The SUbventral-Gland Regulator (SUGR-1) of nematode virulence

Clement Pellegrin, Anika Damm, Alexis L. Sperling, Beth Molloy, Dio S. Shin, Jonathan Long, Paul Brett, Tochukwu Chisom Iguh, Olaf P. Kranse, Andrea Díaz-Tendero Bravo, Sarah Jane Lynch, Beatrice Senatori, Paulo Vieira, Joffrey Mejias, Anil Kumar, Rick E. Masonbrink, Tom R. Maier, Thomas J. Baum, and Sebastian Eves-van den Akker

PNAS; March 10, 2025; 122 (11) e2415861122; https://doi.org/10.1073/pnas.2415861122

Significance

We show that effector deployment at the earliest stages of infection by plant-parasitic nematodes is defined by a feedforward signaling loop, centered on a transcriptional regulator, SUGR-1, and stimulated by plant-derived signals. In conjunction with parallel understanding in prokaryotic systems, we posit a generalizable framework that applies to all pathogens which secrete effectors.

Abstract

Pathogens must precisely tailor their gene expression to cause infection. However, a signaling cascade from host signal to effector production has remained elusive for metazoan pathogens. Here, we show that plants contain molecular signals, termed effectostimulins, that activate the first identified regulator of plant-parasitic nematode effectors. SUGR-1 directly binds effector promoters, and is central to a transcriptional network that activates 58 effector genes. Importantly, we demonstrate that downregulation of sugr-1 inhibits parasitism, underlining SUGR-1 signaling as a valuable target for crop protection and food security. This, in the wider context of nematodes as parasites of humans and other animals, has scope for potentially broader impact: Disrupting effector production could, in principle, be applied to any pathogen that secrets effectors.

See https://www.pnas.org/doi/10.1073/pnas.2415861122

Figure 1

H. schachtii gene expression responds to host cues. (A) S. alba (white mustard) plants were grown in tip boxes filled with water. H. schachtii second-stage juveniles (J2s) were exposed to root diffusate (water) and/or extract prepared from the roots (n = 5). (B) Differential gene expression (n = 5; |log2FC| ≥ 0.5 & Padj ≤ 0.001) clusters that describe H. schachtii response to mustard root diffusate and extract. Enrichment was determined in hypergeometric tests (P < 0.01). (C) Transcriptional effector network, computed from independently generated expression data (31), where nodes represent effector genes predicted in ref. 25 and edges represent correlations in gene expression across the nematode life-cycle of 0.975 or above (distance correlation coefficient). Colors indicate the nematode life stages. (D) Transcriptional effector network highlighting effectors upregulated by mustard root extract in yellow. Extract upregulated transcription factors (TFs) with connections to the effector network (brown) are shown on the z axis where height is determined by connectedness to the effector network.