Temporal kinetics of the transcriptional response to carbon depletion and sucrose readdition in Arabidopsis seedlings

To investigate whether the transcriptional response to carbon (C) depletion and sucrose resupply depends on the duration and severity of the C depletion, Arabidopsis seedlings were grown in liquid culture and harvested 3, 6, 12, 24, 48 and 72h after removing sucrose from the medium and 30min after resupplying sucrose at each time. Expression profiling revealed early transcriptional inhibition of cell wall synthesis and remodelling of signalling, followed by induction of C recycling and photosynthesis and general inhibition of growth. The temporal sequence differed from the published response to progressive exhaustion of C during a night and extended night in vegetatively growing plants. The response to sucrose readdition was conserved across the C-depletion time course. Intriguingly, the vast majority of rapidly responding transcripts decreased rather than increased. The majority of transcripts that respond rapidly to sucrose and many transcripts that respond during C depletion also decrease after treating seedlings with the transcriptional inhibitor cordycepin A. Comparison with published responses to overexpression of otsA, AKIN10 and bZIP11 revealed that many genes that respond to C depletion, and especially sucrose resupply, respond to one or more of these C-signalling components. Thus, multiple factors contribute to C responsiveness, including many signalling components, transcriptional regulation and transcript turnover. There have been many studies of the response of gene expression to chronic C starvation, but little is known about the temporal response during progressive C depletion. In studies with Arabidopsis seedlings in liquid culture, we report progressive changes in transcript levels, with early repression of cell wall synthesis and slower repression of growth-related processes and induction of catabolism and photosynthesis. The response to sucrose resupply was conserved and dominated by transcripts that decreased. Many transcripts that respond during C depletion and most of the transcripts that respond to sucrose readdition also decrease after treating seedlings with the transcriptional inhibitor cordycepin A, revealing an important role for transcript turnover in the response to sucrose.