Phyllosphere Microorganisms: Sources, Drivers, and Their Interactions with Plant Hosts.

The leaves of plants are colonized by various microorganisms. In comparison to the rhizosphere, less is known about the characteristics and ecological functions of phyllosphere microorganisms. Phyllosphere microorganisms mainly originate from soil, air, and seeds. The composition of phyllosphere microorganisms is mainly affected by ecological and abiotic factors. Phyllosphere microorganisms execute multiple ecological functions by influencing leaf functions and longevity, seed mass, fruit development, and homeostasis of host growth. A plant can respond to phyllosphere microorganisms by secondary metabolite secretion and its immune system. Meanwhile, phyllosphere microorganisms play an important role in ecological stability and environmental safety assessment. However, as a result of the instability of the phyllosphere environment and the poor cultivability of phyllosphere microorganisms in the current research, there are still many limitations, such as the lack of insight into the mechanisms of plant-microorganism interactions, the roles of phyllosphere microorganisms in plant growth processes, the responses of phyllosphere microorganisms to plant metabolites, etc. This review summarizes the latest progress made in the research of the phyllosphere in recent years. This is beneficial for deepening our understanding of phyllosphere microorganisms and promoting the research of plant-atmosphere interactions, plant pathogens, and plant biological control.

Effects of S-metolachlor on wheat (Triticum aestivum L.) seedling root exudates and the rhizosphere microbiome.

S-metolachlor (S-ME) is a common chloroacetanilide herbicide. Here, we investigated the effects of S-ME on wheat seedling growth and explored via metabolomics the driver through which S-ME changes the rhizosphere microbiome. The results indicated that 4 mg/kg S-ME had a strong inhibitory effect on plant growth by inducing hydrogen peroxide (H2O2) levels. The richness of the rhizosphere microbiome markedly decreased after S-ME treatment, although the abundance of some potential beneficial rhizobacteria, such as Rhizobiaceae and Burkholderiaceae, increased suggesting that plants recruited potential beneficial microorganisms to resist S-ME-induced stress. Spearman correlation analysis revealed that Rhizobiaceae and Burkholderiaceae were positively correlated with organic acids secreted by plants after S-ME treatment, implying that potential beneficial microorganisms may be attracted mainly by organic acids. Our results demonstrated the phytotoxicity of S-ME on crop growth and indicated both that S-ME could influence rhizosphere microorganism abundance and that recruitment of potential beneficial microorganisms could be the result of root exudate regulation.

Enantioselective effects of imazethapyr residues on Arabidopsis thaliana metabolic profile and phyllosphere microbial communities.

Imazethapyr (IM) is a widely used acetolactate synthase-inhibiting chiral herbicide. It has long-term residuals that may be absorbed by the human body through the edible parts of plants, such as vegetable leaves or fruits. Here, we selected a model plant, Arabidopsis thaliana, to determine the effects of R-IM and S-IM on its leaf structure, photosynthetic efficiency, and metabolites, as well as the structures of microorganisms in the phyllosphere, after 7 days of exposure. Our results indicated enantiomeric differences in plant growth between R-IM and S-IM; 133 µg/kg R-IM showed heavier inhibition of photosynthetic efficiency and greater changes to subcellular structure than S-IM. R-IM and S-IM also had different effects on metabolism and leaf microorganisms. S-IM mainly increased lipid compounds and decreased amino acids, while R-IM increased sugar accumulation. The relative abundance of Moraxellaceae human pathogenic bacteria was increased by R-IM treatment, indicating that R-IM treatment may increase leaf surface pathogenic bacteria. Our research provides a new perspective for evaluating the harmfulness of pesticide residues in soil, phyllosphere microbiome changes via the regulation of plant metabolism, and induced pathogenic bacterial accumulation risks.

Enantioselective effects of imazethapyr on Arabidopsis thaliana root exudates and rhizosphere microbes.

Imazethapyr (IM) is a chiral herbicide with two enantiomers (R-IM and S-IM). Here, we determined the enantioselective effects of IM on Arabidopsis thaliana biomass and chlorophyll content, root exudates and rhizosphere microbes after 7 days of exposure. The results suggested that 133 µg/kg R-IM enantiomer in soil slightly inhibited plant biomass but S-IM did not exert significant inhibitory effects. The rhizosphere microorganism composition was also found to have enantiomeric differences between R- and S-IM. The relative abundance of beneficial rhizosphere microbes such as Bacillus and Ramlibacter increased much more with R-IM treatment than with S-IM treatment, indicating that the rhizosphere recruited some beneficial microbes to resist the herbicide stress. The IM enantiomers exerted a significant influence on root exudates with enantioselectivity. R-IM resulted in higher levels of most amino acids, organic acids, sugars and other metabolites after 7 days of exposure; few metabolites were increased by only the S-IM treatment. The correlation analyses between compounds (sugars, amino acids and organic acid) and microbes at the genus level revealed that the number of microbes was more positively correlated with organic acids than other compounds, indicating that organic acids can attract more microbes than amino acids and sugars. Some organic acids, such as 3-hydroxybutyric acid, may be a carbon source for the beneficial microbe Ramlibacter. This study increases the understanding of the differences in IM enantiomer toxicity with respect to plant physiological activity and soil microorganisms.