Abstract: Plants must coordinate chloroplast biogenesis with environmental conditions during seedling establishment, as failure to do so results in impaired phototrophic growth. Despite the biological importance of this early developmental stage, the influence of environmental factors on chloroplast biogenesis remains poorly understood. Here, we reveal a crucial role for GENOMES UNCOUPLED1 (GUN1)-mediated biogenic retrograde signaling in safeguarding chloroplast development and supporting seedling growth under heat stress. Loss of GUN1 causes severe bleaching and impaired photomorphogenesis at elevated temperatures. Genetic interaction analyses show that EXECUTER1 (EX1) and EXECUTER2 (EX2), key components of chloroplast ROS-associated operational retrograde signaling, modulate the heat-sensitive phenotype of gun1 mutants, indicating crosstalk between biogenic and operational retrograde pathways. We further demonstrate that the de-repressed expression of photosynthesis-associated nuclear genes, that is, genomes uncoupled expression, is a major contributor to the heat sensitivity and failed chloroplast biogenesis in gun1 seedlings under heat stress. These findings extend the current understanding of GUN1 function by showing its contribution to chloroplast development and thermotolerance through biogenic retrograde signaling during early seedling growth.

Key words: EXECUTER1, EXECUTER2, GUN1, retrograde signaling, thermotolerance