The plant-parasitic cyst nematode effector GLAND4 is a DNA-binding protein

Abstract

Cyst nematodes are plant pathogens that infect a wide range of economically important crops. One parasitic mechanism employed by cyst nematodes is the production and in planta delivery of effector proteins to modify plant cells and suppress defences to favour parasitism. This study focuses on GLAND4, an effector of Heterodera glycines and H. schachtii, the soybean and sugar beet cyst nematodes, respectively. We show that GLAND4 is recognized by the plant cellular machinery and is transported to the plant nucleus, an organelle for which little is known about plant nematode effector functions. We show that GLAND4 has DNA-binding ability and represses reporter gene expression in a plant transcriptional assay. One DNA fragment that binds to GLAND4 is localized in an Arabidopsis chromosomal region associated with the promoters of two lipid transfer protein genes (LTP). These LTPs have known defence functions and are down-regulated in the nematode feeding site. When expressed in Arabidopsis, the presence of GLAND4 causes the down-regulation of the two LTP genes in question, which is also associated with increased susceptibility to the plant-pathogenic bacterium Pseudomonas syringae. Furthermore, overexpression of one of the LTP genes reduces plant susceptibility to H. schachtii and P. syringae, confirming that LTP repression probably suppresses plant defences. This study makes GLAND4 one of a small subset of characterized plant nematode nuclear effectors and identifies GLAND4 as the first DNA-binding, plant-parasitic nematode effector.