Effector gene birth in plant parasitic nematodes: Neofunctionalization of a housekeeping glutathione synthetase gene

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.

Shared Transcriptional Control and Disparate Gain and Loss of Aphid Parasitism Genes

“…Therefore, while many effectors are part of paralogous/homologous gene families within a species, as evidenced by the gene duplication data, often only one member of this family is predicted to be an effector. This can be a hallmark of either neofunctionalization following gene duplication ( Lilley et al. 2018 ) or loss of an effector gene following recognition by the plant immune system, and will need to be further explored.…”

Suppression of Plant Immunity by Fungal Chitinase-like Effectors

“…Notably, by showing that fungal pathogens can evolve effectors by repurposing the functions of enzymes that are conserved throughout evolution (i.e., neofunctionalization of chitinases), we shed light on an enigmatic and poorly documented topic: the birth of virulence factors. Given the recent observation that a family of effectors in parasitic nematodes evolved from the glutathione synthetase gene [33], that enzymatically inactive proteases in Phytophthora function as plant glucanase inhibitors [34,35], and that P. sojae secretes a truncated inactive xyloglucanase as a decoy to protect its enzymatically active paralog from a host inhibitor [36], neofunctionalization of enzymes may constitute a widespread strategy for the evolution of virulence factors in pathogens as a whole. Genome mining revealed multiple instances of likely inactive GH18 chitinases in phytopathogenic fungi (Table S4), including Blumeria graminis, Ceratocystis spp., Colletotrichum spp., Fusarium poae, Puccinia spp., Rhizoctonia solani, and Valsa mali.…”

Rapid evolution in plant–microbe interactions – a molecular genomics perspective

“…An extension of this concept is the evolution of catalytically inactive variants of secreted proteins. Examples include the functional conversion of a glutathione synthetase in a plant-parasitic nematode (Lilley et al, 2018), enzymatically inactive fungal chitinases that sequester immunogenic chitin fragments (Fiorin et al, 2018), or the large family of catalytically inactive RNase-like effector proteins in cereal powdery mildews (Pennington et al, 2019).…”