Department of Plant Sciences, The Crop Science Centre, University of Cambridge, Cambridge CB2 3EA, UK.
Present address: Department of Plant Pathology, Washington State University, Pullman 99163, USA.
Mol Biol Evol. 2024 Feb 1;41(2). doi: 10.1093/molbev/msae030.
Plant-parasitic nematodes are one of the most economically important pests of crops. It is widely accepted that horizontal gene transfer-the natural acquisition of foreign genes in parasitic nematodes-contributes to parasitism. However, an apparent paradox has emerged from horizontal gene transfer analyses: On the one hand, distantly related organisms with very dissimilar genetic structures (i.e. bacteria), and only transient interactions with nematodes as far as we know, dominate the list of putative donors, while on the other hand, considerably more closely related organisms (i.e. the host plant), with similar genetic structure (i.e. introns) and documented long-term associations with nematodes, are rare among the list of putative donors. Given that these nematodes ingest cytoplasm from a living plant cell for several weeks, there seems to be a conspicuous absence of plant-derived cases. Here, we used comparative genomic approaches to evaluate possible plant-derived horizontal gene transfer events in plant parasitic nematodes. Our evidence supports a cautionary message for plant-derived horizontal gene transfer cases in the sugar beet cyst nematode, Heterodera schachtii. We propose a 4-step model for horizontal gene transfer from plant to parasite in order to evaluate why the absence of plant-derived horizontal gene transfer cases is observed. We find that the plant genome is mobilized by the nematode during infection, but that uptake of the said "mobilome" is the first major barrier to horizontal gene transfer from host to nematode. These results provide new insight into our understanding of the prevalence/role of nucleic acid exchange in the arms race between plants and plant parasites.
植物寄生线虫是农作物最重要的经济害虫之一。人们普遍认为，水平基因转移——寄生虫线虫自然获取外源基因——有助于寄生。然而，从水平基因转移分析中出现了一个明显的悖论：一方面，与线虫的关系非常疏远，遗传结构差异很大（即细菌），而且据我们所知，与线虫的相互作用只是短暂的，在假定的供体中占主导地位，而另一方面，与线虫的关系更为密切的生物体（即宿主植物），遗传结构相似（即内含子），并有与线虫长期关联的记录，在假定的供体中却很少。鉴于这些线虫在数周内从活植物细胞中摄取细胞质，似乎明显缺乏植物源性的情况。在这里，我们使用比较基因组学方法来评估植物寄生线虫中可能发生的植物源性水平基因转移事件。我们的证据支持了甜菜胞囊线虫（Heterodera schachtii）中植物源性水平基因转移案例的警示信息。我们提出了一个从植物到寄生虫的水平基因转移的 4 步模型，以评估为什么观察到缺乏植物源性水平基因转移案例。我们发现，线虫在感染过程中使植物基因组发生了重排，但上述“移动组”的摄取是阻止宿主到线虫水平基因转移的第一个主要障碍。这些结果为我们理解植物与植物寄生虫之间的核酸交换在军备竞赛中的普遍性/作用提供了新的认识。
