The accumulation of hydrogen peroxide (H2O2) in plants is typically associated with biotic or abiotic stresses. However, H2O2 is continuously produced in cells during normal metabolism. Yet, little is known about how H2O2 accumulation will affect plant metabolism in the absence of pathogens or abiotic stress. Here, we report that a deficiency in the H2O2-scavenging enzyme, cytosolic ascorbate peroxidase (APX1), results in the accumulation of H2O2 in Arabidopsis plants grown under optimal conditions. Knockout-Apx1 plants were characterized by suppressed growth and development, altered stomatal responses, and augmented induction of heat shock proteins during light stress. The inactivation of Apx1 resulted in the induction of several transcripts encoding signal transduction proteins. These were not previously linked to H2O2 signaling during stress and may belong to a signal transduction pathway specifically involved in H2O2 sensing during normal metabolism. Surprisingly, the expression of transcripts encoding H2O2 scavenging enzymes, such as catalase or glutathione peroxidase, was not elevated in knockout-Apx1 plants. The expression of catalase, two typical plant peroxidases, and several different heat shock proteins was however elevated in knockout-Apx1 plants during light stress. Our results demonstrate that in planta accumulation of H2O2 can suppress plant growth and development, interfere with different physiological processes, and enhance the response of plants to abiotic stress conditions. Our findings also suggest that at least part of the induction of heat shock proteins during light stress in Arabidopsis is mediated by H2O2 that is scavenged by APX1.