Arabidopsis Transcriptome Reveals Control Circuits Regulating Redox Homeostasis and the Role of an AP2 Transcription Factor  

Abstract

Sensors and regulatory circuits that maintain redox homeostasis play a central role in adjusting plant metabolism and development to changing environmental conditions. We report here control networks in Arabidopsis (Arabidopsis thaliana) that respond to photosynthetic stress. We independently subjected Arabidopsis leaves to two commonly used photosystem II inhibitors: high light (HL) and 3-(3,4-dichlorophenyl)-1,1-dimethylurea (DCMU). Microarray analysis of expression patterns during the period of redox adjustment to these inhibitors reveals that 20% and 8% of the transcriptome are under HL and DCMU regulation, respectively. Approximately 6% comprise a subset of genes common to both perturbations, the redox responsive genes (RRGs). A redox network was generated in an attempt to identify genes whose expression is tightly coordinated during adjustment to homeostasis, using expression of these RRGs under HL conditions. Ten subnetworks were identified from the network. Hierarchal subclustering of subnetworks responding to the DCMU stress identified novel groups of genes that were tightly controlled while adjusting to homeostasis. Upstream analysis of the promoters of the genes in these clusters revealed different motifs for each subnetwork, including motifs that were previously identified with responses to other stresses, such as light, dehydration, or abscisic acid. Functional categorization of RRGs demonstrated involvement of genes in many metabolic pathways, including several families of transcription factors, especially those in the AP2 family. Using a T-DNA insertion in one AP2 transcription factor (redox-responsive transcription factor 1 [RRTF1]) from the RRGs, we showed that the genes predicted to be within the subnetwork containing RRTF1 were changed in this insertion line (Drrtf1). Furthermore, Drrtf1 showed greater sensitivity to photosynthetic stress compared to the wild type.

Fast Retrograde Signaling in Response to High Light Involves Metabolite Export, MITOGEN-ACTIVATED PROTEIN KINASE6, and AP2/ERF Transcription Factors in Arabidopsis

“…AP2/ERF-TFs are known to be involved in abiotic stress response (Agarwal et al, 2006;Dietz et al, 2010) and light acclimation (Koussevitzky et al, 2007;Khandelwal et al, 2008;Gordon et al, 2012). The identified AP2/ERF-TF coexpression network of 19 members revealed H-light responsiveness (Figure 1), 12 members of which were upregulated at t = 10 min following the L→H shift and upon N→H shift.…”

“…In addition, the chloroplast MDH and alterations in the NADPH-to-NADP + ratio mediated by the malate valve are not involved in the initiation of ERF6, ERF104, and ERF105 accumulation (Supplemental Figure 3). The different expression profile of RRTF1 in the mdh mutant (Supplemental Figure 3) where the redox balance between the chloroplast and cytosol is changed could be due to the previously described involvement of RRTF1 in redox regulation (Khandelwal et al, 2008). The function of RRTF1 in redox homeostasis still remains elusive.…”

“…In addition to this general evidence for a role of AP2/ERF-TFs in retrograde signaling, the AP2/ERF-TF ABSCISIC ACID INSENSITIVE4 acts downstream of the master switch GENOME UNCOUPLED1 (Richly et al, 2003), which mediates signal transmission by pathways originating from protochlorophyllide, photosynthetic electron transport, and oxidative stress in seedlings (Koussevitzky et al, 2007). Khandelwal et al (2008) reported expressional upregulation of REDOX RESPONSIVE TRANSCRIPTION FACTOR1 (RRTF1) in response to high light and DCMU and placed it in the central position of a redox responsive coexpression network. Leaves of a rrtf1 line bleach within 48 h of high-light treatment and the coexpression network of redox-responsive genes collapses.…”

The functions of WHIRLY1 and REDOX-RESPONSIVE TRANSCRIPTION FACTOR 1 in cross tolerance responses in plants: a hypothesis

“…Moreover, aphid fecundity was unaffected in Drrtf1 mutants that lack a functional RRTF1 [47]. RRTF1 transcripts were increased in response to JA [48], and this transcription factor may function alongside JAZ8 and proteins in the JA pathway to regulate plant defence responses [49].…”

“…This difference was presumably due to the accumulation of protective pigments such as anthocyanin in the wild-type but not in the Drrtf1 mutant leaves, because the levels of total chlorophyll, the chlorophyll a/b ratios and the ratios of carotenoid pigments to chlorophyll were similar in both genotypes (figure 2c). A transcriptomic analysis of the leaves of the Drrtf1 mutants suggested an association between RRTF1 and PAP1 [49], which is a transcription factor that is involved in the regulation of anthocyanin biosynthesis. Although the dark-adapted F v /F m values decreased in leaves as a result of transfer from lowlight to high-light growth conditions, the high-light-induced decrease was similar in mutant and wild-type leaves (figure 2d).…”