The release of yeast cells from nitrogen limitation triggers remodeling of cellular physiology to enable a faster rate of cell growth. While the population growth rate increase is not apparent until approximately 2 hours after, the nitrogen upshift triggers extensive transcriptional reprogramming on the timescale of minutes. Conserved signalling pathways, including TORC1 and Ras/PKA, are known to regulate steady-state growth, but the role of these pathways during the first few minutes of a nutrient upshift is unclear. Using the transcriptome to define the cellular state, we show that this upshift doesn’t simply entail a shift from a slow growth steady-state to a fast growth steady-state, but rather proceeds through a transient alternative state. Using time-series modeling of transcriptome dynamics, we show evidence for a pulse of ribosomal component mRNA overproduction and accelerated degradation of high-affinity nitrogen transporter mRNAs, including GAP1 and DIP5. To identify factors regulating this process, we used a branched DNA single molecule RNA FISH (smFISH) assay with flow cytometry to quantify transcript abundance in single cells during the upshift. Combining this assay with FACS and barcode sequencing (Barseq), we screened the pooled homozygous deletion collection for mutants defective in the accelerated degradation of GAP1 mRNA upon a nitrogen upshift. Our approach provides an effective means of screening for mutants defective in transcriptional dynamics that occur on the timescale of minutes.