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Stenotrophomonas sp. SRS1 promotes growth of Arabidopsis and tomato plants under salt stress conditions

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Abstract

Aims

Plant Growth-Promoting Rhizobacteria (PGPR) support plant growth by alleviating plant stresses, among which those triggered by saline soils. We isolated Stenotrophomonas sp. SRS1 from salt-resistant Carex distans (distant sedge) roots to understand how this growth promotion was enabled and whether an active contribution of the bacteria and/or plant was required.

Methods

Various growth assays were used to analyze the effect of bacterial inoculation on Arabidopsis thaliana and Solanum lycopersicum (cherry tomato MicroTom) growth. Furthermore, droplet microfluidics, bacterial genome mining, and bacterial and plant gene expression analysis combined with plant mutant analysis were used for in-depth analysis.

Results

SRS1 application enhanced plant growth in both saline and nonsaline environments. The fresh weight of SRS1-inoculated plants was higher than that of noninoculated plants, whereas the fresh weight ratio between SRS1-inoculated and noninoculated plants differed whether the plants were grown on agar plates, white sand or in soil. We demonstrated that the strain grew well in high salt-containing media and that, besides plant-growth-promotion-related genes, the bacterium contained various active stress genes. Interestingly, inoculation with the strain increased the induction of plant genes related to abscisic acid and auxin signaling pathways under saline conditions.

Conclusions

SRS1 inoculation promoted the growth of Arabidopsis and MicroTom tomato under saline and nonsaline conditions, also when the plants were grown in white sand and potting soil. Overall, genetic traits related to stress alleviation, derived from both the bacteria and the plants, play a crucial role in the impact of this novel PGPR strain on plant performance.

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Data availability

The raw sequence data, assembly, and annotation of SRS1 will be deposited to the National Center for Biotechnology Information database.

Abbreviations

½MS:

half-strength Murashige and Skoog

ABA:

abscisic acid

ACC:

1-aminocyclopropane-1-carboxylate

ANOVA:

analysis of variance

AUX1 :

auxin transporter protein 1 gene

CFU:

colony-forming units

Col-0:

Columbia-0 accession

DAT:

days after treatment

DMRT:

Duncan Multiple Range Test

EPS:

exopolysaccharides

ggpS :

glucosylglycerol-phosphate synthase gene

IAA:

indole-3-acetic acid

IAA12 :

auxin-responsive protein 12 gene

IAR4 :

IAA-alanine resistant 4 gene

katG :

catalase peroxidase gene

mdoB :

phosphoglycerol transferase I gene

MES:

2-morpholinoethanesulfonic acid

ompA :

outer membrane protein A gene

PBS:

phosphate-buffered saline

Pga :

polysaccharide adhesin required for biofilm formation

PGPR:

plant growth-promoting rhizobacteria

R2A:

Reasoner’s 2A

ROS:

reactive oxygen species

SOD:

superoxide dismutase gene

ycaD :

glucosylglycerol transporter gene

References

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Acknowledgments

The authors thank Leo Declercq of the nature reserve “Het Zwin” for the collection of plants, Silvie Van den Hoecke (Tech Watch Innovation, VIB) and Jean-Baptiste Abbe (MilliDrop) for the set-up and processing of the MilliDrop system, Annick De Keyser for technical support, and Martine De Cock for help preparing the manuscript.

Funding

This work was supported by the Research Foundation-Flanders (grant G.0151.18 N to A.W. and S.G.). H.M.T. is indebted to the Vietnam International Education Development (VIED), Ministry of Education, Vietnam for a PhD scholarship.

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Authors and Affiliations

Authors

Contributions

H.M.T., M.V. and S.G. designed all the experiments. H.M.T. performed all the experiments and analyzed the data statistically. S.G.M. and A.W. analyzed the whole-genome data. H.M.T. wrote the first draft of the manuscript. S.G.M., D.L., S.B., M.V. and S.G. revised it. All authors gave final approval for publication.

Corresponding author

Correspondence to Sofie Goormachtig.

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Declaration of competing interest

The authors declare no conflict of interest.

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Responsible Editor: Hans Lambers.

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Manh Tuong, H., Garcia Mendez, S., Vandecasteele, M. et al. Stenotrophomonas sp. SRS1 promotes growth of Arabidopsis and tomato plants under salt stress conditions. Plant Soil 473, 547–571 (2022). https://doi.org/10.1007/s11104-022-05304-9

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  • DOI: https://doi.org/10.1007/s11104-022-05304-9

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