Data from: Effector gene birth in plant parasitic nematodes: neofunctionalization of a housekeeping glutathione synthetase gene

Plant pathogens and parasites are a major threat to global food security. Plant parasitism has arisen four times independently within the phylum Nematoda, resulting in at least one parasite of every major food crop in the world. Some species within the most economically important order (Tylenchida) secrete proteins termed effectors into their host during infection to re-programme host development and immunity. The precise detail of how nematodes evolve new effectors is not clear. Here we reconstruct the evolutionary history of a novel effector gene family. We show that during the evolution of plant parasitism in the Tylenchida, the housekeeping glutathione synthetase (GS) gene was extensively replicated. New GS paralogues acquired multiple dorsal gland promoter elements, altered spatial expression to the secretory dorsal gland, altered temporal expression to primarily parasitic stages, and gained a signal peptide for secretion. The gene products are delivered into the host plant cell during infection, giving rise to “GS-like effectors”. Remarkably, by solving the structure of GS-like effectors we show that during this process they have also diversified in biochemical activity, and likely represent the founding members of a novel class of GS-like enzyme. Our results demonstrate the re-purposing of an endogenous housekeeping gene to form a family of effectors with modified functions. We anticipate that our discovery will be a blueprint to understand the evolution of other plant-parasitic nematode effectors, and the foundation to uncover a novel enzymatic function.

植物病原物与寄生物是全球粮食安全的重大威胁。植物寄生习性已在线虫动物门（Nematoda）中独立起源四次，目前全球每一种主要粮食作物均至少有一种寄生线虫为害。在经济重要性最高的线虫目——垫刃目（Tylenchida）中，部分物种会在侵染宿主过程中分泌一类被称为效应子（effector）的蛋白质，以重编程宿主的发育与免疫过程。目前线虫如何演化出新型效应子的具体机制仍不明确。本研究重构了一个新型效应子基因家族的演化历程。研究发现，在垫刃目线虫演化出植物寄生习性的过程中，其管家基因谷胱甘肽合成酶（glutathione synthetase, GS）发生了广泛复制。新产生的GS旁系同源基因获得了多个背腺启动子元件，表达空间模式转变至分泌型背腺，表达时序调整为主要在寄生阶段进行，并新增了分泌信号肽。该家族基因的编码产物会在侵染过程中被输送至宿主植物细胞内，由此形成“类GS效应子（GS-like effectors）”。值得注意的是，通过解析类GS效应子的三维结构，本研究发现该家族在演化过程中其生化活性也发生了分化，且极有可能代表一类新型类GS酶的祖先成员。本研究结果证实，一条内源管家基因通过功能重定向，演化形成了一类功能修饰后的效应子家族。我们预期该发现将为解析其他植物寄生线虫效应子的演化历程提供研究范式，并为发掘新型酶功能奠定基础。