Significance Nuclear organization and genome expression are subject to massive reprogramming during most developmental transitions. The mechanisms triggering them in response to environmental stimuli are only poorly understood. Here we describe that dynamic changes in higher-order nuclear organization occurring in cotyledons (embryonic leaves) upon germination are impacted by light availability in the plant Arabidopsis thaliana . Upon light perception, master regulators of the light signaling pathway trigger rapid and massive nuclear expansion, condensation of large chromatin domains, and increased transcriptional activity of genes. These findings establish a foundation for deciphering the relationships between topological genome organization and transcriptional regulation associated with the establishment of photosynthesis.