Interactions between plant‐parasitic nematodes and their hosts are mediated by effectors, i.e. secreted proteins that manipulate the plant to the benefit of the pathogen. To understand the role of effectors in host adaptation in nematodes, we analysed the transcriptome of Heterodera sacchari, a cyst nematode parasite of rice (Oryza sativa) and sugarcane (Saccharum officinarum). A multi‐gene phylogenetic analysis showed that H. sacchari and the cereal cyst nematode Heterodera avenae share a common evolutionary origin and that they evolved to parasitise monocot plants from a common dicot‐parasitic ancestor. We compared the effector repertoires of H. sacchari with those of the dicot parasites Heterodera glycines and Globodera rostochiensis to understand the consequences of this transition. While, in general, effector repertoires are similar between the species, comparing effectors and non‐effectors of H. sacchari and G. rostochiensis shows that effectors have accumulated more mutations than non‐effectors. Although most effectors show conserved spatiotemporal expression profiles and likely function, some H. sacchari effectors are adapted to monocots. This is exemplified by the plant‐peptide hormone mimics, the CLAVATA3/EMBRYO SURROUNDING REGION‐like (CLE) effectors. Peptide hormones encoded by H. sacchari CLE effectors are more similar to those from rice than those from other plants, or those from other plant‐parasitic nematodes. We experimentally validated the functional significance of these observations by demonstrating that CLE peptides encoded by H. sacchari induce a short root phenotype in rice, whereas those from a related dicot parasite do not. These data provide a functional example of effector evolution that co‐occurred with the transition from a dicot‐parasitic to a monocot‐parasitic lifestyle.

中文翻译：

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植物寄生性囊肿线虫Heterodera sacchari对单子叶植物寄主的适应性签名。

植物寄生线虫与其宿主之间的相互作用是由效应子介导的，即操纵植物使病原体受益的分泌蛋白。为了了解效应子在线虫宿主适应中的作用，我们分析了Hterodera sacchari（水稻（Oryza sativa）和甘蔗（Saccharum officinarum）的囊肿线虫寄生虫）的转录组。多基因的系统发育分析表明，H.甘蔗和谷物胞囊线虫胞囊蚜都有一个共同的进化起源，他们发展到寄生于单子叶植物从一个共同的双子叶植物寄生祖先。我们比较了H. sacchari的效应库与双子叶植物的寄生虫Heterodera甘氨酸和Globodera rostochiensis一起了解这种转变的后果。通常，物种之间的效应子库相似，但是比较糖精链球菌和罗氏沼虾的效应子和非效应子表明，效应子积累的突变比非效应子更多。尽管大多数效应子显示出保守的时空表达特征和可能的功能，但是一些糖精链球菌效应子适合单子叶植物。植物肽激素模拟物，如CLAVATA3 / EMBRYO SURFROUNDING REGION-like（CLE）效应器就是例证。糖链球菌编码的肽激素与其他植物或其他植物寄生线虫相比，CLE效应子与水稻的效应子更相似。我们通过证明由H. sacchari编码的CLE肽诱导水稻中的短根表型，而来自相关双子叶植物寄生虫的CLE肽，通过实验验证了这些发现的功能意义。这些数据提供了一个从双子叶植物向单子叶植物向寄生虫过渡的效应物进化的功能实例。