Genomic Insights into the Origin of Parasitism in the Emerging Plant Pathogen Bursaphelenchus xylophilus

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.

松材线虫（Bursaphelenchus xylophilus）是引发亚洲与欧洲松树萎蔫病毁灭性流行的病原线虫，其植物寄生习性在线虫中属于近期独立起源的演化分支，在生态学与分类学上均与已获得基因组数据的其他线虫类群截然不同。作为一类重要的植物病原物，松材线虫的基因组为研究植物寄生习性的演化与分子机制提供了独一无二的研究契机。本研究报道了一株近交系松材线虫的高质量草图基因组序列，并依托该序列解析其复杂生态习性的生物学基础——该线虫兼具真菌取食、植物寄生以及与昆虫伴生的多个生活史阶段。本研究重点关注潜在寄生相关基因以及其他关键生物学过程相关基因，结果显示松材线虫富含RNA干扰效应因子、肽能神经递质相关基因（包括首次在寄生线虫中报道的胰岛素样肽（ins）基因家族）、胁迫响应与发育相关基因，同时其化学感受受体家族呈现收缩演化特征。松材线虫拥有目前已知线虫中数量最多的消化蛋白酶家族，同时溶酶体通路基因、ATP结合盒（ABC）转运蛋白以及细胞色素P450通路基因家族均发生了扩张。这类消化与解毒相关蛋白的扩张，或许反映了其在生活史中所利用的食物来源与遭遇的环境具有非同寻常的多样性。此外，松材线虫通过水平基因转移获得了一套独特的植物细胞壁修饰蛋白，这进一步凸显了水平基因转移在线虫植物寄生习性演化过程中的重要作用。加之其缺乏与其他植物寄生线虫效应因子同源的蛋白，这一特征证实了松材线虫演化支植物寄生习性的独特分子基础。松材线虫的基因组序列丰富了线虫类群的基因组数据资源，将成为解析这类特殊病原线虫生物学特性的重要研究工具。