Age-driven regulation of plant specialized metabolism: integration of transcriptional, hormonal, and epigenetic signals

Abstract Plant specialized metabolites are essential determinants of nutritional quality, stress adaptation, and medicinal value. Although the biosynthetic pathways of many metabolite classes have extensively characterized, far less is understood about how their accumulation is regulated over time. Increasing evidence indicates that metabolite profiles change with plant age, however, these changes occur in distinct temporal contexts that should be considered separately. In this review, we distinguish among developmental phase transition, organ developmental progression, and chronological aging, and discuss how each influences the accumulation of flavonoids, terpenoids, alkaloids, and other specialized metabolites. We highlight the miR156-SPL pathway as the well characterized mechanistic linking developmental phase transition to specialized metabolism in angiosperms. We also discuss DAL1-mediated age regulation in gymnosperms as an evolutionarily distinct developmental timing system whose direct links to specialized metabolism are emerging. For organ developmental progression and chronological aging, we emphasize epigenetic modifications as key regulators that drive or reprogram metabolic pathways. In particular, DNA methylation acts not only as a plant epigenetic clock, but also as an important regulatory mechanism during leaf senescence, fruit ripening, and chronological aging. In addition, we examine how hormonal and environmental cues interact with age pathways to modulate metabolic outputs. Finally, we discuss current conceptual and methodological challenges in this field and propose future directions for using age regulation to optimize the production of bioactive compounds with high value in crops and medicinal plants.