A molecular link between autophagy and circadian rhythm in plants

Abstract

Extremely high or low autophagy levels disrupt plant survival under nutrient starvation. Recently, autophagy has been reported to display rhythms in animals. However, the mechanism of circadian regulation of autophagy is still unclear. Here, we observed that autophagy has a robust rhythm and that various autophagy‐related genes (ATGs) are rhythmically expressed in Arabidopsis. Chromatin immunoprecipitation (ChIP) and dual‐luciferase (LUC) analyses showed that the core oscillator gene TIMING OF CAB EXPRESSION 1 (TOC1) directly binds to the promoters of ATG (ATG1a, ATG2, and ATG8d) and negatively regulates autophagy activities under nutritional stress. Furthermore, autophagy defects might affect endogenous rhythms by reducing the rhythm amplitude of TOC1 and shortening the rhythm period of CIRCADIAN CLOCK‐ASSOCIATED 1 (CCA1). Autophagy is essential for the circadian clock pattern in seedling development and plant sensitivity to nutritional deficiencies. Taken together, our studies reveal a plant strategy in which the TOC1‐ATG axis involved in autophagy‐rhythm crosstalk to fine‐tune the intensity of autophagy.

The plant circadian clock regulates autophagy rhythm through transcription factor LUX ARRHYTHMO

“…Molecular mechanisms of the circadian regulation of autophagy are well characterized in animals (Ma et al, 2011; Xiong et al, 2012; Huang et al, 2016), however, surprisingly little is known about whether and how the circadian clock controls autophagic processes in plants. In Arabidopsis , transcription factor TOC1 contributes to the regulation of autophagy rhythm by binding to the promoters of ATG1a , ATG2 , and ATG8d (Chen et al, 2022). Here, we identified a new regulatory mechanism underlying circadian autophagy rhythm in plants.…”

“…Therefore, we suspected that the expression of ATG1a is regulated via a distinct mechanism. There is a possible involvement of TOC1, a core circadian clock component, which directly binds to the ATG1a promoter and regulates autophagy rhythm (Chen et al, 2022). Moreover, the phases of most ATGs are quite close, but not identical (Figures 1, 2, S1, S2).…”

“…A similar phenomenon was also reported in plants where autophagy deficiency led to decreased resistance to multiple stresses in Arabidopsis (Signorelli et al, 2019). On the contrary, the Arabidopsis toc1‐2 mutant with an elevated autophagy activity is hypersensitive to both carbon and nitrogen starvation (Chen et al, 2022). Consistently, our results showed that the Cas9‐lux mutant with enhanced autophagy activity at night also displays a sensitive phenotype to dark‐induced carbon starvation (Figures 4, 6).…”

Acyl coenzyme A binding protein (ACBP): An aging‐ and disease‐relevant “autophagy checkpoint”

“…ACBP3 can be induced by pathogens and is subjected to circadian regulation (Zheng et al, 2012 ). It appears plausible, yet remains to be confirmed, that ACBP3 is secreted through an autophagy‐dependent process, which is known to be subjected to marked circadian fluctuations in plants (Chen et al, 2022 ; Yang, Zhu, et al, 2022 ).…”