Genomic Insights into the Origin of Parasitism in the Emerging Plant Pathogen <em>Bursaphelenchus xylophilus</em>

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）是引发亚洲与欧洲地区松材萎蔫病毁灭性流行的病原线虫，其植物寄生习性在线虫类群中属于近期独立起源的演化分支，在生态学与分类学层面均与已公开基因组数据的其他线虫存在显著差异。作为一类极具危害性的植物病原物，松材线虫的基因组为研究线虫植物寄生习性的演化历程与分子机制提供了独一无二的研究载体。本研究报道了松材线虫近交系的高质量基因组草图序列，并以此为基础解析其复杂生态学特性的生物学基础——该线虫兼具真菌摄食、植物寄生与昆虫伴生的多重生活史阶段。研究团队重点聚焦于潜在寄生相关基因以及其他关键生物学过程相关基因，研究发现松材线虫拥有丰富的RNA干扰（RNA interference, RNAi）效应因子、肽能神经递质（包括首次在寄生线虫中报道的ins基因）、应激响应与发育相关基因，同时其化学感受受体家族发生了明显收缩。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（ATP-binding cassette, ABC）转运蛋白以及细胞色素P450通路基因家族均发生了显著扩张。这类消化与解毒相关蛋白的家族扩张，或许反映了其在生命周期中所利用的食物来源与所处微环境的异常多样性。此外，松材线虫还拥有一套通过水平基因转移（horizontal gene transfer, HGT）获得的独特植物细胞壁修饰蛋白组合，这进一步凸显了该过程对线虫植物寄生习性演化的关键影响。相较于其他植物寄生线虫的效应因子同源蛋白，松材线虫缺乏此类蛋白，这证实了松材线虫谱系中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物生物学特性的重要科研资源。