Redox Responsive Transcription Factor1 （RRTF1） in Arabidopsis is rapidly and transiently upregulated by H202, as well as biotic- and abiotic-induced redox signals. RRTF1 is highly conserved in angio- sperms, but its physiological role remains elusive. Here we show that inactivation of RRTF1 restricts and overexpression promotes reactive oxygen species （ROS） accumulation in response to stress. Transgenic lines overexpressing RRTF1 are impaired in root and shoot development, light sensitive, and susceptible to Alternaria brassicae infection. These symptoms are diminished by the beneficial root endophyte Piriformospora indica, which reduces ROS accumulation locally in roots and systemi- cally in shoots, and by antioxidants and ROS inhibitors that scavenge ROS. More than 800 genes were detected in mature leaves and seedlings of transgenic lines overexpressing RRTF1; ∽40% of them have stress-, redox-, ROS-regulated-, ROS-scavenging-, defense-, cell death- and related functions. Bioinformatic analyses and in vitro DNA binding assays demonstrate that RRTF1 binds to GCC-box-like sequences in the promoter of RRTFl-responsive genes. Upregulation of RRTF1 by stress stimuli and H202 requires WRKY18/40/60. RRTF1 is co-regulated with the phylogenet- ically related RAP2.6, which contains a GCC-box-like sequence in its promoter, but transgenic lines overexpressing RAP2.6 do not accumulate higher ROS levels. RRTF1 also stimulates systemic ROS accumulation in distal non-stressed leaves. We conclude that the elevated levels of the highly conserved RRTF1 induce ROS accumulation in response to ROS and ROS-producing abiotic and biotic stress signals.