Antagonistic action of a nuclear hormone receptor pair coordinates a switch from lytic to biotrophic effector production in a plant-parasitic nematode

Abstract

Pathogens secrete overlapping and sequential waves of effectors to manipulate their host, and yet the regulators that conduct the ensemble are poorly understood. Here, we identify the Dorsal Gland Regulator DGR-1 in the beet cyst nematode Heterodera schachtii. DGR-1 controls the expression of 131 putative effectors, acting as a dual-functional switch that "switches off" early stage effectors involved in plant invasion, and "switches on" later stage effectors associated with biotrophic establishment in the host. Interestingly, DGR-1 works antagonistically with the only other known transcriptional regulator of effectors in plant-parasitic nematodes, the Subventral Gland Regulator-1 (SUGR-1), to coordinate this apparent switch from lytic to biotrophic effector production. Together, DGR-1 and SUGR-1 control the expression of nearly one half of all H. schachtii early-stage effectors, and over one fifth of effectors of any kind. The requirement to activate lytic effector functions in the cortex, and biotrophic effector functions in the vascular cylinder, suggests that this transcription factor pair must differentially respond to signals from the host. Consistent with this, we find that diffusates from the roots of A. thaliana Casparian strip mutant myb36/sgn3, which are enriched in molecules ordinarily restricted to the vascular cylinder, upregulate dgr-1, but not sugr-1, compared to Col-0. Taken together, these data indicate that H. schachtii responds to compartmentalised host-derived signals to appropriately regulate spatiotemporal effector expression during infection. Given that misregulating DGR-1 results in delayed development of parasitic nematodes in Arabidopsis and Mustard, strategies which impair effector regulation as a whole may hold promise for crop protection against these agriculturally important pathogens.