TABLE 2.
Genes and operons regulated by Rho in a conditional manner
| Type | Regulated locus | Species | Metabolic pathway | Inducer(s) | Inducer effect | Mechanism | Year |
|---|---|---|---|---|---|---|---|
| sRNA-dependent | chiPQ | Salmonella | Carbon utilization | sRNA ChiX | Termination | Inhibition of translation upon ChiX pairing to chiP leader unmasks intragenic terminator in chiP CDS (Bossi et al. 2012). | 2012 |
| galKM | E. coli | Galactose catabolism | sRNA Spot 42 (aka spf) | Termination | sRNA binding inhibits galK translation and activates RDTT; exact mechanism still unclear but likely involves translation uncoupling (Jeon et al. 2022). | 2015 | |
| oppABCDFZ | Vibrio cholerae | Oligopeptide uptake | sRNA OppZ | Termination | OppZ binding to the oppAB intergenic region inhibits oppB translation and unmasks an intragenic terminator in oppB (Hoyos et al. 2020). | 2020 | |
| rpoS | E. coli | General stress response | sRNAs DsrA, ArcZ, rprA | Antitermination | rpoS transcription is stimulated by sRNA binding to the rpoS leader (Sedlyarova et al. 2016; Nadiras et al. 2018b) at a site overlapping with a putative Rut site (Delaleau et al. 2022). | 2016 | |
| astE | E. coli | Arginine catabolism | sRNAs DsrA, ArcZ | Antitermination | Putative ArcZ and DsrA binding sites in astE leader (Sedlyarova et al. 2016); exact mechanism undetermined. | 2016 | |
| fadE | E. coli | Carbon source utilization | sRNAs DsrA, ArcZ | Antitermination | Putative ArcZ binding site in fadE leader (Sedlyarova et al. 2016); exact mechanism undetermined. | 2016 | |
| yqeC | E. coli | Unknown | sRNAs DsrA, ArcZ | Antitermination | Putative ArcZ and DsrA binding sites in yqeC leader (Sedlyarova et al. 2016); exact mechanism undetermined. | 2016 | |
| rho | Salmonella | RDTT regulation | sRNA SraL | Antitermination | SraL binding site overlaps with a putative Rut site suggesting a binding competition mechanism (Silva et al. 2019). | 2019 | |
| CRISP-2 | Pseudomonas aeruginosa | Adaptive immunity | sRNA PhrS | Antitermination | Exact mechanism undetermined (Lin et al. 2019) | 2019 | |
| trpE | E. coli | Tryptophan biosynthesis | sRNA RydC | Unknown | Predicted from H-SELEX screening, putative Rut site in trpE CDS (Delaleau et al. 2022); awaits experimental validation. | 2022 | |
| Riboswitch | ribB | E. coli | Riboflavin biosynthesis | FMN (flavin mononucleotide) | Termination | Restructuring of ribB leader by FMN likely unmasks Rut site otherwise sequestered in alternative structure (Hollands et al. 2012; Bastet et al. 2017). | 2012 |
| btuB | E. coli | Cobalamin (vitamin B12) transport | Adenosylcobalamin | Termination | Exact mechanism undetermined but RDTT requires upstream section of the btuB CDS (Nadiras et al. 2018a; Bastet et al. 2024); btuB is also regulated by sRNAs OmrA/B in a Rho-independent manner (Bastet et al. 2024). | 2024 | |
| lysC | E. coli | Lysine biosynthesis | Lysine | Termination | Restructuring of lysC leader by Lysine unmasks Rut site otherwise sequestered in alternative structure (Sedlyarova et al. 2016; Bastet et al. 2017; Ghosh et al. 2024). | 2017 | |
| thiBPQ | E. coli | Thiamine uptake | TPP (thiamin pyrophosphate) | Termination | Exact mechanism undetermined; putative Rut site in thiB leader (Bastet et al. 2017; Delaleau et al. 2022) | 2017 | |
| thiCEFSGH | E. coli | Vitamin B1 biosynthesis | TPP (thiamin pyrophosphate) | Termination | Restructuring of thiC leader by FMN likely unmasks Rut site otherwise sequestered in alternative structure (Bastet et al. 2017; Chauvier et al. 2017). | 2017 | |
| thiMD | E. coli | Vitamin B1 biosynthesis | TPP (thiamin pyrophosphate) | Termination | Restructuring of thiM leader by TPP inhibits translation and unmasks intragenic Rut site in thiM (Bastet et al. 2017; Delaleau et al. 2022). | 2017 | |
| ribM | Corynebacterium glutamicum | Riboflavin transport | FMN (flavin mononucleotide) | Termination | Exact mechanism undetermined but likely involves RDTT and mRNA decay (Takemoto et al. 2015). | 2015 | |
| mntP | E. coli | Manganese homeostasis | Mn2+ ion | Antitermination | Binding of Mn2+ to the riboswitch restores translation-transcription coupling and expression of the MntP efflux pump (Prakash et al. 2024). Evidence for Rut site in upstream part of mntP CDS (Delaleau et al. 2022). | 2024 | |
| Riboswitch-like | trpEDCFBA | Bacillus subtilis | Tryptophan biosynthesis | TRAP protein | Termination | TRAP binding to the trpE leader inhibits translation and unmasks intragenic terminator(s) (Yakhnin et al. 2001). | 2001 |
| pgaABCD | E. coli | Biofilm formation | CsrA protein | Termination | Restructuring of pgaA leader by CsrA unmasks Rut site otherwise sequestered in a RNA hairpin (Figueroa-Bossi et al. 2014). | 2014 | |
| tkt-gap-lpp0152-lpp0151 | Legionella pneumophila | Pyruvate metabolism | CsrA protein | Antitermination | CsrA binding to an AGGA motif in the gap CDS inhibits RDTT in vitro, presumably upon RNA restructuring (Sahr et al. 2017). This effect correlates with a lower amount of gap RNA in csrA− versus csrA+ strains, although Rho involvement in vivo was not tested formally (Sahr et al. 2017). | 2017 | |
| ABUW_1645, ABUW_1959, ABUW_2818 | Acinetobacter baumannii | Phase variation and virulence | CsrA protein | Antitermination | CsrA inhibits RDTT by binding to a GGA-rich region of the ABUW_1645 mRNA leader, which also contains a Rut site. The ATPase activity of Rho is inhibited in vitro by CsrA binding to ABUW_1645 mRNA leader (Singh et al. 2025). | 2025 | |
| cspA/B/G | E. coli (cspA/B/G) and Salmonella (CspA) | Cold stress response | Cold temperature | Antitermination | Restructuring of cspA/B/G leader at low temperature blocks access to Rut site; CspA binding to the mRNA leader unmasks the Rut site (Delaleau et al. 2024). | 2024 | |
| CspA protein | Termination | ||||||
| nsrR-rnr-yjfHI | E. coli | Cold stress response | Cold temperature | Antitermination | Restructuring of nsrR-rnr-yjfHI leader at low temperature blocks access to Rut site; CspA binding to the mRNA leader unmasks the Rut site (Delaleau et al. 2024). | 2024 | |
| CspA protein | Termination | ||||||
| cspI | E. coli | Cold stress response | Cold temperature | Antitermination | Exact mechanism undetermined; Putative Rut site upstream of promoter (Delaleau et al. 2024) | 2024 | |
| DeaD | E. coli | Cold stress response | Cold temperature | Antitermination | Exact mechanism undetermined (Delaleau et al. 2024); Rut site identified in 5′UTR (Ojha and Jain 2020) | 2024 | |
| uORF-mediated | tnaCAB | E. coli | Tryptophan catabolism | Tryptophan | Antitermination | Tryptophan binding to the ribosome prevents its release from the last codon of the tnaC uORF, thereby shielding an adjacent Rut site (van der Stel et al. 2021). | 1985 |
| mgtA | Salmonella | Magnesium homeostasis | Mg2+ ion | Termination | Magnesium stimulates translation of uORF mgtL, which promotes restructuring of the mgtA leader, unmasks the Rut site, and stimulates RNAP pausing (Hollands et al. 2012, 2014; Gall et al. 2016); may not be conserved in E. coli (Bastet et al. 2017). | 2012 | |
| corA | Salmonella and E. coli | Magnesium homeostasis | Mg2+ ion | Termination | Magnesium stimulates translation of corL uORF and restructuring of corA leader, which unmasks Rut site and stimulates RNAP pausing (Kriner and Groisman 2015; Kriner and Groisman 2017; Vezina Bedard et al. 2024); putative Rut site in the corA leader of E. coli (Delaleau et al. 2022; Vezina Bedard et al. 2024). | 2015 | |
| mgtCBR | Salmonella | Magnesium homeostasis | Mg2+ ion | Termination | Magnesium stimulates translation of uORF mgtM, which promotes restructuring of the mgtC leader and sequestering of the RARE antitermination sequence that otherwise inhibits the Rho-Rut complex (Sevostyanova and Groisman 2015). | 2015 | |
| speF | E. coli and Salmonella | Polyamine homeostasis | Ornithine | Antitermination | During translation of the uORF speFL, ornithine invades the ribosomal exit channel and stalls the ribosome on the termination codon, which masks a Rut site and allows expression of the ornithine decarboxylase SpeF (Ben-Zvi et al. 2019; Herrero Del Valle et al. 2020). | 2020 | |
| cruR-bfrG-bp2921 | Bordetella pertussis | Copper homeostasis | Copper | Termination | Copper binding to the CruR leader peptide triggers release of stalled ribosome otherwise shielding an intragenic Rut site in the uORF (Roy et al. 2022). | 2022 | |
| hisGDCBHAFI | E. coli and Salmonella | Histidine biosynthesis | Charged tRNAHis | Termination | Shortage of charged tRNAHis slows translation of His-rich hisL uORF, inducing an antitermination conformation of the mRNA leader. Attenuation may combine intrinsic termination (Frunzio et al. 1981) and RDTT (Lawther and Hatfield 1978). Intragenic RDTT sites have been identified in the hisGDC cistrons of Salmonella (Ciampi and Roth 1988; Alifano et al. 1991). | 1978 | |
| uORF-like | tufB | Salmonella | Translation regulation | Tu protein | Termination | Tu promotes rapid displacement of the elongating ribosome and folding of the tufB leader that unmasks a Rut site. Ribosome traffic jam in absence of Tu favors formation of the antitermination conformation (Brandis et al. 2016). | 2016 |
| mdtJI | E. coli | Polyamine homeostasis | Spermidine | Antitermination | Expression of mdtjI is regulated by Rho, the translation of an uORF, and spermidine. but the exact mechanism is undetermined (Adams et al. 2021). | 2021 | |
| topAI (yjhX) | E. coli | Type II toxin–antitoxin system | Antibiotics | Termination | Antibiotic-induced ribosome stalling unmasks intragenic terminator within topAI. Regulation also depends on upstream uORF toiL (Baniulyte and Wade 2025). Putative Rut sites in both topAI and toiL (Delaleau et al. 2022). Exact mechanism remains to be determined. | 2024 | |
| iRAP | nadD | E. coli | NAD+/NADP+ biosynthesis | Unknown, related to growth phase or oxidative stress | Termination | iRAP sequence in CDS promotes ribosome stalling and unmasking of intragenic terminator (Sedlyarova et al. 2017); mechanism of conditional Rho activation not determined. | 2017 |
| Invertible DNA | fimAICDFGH operon | E. coli | Phase variation and virulence | DNA inversion by FimB and FimE recombinases (expression is growth- and condition-dependent) | Termination | The DNA switch in the OFF orientation enables RDTT (Hinde et al. 2005). | 2002 |
| flgB operon | Clostridioides difficile | Phase variation and virulence | DNA inversion mediated by random activation of recombination? | Termination | The DNA switch in the OFF orientation enables RDTT; exact mechanism undetermined (Warren Norris et al. 2024). | 2020 |
