April 1, 2014

Review: Fast retrograde signaling in response to high light Involves metabolite export, MITOGEN-ACTIVATED PROTEIN KINASE6, and AP2/ERF transcription factors in Arabidopsis

Published online at The Plant Cell before print: www.plantcell.org/cgi/doi/10.1105/tpc.113.121061

Marc Oliver Vogela, Marten Moorea, Katharina K├Âniga, Pascal Pecherb, Khalid Alsharafa a, Justin Lee b, and Karl-Josef Dietza*
* Corresponding author
a Biochemistry and Physiology of Plants, Bielefeld University, 33501 Bielefeld, Germany
b Leibniz Institute of Plant Biochemistry, 06120 Halle, Germany
    As photosynthetic organisms, it follows naturally that plants are highly sensitive to changes in their light environment. Plants must adjust their metabolism and transcriptional programs rapidly in response to such changes. Complex regulatory cascades enable the plant to react quickly at transcript, protein, and metabolite levels that facilitate continual adjustment to environmental changes, including light levels. Because most of the protein machinery dealing with light is located in the chloroplast, while most genes encoding such proteins are part of the nuclear genome, a communication network would seem necessary by which chloroplasts can signal changes to the nucleus via direct feedback regarding the status of the cellular pool of chloroplasts. Such communication is in fact well documented and has been dubbed retrograde signaling. 

    The sensitivity to light changes provided by this light-sensitive network alternately helps the organism conserve resources when light is low and quickly ramp up photosynthetic rates when light levels are high. The responsiveness to light becomes especially important under high light intensity, i.e. light stress. The potential for irreversible photooxidative damage is significant, and dangerous imbalances to metabolite pools can occur without metabolic overflow shunts that avoid destabilizing metabolic buildups. The many responses to changes in ambient light must be implemented in a coordinated manner in the plant cell, and the implications of this phenomenon on agriculture are significant enough to make this a highly competitive and active area of original research.

    German investigators at Bielefeld University and the Leibniz Institute for Plant Biochemistry have published a report in The Plant Cell which advances our knowledge of the early events in high light signaling. Using Arabidopsis, Vogel et al.1 examined changes in transcript levels in a family of transcription factors known as APETALA2/ETHYLENE RESPONSE FACTOR (ERF). Quantitative PCR revealed that multiple ERF genes were upregulated in a little as 10 minutes following transfer of dark adapted plants to high light. However, this induction was blocked in tpt2, a mutant defective in the triose phosphate transporter which shuttles dihydroxyacetone phosphate (DHAP) between the plastid and cytosol. This implicated metabolite transport in the early signaling response to light. This process was necessary to activate MAP kinase 6 (MAPK6), which in turn activates ERFs.

    Antibodies which specifically recognize phosphorylated forms of MAPK6 were used to show that the activation of this protein occurs on the timescale of 1-2 minutes after transfer of plants to light. However, MAPK6 transcripts do not change upon light exposure; only phosphorylation of extant MAPK6 protein is required, versus translation of new protein, in effect shortening the response time of this signaling cascade. The authors pinpointed a time frame of 1-2 minutes as the point of no return for ERF transcriptional activation based on the fast activation of MAPK6. The well known biotic stress responsive gene PR1 as well as heat shock proteins and chitinases were upregulated downstream as a result of ERF activation, a result supported by microarray data using the erf6 mutant. Because of kinetic data in light induction time courses, the authors were able to rule out H2O2 as an early signal due to its late appear (>10 min) on the time scale of responses relative to MAPK6 activation and triose phosphate efflux from the plastid (seconds after light exposure). 

    The authors propose a model for early events in high light signaling which begins with efflux of triose phosphates as a direct response to the transition to high light due to increased flux in the Calvin-Benson-Bassham cycle. This is followed by activation of MAPK6 by unidentified protein kinases and transcription factor which in turn induce transcript accumulation of ERF transcription factors. Following de novo synthesis of the encoded ERF proteins, the metabolic shift in preparation for high light conditions is completed by the induction of heat shock proteins, additional cascade components, and formation of H2O2, a previously known metabolite signal belonging to the reactive oxygen species (ROS) group. The authors are congratulated for the publication of this excellent work which advances our understanding of the elements which govern the light response process in plants.

    Additional questions: While considerable evidence is presented to clearly define novel components of light signaling, the metabolic data and the specific role of metabolite efflux are less clear. How can the authors be certain it is DHAP export from the plastid which promotes MAPK6 phosphorylation? While the tpt2 mutant data is convincing, it is unclear how this specific metabolite can exert the alleged effects. Also, the authors conclude by mentioning a variety of metabolites which could feasibly contribute to operational retrograde signaling, including H2O2, singlet oxygen, and hormones. However, one molecule could be added to this list: 2-C-methylerythritol-2,4-cyclodiphosphate, an intermediate of the 2-C-methylerythritol phosphate pathway for plastid isoprenoid biosynthesis. This intermediate accumulates under high light2 and has been implicated in biotic3 and abiotic4 stress signaling by export from the plastid. Given the sensitivity of MEcPP to light and its alleged secondary signaling function outside the plastid, it seems plausible that it could also play a role in the high light response described by Vogel et al. The present work provides new perspective on light signaling and suggests several new avenues of research.

1.         Vogel, M. O. et al. Fast retrograde signaling in response to high light Involves metabolite export, MITOGEN-ACTIVATED PROTEIN KINASE6, and AP2/ERF transcription factors in Arabidopsis. Plant Cell (2014).
2.         Li, Z. & Sharkey, T. D. Metabolic profiling of the methylerythritol phosphate pathway reveals the source of post-illumination isoprene burst from leaves. Plant, Cell & Environment 36, 429-437 (2012).
3.         Gil, M. J., Coego, A., Mauch-Mani, B., Jorda, L. & Vera, P. The Arabidopsis csb3 mutant reveals a regulatory link between salicylic acid-mediated disease resistance and the methyl-erythritol 4-phosphate pathway. Plant J 44, 155-166 (2005).
4.         Xiao, Y. et al. Retrograde signaling by the plastidial metabolite MEcPP regulates expression of nuclear stress-response genes. Cell 149, 1525-1535 (2012).

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