The coordination of chloroplast function with the rest of cellular activity requires a continual stream of communication from this organelle to the nucleus. Chloroplasts are major sites of the production of reactive oxygen species (ROS) as either by-products of the reduction of molecular oxygen (O(2)) or its excitation in the presence of highly energised pigments. Such ROS, while potentially damaging to the cell, are also important initiators or transducers of signals from these organelles to the nucleus in response to environmental cues. ROS can initiate such retrograde signalling pathways that trigger either programmed cell death or adjustment to changed conditions. Such different outcomes have implications for the way in which signal transduction by ROS is accomplished and is the subject of this review. In response to mild-stress situations, and as a consequence of their reactivity or because of their containment by cellular antioxidant systems, it is proposed that ROS engage with or initiate signalling at or very near their site of production. In contrast, under more extreme conditions, ROS are proposed to diffuse away from their site of production and consequently elicit a different set of signalling events.