Diet-regulated transcriptional plasticity of plant parasites in plant–mutualist environments

M. Willow H. Maxwell, Barry E. Causier, Jasper Chippendale, James R. Ault , and Chris A. Bell

PNAS; April 17, 2025; 122 (16) e2421367122; https://doi.org/10.1073/pnas.2421367122

Significance

Successful parasitism, regardless of the taxonomy of the host, relies upon the acquisition of host resources by the parasite. As well as with parasites, plants interact with a myriad of organisms within soils, including beneficial mutualists. Here, we outline the ability of a parasite to transcriptionally respond to fluctuations in food intake that are induced by a plant-beneficial fungus competing for the finite reserve of host resources. This adaptive mechanism potentially supports the long-term biotrophy of pathogens in diverse and dynamic living conditions and “off-sets” deficiencies that may be induced by interkingdom competition.

Abstract

Crop pathogens often lack exclusive access to their host and must interact with plants concurrently engaged with numerous other symbionts. Here, we demonstrate that the colonization of hosts by plant–mutualistic mycorrhizal fungi can indirectly induce transcriptional responses of a major plant parasite, the nematode Globodera pallida, via a modified host resource profile. A shift in the resource profile of the root, where the parasite feeds, is perceived and responded to by the parasite through transcriptional changes, potentially to optimize resource intake. Specifically, G. pallida react to reduced host-photosynthate influx due to concurrent mycorrhizal-host symbiosis by upregulating the expression of a sugar transporter (SWEET3) in the nematode intestine. We identify this gene’s role in parasite growth and development, regulated by the putative diet-responsive transcription factor Gp-HBL1. Overall, our data unveil a mechanism by which a parasitic animal responds to fluctuations in host plant quality that is induced by a plant–mutualistic fungus, to enhance parasitism and reproduction.

See https://www.pnas.org/doi/10.1073/pnas.2421367122

Figure 1: Identification and characterization of the potentially diet-responsive Gp-SWEET3. The impact of distal colonization of potato roots by AM fungi on coinfecting G. pallida. (A) The gene expression profile of G. pallida from root systems ± AM fungi (P < 0.001; FDR DESeq2). (B) Gp-SWEET3 expression of G. pallida from root systems ± AM fungi (P < 0.001; FDR DESeq2). (C) Glucose and fructose content of G. pallida from root systems ± AM fungi (** denotes significance at P < 0.01, ns indicates P = 0.056; Two-sample t test). (D) Temporal expression of Gp-SWEET3 throughout the G. pallida life cycle (25). (E) Spatial expression of Gp-SWEET3 via in situ hybridization with digoxigenin probes on parasitic life stages (+ antisense probe, − negative control sense probe). Four biological replicates were conducted for A–C.