The origin, deployment, and evolution of a plant-parasitic nematode effectorome

Authors: MOLLOY, BETH - University Of Cambridge; SHI, DIO - University Of Cambridge; LONG, JONATHAN - University Of Cambridge; PELLEGRIN, CLEMENT - University Of Cambridge; SENATORI, BEATRICE - University Of Cambridge; Vieira, Paulo; THORPE, PETER - University Of Dundee; DAMM, ANIKA - University Of Cambridge; AHMAD, MARIAM - University Of Cambridge; EVES-VAN DEN AKKER, SEBASTIAN - University Of Cambridge; DEREVNINA, LIDA - University Of Cambridge; WEI, SIYUAN - University Of Cambridge; SPERLING, ALEXIS - University Of Cambridge; ESTEVEZ, ESTEFANY - University Of Cambridge; BRUTY, SAMUAL - University Of Cambridge; HUGO, VICTOR - University Of Cambridge; KRANSE, OLAF - University Of Cambridge; MAIER, TOM - Iowa State University; BAUM, THOMAS - Iowa State University

Submitted to: PLoS Pathogens
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 7/7/2024
Publication Date: 7/29/2024
Citation: Molloy, B., Shi, D., Long, J., Pellegrin, C., Senatori, B., Reis Vieira, P.C., Thorpe, P., Damm, A., Ahmad, M., Eves-Van Den Akker, S., Derevnina, L., Wei, S., Sperling, A., Estevez, E., Bruty, S., Hugo, V., Kranse, O., Maier, T., Baum, T. 2024. The origin, deployment, and evolution of a plant-parasitic nematode effectorome. PLoS Pathogens. e1012395. https://doi.org/10.1371/journal.ppat.1012395.
DOI: https://doi.org/10.1371/journal.ppat.1012395

Interpretive Summary: Plant-parasitic nematodes (PPNs) are devastating crop parasites that present a considerable threat to global food security with collective annual damage estimated at over 100 billion dollars worldwide. The most damaging are those capable of forming long-term relationships with their host plant–namely, the cyst (genera Heterodera and Globodera) and root-knot nematodes (genus Meloidogyne). These species can alter their plant hosts by creating a feeding site from which they get their nutrition. Scientists do not yet have a full understanding of this process. In this study, genes potentially contributing to this process were identified by RNA sequencing. This work will benefit scientists engaged in research on the disease process and in developing methods for controlling these devastating plant pests.

Technical Abstract: During parasitism, plant-parasitic nematodes (PPNs) secrete effectors-produced in two sets of pharyngeal gland cells into the host plant. These effectors elicit profound changes in host biology to suppress immunity and establish a unique feeding organ from which the nematode draws nutrition. Despite the importance of nematode effectors in parasitism, the PPN effector repertoire remains undefined. To address this, we take advantage of recent techniques for gland cell isolation and transcriptional analysis to define a stringent annotation of putative effectors for the cyst nematode Heterodera schachtii at three key life-stages. We define 659 effector gene loci: 293 ‘known’ high-confidence homologs of plant-parasitic nematode effectors, and 366 ‘novel’ effectors with high gland cell expression. In doing so we define a comprehensive ‘effectorome’ of a plant-parasitic nematode. Using this definition, we provide the first systems-level understanding of the origin, deployment and evolution of a plant parasitic nematode effectorome. Robust identification of the comprehensive effectorome of a plant-parasitic nematode underpins our understanding of nematode pathology, and hence crop protection. Results from this work provide an overview of cyst nematode parasitism which can inform further functional studies of effectors and validates gland-cell transcriptomics as a method for effector discovery. Uncovering the development altering ‘toolbox’ of plant-parasitic nematodes can enable biotechnology, crop protection and uncover fundamental aspects of plant biology. This cross-transcriptional network can provide a basis for identifying potential targets for future functional work in plant-parasitic nematode effector biology.