Understanding microbiome shifts and their impacts on plant health during pathogen infections.

Abstract

Pathogen infections can drastically reshape plant-associated microbiomes, yet the mechanisms underlying these shifts and their consequences for plant health remain elusive. In this review, we integrate recent advances to delineate how pathogen attack drives both local and systemic microbiome restructuring via three major processes: (i) collateral effects of the plant immune system, including alterations to the local physicochemical niche; (ii) active recruitment of beneficial microbes through pathogen-induced root exudates (primary and secondary metabolites, volatiles and organic compounds); and (iii) pathogen-mediated manipulation of the host microbiome through microbial effectors, antimicrobial production, or niche competition. By contrasting adaptive outcomes (enrichment of disease-suppressive taxa) with detrimental consequences (dysbiosis, mutualist loss or proliferation of disease-promoting microbes), we emphasize the need for time-resolved, mechanistic studies that move beyond correlative surveys. Although the enrichment of protective microbes is a recurring theme in current literature, it is important to recognize that not all microbiome shifts are adaptive or host-directed. Considering alternative explanations is critical to avoid survivorship bias and to accurately interpret microbiome dynamics in the context of plant-pathogen interactions. Building on these insights, we discuss the rational design of microbiome-based interventions to enhance crop resilience, including synthetic microbial consortia and elicitor-mediated recruitment of beneficial microbes. Notably, integrating microbiome dynamics into plant pathology offers a promising path toward sustainable disease management, transforming the microbiome from a passive background into an active, designable component of plant immunity.