Microbiome-Mediated Protection against Pathogens in Woody Plants

Abstract

Pathogens, especially invasive species, have caused significant global ecological, economic, and social losses in forests. Plant disease research has traditionally focused on direct interactions between plants and pathogens in an appropriate environment. However, recent research indicates that the microbiome can interact with the plant host and pathogens to modulate plant resistance or pathogen pathogenicity, thereby altering the outcome of plant-pathogen interactions. Thus, this presents new opportunities for studying the microbial management of forest diseases. Compared to parallel studies on human and crop microbiomes, research into the forest tree microbiome and its critical role in forest disease progression has lagged. The rapid development of microbiome sequencing and analysis technologies has resulted in the rapid accumulation of a large body of evidence regarding the association between forest microbiomes and diseases. These data will aid the development of innovative, effective, and environmentally sustainable methods for the microbial management of forest diseases. Herein, we summarize the most recent findings on the dynamic structure and composition of forest tree microbiomes in belowground and aboveground plant tissues (i.e., rhizosphere, endosphere, and phyllosphere), as well as their pleiotropic impact on plant immunity and pathogen pathogenicity, highlighting representative examples of biological control agents used to modulate relevant tree microbiomes. Lastly, we discuss the potential application of forest tree microbiomes in disease control as well as their future prospects and challenges.

Keywords: biological control agents; endosphere; microbiome; pathogen suppression; phyllosphere; plant immunity; rhizosphere; woody plants.

Figure 1

The phyllosphere, endosphere, and rhizosphere are depicted schematically as the major habitats for the diverse microflora that compose plant-associated communities.

Figure 2

Both interactions of the microbiome with the host and pathogens contribute to plant protection against pathogens. Plants infected by pathogens can recruit and enrich beneficial microbial communities to directly antagonize the pathogens via a variety of methods, such as the “cry for help” strategy. Specific mechanisms include secretion of antagonistic compounds (such as antibiotics, lysozyme, and volatile substances), competition with pathogens for ecological niche and nutrients, inhibition of pathogens’ signaling systems, parasitism, and predation, and so on, thus directly inhibiting pathogen proliferation and infection. On the other hand, the plant microbiome can also act indirectly by priming plant immunity, such as induced systemic resistance (ISR) triggered by microbe-associated molecular patterns (MAMPs), defense hormones, PGPRs, and so on, to inhibit pathogen invasion and protect the underground and aboveground parts from encroachment.