Complementary Proteome and Transcriptome Profiling in Phosphate-deficient Arabidopsis Roots Reveals Multiple Levels of Gene Regulation

Phosphate (P-i) deficiency impairs plant growth and productivity in many agricultural ecosystems, causing severe reductions in crop yield. To uncover novel aspects in acclimation to P-i starvation, we investigated the correlation between P-i deficiency-induced changes in transcriptome and proteome profiles in Arabidopsis roots. Using exhaustive tandem mass spectrometry-based shotgun proteomics and whole-genome RNA sequencing to generate a nearly complete catalog of expressed mRNAs and proteins, we reliably identified 13,298 proteins and 24,591 transcripts, subsets of 356 proteins and 3106 mRNAs were differentially expressed during P-i deficiency. Most dramatic changes were noticed for genes involved in P-i acquisition and in processes that either liberate P-i or bypass P-i/ATP-consuming metabolic steps, for example during membrane lipid remodeling and glycolytic carbon flux. The concordance between the abundance of mRNA and its encoded protein was generally high for highly up-regulated genes, but the analysis also revealed numerous discordant changes in mRNA/protein pairs, indicative of divergent regulation of transcription and post-transcriptional processes. In particular, a decreased abundance of proteins upon P-i deficiency was not closely correlated with changes in the corresponding mRNAs. In several cases, up-regulation of gene activity was observed solely at the protein level, adding novel aspects to key processes in the adaptation to P-i deficiency. We conclude that integrated measurement and interpretation of changes in protein and transcript abundance are mandatory for generating a complete inventory of the components that are critical in the response to environmental stimuli. Molecular & Cellular Proteomics 11: 10.1074/mcp.M112.020461, 1156-1166, 2012.