Plants under the Attack of Allies: Moving towards the Plant Pathobiome Paradigm

Abstract

Plants are functional macrobes living in a close association with diverse communities of microbes and viruses as complex systems that continuously interact with the surrounding environment. The microbiota within the plant holobiont serves various essential and beneficial roles, such as in plant growth at different stages, starting from seed germination. Meanwhile, pathogenic microbes—differentiated from the rest of the plant microbiome based on their ability to damage the plant tissues through transient blooming under specific conditions—are also a part of the plant microbiome. Recent advances in multi-omics have furthered our understanding of the structure and functions of plant-associated microbes, and a pathobiome paradigm has emerged as a set of organisms (i.e., complex eukaryotic, microbial, and viral communities) within the plant’s biotic environment which interact with the host to deteriorate its health status. Recent studies have demonstrated that the one pathogen–one disease hypothesis is insufficient to describe the disease process in many cases, particularly when complex organismic communities are involved. The present review discusses the plant holobiont and covers the steady transition of plant pathology from the one pathogen–one disease hypothesis to the pathobiome paradigm. Moreover, previous reports on model plant diseases, in which more than one pathogen or co-operative interaction amongst pathogenic microbes is implicated, are reviewed and discussed.

Metagenomic Analyses of the Soybean Root Mycobiome and Microbiome Reveal Signatures of the Healthy and Diseased Plants Affected by Taproot Decline

“…The stability of mixed communities is detemined by the antagonistic and mutualistic interspecies interactions occurring within individual biomes and over an evolutionary timescale [ 40 ]. However, perturbations such as pathogen invasion can disrupt the equilibrium of the system and favor species with pathogenic potential that drive the development of disease [ 41 ]. While the effect of pathogens in human- and animal-associated biomes has been extensively explored [ 42 , 43 ], we only have limited information on the processes underlying the transition from a healthy plant-associated biome to a pathobiome [ 41 , 44 , 45 , 46 ].…”

“…However, perturbations such as pathogen invasion can disrupt the equilibrium of the system and favor species with pathogenic potential that drive the development of disease [ 41 ]. While the effect of pathogens in human- and animal-associated biomes has been extensively explored [ 42 , 43 ], we only have limited information on the processes underlying the transition from a healthy plant-associated biome to a pathobiome [ 41 , 44 , 45 , 46 ]. Moreover, only scarce information exists on the diverse types of plant–microbe interactions occurring during natural outbreaks of known pathogens in agricultural fields [ 47 ].…”

Olive Fungal Epiphytic Communities Are Affected by Their Maturation Stage

“…More recently, the overall microbial community that is naturally associated with plants has been recognized as affecting the infection ability of pathogens and even disturbing disease progression [9]. More important than the one-pathogen-one-disease concept, the scientific community is becoming aware of the importance of all pathobiome, in which the combined effect of microbial communities, host and environment plays an important role in host responses and/or conditions [10]. Therefore, olive-phyllosphereassociated microorganisms have been explored to search for biocontrol agents and to design new strategies for the control of olive diseases (e.g., [11][12][13]).…”

A Review: Late Wilt of Maize—The Pathogen, the Disease, Current Status, and Future Perspective

“…The letters can be referred to as the plant's pathobiome [66]. The plant's pathobiomes comprise coexisting phytopathogens that affect each other and the plant [67]. They are formed by pathogens inhabiting the same ecological niche and either cooperating or competing for the same plant resources.…”