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Expression of pathways for dissimilation of toxic aromatic compounds such as (methyl)phenols interfaces both stress-response and carbon catabolite repression control cascades. InPseudomonas putida, carbon catabolite repression is mediated by the protein Crc – a translational repressor that counteracts utilization of less-preferred carbon sources as growth substrates until they are needed. In this work we dissect the regulatory role of the 5′-leader region (5′-LR) of thedmpRgene that encodes the master regulator of (methyl)phenol catabolism. Using deletion and substitution mutants combined with artificial manipulations of Crc availability inP. putida, we present evidence that a DNA motif within the 5′-leader region is critical for inhibition of the output from the Pr promoter that drives transcription ofdmpR, while the RNA chaperone Hfq facilitates Crc-mediated translation repression through the 5′-leader region of thedmpRmRNA. The results are discussed in the light of a model in which Hfq assists Crc to target a sequence within a loop formed by secondary structure of the 5′-LR mRNA. Our results support the idea that Crc functions as a global translational inhibitor to co-ordinate hierarchical carbon utilization in Pseudomonads.