Reactive oxygen species (ROS) have challenged aerobic organisms since the emergence of oxygenic metabolism. Beyond causing macromolecular damage, ROS act as conserved second messengers that coordinate growth, defence, and stress acclimation. Here, we synthesise the current understanding of how ROS mediate retrograde communication between chloroplasts and mitochondria during abiotic stress (e.g., drought, heat, and salinity). This study provides a unique conceptual framework for ROS interactions between chloroplasts and mitochondria, retrograde signaling, redox homeostasis, and transcriptional reprogramming under abiotic stress. Unlike previous reviews, the present study offers an integrated and critical review of ROS-dependent retrograde signaling between organelles, with a particular focus on the signaling roles of different ROS species, the interrelationship between organelles, recent mechanistic advances (2023–2026), and innovative approaches to enhancing plant resistance to abiotic stress. This review further highlights its distinctive scope and added value compared with previous reviews. Under stress, organellar ROS act within integrated redox networks to initiate signalling cascades that reprogram nuclear gene expression, adjust metabolism, and enhance tolerance. We summarise the principal sources of ROS in photosynthetic and respiratory electron transport, the antioxidant systems that shape their spatiotemporal dynamics, and the key retrograde pathways and transcriptional nodes that couple organelles to the nucleus. Finally, we highlight candidate genes and engineering strategies, particularly those targeting organelle-to-nucleus signalling, to improve stress resilience in crops, and outline outstanding challenges in resolving ROS-driven organellar crosstalk.
