Abstract
Mechanisms adjusting replication initiation and cell cycle progression in response to environmental conditions are crucial for microbial survival. Functional characterization of the trans-encoded small non-coding RNA (trans-sRNA) EcpR1 in the plant-symbiotic alpha-proteobacterium Sinorhizobium meliloti revealed a role of this class of riboregulators in modulation of cell cycle regulation. EcpR1 is broadly conserved in at least five families of the Rhizobiales and is predicted to form a stable structure with two defined stem-loop domains. In S. meliloti, this trans-sRNA is encoded downstream of the divK-pleD operon. ecpR1 belongs to the stringent response regulon, and its expression was induced by various stress factors and in stationary phase. Induced EcpR1 overproduction led to cell elongation and increased DNA content, while deletion of ecpR1 resulted in reduced competitiveness. Computationally predicted EcpR1 targets were enriched with cell cycle-related mRNAs. Post-transcriptional repression of the cell cycle key regulatory genes gcrA and dnaA mediated by mRNA base-pairing with the strongly conserved loop 1 of EcpR1 was experimentally confirmed by two-plasmid differential gene expression assays and compensatory changes in sRNA and mRNA. Evidence is presented for EcpR1 promoting RNase E-dependent degradation of the dnaA mRNA. We propose that EcpR1 contributes to modulation of cell cycle regulation under detrimental conditions.
Highlights
Non-coding RNAs have shot to prominence as significant and ubiquitous regulators that are involved in the control of various cellular processes in most eukaryotic and prokaryotic organisms
We report the first example of a trans-sRNA (EcpR1) with two experimentally confirmed targets in the core of cell cycle regulation and demonstrate that in the plant-symbiotic alpha-proteobacterium Sinorhizobium meliloti
Targets predicted for the sRNA family established by the S. meliloti trans-sRNA SmelC291 show a significant enrichment (P-value = 2.5Ã10-5) of cell cycle-related mRNAs (n = 7) among the top-ranked candidates (P 0.01, n = 89; S1 Table) [27]
Summary
Non-coding RNAs (ncRNAs) have shot to prominence as significant and ubiquitous regulators that are involved in the control of various cellular processes in most eukaryotic and prokaryotic organisms. The development of deep-sequencing technologies has allowed for the identification of an ever-growing number of ncRNAs the biological functions and regulatory mechanisms of the vast majority remain veiled. Short-interfering RNAs (siRNA) and microRNAs (miRNAs) have emerged as a priority research area in biomedicine [1] since they control crucial cellular processes, such as cell development, differentiation and oncogenic transformation [2]. The miR-34 family mimics p53 activity, inducing cell-cycle arrest and apoptosis [3]. Plant ncRNAs have been reported to regulate stress adaptation and defence responses, and cell differentiation, such as miR169 that was associated with nodule development in legumes [4,5]. In the fission yeast Schizosaccharomyces pombe, meiRNA plays a role in recognition of homologous chromosomes for pairing and is essential for progression of meiosis [6,7]
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