Cytokinin downregulates Photosystem II photochemistry during prolonged darkness in a phytochrome B-dependent manner

Cytokinins (CKs) delay dark-induced senescence, but how they tune photosynthetic function in darkness remains unclear. We investigated the effects of classical aromatic CK benzylaminopurine and CK-derived compound 1-(2-methoxyethyl)-3-(1,2,3-thiadiazol-5-yl)urea on detached Arabidopsis leaves at different time points during dark incubation. Notably, while both compounds mitigated the progression of senescence, they unexpectedly downregulated Photosystem II (PSII) photochemistry during the early stages of dark incubation. Despite this downregulation, CK-treated leaves preserved functional photochemistry and substantially delayed Chl degradation at later time points. Transcriptomic analysis at the early stage of darkening revealed that a significant portion of CK-responsive genes is associated with photosynthesis, PSII function, and light sensing, including red-light signaling pathways. Differential proteomics further supported a CK-induced shift to a metabolically suppressed state. The early PSII downregulation required phytochrome B, indicating a CK-phyB module that places darkened leaves into a reversible 'standby' mode, limiting energy demand and enabling rapid, safer recovery of photosynthesis upon re-illumination. At the same time, it may also protect the photosynthetic apparatus against photo-oxidative damage during the transition from dark- to light-adapted states.