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The circadian clock regulates the daily pattern of temporal gene expression. In Arabidopsis, aging is associated with a shortening of the endogenous period of circadian rhythms under circadian conditions. However, the functional link between the circadian clock and aging under diurnal conditions and its physiological relevance remain elusive. In this study, we investigate and characterize the effect of aging on the waveforms of rhythmic gene expression patterns under light/dark cycles. Our analysis revealed that the diurnal rhythmic patterns of core clock genes undergo significant rhythmic alteration with phase shift and change of waveforms in aged plants compared to younger plants. Transcriptomic analysis indicated that this age-dependent rhythmic alteration occurs not only in core clock genes but also globally. Due to the rhythmic alteration patterns of the diurnal rhythmic gene expression, aged plants experience subjectively a shorter day and longer night. We also observed that genetic mutants of core clock component genes exhibited broadly yet distinctively altered changes in diurnal rhythmic gene expression patterns as aging progresses. Collectively, our findings support that age-dependent rhythmic alteration of diurnal gene expression rhythms reprograms the timetable of daily gene expression, leading to the physiological changes required for plant senescence.

Leaf senescence, the last stage of leaf development, is essential for whole-plant fitness as it marks the relocation of nutrients from senescing leaves to reproductive or other developing organs. Temporally coordinated physiological and functional changes along leaf aging are fine-tuned by a highly regulated genetic program involving multi-layered regulatory mechanisms. Long noncoding RNAs (lncRNAs) are newly emerging as hidden players in many biological processes; however, their contribution to leaf senescence has been largely unknown. Here, we performed comprehensive analyses of RNA-seq data representing all developmental stages of leaves to determine the genome-wide lncRNA landscape along leaf aging. A total of 771 lncRNAs, including 232 unannotated lncRNAs, were identified. Time-course analysis revealed 446 among 771 developmental age-related lncRNAs (AR-lncRNAs). Intriguingly, the expression of AR-lncRNAs was regulated more dynamically in senescing leaves than in growing leaves, revealing the relevant contribution of these lncRNAs to leaf senescence. Further analyses enabled us to infer the function of lncRNAs, based on their interacting miRNA or mRNA partners. We considered functionally diverse lncRNAs including antisense lncRNAs (which regulate overlapping protein-coding genes), competitive endogenous RNAs (ceRNAs; which regulate paired mRNAs using miRNAs as anchors), and mRNA-interacting lncRNAs (which affect the stability of mRNAs). Furthermore, we experimentally validated the senescence regulatory function of three novel AR-lncRNAs including one antisense lncRNA and two mRNA-interacting lncRNAs through molecular and phenotypic analyses. Our study provides a valuable resource of AR-lncRNAs and potential regulatory networks that link the function of coding mRNA and AR-lncRNAs. Together, our results reveal AR-lncRNAs as important elements in the leaf senescence process.

Leaf senescence is an integrated response of the cells to develop age information and various environmental signals. Thus, some of the genes involved in the response to environmental changes are expected to regulate leaf senescence. Light acts not only as the primary source of energy for photosynthesis but also as an essential environmental cue that directly control plant growth and development including leaf senescence. The molecular mechanisms linking light signaling to leaf senescence have recently emerged, exploring the role of Phytochrome-Interacting Factors (PIFs) as a central player leading to diverse senescence responses, senescence-promoting gene regulatory networks (GRNs) involving PIFs, and structural features of transcription modules in GRNs. The circadian clock is an endogenous time-keeping system for the adaptation of organisms to changing environmental signals and coordinates developmental events throughout the life of the plant. Circadian rhythms can be reset by environmental signals, such as light-dark or temperature cycles, to match the environmental cycle. Research advances have led to the discovery of the role of core clock components as senescence regulators and their underlying signaling pathways, as well as the age-dependent shortening of the circadian clock period. These discoveries highlight the close relationship between the circadian system and leaf senescence. Key issues remain to be elucidated, including the effect of light on leaf senescence in relation to the circadian clock, and the identification of key molecules linking aging, light, and the circadian clock, and integration mechanisms of various senescence-affecting signals at the multi-regulation levels in dynamics point of view.