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Other examples of efflux pumps involved in bacteria/plant interactions are highlighted below. In A. tumefaciens, the IfeAB efflux pump is involved in the competitive colonization of alfalfa roots and can confer measurable ecological benefits to these bacteria in an environment where flavonoids are present [114]. The EmrAB efflux system in S. meliloti is induced by flavonoids and bacterial symbiosis with Medicago sativa is impaired when emrR, the gene encoding the TetR repressor of this efflux pump, is deleted [115,119]. Another multidrug efflux system of S. meliloti that plays an important role in nodulation competitiveness by mediating resistance toward antimicrobial compounds produced by the host plant is SmeAB [120]. The BjG30 efflux pump from B. japonicum may play a role in the early stage of symbiosis of this microorganism with soybean by balancing the dual functions of genistein as both a nod gene inducer and as a toxic compound [112]. Notably, B. japonicum presents another efflux pump, BdeAB, which seems to be involved in the symbiotic nitrogen-fixation activity of this microorganism in soybean; mutants deficient in this efflux pump, in addition of presenting symbiotic defects, are more susceptible to aminoglycosides [121], showing that antibiotic resistance is interlinked with other relevant functions of efflux pumps. Erwinia chrysanthemi is another example of the need of efflux pumps to colonize plant tissues. The infection by E. chrysanthemi causes salicylic acid accumulation in the host, leading to an amplification of the plant defence response and the production of pathogenesis-related proteins and toxic antimicrobial compounds. The combination of salicylic acid and its precursors activates the expression of multidrug efflux pump-encoding genes and enhances the survival of the bacterium [122].
It is important to highlight that efflux pumps may play a double functional role by modulating bacteria/plant and intermicrobial interactions. Indeed, a tolC mutant of E. chrysanthemi is defective in the efflux of berberine, an antimicrobial plant compound, and it is unable to cause plant tissue maceration in planta. In addition, this mutant is impaired for competing with the microbial community present in the same ecosystems, indicating that these efflux pumps have a role in microbial interspecific competition [123]. In line with the potential role of efflux pumps on bacterial competition, it has been shown that an E. chrysanthemi mutant defective in the ABC transporter YbiT conserves virulence in potato tubers but is less infectious than the wild type strain when growing together with saprophytic bacteria such as P. fluorescens or P. putida, possibly because this efflux pump can extrude toxic compounds produced by these bacteria [124].
Another important gut pathogen is Campylobacter jejuni. Among the known antibiotic resistance mechanisms of this microorganism, the CmeABC efflux pump is a relevant player and confers resistance to structurally-diverse antibiotics and toxic compounds [138], including those naturally present in its animal host, as bile salts [130]. CmeABC belongs to the RND family of efflux transporters and its expression is regulated by the transcriptional repressor CmeR, which binds to a specifi