Plant pathobiome and the hierarchy of keystone drivers in disease complexes

As plant disease complexes are recognized as polymicrobial systems in which multiple pathogens interact within the same host, the concept of the monomicrobial paradigm, which originated from Koch’s postulates, is therefore insufficient to explain the dynamics of many plant disease complexes. This review proposes that primary pathogens function as keystone drivers for disease complexes, and that secondary pathogens depend mainly on host modifications for colonization. The transformation of resistant plant tissues into permissive conditions by primary initiators occurs through breaching of structural barriers such as the cuticle and cell wall, suppression of plant immunity responses like pattern-triggered and effector-triggered immunity, and the generation of nutritional niches through the formation of feeding sites or metabolic manipulation. These means allow opportunistic or facultative pathogens to establish and to increase disease severity. We propose a hierarchical concept to distinguish obligate secondary pathogens, facultative secondary pathogens, and co-primary pathogens. The review also examines factors such as antagonistic interactions, priority effects, the influence of host microbiomes, and environmental conditions that may alter or challenge pathogen hierarchies. To address these complexities and improve disease prediction, diagnosis, and management, we advocate for the integration of multi-omics strategies, network-level analyses, and synthetic microbial communities (SynComs). Additionally, we stress the importance of considering temporal dynamics and climate extremes that can shift pathogen composition and disrupt established hierarchies over time.