High REDOX RESPONSIVE TRANSCRIPTION FACTOR1 Levels Result in Accumulation of Reactive Oxygen Species in Arabidopsis thaliana Shoots and Roots

Abstract

Redox Responsive Transcription Factor1 (RRTF1) in Arabidopsis is rapidly and transiently upregulated by H2O2, as well as biotic- and abiotic-induced redox signals. RRTF1 is highly conserved in angiosperms, 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 systemically 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 senescence-related functions. Bioinformatic analyses and in vitro DNA binding assays demonstrate that RRTF1 binds to GCC-box-like sequences in the promoter of RRTF1-responsive genes. Upregulation of RRTF1 by stress stimuli and H2O2 requires WRKY18/40/60. RRTF1 is co-regulated with the phylogenetically 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.

ROS, Calcium, and Electric Signals: Key Mediators of Rapid Systemic Signaling in Plants

“…A recent study demonstrated that REDOX RE-SPONSIVE TRANSCRIPTION FACTOR1 (RRTF1) might function as a key regulator of systemic ROSdependent responses during high light stress (Matsuo et al, 2015). RRTF1-dependent systemic signaling was shown to be regulated by WRKY transcription factors (Matsuo et al, 2015), whose expression is enhanced during RBOHD-dependent SAA (Miller et al, 2009), but its rate of systemic response is slower than that of the ROS wave.…”

“…RRTF1-dependent systemic signaling was shown to be regulated by WRKY transcription factors (Matsuo et al, 2015), whose expression is enhanced during RBOHD-dependent SAA (Miller et al, 2009), but its rate of systemic response is slower than that of the ROS wave. RRTF1 could therefore play a role in the regulation of gene expression downstream to the ROS wave during SAA (Fig.…”

A Poly(A) Ribonuclease Controls the Cellotriose-Based Interaction between Piriformospora indica and Its Host Arabidopsis

“…Total RNA from roots of transgenic A. thaliana (Col-0) expressing cytosolic apoaequorin 729 (pMAQ2, Knight et al, 1991, Polisensky andBraam, 1996) procedure and determination of the ABA concentrations were performed as described in 775 Matsuo et al (2015). Stomata closure was determined as described in Vahabi et al (2016).…”

Recent Progress in Understanding the Role of Reactive Oxygen Species in Plant Cell Signaling

“…Several members of the FAR-RED-IMPAIRED RESPONSE1-related sequence family of transcription factors were also recently implicated in integrating ROS with different developmental and environmental responses (Wang and Wang, 2015). Additional ROS-response regulatory proteins identified in recent years include the APETALA2/ethylene response transcription factor REDOX RESPONSIVE TRANSCRIP-TION FACTOR1 that is regulated by different WRKYs (Matsuo et al, 2015), different members of the NAC family of transcription factors (e.g. Fang et al, 2015;Chen et al, 2016;Zhu et al, 2016), and different zinc-finger proteins such OXIDATIVE STRESS2 (He et al, 2016).…”