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Whole-Genome Resequencing of Spontaneous Oxidative Stress-Resistant Mutants Reveals an Antioxidant System of Bradyrhizobium japonicum Involved in Soybean Colonization

  • Plant Microbe Interactions
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Abstract

Soybean is the most inoculant-consuming crop in the world, carrying strains belonging to the extremely related species Bradyrhizobium japonicum and Bradyrhizobium diazoefficiens. Currently, it is well known that B. japonicum has higher efficiency of soybean colonization than B. diazoefficiens, but the molecular mechanism underlying this differential symbiotic performance remains unclear. In the present study, genome resequencing of four spontaneous oxidative stress–resistant mutants derived from the commercial strain B. japonicum E109 combined with molecular and physiological studies allowed identifying an antioxidant cluster (BjAC) containing a transcriptional regulator (glxA) that controls the expression of a catalase (catA) and a phosphohydrolase (yfbR) related to the hydrolysis of hydrogen peroxide and oxidized nucleotides, respectively. Integrated synteny and phylogenetic analyses supported the fact that BjAC emergence in the B. japonicum lineage occurred after its divergence from the B. diazoefficiens lineage. The transformation of the model bacterium B. diazoefficiens USDA110 with BjAC from E109 significantly increased its ability to colonize soybean roots, experimentally recapitulating the beneficial effects of the occurrence of BjAC in B. japonicum. In addition, the glxA mutation significantly increased the nodulation competitiveness and plant growth–promoting efficiency of E109. Finally, the potential applications of these types of non-genetically modified mutant microbes in soybean production worldwide are discussed.

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Acknowledgements

We thank Andrea Puebla and Pablo Vera (IABIMO) for their technical support in genomic sequencing.

Funding

This work was supported by Grants PICT-2017–0674 and FVT-39–2017, PICT-2018–02644 provided to Dr. Nicolas Ayub and by PE I115 and PE I116 (Biotechnology Program of INTA).

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Authors and Affiliations

  1. Instituto de Agrobiotecnología Y Biología Molecular (INTA-CONICET), Buenos Aires, Argentina

    Karen Liebrenz, Cristina Gómez, Silvina Brambilla, Romina Frare, Margarita Stritzler, Cecilia Pascuan, Gabriela Soto & Nicolás Ayub

  2. Instituto de Genética (IGEAF), INTA, De los Reseros S/N, Castelar C25(1712), Buenos Aires, Argentina

    Karen Liebrenz, Cristina Gómez, Silvina Brambilla, Romina Frare, Margarita Stritzler, Cecilia Pascuan, Gabriela Soto & Nicolás Ayub

  3. Instituto Tecnológico Chascomús (INTECH-CONICET), Buenos Aires, Argentina

    Vanina Maguire & Oscar Ruiz

  4. Estación Experimental Agropecuaria Marcos Juárez, INTA, Córdoba, Argentina

    Diego Soldini

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  1. Karen Liebrenz
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Contributions

All authors contributed to the study conception and design. Conceived and designed the experiments: K. L., G. S., and N. A. Performed the experiments: K. L., C. G., S. B., R. F., M. S., and V. M. Analyzed the data: O. R., D. S., C. P., G. S., and N. A.. Wrote the paper: N. A. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Nicolás Ayub.

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Liebrenz, K., Gómez, C., Brambilla, S. et al. Whole-Genome Resequencing of Spontaneous Oxidative Stress-Resistant Mutants Reveals an Antioxidant System of Bradyrhizobium japonicum Involved in Soybean Colonization. Microb Ecol 84, 1133–1140 (2022). https://doi.org/10.1007/s00248-021-01925-2

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