Skip to main page content
U.S. flag

An official website of the United States government

Dot gov

The .gov means it’s official.
Federal government websites often end in .gov or .mil. Before sharing sensitive information, make sure you’re on a federal government site.

Https

The site is secure.
The https:// ensures that you are connecting to the official website and that any information you provide is encrypted and transmitted securely.

Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
Review
. 2021 Apr;15(4):949-964.
doi: 10.1038/s41396-020-00835-4. Epub 2020 Nov 23.

Engineering rhizobacteria for sustainable agriculture

Timothy L Haskett  1 , Andrzej Tkacz  2 , Philip S Poole  2
Affiliations
Review

Engineering rhizobacteria for sustainable agriculture

Timothy L Haskett et al. ISME J. 2021 Apr.

Abstract

Exploitation of plant growth promoting (PGP) rhizobacteria (PGPR) as crop inoculants could propel sustainable intensification of agriculture to feed our rapidly growing population. However, field performance of PGPR is typically inconsistent due to suboptimal rhizosphere colonisation and persistence in foreign soils, promiscuous host-specificity, and in some cases, the existence of undesirable genetic regulation that has evolved to repress PGP traits. While the genetics underlying these problems remain largely unresolved, molecular mechanisms of PGP have been elucidated in rigorous detail. Engineering and subsequent transfer of PGP traits into selected efficacious rhizobacterial isolates or entire bacterial rhizosphere communities now offers a powerful strategy to generate improved PGPR that are tailored for agricultural use. Through harnessing of synthetic plant-to-bacteria signalling, attempts are currently underway to establish exclusive coupling of plant-bacteria interactions in the field, which will be crucial to optimise efficacy and establish biocontainment of engineered PGPR. This review explores the many ecological and biotechnical facets of this research.

PubMed Disclaimer

Conflict of interest statement

The authors declare that they have no conflict of interest.

Figures

Fig. 1
Fig. 1. Limitations of natural PGPR.
The benefits of PGPR in agriculture are restricted by three factors. a Inoculant bacteria may fail to colonise the rhizosphere of target crops to exert their beneficial effects due to competition with resilient resident microbes that may have become well-adapted to the soil conditions over years of evolutionary selection. Abiotic stresses may also impact negatively on persistence in the bulk-soil. b Although plants can exert some control over the structure of their rhizomicrobiome, there is no stringent host-specificity for bacterial colonisation of plant roots. Thus, inoculant PGPR may provide their beneficial services to non-target invasive species, creating competition for the target plant. c Some PGPR have evolved agriculturally undesirable modes of genetic regulation that repress expression and/or activity of PGP traits when conditions are not conducive for the bacteria (See Fig. 2 for additional information). Such regulation can assist the bacteria in conservation of energy and resources but renders the bacteria of little benefit to plants.
Fig. 2
Fig. 2. Examples of multi-layered NH3+-dependent repression of N-fixation.
NH3+-dependent negative feedback regulation of N-fixation is ubiquitous in diazotrophic bacteria and involves diverse multi-layered strategies that primarily target the “master regulator” of N-fixation NifA, which acts in association with the sigma factor σ54 to drive expression of a large suite of nitrogenase (nif) and accessory genes. For simplicity, σ54 is not shown here, and only the structural nitrogenase genes nifHDK are shown as induced by NifA. In all bacteria, the N-status of the cell is sensed via GlnD, which under low N-conditions, uridylylates one or more global N-regulatory PII protein(s) (GlnK, GlnB and GlnZ in the depicted systems) [14]. a In Klebsiella pneumoniae, uridylylated GlnK phosphorylates NtrB leading to subsequent phosphorylation of NtrC which in turn activates transcription of nifLA [141]. NifL is able to bind NifA and inhibit its activity, but is itself inactivated by binding to uridylylated GlnK under low NH3+ conditions. b In Azospirillum brasilense, nifA expression is constiutitve but the NifA protein requires binding to uridylylated GlnB for activation [142]. Nitrogenase activity is additionally regulated via the DraT-DraG system in this strain [142]. Under high NH3+ conditions, DraT binds to de-uridylylated GlnB and inactivates nitrogenase through ADP-ribosylation, whereas DraG binds to de-uridylylated GlnZ and is sequested to the membrane. Under low NH3+ conditions, nor DraT or DraG bind their cognate PII protein and DraG subsequently re-activates nitrogenase by reversal of ADP-ribosylation.
Fig. 3
Fig. 3. Rhizopine signalling to control PGPR.
a To enable signalling between plants and bacteria, a synthetic biosynthesis pathway has been engineered into barley and Medicago that facilitates production of the rhizopine scyllo-inosamine (SI) from myo-inositol [17]. b SI biosensor plasmids encoding the periplasmic rhizopine-binding protein MocB and rhizopine-dependent transcription factor MocR can be introduced into bacteria enabling genes placed downstream of the rhizopine-inducible promoter PmocB to be expressed under rhizopine control. c SI signalling circuitry can be used to establish plant host-specific expression of rhizobacterial PGP genes, effectively coupling interactions in the field and preventing growth promotion of non-target plants. SI signalling could also be used to enrich the rhizosphere for engineered bacteria that carry the catabolic moc gene which permits utilisation of SI as a sole carbon and nitrogen source [108, 115, 116]. Like most signalling circuitry, the functionality of SI signalling is not ubiquitous across bacterial taxa. By bringing biosynthesis of a secondary signalling molecule such as DAPG depicted here, under SI control, the SI signal could be relayed to diverse bacteria carrying a second cognate inducible or derepressible promoter system such as the DAPG-dependent system controlled by PhlF. SI signalling could also be integrated to control multi-layered biocontainment systems such as that described by Ronchel et al. [127] where the essential acdS gene and lacI repressor, targeted for the gef toxin, are each expressed in response to an external stimulus. Integration of this signal could restrict proliferation of engineered rhizobacteria to the rhizosphere.
See this image and copyright information in PMC

Similar articles

See all similar articles

Cited by

See all "Cited by" articles

References

    1. Hunter MC, Smith RG, Schipanski ME, Atwood LW, Mortensen DA. Agriculture in 2050: recalibrating targets for sustainable intensification. Bioscience. 2017;67:386–91. doi: 10.1093/biosci/bix010. - DOI
    1. Tilman D, Balzer C, Hill J, Befort BL. Global food demand and the sustainable intensification of agriculture. Proc Natl Acad Sci USA. 2011;108:20260. doi: 10.1073/pnas.1116437108. - DOI - PMC - PubMed
    1. Alexandratos N, Bruinsma J. World agriculture towards 2030/2050: the 2012 revision. ESA Working Papers 12-03. Rome: FAO; 2012.
    1. Cordell D, White S. Tracking phosphorus security: indicators of phosphorus vulnerability in the global food system. Food Secur. 2015;7:337–50. doi: 10.1007/s12571-015-0442-0. - DOI
    1. Santos MS, Nogueira MA, Hungria M. Microbial inoculants: reviewing the past, discussing the present and previewing an outstanding future for the use of beneficial bacteria in agriculture. AMB Express. 2019;9:205–205.. doi: 10.1186/s13568-019-0932-0. - DOI - PMC - PubMed

Publication types