SignificanceThe circadian clock is involved in aging in animals, where mutations in core clock genes accelerate aging. However, little is known about the relationship between aging and the circadian clock in plants. Using the well-studied process of leaf senescence in Arabidopsis, a higher plant, as a model for aging, we show that the circadian clock has a critical role in regulating the aging process in plants. Specifically, we show that PSEUDO-RESPONSE REGULATOR 9 (PRR9), a core clock component, positively regulates leaf senescence. ORESARA 1 (ORE1), an aging regulator, is controlled by PRR9 via direct transcriptional activation and indirectly by suppressing miR164, a posttranscriptional repressor of ORE1, thus forming a coherent feed-forward regulatory loop.
Leaf senescence is regulated by diverse developmental and environmental factors to maximize plant fitness. The red to far-red light ratio (R:FR) detected by plant phytochromes is reduced under vegetation shade, thus initiating leaf senescence. However, the role of phytochromes in promoting leaf senescence under FR-enriched conditions is not fully understood. In this study, we investigated the role of phyA and phyB in regulating leaf senescence under FR in Arabidopsis thaliana (Arabidopsis). FR enrichment and intermittent FR pulses promoted the senescence of Arabidopsis leaves. Additionally, phyA and phyB mutants showed enhanced and repressed senescence phenotypes in FR, respectively, indicating that phyA and phyB antagonistically regulate FR-dependent leaf senescence. Transcriptomic analysis using phyA and phyB mutants in FR identified differentially expressed genes (DEGs) involved in leaf senescence-related processes, such as responses to light, phytohormones, and temperature, photosynthesis, and defense, showing opposite expression patterns in phyA and phyB mutants. These contrasting expression profiles of DEGs support the antagonism between phyA and phyB in FR-dependent leaf senescence. Among the genes showing antagonistic regulation, we confirmed that the expression of WRKY6, which encodes a senescence-associated transcription factor, was negatively and positively regulated by phyA and phyB, respectively. The wrky6 mutant showed a repressed senescence phenotype compared with the wild type in FR, indicating that WRKY6 plays a positive role in FR-dependent leaf senescence. Our results imply that antagonism between phyA and phyB is involved in fine-tuning leaf senescence under varying FR conditions in Arabidopsis.
Leaf senescence is influenced by its life history, comprising a series of developmental and physiological experiences. Exploration of the biological principles underlying leaf lifespan and senescence requires a schema to trace leaf phenotypes, based on the interaction of genetic and environmental factors. We developed a new approach and concept that will facilitate systemic biological understanding of leaf lifespan and senescence, utilizing the phenome high-throughput investigator (PHI) with a single-leaf-basis phenotyping platform. Our pilot tests showed empirical evidence for the feasibility of PHI for quantitative measurement of leaf senescence responses and improved performance in order to dissect the progression of senescence triggered by different senescence-inducing factors as well as genetic mutations. Such an establishment enables new perspectives to be proposed, which will be challenged for enhancing our fundamental understanding on the complex process of leaf senescence. We further envision that integration of phenomic data with other multi-omics data obtained from transcriptomic, proteomic, and metabolic studies will enable us to address the underlying principles of senescence, passing through different layers of information from molecule to organism.
Summary
Leaf senescence affects plant fitness. Plants that evolve in different environments are expected to acquire distinct regulations of leaf senescence. However, the adaptive and evolutionary roles of leaf senescence are largely unknown.
We investigated leaf senescence in 259 natural accessions of Arabidopsis by quantitatively assaying dark‐induced senescence responses using a high‐throughput chlorophyll fluorescence imaging system. A meta‐analysis of our data with phenotypic and climatic information demonstrated biological and environmental links with leaf senescence. We further performed genome‐wide association mapping to identify the genetic loci underlying the diversity of leaf senescence responses.
We uncovered a new locus, Genetic Variants in leaf Senescence (GVS1), with high similarity to reductase, where a single nonsynonymous nucleotide substitution at GVS1 mediates the diversity of the senescence trait. Loss‐of‐function mutations of GVS1 in Columbia‐0 delayed leaf senescence and increased sensitivity to oxidative stress, suggesting that this GVS1 variant promotes optimal responses to developmental and environmental signals. Intriguingly, gvs1 loss‐of‐function mutants display allele‐ and accession‐dependent phenotypes, revealing the functional diversity of GVS1 alleles not only in leaf senescence, but also oxidative stress.
Our discovery of GVS1 as the genetic basis of natural variation in senescence programs reinforces its adaptive potential in modulating life histories across diverse environments.
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