Plant pathogenesis: Toward multidimensional understanding of the microbiome

Abstract

Single pathogen-targeted disease management measure has shown drawbacks in field efficacy under the scenario of global change. An in-depth understanding of plant pathogenesis will provide a promising solution but faces the challenges of the emerging paradigm involving the plant microbiome. While the beneficial impact of the plant microbiome is well characterized, their potential role in facilitating pathological processes has so far remained largely overlooked. To address these unsolved controversies and emerging challenges, we hereby highlight the pathobiome, the disease-assisting portion hidden in the plant microbiome, in the plant pathogenesis paradigm. We review the detrimental actions mediated by the pathobiome at multiple scales and further discuss how natural and human triggers result in the prevalence of the plant pathobiome, which would probably provide a clue to the mitigation of plant disease epidemics. Collectively, the article would advance the current insight into plant pathogenesis and also pave a new way to cope with the upward trends of plant disease by designing the pathobiome-targeted measure.

Keywords: disease epidemics; multitrophic interaction; pathobiome; plant microbiome; plant pathogenesis.

Figure 1

The schematic representation of the pathobiome paradigm in the plant pathological process. Alongside the pathological process of host plants, certain members of the resident microbiota can be manipulated by the invasive pathogen, forming a partnership within the reassembled community. This ultimately results in the development of a unique microbial community that corresponds to the disease status of the host plants. The microbial consortia associated with host pathogenesis, present from disease onset to progression, are collectively and contemporarily conceptualized as the pathobiome.

Figure 2

Intramicrobiome interaction models involved in plant pathogenesis. Establishment of the mutualistic relationships between the invasive pathogen and the native potentially pathogenic microbial members in the host plants has been hypothesized to impair the homeostasis of plant vegetative and reproductive organs, drive the outcome of pathogen infection, and result in disease onset and progression. Such microbial mutualistic relationship is hidden in the complex intramicrobiome interaction throughout the below‐to‐above compartments from intraspecies to interspecies and interkingdom and driven by physical and chemical interactions mediated with an array of molecules, such as small molecules, effectors, and unidentified signals.

Figure 3

The pathobiome‐coordinated multiscale actions. The pathobiome‐mediated interaction is omnipresent at multiple scales including the plant–microbe system, microbe–insect system, and the multitrophic network involving both plants and insects, which governs the deleterious actions on the host plants. In the binary interaction model of plants and microbes, the pathobiome members are capable of releasing the active macro‐molecules such as effectors to induce host susceptibility by manipulating the traits controlled by the S genes. Various small‐molecule‐type virulence factors are also deployed to disable the plant's innate immunity‐based defense and further drive the infection to move toward disease progression. Moreover, the plant pathobiome members also participate in promoting disease epidemics by manipulating the multitrophic interactions. For instance, the pathobiome member stimulates the emission of insect‐attractive host volatiles to manipulate the host attraction to herbivore vectors for the spread of the whole pathogenic microbial community or influences the cross‐talk between the JA and SA to compromise defense against herbivores. ETI, effector‐triggered immunity; ETS, effector‐triggered susceptibility; JA, jasmonic acid; PTI, PAMP‐triggered immunity; R genes, resistance genes; S genes, susceptible genes; SA, salicylic acid.

Figure 4

Potential triggers responsible for the plant pathobiome prevalence. Given that plant disease epidemics arise under the scenario of global change, a series of natural and human triggers responsible for the prevalence of the plant pathobiome are highlighted. An increasing trend of plant disease outbreaks has been observed with climate change, such as global warming, and increased frequency of extreme weather events (e.g., drought stress, flooding, and storms). Global climate change has been hypothesized to trigger the plant pathobiome prevalence by promoting the assembly of the pathobiome member. As drivers of global change in the current human‐dominated epoch, anthropogenic activity (e.g., agriculture, industrialization, energy production, and transportation) and anthropogenic activity‐associated environmental pollutants further strengthen plant microbiome prevalence through a “vacuum effect,” which enable the nonnative potentially pathogenic microbes from the surrounding environment settling in below‐to‐above compartments of host plants.