Expression changes of ribosomal proteins in phosphate- and iron-deficient Arabidopsis roots predict stress-specific alterations in ribosome composition

BACKGROUND: Ribosomes are essential ribonucleoprotein complexes that are engaged in translation and thus indispensable for growth. Arabidopsis thaliana ribosomes are composed of 80 distinct ribosomal proteins (RPs), each of which is encoded by two to seven highly similar paralogous genes. Little information is available on how RP genes respond to a shortage of essential mineral nutrients such as phosphate (Pi) or iron (Fe). In the present study, the expression of RP genes and the differential accumulation of RPs upon Pi or Fe deficiency in Arabidopsis roots were comprehensively analyzed. RESULTS: Comparison of 3,106 Pi-responsive genes with 3,296 Fe-responsive genes revealed an overlap of 579 genes that were differentially expressed under both conditions in Arabidopsis roots. Gene ontology (GO) analysis revealed that these 579 genes were mainly associated with abiotic stress responses. Among the 247 RP genes retrieved from the TAIR10 release of the Arabidopsis genome (98 small subunit RP genes, 143 large subunit RP genes and six ribosome-related genes), seven RP genes were not detected in Arabidopsis roots by RNA sequencing under control conditions. Transcripts from 20 and 100 RP genes showed low and medium abundance, respectively; 120 RP genes were highly expressed in Arabidopsis roots. As anticipated, gene ontology (GO) analysis indicated that most RP genes were related to translation and ribosome assembly, but some of the highly expressed RP genes were also involved in the responses to cold, UV-B, and salt stress. Only three RP genes derived from three ‘sets’ of paralogous genes were differentially expressed between Pi-sufficient and Pi-deficient roots, all of which were induced by Pi starvation. In Fe-deficient plants, 81 RP genes from 51 ’sets’ of paralagous RP genes were significantly down-regulated in response to Fe deficiency. The biological processes ’translation’ (GO: 0006412), ’ribosome biogenesis (GO: 0042254), and ’response to salt (GO: 0009651), cold (GO: 0009409), and UV-B stresses (GO: 0071493)’ were enriched in this subset of RP genes. At the protein level, 21 and two RPs accumulated differentially under Pi- and Fe-deficient conditions, respectively. Neither the differentially expressed RP genes nor the differentially expressed RPs showed any overlap between the two growth types. CONCLUSIONS: In the present study three and 81 differentially expressed RP genes were identified under Pi and Fe deficiency, respectively. At protein level, 21 and two RP proteins were differentially accumulated under Pi- and Fe-deficient conditions. Our study shows that the expression of paralogous genes encoding RPs was regulated in a stress-specific manner in Arabidopsis roots, presumably resulting in an altered composition of ribosomes and biased translation. These findings may aid in uncovering an unexplored mechanism by which plants adapt to changing environmental conditions.