Aging induces gradual yet massive cell death in higher organisms, including annual plants. Even so, the underlying regulatory mechanisms are barely known, despite the long-standing interest in this topic. Here, we demonstrate that ORE1, which is a NAC (NAM, ATAF, and CUC) transcription factor, positively regulates aging-induced cell death in Arabidopsis leaves. ORE1 expression is up-regulated concurrently with leaf aging by EIN2 but is negatively regulated by miR164. miR164 expression gradually decreases with aging through negative regulation by EIN2, which leads to the elaborate up-regulation of ORE1 expression. However, EIN2 still contributes to aging-induced cell death in the absence of ORE1. The trifurcate feed-forward pathway involving ORE1, miR164, and EIN2 provides a highly robust regulation to ensure that aging induces cell death in Arabidopsis leaves.

Leaf senescence is an important developmental process involving orderly disassembly of macromolecules for relocating nutrients from leaves to other organs and is critical for plants’ fitness. Leaf senescence is the response of an intricate integration of various environmental signals and leaf age information and involves a complex and highly regulated process with the coordinated actions of multiple pathways. Impressive progress has been made in understanding how senescence signals are perceived and processed, how the orderly degeneration process is regulated, how the senescence program interacts with environmental signals, and how senescence regulatory genes contribute to plant productivity and fitness. Employment of systems approaches using omics-based technologies and characterization of key regulators have been fruitful in providing newly emerging regulatory mechanisms. This review mainly discusses recent advances in systems understanding of leaf senescence from a molecular network dynamics perspective. Genetic strategies for improving the productivity and quality of crops are also described.

Cytokinins are plant hormones with profound roles in growth and development, including control of leaf longevity. Although the cytokinin signal is known to be perceived by histidine kinase receptors, the underlying molecular mechanism and specificity of the receptors leading to delayed leaf senescence have not yet been elucidated. Here, we found that AHK3, one of the three cytokinin receptors in Arabidopsis, plays a major role in controlling cytokinin-mediated leaf longevity through a specific phosphorylation of a response regulator, ARR2. This result was obtained through identification of a gain-of-function Arabidopsis mutant that shows delayed leaf senescence because of a missense mutation in the extracellular domain of AHK3. A loss-of-function mutation in AHK3, but not of the other cytokinin receptors, conferred a reduced sensitivity to cytokinin in cytokinin-dependent delay of leaf senescence and abolished cytokinin-dependent phosphorylation of ARR2. Consistently, transgenic overexpression of wild-type, but not an unphosphorylatable mutant ARR2, led to delayed senescence of leaves.histidine kinase 3 ͉ cytokinin ͉ leaf senescence L eaf senescence is typically observed in autumn leaves and during the death process of monocarpic plants (1). During senescence, leaf cells experience striking changes in cellular metabolism and structure (2). The first visible change is yellowing of the leaves caused by chlorophyll breakdown during chloroplast disassembly (3), accompanied by hydrolysis of macromolecules such as lipids, proteins, and nucleic acids. The products of this catabolic process are reallocated to developing organs, such as younger leaves and germinating seeds (4). Therefore, senescence is not a simple degenerative process but is considered as a genetically programmed, active process that contributes to the fitness of plants. Although occurring in an age-dependent manner, leaf senescence is greatly affected by various endogenous and environmental signals to attune the life span of leaves to optimized fitness of plants (5, 6). Among the endogenous developmental signals, the plant hormones cytokinins have a particularly profound effect on longevity of plant organs (7-9). For example, it has been shown that the transgenic modification of cytokinin biosynthesis during the senescence phase can significantly delay the senescence of plant organs, including leaves, and improve plant productivity by up to 50% (8, 10).Besides control of longevity, cytokinins have many critical functions in plants, such as the control of cell proliferation, shoot formation, nutrient relocation, and shoot branching (11,12). In Arabidopsis, cytokinins are known to be perceived by three cytokinin receptors, AHK2, AHK3, and AHK4͞CRE1͞WOL, which possess the structural features of hybrid histidine kinases (13,14). In the model proposed for the cytokinin signaltransduction pathway (15-17), a histidine protein kinase initiates the cytokinin signal-transduction pathway through phosphorelay to histidine phosphotransfer (AHP) proteins. AHP protei...