The root lesion nematode effector Ppen10370 is essential for parasitism of Pratylenchus penetrans

Authors: VIEIRA, PAULO - Virginia Tech; VICENTE, CLAUDIA - Universidade De Evora; BRANCO, JORDANA - Universidade De Evora; Bauchan, Gary; MOTA, MANUEL - Universidade De Evora; Nemchinov, Lev

Submitted to: Molecular Plant-Microbe Interactions
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/5/2021
Publication Date: 1/5/2021
Citation: Vieira, P., Vicente, C.S., Branco, J., Bauchan, G.R., Mota, M., Nemchinov, L.G. 2021. The root lesion nematode effector Ppen10370 is essential for parasitism of Pratylenchus penetrans. Molecular Plant-Microbe Interactions. https://doi.org/10.1094/MPMI-09-20-0267-R.
DOI: https://doi.org/10.1094/MPMI-09-20-0267-R

Interpretive Summary: Root lesion nematodes (RLN) inflict significant damage to many agriculturally important crops, including alfalfa, the third most valuable crop in the U.S. Pratylenchus penetrans is one of the RLN species with a wide range distribution and more than 400 hosts worldwide. An important feature of all plant parasitic nematodes is the presence of a repertoire of secreted proteins, known as effectors, which are critical components determining the outcome of plant-nematode interactions and likely the ability of P. penetrans to parasitize on a wide range of hosts. Although a growing number of the nematode effectors have been identified, their biological roles and host targets remain unknown. In this study, we have characterized a novel gene encoding candidate effector of P. penetrans and proposed its functional roles in the nematode parasitism. It is expected that this work will be of interest to plant pathologists, nematologists and plant molecular biologists working in the fields of crop protection and improvement.

Technical Abstract: The root lesion nematode, Pratylenchus penetrans, is a migratory species that attacks a broad range of crops. Like other plant pathogens, P. penetrans deploys a repertoire of secreted protein effectors to manipulate plant hosts and induce disease. Although several candidate effectors of P. penetrans have been identified, detailed mechanisms of their functions and particularly their host targets remain largely unexplored. In this study, a set of candidate genes encoding pioneer effectors of P. penetrans was amplified from mixed life stages of the nematode, cloned and subjected to transient expression in a heterologous host Nicotiana benthamiana using potato virus X-based gene vector. Among seven analyzed genes, candidate effector designated Ppen10371 triggered pleiotropic phenotypes substantially different from those produced by wild type infection. Transcriptome analysis of plants expressing Ppen10370 demonstrated that observed phenotypic changes were likely related to disruption of core biological processes in the plant due to effector-originated activities. Cross-species comparative analysis of the Ppen10371 identified homologues gene sequences in five other Pratylenchus species and their transcripts were found to be localized specifically in the nematode esophageal glands by in situ hybridization. RNA silencing of the Ppen10370 resulted in a significant reduction of nematode propagation and development, demonstrating an important role of the esophageal gland effector for the onset of parasitism.