Genome Expression Dynamics Reveal the Parasitism Regulatory Landscape of the Root-Knot Nematode Meloidogyne incognita and a Promoter Motif Associated with Effector Genes

Martine Da Rocha,Clément Pellegrin,Peter Thorpe,Etienne G J Danchin,Marc Bailly-Bechet,Laetitia Perfus-Barbeoch,Julie Dazenière,Priscila Grynberg,Caroline Bournaud,Arthur Péré,Sebastian Eves-Van Den Akker

doi:10.3390/genes12050771

Abstract

Root-knot nematodes (genus Meloidogyne) are the major contributor to crop losses caused by nematodes. These nematodes secrete effector proteins into the plant, derived from two sets of pharyngeal gland cells, to manipulate host physiology and immunity. Successful completion of the life cycle, involving successive molts from egg to adult, covers morphologically and functionally distinct stages and will require precise control of gene expression, including effector genes. The details of how root-knot nematodes regulate transcription remain sparse. Here, we report a life stage-specific transcriptome of Meloidogyne incognita. Combined with an available annotated genome, we explore the spatio-temporal regulation of gene expression. We reveal gene expression clusters and predicted functions that accompany the major developmental transitions. Focusing on effectors, we identify a putative cis-regulatory motif associated with expression in the dorsal glands, providing an insight into effector regulation. We combine the presence of this motif with several other criteria to predict a novel set of putative dorsal gland effectors. Finally, we show this motif, and thereby its utility, is broadly conserved across the Meloidogyne genus, and we name it Mel-DOG. Taken together, we provide the first genome-wide analysis of spatio-temporal gene expression in a root-knot nematode and identify a new set of candidate effector genes that will guide future functional analyses.

Highlights

Plant parasitic nematodes are microscopic worms that threaten the security of most major agricultural crops such as soybean, cotton, peanut, banana, coffee, and potato [1,2].Damage caused by nematodes represents an important constraint on global food security in the developed and developing world and is estimated to cost world agriculture173 billion US dollar per year [3]
The majority of these loses are attributed to the obligate biotrophic sedentary endoparasites: the root-knot nematodes (RKN; Meloidogyne spp.) and the cyst nematodes (CN; Heterodera spp. and Globodera spp.)
Given that effectors in M. incognita are regulated in space and time, to other phytoparasites, we extended the search of cis-regulatory sequence motifs enriched in the promoters of genes related to RKN

Summary

Introduction

Plant parasitic nematodes are microscopic worms that threaten the security of most major agricultural crops such as soybean, cotton, peanut, banana, coffee, and potato [1,2].Damage caused by nematodes represents an important constraint on global food security in the developed and developing world and is estimated to cost world agriculture173 billion US dollar per year [3]. Root penetration is made possible by a combination of mechanical and enzymatic disruption of the plant cell wall At this stage, cell wall degrading/modifying enzymes (referred to as CWMEs) are secreted through a syringe-like stylet connected to secretory gland cells. Upon reaching the host vasculature, the parasitic nematode induces the formation of five to seven hypertrophied and multinucleated giant cells from parenchymal root cells via the secretion of effector proteins and other molecules that manipulate host cell division and other functions. These metabolically hyperactive giant cells will remain the sole source of nutrition for the developing endoparasite. The parasitic J2 undergoes two successive molts to reach the J3 and J4 juvenile stages

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