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Organisms use circadian clocks to synchronize physiological processes to anticipate the Earth’s day-night cycles and regulate responses to environmental signals to gain competitive advantage. While divergent genetic clocks have been studied extensively in bacteria, fungi, plants, and animals, an ancient conserved circadian redox rhythm has been recently reported. However, its biological function and physiological outputs remain elusive. Here, we uncovered the coexistence of redox and genetic rhythms with distinct period lengths and transcriptional targets through concurrent metabolic and transcriptional time-course measurements in anArabidopsislong-period clock mutant. Analysis of the target genes indicated regulation of the immune-induced programmed cell death (PCD) by the redox rhythm. Moreover, this time-of-day-sensitive PCD was eliminated by redox perturbations and by blocking the signaling pathway of the plant defense hormones jasmonic acid/ethylene, while remaining intact in genetic clock-defective backgrounds. This study shows that compared to robust genetic clocks, the more sensitive circadian redox rhythm serves as a signaling hub in regulating incidental energy-intensive processes, such as immune-induced PCD involving reprogramming of chloroplast and mitochondria activities, to provide organisms a flexible strategy to mitigate metabolic overload during stress responses. 

In plants, a local infection can lead to systemic acquired resistance (SAR) through increased production of salicylic acid (SA). For many years, the identity of the mobile signal and its direct transduction mechanism for systemic SA synthesis in initiating SAR have been debated. We found that in Arabidopsis thaliana, after a local infection, the conserved cysteine residue of the transcription factor CCA1 HIKING EXPEDITION (CHE) undergoes sulfenylation in systemic tissues, which enhances its binding to the promoter of the SA-synthesis gene ISOCHORISMATE SYNTHASE1 (ICS1) and increases SA production. Furthermore, hydrogen peroxide (H2O2) produced through NADPH oxidases is the mobile signal that sulfenylates CHE in a concentration-dependent manner. Accumulation of SA and the previously reported signal molecules, such as N-hydroxypipecolic acid (NHP), then form a signal amplification loop to establish SAR. 

Abstract As the most widely used herbal medicine in human history and a major defence hormone in plants against a broad spectrum of pathogens and abiotic stresses, salicylic acid (SA) has attracted major research interest. With applications of modern technologies over the past 30 years, studies of the effects of SA on plant growth, development, and defence have revealed many new research frontiers and continue to deliver surprises. In this review, we provide an update on recent advances in our understanding of SA metabolism, perception, and signal transduction mechanisms in plant immunity. An overarching theme emerges that SA executes its many functions through intricate regulation at multiple steps: SA biosynthesis is regulated both locally and systemically, while its perception occurs through multiple cellular targets, including metabolic enzymes, redox regulators, transcription cofactors, and, most recently, an RNA-binding protein. Moreover, SA orchestrates a complex series of post-translational modifications of downstream signaling components and promotes the formation of biomolecular condensates that function as cellular signalling hubs. SA also impacts wider cellular functions through crosstalk with other plant hormones. Looking into the future, we propose new areas for exploration of SA functions, which will undoubtedly uncover more surprises for many years to come. 

Plants employ distinct mechanisms to respond to environmental changes. Modification of mRNA byN⁶-methyladenosine (m⁶A), known to affect the fate of mRNA, may be one such mechanism to reprogram mRNA processing and translatability upon stress. However, it is difficult to distinguish a direct role from a pleiotropic effect for this modification due to its prevalence in RNA. Through characterization of the transient knockdown-mutants of m⁶A writer components and mutants of specific m⁶A readers, we demonstrate the essential role that m⁶A plays in basal resistance and pattern-triggered immunity (PTI). A global m⁶A profiling of mock and PTI-inducedArabidopsisplants as well as formaldehyde fixation and cross-linking immunoprecipitation-sequencing of the m⁶A reader, EVOLUTIONARILY CONSERVED C-TERMINAL REGION2 (ECT2) showed that while dynamic changes in m⁶A modification and binding by ECT2 were detected upon PTI induction, most of the m⁶A sites and their association with ECT2 remained static. Interestingly, RNA degradation assay identified a dual role of m⁶A in stabilizing the overall transcriptome while facilitating rapid turnover of immune-induced mRNAs during PTI. Moreover, polysome profiling showed that m⁶A enhances immune-associated translation by binding to the ECT2/3/4 readers. We propose that m⁶A plays a positive role in plant immunity by destabilizing defense mRNAs while enhancing their translation efficiency to create a transient surge in the production of defense proteins. 

Abstract Translational reprogramming allows organisms to adapt to changing conditions. Upstream start codons (uAUGs), which are prevalently present in mRNAs, have crucial roles in regulating translation by providing alternative translation start sites^1–4. However, what determines this selective initiation of translation between conditions remains unclear. Here, by integrating transcriptome-wide translational and structural analyses during pattern-triggered immunity inArabidopsis, we found that transcripts with immune-induced translation are enriched with upstream open reading frames (uORFs). Without infection, these uORFs are selectively translated owing to hairpins immediately downstream of uAUGs, presumably by slowing and engaging the scanning preinitiation complex. Modelling using deep learning provides unbiased support for these recognizable double-stranded RNA structures downstream of uAUGs (which we term uAUG-ds) being responsible for the selective translation of uAUGs, and allows the prediction and rational design of translating uAUG-ds. We found that uAUG-ds-mediated regulation can be generalized to human cells. Moreover, uAUG-ds-mediated start-codon selection is dynamically regulated. After immune challenge in plants, induced RNA helicases that are homologous to Ded1p in yeast and DDX3X in humans resolve these structures, allowing ribosomes to bypass uAUGs to translate downstream defence proteins. This study shows that mRNA structures dynamically regulate start-codon selection. The prevalence of this RNA structural feature and the conservation of RNA helicases across kingdoms suggest that mRNA structural remodelling is a general feature of translational reprogramming.