Abstract
Plant pathogens and parasites are a major threat to global food security. Plant parasitism has arisen four times independently within the phylum Nematoda, resulting in at least one parasite of every major food crop in the world. Some species within the most economically important order (Tylenchida) secrete proteins termed effectors into their host during infection to re-programme host development and immunity. The precise detail of how nematodes evolve new effectors is not clear. Here we reconstruct the evolutionary history of a novel effector gene family. We show that during the evolution of plant parasitism in the Tylenchida, the housekeeping glutathione synthetase (GS) gene was extensively replicated. New GS paralogues acquired multiple dorsal gland promoter elements, altered spatial expression to the secretory dorsal gland, altered temporal expression to primarily parasitic stages, and gained a signal peptide for secretion. The gene products are delivered into the host plant cell during infection, giving rise to “GS-like effectors”. Remarkably, by solving the structure of GS-like effectors we show that during this process they have also diversified in biochemical activity, and likely represent the founding members of a novel class of GS-like enzyme. Our results demonstrate the re-purposing of an endogenous housekeeping gene to form a family of effectors with modified functions. We anticipate that our discovery will be a blueprint to understand the evolution of other plant-parasitic nematode effectors, and the foundation to uncover a novel enzymatic function.
Highlights
The ability of nematodes to exploit living plants as a food resource has arisen independently in four of the twelve major lineages of the phylum Nematoda [1]
glutathione synthetase (GS)-like effectors supported by Biotechnology and Biological Sciences Research Council (BBSRC) grant BB/ N016866/1 to PEU
SEvdA is supported by BBSRC grant BB/M014207/1
Summary
The ability of nematodes to exploit living plants as a food resource has arisen independently in four of the twelve major lineages of the phylum Nematoda [1]. Clade 12 of the phylum encompasses representatives of all major modes of parasitism; migratory ectoparasites, migratory endoparasites, and the most economically important and highly specialized obligate biotrophs—the sedentary endoparasites [2]. The latter induce the re-differentiation of root cells to form a unique nutrient-rich feeding site which is maintained for several weeks in a prolonged biotrophic interaction. Nematodes deploy hundreds of effector proteins to induce profound molecular and physiological changes associated with feeding site induction and maintenance. The majority of all described effectors are secreted from three pharyngeal gland cells (one dorsal and two subventral) through a hollow, protrusible needle-like stylet, into the plant
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