Data from: Functional C-terminally encoded plant peptide (CEP) hormone domains evolved de novo in the plant parasite Rotylenchulus reniformis

Sedentary Plant-Parasitic Nematodes (PPNs) induce and maintain an intimate relationship with their host, stimulating cells adjacent to root vascular tissue to re-differentiate into unique and metabolically active “feeding sites”. The interaction between PPNs and their host is mediated by nematode effectors. We describe the discovery of a large and diverse family of effector genes, encoding C-terminally Encoded Peptide (CEP) plant hormone mimics (RrCEPs), in the syncytia-forming plant-parasite Rotylenchulus reniformis. The particular attributes of RrCEPs distinguish them from all other CEPs, regardless of origin. Together with the distant phylogenetic relationship of R. reniformis to the only other CEP-encoding nematode genus identified to date (Meloidogyne), this suggests CEPs likely evolved de novo in R. reniformis. We have characterised the first member of this large gene family (RrCEP1), demonstrating its significant upregulation during the plant-nematode interaction and expression in the effector-producing pharyngeal gland cell. All internal CEP domains of multi-domain RrCEPs are followed by di-basic residues, suggesting a mechanism for cleavage. A synthetic peptide corresponding to RrCEP1 domain 1 is biologically active and capable of upregulating plant nitrate transporter (AtNRT2.1) expression, while simultaneously reducing primary root elongation. When a non-CEP containing, syncytia-forming PPN species (Heterodera schachtii) infects Arabidopsis in a CEP-rich environment a smaller feeding site is produced. We hypothesise that CEPs of R. reniformis represent a two-fold adaptation to sustained biotrophy in this species; 1) increasing host nitrate uptake while 2) limiting the size of the syncytial feeding site produced.固着型植物寄生线虫（Sedentary Plant-Parasitic Nematodes, PPNs）会诱导并维持与宿主的紧密互作，促使根维管组织旁的细胞重新分化为独特且代谢活跃的“取食位点”。线虫与宿主之间的互作由线虫效应蛋白（nematode effectors）介导。本研究报道了在合胞体形成型植物寄生线虫肾状肾线虫（Rotylenchulus reniformis）中发现的一类庞大且多样的效应蛋白基因家族，该家族编码羧基端编码肽（C-terminally Encoded Peptide, CEP）植物激素模拟物，暂命名为RrCEPs。RrCEPs的独特属性使其区别于所有其他来源的CEP家族成员。结合肾状肾线虫与目前已知唯一编码CEP的线虫属——根结线虫属（Meloidogyne）之间较远的系统发育关系，这一结果提示CEP家族很可能在肾状肾线虫中独立进化而来。我们对该庞大基因家族的首个成员（RrCEP1）进行了功能表征，结果显示其在植物-线虫互作过程中显著上调表达，且在产生效应蛋白的咽腺细胞（pharyngeal gland cell）中特异性表达。多结构域RrCEPs的所有内部CEP结构域之后均带有双碱性残基（di-basic residues），这提示其存在切割加工机制。一段对应RrCEP1结构域1的合成肽具有生物学活性，能够上调拟南芥硝酸盐转运蛋白（AtNRT2.1）的表达，同时抑制主根伸长。当不含CEP的合胞体形成型植物寄生线虫——甜菜孢囊线虫（Heterodera schachtii）在富含CEP的环境中侵染拟南芥（Arabidopsis）时，其形成的取食位点尺寸更小。我们推测，肾状肾线虫的CEP家族代表了该物种对持续活体营养的双重适应性策略：1）增强宿主对硝酸盐的吸收；2）限制所形成的合胞体取食位点的尺寸。