Abstract
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.
Highlights
From the ‡Institute of Plant and Microbial Biology, Academia Sinica, Taipei, Taiwan; §Graduate Institute of Biotechnology, National Chung Hsing University, Taichung, Taiwan; ¶Genome and Systems Biology Degree Program, College of Life Science, National Taiwan University, Taipei, Taiwan
We argue that this “molecular compendium” of gene and protein expression data provides an informative readout about the physiological state of Pi-deficient roots, uncovering several novel aspects in the metabolism of Pi-deficient plants and provides a comprehensive reference map of gene activity in Arabidopsis roots
Proteins were extracted, digested in solution, and iTRAQ-labeled peptides were analyzed by liquid chromatography combined with tandem mass spectroscopy on an LTQ Orbitrap with higher-energy collisional dissociation (HCD) and collision-induced dissociation capabilities
Summary
In an attempt to identify nodes that are important for the function of roots under conditions of Pi starvation, we cataloged differences in the abundance of mRNAs and proteins by integrated profiling of gene activity using RNA-seq and highresolution quantitative iTRAQ proteomics. Transcriptomic and proteomic expression profiles were remarkably well correlated, but our analysis revealed several exceptions indicative of different control mechanisms that dictate gene activity. We argue that this “molecular compendium” of gene and protein expression data provides an informative readout about the physiological state of Pi-deficient roots, uncovering several novel aspects in the metabolism of Pi-deficient plants and provides a comprehensive reference map of gene activity in Arabidopsis roots
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