Evergreenness is a key survival strategy for plants in temperate and boreal regions, occurring as frequently as deciduousness. However, whether evergreen plants adjust their foliage functions seasonally remains unclear. In this study, we investigated the seasonal regulation of leaf senescence in the evergreen perennial Arabidopsis halleri through an in natura approach. By monitoring leaf longevity over four years across 102 biweekly cohorts (leaves emerging every two weeks), we identified two distinct groups: growth-season (GS) cohorts with short-lived leaves and overwintering (OW) cohorts with extended longevity. This differentiation allowed us to define three functional phases of foliage: the growth, overwintering, and reproductive seasons.
Our findings revealed that photoperiod during leaf expansion serves as a primary regulator, determining whether leaves belong to the GS or OW cohorts and thereby controlling seasonal leaf senescence. Notably, senescence was effectively suppressed throughout winter. Field experiments integrating phenotypic and transcriptomic analyses further demonstrated that shade-induced senescence predominates during the growth season, while reproductive-sink-driven senescence is active in the reproductive season. These secondary regulatory mechanisms led to desynchronized senescence during vegetative growth and synchronized senescence during reproduction.
In conclusion, we propose that the seasonal modulation of leaf senescence optimizes resource allocation—enhancing production, storage, and redistribution in accordance with seasonal demands—thus reinforcing the adaptive advantage of the evergreen strategy in seasonal environments.