Functional C‐TERMINALLY ENCODED PEPTIDE (CEP) plant hormone domains evolved de novo in the plant parasite Rotylenchulus reniformis

Abstract

SummarySedentary 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 that CEPs probably evolved de novo in R. reniformis. We have characterized the first member of this large gene family (RrCEP1), demonstrating its significant up‐regulation 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 up‐regulating plant nitrate transporter (AtNRT2.1) expression, whilst 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 hypothesize that CEPs of R. reniformis represent a two‐fold adaptation to sustained biotrophy in this species: (i) increasing host nitrate uptake, whilst (ii) limiting the size of the syncytial feeding site produced.

A microbially derived tyrosine sulfated peptide mimics a plant peptide hormone

“…Plant CEPs inhibit root growth and increase the gene expression of a nitrogen transporter in response to nitrogen starvation. It is hypothesized that the parasite produced CEPs promote nitrogen uptake and reduce the size of the feeding site where the PPNs maintain biotrophic interactions (Eves-Van Den Akker et al, 2016). Finally, the root-infecting fungus Fusarium oxysporum secretes a functional mimic of plant regulatory peptide RALF ( r apid al kalinization f actor).…”

A microbially derived tyrosine‐sulfated peptide mimics a plant peptide hormone

“…Plant CEPs inhibit root growth and increase the gene expression of a nitrogen transporter in response to nitrogen starvation. It is hypothesized that the parasite-produced CEPs promote nitrogen uptake and reduce the size of the feeding site where the PPNs maintain biotrophic interactions (Eves-Van Den Akker et al, 2016). Finally, the root-infecting fungus Fusarium oxysporum secretes a functional mimic of plant regulatory peptide RALF (rapid alkalinization factor).…”

Look Closely, the Beautiful May Be Small: Precursor-Derived Peptides in Plants

“…Peptide mimicry by nonplant organisms also occurs and is an important component of nematode parasitism and plant-pathogen interactions. Several precursor-derived peptide families are found in a wide range of parasitic species associated with plants, including cyst, root-knot, and reniform nematodes (45,56,83,99,156,195,206,211). The first cyst nematode CLE gene was identified from the soybean pest Heterodera glycines, and others soon followed (50,202,206).…”

“…One hypothesis to explain this difference is that CLE-like motifs from nematodes may have arisen through convergent evolution with their host (5); another possibility is that CLE genes from parasitic organisms may have evolved through horizontal gene transfer (31). CEPs have also been identified in plant-parasitic nematodes (8,10,45). Interestingly, because R. reniformis CEP genes share no sequence similarity with any other plant or animal CEPs except the conserved CEP domains and because R. reniformis is only distantly related to root-knot nematodes, R. reniformis CEPs may have evolved independently from both plant and root-knot nematode CEPs (45).…”

“…CEPs have also been identified in plant-parasitic nematodes (8,10,45). Interestingly, because R. reniformis CEP genes share no sequence similarity with any other plant or animal CEPs except the conserved CEP domains and because R. reniformis is only distantly related to root-knot nematodes, R. reniformis CEPs may have evolved independently from both plant and root-knot nematode CEPs (45).…”