Seasonal switching of integrated leaf senescence controls in an evergreen perennial Arabidopsis

Evergreeness is a substantial strategy for temperate and boreal plants and is as common as deciduousness. However, whether evergreen plants switch foliage functions between seasons remains unknown. We conduct an in natura study of leaf senescence control in the evergreen perennial, Arabidopsis halleri. A four-year census of leaf longevity of 102 biweekly cohorts allows us to identify growth season (GS) and overwintering (OW) cohorts characterised by short and extended longevity, respectively, and to recognise three distinct periods in foliage functions, i.e., the growth, overwintering, and reproductive seasons. Photoperiods during leaf expansion separate the GS and OW cohorts, providing primal control of leaf senescence depending on the season, with leaf senescence being shut down during winter. Phenotypic and transcriptomic responses in field experiments indicate that shade-induced and reproductive-sink-triggered senescence are active during the growth and reproductive seasons, respectively. These secondary controls of leaf senescence cause desynchronised and synchronised leaf senescence during growth and reproduction, respectively. Conclusively, seasonal switching of leaf senescence optimises resource production, storage, and translocation for the season, making the evergreen strategy adaptively relevant.