Circadian control of <i>ORE1</i> by PRR9 positively regulates leaf senescence in <i>Arabidopsis</i>

Abstract

The circadian clock coordinates the daily cyclic rhythm of numerous biological processes by regulating a large portion of the transcriptome. In animals, the circadian clock is involved in aging and senescence, and circadian disruption by mutations in clock genes frequently accelerates aging. Conversely, aging alters circadian rhythmicity, which causes age-associated physiological alterations. However, interactions between the circadian clock and aging have been rarely studied in plants. Here, we investigated potential roles for the circadian clock in the regulation of leaf senescence in plants. Members of the evening complex in <i>Arabidopsis</i> circadian clock, EARLY FLOWERING 3 (ELF3), EARLY FLOWERING 4 (ELF4), and LUX ARRHYTHMO (LUX), as well as the morning component PSEUDO-RESPONSE REGULATOR 9 (PRR9), affect both age-dependent and dark-induced leaf senescence. The circadian clock regulates the expression of several senescence-related transcription factors. In particular, PRR9 binds directly to the promoter of the positive aging regulator <i>ORESARA1</i> (<i>ORE1</i>) gene to promote its expression. PRR9 also represses <i>miR164</i>, a posttranscriptional repressor of <i>ORE1</i> Consistently, genetic analysis revealed that delayed leaf senescence of a <i>prr9</i> mutant was rescued by <i>ORE1</i> overexpression. Thus, PRR9, a core circadian component, is a key regulator of leaf senescence via positive regulation of <i>ORE1</i> through a feed-forward pathway involving posttranscriptional regulation by <i>miR164</i> and direct transcriptional regulation. Our results indicate that, in plants, the circadian clock and leaf senescence are intimately interwoven as are the clock and aging in animals.