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Cytokinin drives assembly of the phyllosphere microbiome and promotes disease resistance through structural and chemical cues

Abstract

The plant hormone cytokinin (CK) is an important developmental regulator, promoting morphogenesis and delaying differentiation and senescence. From developmental processes, to growth, to stress tolerance, CKs are central in plant life. CKs are also known to mediate plant immunity and disease resistance, and several classes of microbes can also produce CKs, affecting the interaction with their plant hosts. While host species and genotype can be a driving force in shaping the plant microbiome, how plant developmental hormones such as CK can shape the microbiome is largely uninvestigated. Here, we examined the relationship between CK and the phyllosphere microbiome, finding that CK acts as a selective force in microbiome assembly, increasing richness, and promoting the presence of Firmicutes. CK-mediated immunity was found to partially depend on the microbial community, and bacilli isolated from previously described CK-rich plant genotypes, which overexpress a CK biosynthesis gene or have increased CK sensitivity, induced plant immunity, and promoted disease resistance. Using a biomimetic system, we investigated the relationship between the leaf microstructure, which is differentially patterned upon changes in CK content or signaling, and the growth of different phyllosphere microbes. We found that leaf structures derived from CK-rich plant genotypes support bacilli in the biomimetic system. CK was able to promote the growth, swarming, and biofilm formation of immunity inducing bacillus isolates in vitro. Overall, our results indicate that host genotype and hormonal profiles can act as a strong selective force in microbiome assembly, underlying differential immunity profiles, and pathogen resistance as a result.

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Fig. 1: Endogenous cytokinin supports Gram-positive bacteria in the pylloshpere.
Fig. 2: Exogenous cytokinin supports Gram-positive bacteria in the pylloshpere.
Fig. 3: Endogenous cytokinin supports Gram-positive bacteria in the phyllosphere under sterile conditions.
Fig. 4: Cytokinin mediated immunity is bacterial community dependent.
Fig. 5: Leaf physical properties of indicated genotypes.
Fig. 6: Preference of Gram-positive bacteria and aversion of Gram-negative bacteria to synthetic leaf structures derived from high cytokinin content/signaling genotypes.
Fig. 7: Gram-positive bacteria exhibit decreased circularity on synthetic leaf structures derived from high cytokinin content/signaling genotypes.
Fig. 8: Preference of Gram-positive bacteria to leaf replica structures derived from high cytokinin content/signaling genotypes, in a pairwise community context.
Fig. 9: Direct effect of cytokinin on phyllosphere derived microbes.

Data availability

The authors declare that the data supporting the findings of this study are available within the paper and its Supplementary Information files. Raw data is available through NCBI-SRA, Bioproject PRJNA729221.

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Acknowledgements

The authors wish to thank Dror Minz, Stefan J Green and Jonathan Friedman for providing bacterial strains and for helpful discussions, and the Bar, Jami and Kleiman group members for continuous discussion and support.

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MK and MB: Conceptualization. RG, ML-M, TS, EJ, MK, and MB: Methodology. RG, DE, ML-M, TS, and AS: Experimentation. RG, DE, ML-M, TS, AS, EJ, MK, and MB: Analysis. RG, EJ, MK, and MB: Manuscript.

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Correspondence to Maya Bar.

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Gupta, R., Elkabetz, D., Leibman-Markus, M. et al. Cytokinin drives assembly of the phyllosphere microbiome and promotes disease resistance through structural and chemical cues. ISME J 16, 122–137 (2022). https://doi.org/10.1038/s41396-021-01060-3

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  • DOI: https://doi.org/10.1038/s41396-021-01060-3

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