Core Microbiome. Группа авторов

associated with aerial parts of plants have been known as epiphytes [87]. Proteobacteria, Actinobacteria, Bacteriodetes, and Firmicutes are consistent microbial phylotypes [88]. 16S rRNA sequencing has provided information about important phyllosphere colonizing bacteria, including diazotrophic and methylotrophic bacteria viz., Beijerinckia and Methylobacterium that consume nitrogen and methanol compounds, respectively [89]. Methylobacterium, Sphingomonas, and Pseudomonas are the most dominant genera in the phyllosphere microbial diversity, which possess specific adaptation factors to the phyllosphere [90,91]. For instance, the Sphingomonas spp. manage to survive in a nutrient-deficient environment by metabolizing many carbon sources [90]. Similarly, Pseudomonas spp. can move at auspicious sites by using flagellar motility [92]. The most enriched fungal communities in the phyllosphere are Ascomycota and basidiomycetous yeasts, and the most common genera are Cladosporium, Aureobasidium, and Taphrina [85].

      2.4.2 Biocontrol Mechanism in the Phyllosphere

The plant immune system plays a crucial role in controlling phyllosphere diversity [93]. Phyllosphere microbiota has adapted against extreme environmental conditions along with biocontrol activity that contains pathogenic microorganisms. A large amount of the inhibitory strains carries gene clusters encoding metabolites with prophylactic effects. The Brevibacillus sp. was reported to produce several antimicrobial compounds, such as marthiapeptide A, streptocidin D, and an unusual lysophospholipid that acts on gram-negative bacteria [94].

      2.4.2.1 Competition

Leaf exudates are carbon sources for both resident microbiota and pathogens, which allow plant–microbe and microbe–microbe interaction. Competition for carbon source determines the phyllosphere community; for example, methylotrophic yeast Candida boidinii in Arabidopsis thaliana and Methylobacterium extorquens in the rice phyllosphere can metabolize methanol compounds emitted by plant leaves and survive on the leaves [95,96].

      2.4.2.2 Parasitism

Parasitism acts by producing antagonistic agents that can parasite other fungi and feed on them. Biocontrol agents either destroy fungal propagules or cause partial obstruction and lysis of pathogen structure by producing hydrolytic enzymes. The host plant also acquires a defense mechanism by delivering chitinases and β-1,3-glucanase, which act on pathogen cell walls [97]. Under field conditions, strawberry plants are protected by Bacillus subtilis against Bacillus cinerea by the secreting extracellular enzymes viz., chitinase and proteases [98]. Moreover, five species of Tilletiopsis from the phyllosphere have antagonistic activity against powdery mildew by producing chitinase and endo- and exo- β-1,3-glucanase [99].

      2.4.2.3 Antagonism

Microorganisms with antagonistic activity suppress the growth of phytopathogens and inhibits the subsequent development and activity of infectious agents. The richness of bacterial species and negative interactions positively promote the growth and development of the plant [100]. Moesziomyces albugensis carries potent antagonistic activity against the oomycete pathogen Albugo laibachii in the phyllosphere of wild A. thaliana [101]. Trichoderma strains with the antagonistic potential of secreting cell-wall hydrolyzing enzymes such as chitinases, proteases, and β-glucanases can degrade the cell wall of pathogens [102].

Pseudomonas strains directly inhibit wide variety of pathogens (i.e., P. syringae and B. cinerea) in the laboratory as well as infield [103,104]. Pseudomonas spp. produced phenazines, a group of heterocyclic secondary metabolites that antagonize phytopathogens [105]. The Pseudomonas spp. is also reported to produce many other potential biocontrol metabolites, i.e., siderophores, 4-hydroxy-2-alkylquinolines, cyclic lipopeptides, and rhamnolipids, which are a class of biosurfactants [106]. Xanthomonas oryzae pv. oryzae is responsible for bacterial blight, which is the most destructive and serious disease-affecting rice. Among bacteria, actinomycetes are gram-positive and produce 70% of the compounds with biological effects. A total of eight strains of actinomycetes are reported to have shown a positive effect on controlling Xanthomonas in vitro and reducing disease severity of bacterial leaf blight. STG-15 can control bacterial leaf blight incidence and is identified as Nonomuraea sp [107].

      2.4.2.4 Induced Systemic Resistance

The Plant immune system responds the same way toward both pathogenic and nonpathogenic microbes. However, response toward nonpathogenic microbes remains mild as they lack virulence factors. The ISR mechanism is well characterized in the rhizosphere and endosphere. Sphingomonas melonis fr1, a phyllosphere bacteria, suppressed disease development in Arabidopsis thaliana by inducing camalexin production [108]. Camalexin is a tryptophan-derived alkaloid that interferes with the membrane integrity of bacteria and fungi [109]. Foliar application of Bacillus amyloliquefasciens 5B6 decreased the relative abundance of cucumber mosaic virus by activating SA and ethylene signaling pathway in three years of field trials [110].

      2.4.3 Plant Disease Management

Pathogens and pests are responsible for 15–30% of crop yield losses worldwide [111]. We depend on chemical-based crop production and protection strategies using chemical fertilizers, pesticides, herbicides, and fungicides for a sufficient and steady yield. Biological chemical-free agriculture is gaining more and more support ecologically. For disease control, ecological control has been the desirable policy in which nonpathogenic microorganisms are applied to the foliar parts of the plant to affect disease suppression [112]. Microorganisms of the phyllosphere take over a large assortment of adaptation and biocontrol factors, which permit them to adopt the phyllosphere condition and discourage pathogen growth, thus assisting in plant health [113].

The genera of Pantoea and Sphingomonas have a vital contribution to wildfire disease inhibition [114]. Bacillus amyloliquefaciens as a biocontrol agent to mandarin fruit suppresses Penicillium digitatum infection by 77% [115]. Trichoderma atroviridae can be correlated with reduced infection of Botrytis cinerea in strawberries by 88% [116]. Black leaf streak disease in bananas caused by Pseudocercospora musae is restrained by Bacillus subtilis B106 up to 72% [117]. The biocontrol agent Trichoderma koningii controls up to 93% of Phytophthora cactorum pathogen that causes collar rot in apples [118]. Similarly, infection caused by Phytophthora medium in rubber trees can be controlled by using biocontrol agents, such as Alcaligenes sp. EIL-2 [119].

      2.5 Conclusion and Prospects

We studied the plant microbiome, aiming to elucidate on the new and improved tools for developing products that can enhance disease management. Our first step was to explore and discover prospective products that can invade phytopathogens and help in maintaining the overall health of plants. Plant microbiota are very useful in improving plant growth as they produce secondary metabolites that confer resistance to a wide variety of pathogens. As a whole, metabolites secreted by the plant microbiome will offer an immense contribution in opening up new opportunities to fight challenges in the environment and agriculture. Finally, the advances in metagenomics combined with NGS techniques will uncover new pools of defense metabolites by novel microbes in the rhizosphere, endosphere, and phyllosphere.

      References

      1 1 Kumar, V., Prasad, R., Kumar, M., and Choudhary, D.K., (eds). (2019). Microbiome in Plant Health and Disease: Challenges and Opportunities. Springer. Aug 10.

      2 2 Hammonds, K., Trivedi, P., Garg, A., Janitz, C., Grinyer, J., Holford, P., Botha, F.C., Anderson, I.C., and Singh, B.K. (2018). Field study reveals core plant microbiota and the relative importance of their drivers. Environmental Microbiology