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The auxin-producing Bacillus thuringiensis RZ2MS9 promotes the growth and modifies the root architecture of tomato (Solanum lycopersicum cv. Micro-Tom)

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Abstract

Strains of Bacillus thuringiensis (Bt) are commonly commercialized as bioinoculants for insect pest control, but their benefits go beyond their insecticidal property: they can act as plant growth-promoters. Auxins play a major role in the plant growth promotion. However, the mechanism of auxin production by the Bacilli group, and more specifically by Bt strains, is unclear. In previous work, the plant growth-promoting rhizobacterium (PGPR) B. thuringiensis strain RZ2MS9 increased the corn roots. This drew our attention to the strain’s auxin production trait, earlier detected in vitro. Here, we demonstrate that in its genome, RZ2MS9 harbours the complete set of genes required in two pathways that are used for Indole acetic acid (IAA) production. We also detected that the strain produces almost five times more IAA during the stationary phase. The bacterial application increased the shoot dry weight of the Micro-Tom (MT) tomato by 24%. The application also modified MT root architecture, with an increase of 26% in the average lateral root length and inhibition of the axial root. At the cellular level, RZ2MS9-treated MT plants presented elongated root cortical cells with intensified mitotic activity. Altogether, these are the best characterized auxin-associated phenotypes. Besides that, no growth alteration was detected in the auxin-insensitive diageotropic (dgt) plants either with or without the RZ2MS9 inoculation. Our results suggest that auxins play an important role in the ability of B. thuringiensis RZ2MS9 to promote MT growth and provide a better understanding of the auxin production mechanism by a Bt strain.

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Fig. 1

adapted from Zhang et al. (2019). Arrows with solid lines indicate the enzymes which genes were detected in the B. thuringiensis RZ2MS9 genome. Arrows with dashed lines indicate the enzymes which genes were not detected in RZ2MS9 genome. ORD, oxidoreductase; IAOxD, indole-3-acetaldoxime dehydratase; TMO, tryptophan-2-monooxygenase; IAH, indole-3-acetamide hydrolase; AAT, aromatic amino transferase; IPDC, indole-3-pyruvate decarboxylase; ALDH, aldehyde dehydrogenase; TDC, tryptophan decarboxylase; MAO, monoamine oxidase

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All data generated or analysed during this study are included in this published article and its supplementary information files.

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Acknowledgements

We are grateful for the technical assistance provided by the Laboratory of Electron Microscopy “Elliot W. Kitajima”—ESALQ/USP.

Funding

This work was supported by grants from the “São Paulo Research Foundation” (FAPESP) (Proc. No. 2015/01188-9) and “National Council for Scientific and Technological Development” (CNPq) (Proc. No. 427669/2018-9). We thank CNPq for the fellowships to BDB, MND and ROH. We would like to thank FAPESP for the fellowship to EFF (Proc. No. 2017/11026-1). We also thank “Coordination for the Improvement of Higher Education Personnel” (CAPES) for the fellowship to JPRM and MLB.

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BDB and MCQ conceived the research plan. BDB performed the in-silico analysis for genome mining. BDB, ROH, FAP, MND carried out the experiments (in vitro and in vivo—greenhouse). JPRM analysed the anatomical changes in plant roots using microscopy. MLB and MLS performed the taxonomic analysis. BDB and MCQ wrote the manuscript with the support of EFF, JLA and MLB. All authors provided critical feedback and helped to shape the research, analysis and final manuscript.

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Correspondence to Maria Carolina Quecine.

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Communicated by Erko Stackebrandt.

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Batista, B.D., Dourado, M.N., Figueredo, E.F. et al. The auxin-producing Bacillus thuringiensis RZ2MS9 promotes the growth and modifies the root architecture of tomato (Solanum lycopersicum cv. Micro-Tom). Arch Microbiol 203, 3869–3882 (2021). https://doi.org/10.1007/s00203-021-02361-z

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  • DOI: https://doi.org/10.1007/s00203-021-02361-z

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