Abstract
Plants have to coordinate eukaryotic ribosomes (cytoribosomes) and prokaryotic ribosomes (plastoribosomes and mitoribosomes) production to balance cellular protein synthesis in response to environmental variations. We identified 429 genes encoding potential ribosomal proteins (RP) in Arabidopsis thaliana. Because cytoribosome proteins are encoded by small nuclear gene families, plastid RP by nuclear and plastid genes and mitochondrial RP by nuclear and mitochondrial genes, several transcriptional pathways were attempted to control ribosome amounts. Examining two independent genomic expression datasets, we found two groups of RP genes showing very different and specific expression patterns in response to environmental stress. The first group represents the nuclear genes coding for plastid RP whereas the second group is composed of a subset of cytoribosome genes coding for RP isoforms. By contrast, the other cytoribosome genes and mitochondrial RP genes show less constraint in their response to stress conditions. The two subsets of cytoribosome genes code for different RP isoforms. During stress, the response of the intensively regulated subset leads to dramatic variation in ribosome diversity. Most of RP genes have same promoter structure with two motifs at conserved positions. The stress-response of the nuclear genes coding plastid RP is related with the absence of an interstitial telomere motif known as telo box in their promoters. We proposed a model for the “ribosome code” that influences the ribosome biogenesis by three main transcriptional pathways. The first pathway controls the basal program of cytoribosome and mitoribosome biogenesis. The second pathway involves a subset of cytoRP genes that are co-regulated under stress condition. The third independent pathway is devoted to the control of plastoribosome biosynthesis by regulating both nuclear and plastid genes.
Highlights
For their survival, cells need to safeguard energy and to adapt their growth and differentiation to the local environmental fluctuations
Among these ribosomal proteins (RP) genes, 48% are implicated in cytoplasmic RP (cytoRP) synthesis
Some new AGI have been identified for cytoRP predicted previously by Barakat et al [3] and additional new cytoRP genes have been found (Table 1)
Summary
Cells need to safeguard energy and to adapt their growth and differentiation to the local environmental fluctuations. Ribosomes are integral to the translation of mRNA into proteins and, as such, are considered as housekeeping components of the cells. Ribosomal biogenesis, as all protein synthesis, is energy-consuming. It has been reported that at least 75% of the transcriptional activity is dedicated to ribosome biogenesis [1]. In response to stress such as nutritional limitation, repression of ribosomal protein synthesis has been observed in all kingdoms: bacteria, yeast, animal and plants [2]. Ribosome proteins are among the most highly conserved proteins across evolution in all kingdoms, the regulatory pathways controlling the genes encoding these proteins remain unclear
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