Spatiotemporal Patterning of Reactive Oxygen Production and Ca2+ Wave Propagation in Fucus Rhizoid Cells

Both Ca(2+) and reactive oxygen species (ROS) play critical signaling roles in plant responses to biotic and abiotic stress. However, the positioning of Ca(2+) and ROS (in particular H(2)O(2)) after a stress stimulus and their subcellular interactions are poorly understood. Moreover, although information can be encoded in different patterns of cellular Ca(2+) signals, little is known about the subcellular spatiotemporal patterns of ROS production or their significance for downstream responses. Here, we show that ROS production in response to hyperosmotic stress in embryonic cells of the alga Fucus serratus consists of two distinct components. The first ROS component coincides closely with the origin of a Ca(2+) wave in the peripheral cytosol at the growing cell apex, has an extracellular origin, and is necessary for the Ca(2+) wave. Patch-clamp experiments show that a nonselective cation channel is stimulated by H(2)O(2) and may underlie the initial cytosolic Ca(2+) increase. Thus, the spatiotemporal pattern of the Ca(2+) wave is determined by peripheral ROS production. The second, later ROS component localizes to the mitochondria and is a direct consequence of the Ca(2+) wave. The first component, but not the second, is required for short-term adaptation to hyperosmotic stress. Our results highlight the role of ROS in the patterning of a Ca(2+) signal in addition to its function in regulating cell wall strength in the Fucus embryo.