Complementary proteome and transcriptome profiling in phosphate-deficient Arabidopsis roots reveals multiple levels of gene regulation.

Phosphate (Pi) deficiency impairs plant growth and productivity in many agricultural ecosystems, causing severe reductions in crop yield. To uncover novel aspects in acclimation to Pi starvation, we investigated the correlation between Pi 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 Pi deficiency. Most dramatic changes were noticed for genes involved in Pi acquisition and in processes that either liberate Pi or bypass Pi/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 Pi 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 Pi 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.