Multilevel genomics analysis of carbon signalling during low carbon availability: coordinating the supply and utilisation of carbon in a fluctuating environment
Mark Stitt A B , Yves Gibon A , John E. Lunn A and Maria Piques AA Max-Planck-Institute of Molecular Plant Physiology, Am Mühlenberg 1, 14424 Golm, Germany.
B Corresponding author. Email: mstitt@mpimp-golm.mpg.de
C This paper originates from a presentation at the 8th International Congress of Plant Molecular Biology, Adelaide, Australia, August 2006.
Functional Plant Biology 34(6) 526-549 https://doi.org/10.1071/FP06249
Submitted: 30 October 2006 Accepted: 6 December 2006 Published: 1 June 2007
Abstract
Plants alternate between a net surplus of carbon in the light and a net deficit at night. This is buffered by accumulating starch in the light and degrading it at night. Enough starch is accumulated to support degradation throughout the night, with a small amount remaining at the end of the 24-h diurnal cycle. This review discusses how this balance between the supply and utilisation of carbon is achieved in Arabidopsis. It is important to regulate starch turnover to avoid an acute carbon deficiency. A 2–4 h extension of the night leads to exhaustion of starch, a collapse of sugars, a switch from biosynthesis to catabolism and an acute inhibition of growth by low carbon, which is not immediately reversed when carbon becomes available again. In starchless pgm mutants, where sugars are depleted each night, this leads to a recurring inhibition of growth that is not reversed until 5–6 h into the following light period. Several lines of evidence show that starch accumulation is regulated in response to events that are initiated during periods of low carbon. Starch accumulation is decreased when small amounts of sucrose are included in the growth medium. Sets of sugar-responsive genes were identified by supplying sugars to carbon-starved seedlings, or by illuminating 5-week-old plants in the presence of 350 or 50 ppm [CO2]. Almost all of these genes show large diurnal changes in starchless pgm mutants, which are driven by the depletion of carbon during the night. Many show significant diurnal changes in wild type plants, showing that ‘anticipatory’ changes in signalling pathways occur before acute carbon limitation develops. However, these diurnal changes of transcripts do not lead to immediate changes of enzyme activities. Whereas an extension of the night leads to major changes of transcripts within 4–6 h, changes in enzyme activities require several days. In pgm, enzyme activities and the levels of >150 metabolites resemble those found in wild type plants after several days in the dark. It is concluded that diurnal changes in transcript levels are integrated, over days, as changes in the levels of enzymes. We hypothesise that this facilitates an adjustment of metabolism to a mid-term shift in the conditions, while ignoring noise due to diurnal changes and day-to-day fluctuations. The rapid adjustment of starch synthesis after a period of acute carbon depletion is a consequence of the transient inhibition of growth. This leads to accumulation of sugars when carbon becomes available again, which triggers a large increase in trehalose-6-phosphate. This signal metabolite promotes thioredoxin-dependent post-translational activation of ADP glucose pyrophosphorylase. Mid-term acclimation to a decreased carbon supply may be mediated by a combination of post-translational regulation, longer-term changes in enzyme activities, and a decrease in the rate of growth.
Additional keywords: Arabidopsis, diurnal, enzyme activities, expression arrays, growth, metabolite profile, starch, sucrose, sugars.
Acknowledgements
We acknowledge the contributions of Oliver Bläsing, Björn Usadel, Oliver Thimm, Daniel Osuna, Wolf-Rüdiger Scheible, Rosa Morcuende, Melanie Höhne, Manuela Günter, Uschi Krause and Regina Feil to the research described in this review. The concept of ‘acclimatory’ responses was developed in discussion with Alison Smith, Nick Harberd, Gerrit Beemster and Dirk Inzé. The research described in this review was supported by the BMBF (GABI-Gauntlets) and the Max Planck Society. The work was supported by the Max-Planck-Society and the BMBF-funded project GABI Verbund Arabidopsis III ‘Gauntlets, Carbon and Nutrient Signalling: Test Systems, and Metabolite and Transcript Profiles’ (0312277A).
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