When plants grow in close proximity, basic resources such as light might become limiting. Under such conditions, plants respond to anticipate and/or adapt to the light shortage, a process known as the shade avoidance syndrome (SAS). After a genetic screening using a shade-responsive luciferase reporter line (PHYB:LUC), we identified DRACULA2 (DRA2) that encodes an Arabidopsis homolog to mammalian nucleoporin 98, a component of the nuclear pore complex (NPC). DRA2, together with other nucleoporines, positively participates in the control of the hypocotyl elongation response to plant proximity, a role that can be considered as dependent on the nucleocytoplasmic transport of macromolecules (i.e., transport-dependent). In addition, our results reveal a specific role for DRA2 in controlling shade-induced gene expression. We suggest that this novel regulatory role of DRA2 is transport-independent, and it might rely on its dynamic localization in and off the NPC. These results provide mechanistic insights on how SAS responses are rapidly established by light conditions. They also indicate that nucleoporins have an active role in plant signaling.