Rhizosphere Microbes Influence Host Circadian Clock Function

Abstract

The circadian clock is an important determinant of fitness that is entrained by local conditions. Aside from abiotic factors, individual pathogenic soil bacteria affect circadian clock function in plant hosts. Yet, in nature, plants interact with diverse microbial communities, and the effect of complex communities on clock function remains unclear. In Arabidopsis thaliana and its wild relative, Boechera stricta, we used diverse rhizosphere inoculates and host genotypes to test the effect of complex rhizosphere microbial communities on the host circadian clock. Arabidopsis thaliana plants with an intact rhizosphere microbiome expressed a circadian period closer to 24h in duration and significantly shorter (by 48 minutes on average) relative to plants grown with a disrupted microbiome. Wild-type host genotypes of A. thaliana differed in clock sensitivity to microbes, with one genotype (Landsberg erecta) expressing a 119-minute difference in circadian period length across rhizosphere microbial treatments. A similar pattern of clock sensitivity to soil microbes was observed in B. stricta. Finally, rhizosphere microbes collected from the mutant genotype toc1-21 of A. thaliana with a short-period phenotype and used as inoculate significantly shortened the long-period phenotype of the clock mutant genotype ztl-1. The results indicate that complex rhizosphere microbial communities affect host clock function.

Microbial circadian clocks: host-microbe interplay in diel cycles

“…Recent work in A. thaliana and its wild relative Boechera stricta demonstrated that the rhizosphere microbes also influence host circadian rhythms. In plants where the rhizosphere microbial community was disrupted, the length of the circadian period was extended, lasting longer than 24 h, suggesting a role for the microbial community in regulating host circadian rhythms [ 20 ].…”

Synchronization of Circadian Clock Gene Expression inArabidopsisandHyaloperonospora arabidopsidisand its Impact on Host-Pathogen Interactions

“…It is well documented that host clock can influence rhizosphere microbial community (Hubbard et al ., 2018; Lu et al ., 2021; Newman et al ., 2022). Similarly, the rhizosphere microbial community affects the host clock function (Hubbard et al ., 2021). These studies suggest there is a bidirectional rhythmic interaction between plants and their rhizomicrobiome (Xu & Dodd, 2022).…”

Circadian regulation of metabolism across photosynthetic organisms

“…Comparison of the microbial communities inhabiting the rhizosphere of wild‐type, clock mutant, and clock gene‐overexpressing Arabidopsis has revealed differences between the rhizomicrobiome community structure of these genotypes (Hubbard et al., 2018 , 2021 ; Newman et al., 2022 ; Staley et al., 2017 ). Collectively, these studies imply a role for the circadian oscillator in root metabolite release, because exudation shapes rhizomicrobiome community structure (e.g.…”

“…Such investigations will benefit from non‐targeted root exudate profiling approaches to obtain a holistic assessment of circadian involvement in the release of different metabolite classes, because identification and quantification of various compound types is sensitive to the technical approach used (reviewed in Pantigoso et al., 2021 ; Salem et al., 2022 ). Assess relationships between diel or circadian exudation cycles and wider rhizosphere processes : Whilst researchers have started to analyze the effect of core circadian oscillator genes on rhizomicrobiome composition (Hubbard et al., 2018 , 2021 ; Newman et al., 2022 ; Staley et al., 2017 ), work is needed to directly assess rhythmic metabolic interactions between root exudates and rhizosphere microbial communities (Figure 2b,c ). One approach to studying these potential rhythmic interactions could be to use microfluidics (Massalha et al., 2017 ).…”