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

Author:

Molloy Beth,Shin Dio S.,Long Jonathan,Pellegrin Clement,Senatori Beatrice,Vieira Paulo,Thorpe Peter J.,Damm Anika,Ahmad Mariam,Vermeulen Kerry,Derevnina Lida,Wei Siyuan,Sperling Alexis,Reyes Estévez Estefany,Bruty Samuel,de Souza Victor Hugo Moura,Kranse Olaf Prosper,Maier Tom,Baum Thomas,Eves-van den Akker SebastianORCID

Abstract

Plant-parasitic nematodes constrain global food security. During parasitism, they secrete effectors into the host plant from two types of pharyngeal gland cells. 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 effectors in nematode parasitism, there has been no comprehensive identification and characterisation of the effector repertoire of any plant-parasitic nematode. To address this, we advance 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 717 effector gene loci: 269 “known” high-confidence homologs of plant-parasitic nematode effectors, and 448 “novel” effectors with high gland cell expression. In doing so we define the most comprehensive “effectorome” of a plant-parasitic nematode to date. Using this effector definition, we provide the first systems-level understanding of the origin, deployment and evolution of a plant-parasitic nematode effectorome. The robust identification of the effector repertoire of a plant-parasitic nematode will underpin our understanding of nematode pathology, and hence, inform strategies for crop protection.

Funder

Biotechnology and Biological Sciences Research Council

Leverhulme Trust

UK Research and Innovation

Engineering and Physical Sciences Research Council

USDA-ARS National Programs 303

Horizon 2020 Framework Programme

British Society of Plant Pathology

Publisher

Public Library of Science (PLoS)

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