information developed for C. elegans [1]

  • It seems likely that B. xylophilus has a larger number of detoxification enzymes than other plant parasitic nematodes (M. incognita and M. hapla), with similar or expanded repertoires of such genes to those reported for the free-living C. elegans and the necromenic P. pacificus [62] for the various components of the

  • Concluding remarks In addition to its status as an economically important plant pathogen, B. xylophilus is remarkable for its unusual biological traits that relate to its complex ecology

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Summary

Introduction

The nematode Caenorhabditis elegans was the first multicellular organism for which a complete genome sequence was available, and subsequent genomics research on a wider range of nematodes has provided information on many important biological processes and is underpinned by the information developed for C. elegans [1]. While C. elegans is a free-living bacterial feeder, nematodes exhibit a wide range of ecological interactions, including important parasites of humans and livestock that have huge agricultural and medical impacts [2]. Plant parasitic nematodes cause damage to crops globally. Within the Nematoda, the ability to parasitise plants has evolved independently on several occasions [3] and nematodes use a wide range of strategies to parasitise plants. Some nematodes are migratory ectoparasites which remain outside the roots and have a very limited interaction with their hosts. Migratory endoparasitic nematodes invade their host and cause extensive damage as they

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