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

Abstract

Regulation of the expression of nuclear genes encoding chloroplast proteins allows for metabolic adjustment in response to changing environmental conditions. This regulation is linked to retrograde signals that transmit information on the metabolic state of the chloroplast to the nucleus. Transcripts of several APETALA2/ETHYLENE RESPONSE FACTOR transcription factors (AP2/ERF-TFs) were found to respond within 10 min after transfer of low-light-acclimated Arabidopsis thaliana plants to high light. Initiation of this transcriptional response was completed within 1 min after transfer to high light. The fast responses of four AP2/ERF genes, ERF6, RRTF1, ERF104, and ERF105, were entirely deregulated in triose phosphate/ phosphate translocator (tpt) mutants. Similarly, activation of MITOGEN-ACTIVATED PROTEIN KINASE6 (MPK6) was upregulated after 1 min in the wild type but not in the tpt mutant. Based on this, together with altered transcript regulation in mpk6 and erf6 mutants, a retrograde signal transmission model is proposed starting with metabolite export through the triose phosphate/phosphate translocator with subsequent MPK6 activation leading to initiation of AP2/ERF-TF gene expression and other downstream gene targets. The results show that operational retrograde signaling in response to high light involves a metabolite-linked pathway in addition to previously described redox and hormonal pathways.

Acclimation of metabolism to light in Arabidopsis thaliana: the glucose 6‐phosphate/phosphate translocator GPT2 directs metabolic acclimation

“…2014). Mutants lacking TPT have previously been shown to be unable to acclimate to high irradiances (Walters et al .…”

“…2004. Rapid transient expression of transcription factors observed following an increase in irradiance is suppressed in the tpt2 mutant of Col‐0 (Vogel et al ., 2014). This suggests that cytosolic concentrations of triose phosphates and/or other primary metabolites are important in regulating gene expression in a highly dynamic way.…”

The acclimation response to high light is initiated within seconds as indicated by upregulation of AP2/ERF transcription factor network inArabidopsis thaliana

“…A subgroup of the AP2/ERF TF family is transcriptionally induced within 10 min after light shift. 15 Such rapid response systems serve as immediate reaction to counter the effects of fluctuating conditions and are important to allow for subsequent long term acclimation. Deep insight into early acclimation processes requires knowledge on the chronological order of events.…”

“…13,14 Recently, it has been shown that the predominant assimilate transporter, the triosephosphate-phosphate translocator (TPT), participates in rapid information transmission controlling transcript accumulation. 15 Rapid regulation relies on existing transcription factors (TF) which conditionally adjust gene expression in response to stress stimuli. 16 Downstream inducible TFs realize the acclimation response.…”

“…This treatment is called L-light to H-light to L-light condition (LH!L). 15 The previously identified early responding AP2/ ERF-TF network with ERF6 (At4g17490), ERF104 (At5g61600), ERF105 (At5g51190) and RRTF1 (At4g34410) as elements was chosen as indicator of successful signal transmission (Fig. 1).…”