A PIF- and GUN1-regulated switch in cell axis growth drives cotyledon expansion through tissue-specific cell expansion and division

Despite its crucial role during seedling deetiolation, cotyledon expansion has been largely overlooked, with hypocotyl elongation favored as the primary phenotypic readout in light signaling research. Here, we investigate how cotyledon expansion is regulated during seedling establishment, and reveal that light-induced cotyledon expansion involves a rapid switch in growth direction - from longitudinal in darkness to transversal upon initial light exposure. Using PIFq- and phyA/phyB-deficient Arabidopsis mutants, we demonstrate that this switch is repressed by PIFs in the dark and promoted by phytochromes under red light. Notably, expansion is antagonistically regulated in the light by GUN1-mediated plastid retrograde signaling. Cotyledon expansion involves rapid epidermis cell expansion, transitioning from rectangular in darkness to characteristic lobed cells in light. Importantly, our findings show that mesophyll extension is driven not only by cell enlargement but also by palisade cell division, consistent with an enrichment of cell cycle-related genes that are antagonistically regulated by the PIF/phy system and retrograde signaling in the cotyledon. Finally, using mutant lines expressing PIF1 and phyB specifically in the epidermis, we establish that epidermal expansion can drive palisade cell growth, while mesophyll cell division is predominantly regulated by light at the tissue-specific level. This study provides a novel framework for investigating cotyledon expansion during seedling deetiolation, incorporating tissue-level regulation. We propose that cotyledons serve as an excellent model for studying morphogenesis and organ geometry, which in plants is governed by directional cell growth.