Xingwei Wang

The circadian clock synchronises plant physiology with environmental oscillations to promote plant fitness. The commonly-used methods for rhythm monitoring in dicots include rhythmic leaf movement tracking and luciferase-based imaging. For monocots, however, the leaf erectness makes these methods ineffective. Leveraging over 11,000 transcriptome samples, the circadian time-course profiling, the simulation-based algorithm optimisation, and the experimental validation, we developed SPIRAL, an online single time-point circadian analysis platform for rice and unexpectedly revealed a ∼28-hour endogenous rhythm in V4-stage Nipponbare leaves, making period-matched or long-day photoperiods comparatively more permissive growth conditions for the assayed experimental system. We demonstrated the versatility of SPIRAL by quantifying global rhythm sensitivity to abiotic stresses, pinpointing when nitrogen deficiency starts to perturb rhythms, a temporal resolution surpassing that of the state-of-the-art methods, and identifying candidate components connecting the clock to stresses through factorial analyses. Online deployment of SPIRAL enables platform-independent analysis of public and user-supplied rice transcriptomes to accelerate discoveries in crop adaptation and chronoculture.

The intertwining between the life cycle of plants and their pathogens made the plant circadian clock an integral constituent of the plant immune system. Reciprocally, pathogens were also found to perturb the expression pattern of certain clock genes. However, how pathogens influence clock components remains largely unknown. Here we show that an oomycete effector HaRxL10 directly targets Arabidopsis central clock component CCA1 HIKING EXPEDITION (CHE) to manipulate its function. HaRxL10 stabilises CHE by disrupting E3 ligase ZEITLUPE-mediated CHE protein degradation. Surprisingly, the accumulation of CHE does not enhance but rather suppresses CHE function, inhibiting its binding to the downstream gene promoter. HaRxL10 triggers reprogramming of the transcriptome including expression of genes related to circadian oscillations. Moreover, HaRxL10 hijacks CHE to repress plant immunity and manipulate physiological processes, including hypocotyl growth and flowering. Taken together, our study discovers the first plant pathogen effector that directly targets a plant circadian clock component and elucidates the underlying molecular mechanism.

The circadian clock, an endogenous timing system, exists in nearly all organisms on Earth. The plant circadian clock has been found to be intricately linked with various essential biological activities. Extensive studies of the plant circadian clock have yielded valuable applications. However, the distinctions of circadian clocks in two important plant species, Arabidopsis thaliana and Glycine max (soybean), remain largely unexplored. This study endeavors to address this gap by conducting a comprehensive comparison of the circadian transcriptome profiles of Arabidopsis and soybean to uncover their distinct circadian characteristics. Utilizing non-linear regression fitting (COS) integrated with weights, we identified circadian rhythmic genes within both organisms. Through an in-depth exploration of circadian parameters, we unveiled notable differences between Arabidopsis and soybean. Furthermore, our analysis of core circadian clock genes shed light on the distinctions in central oscillators between these two species. Additionally, we observed that the homologous genes of Arabidopsis circadian clock genes in soybean exert a significant influence on the regulation of flowering and maturity of soybean. This phenomenon appears to stem from shifts in circadian parameters within soybean genes. These findings highlight contrasting biological activities under circadian regulation in Arabidopsis and soybean. This study not only underscores the distinctive attributes of these species, but also offers valuable insights for further scrutiny into the soybean circadian clock and its potential applications.

Phenolic acids (PAs) secreted by donor plants suppress the growth of their susceptible plant neighbours. However, how structurally diverse ensembles of PAs are perceived by plants to mediate interspecific competition remains a mystery. Here we show that a plant stress granule (SG) marker, RNA-BINDING PROTEIN 47B (RBP47B), is a sensor of PAs in Arabidopsis. PAs, including salicylic acid, 4-hydroxybenzoic acid, protocatechuic acid and so on, directly bind RBP47B, promote its phase separation and trigger SG formation accompanied by global translation inhibition. Salicylic acid-induced global translation inhibition depends on RBP47 family members. RBP47s regulate the proteome rather than the absolute quantity of SG. The rbp47 quadruple mutant shows a reduced sensitivity to the inhibitory effect of the PA mixture as well as to that of PA-rich rice when tested in a co-culturing ecosystem. In this Article, we identified the long sought-after PA sensor as RBP47B and illustrated that PA-induced SG-mediated translational inhibition was one of the PA perception mechanisms.