Significance Management of oxidative stress in plant chloroplasts involves signaling pathways to the nucleus that trigger stress response mechanisms. Yet, how oxidative stress is initially sensed in the chloroplast to activate accumulation of a stress signal remains enigmatic. We show that inactivation of a phosphatase, SAL1, by oxidative stress in chloroplasts controls accumulation of its substrate, as a plant stress signal. This regulatory mechanism is highly conserved across the plant kingdom and confers a second function to this metabolic enzyme as an oxidative stress sensor.