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Alterations of Primary Metabolites in Root Exudates of Intercropped Cajanus cajan–Zea mays Modulate the Adaptation and Proteome of Ensifer (Sinorhizobium) fredii NGR234

Abstract

Legume-cereal intercropping systems, in the context of diversity, ecological function, and better yield have been widely studied. Such systems enhance nutrient phytoavailability by balancing root-rhizosphere interactions. Root exudates (RE) play an important role in the rhizospheric interactions of plant-plant and/or plant-microbiome interaction. However, the influence of the primary metabolites of RE on plant-rhizobia interactions in a legume-cereal intercrop system is not known. To understand the plant communication with rhizobia, Cajanus cajan-Zea mays intercropped plants and the broad host range legume nodulating Ensifer fredii NGR234 as the model plants and rhizobium used respectively. A metabolomics-based approach revealed a clear separation between intercropped and monocropped RE of the two plants. Intercropped C. cajan showed an increase in the myo-inositol, and proline, while intercropped Z. mays showed enhanced galactose, D-glucopyranoside, and arginine in the RE. Physiological assays of NGR234 with the RE of intercropped C. cajan exhibited a significant enhancement in biofilm formation, while intercropped Z. mays RE accelerated the bacterial growth in the late log phase. Further, using label-free proteomics, we identified a total of 2570 proteins of NGR234 covering 50% annotated protein sequences upon exposure to Z. mays RE. Furthermore, intercropped Z. mays RE upregulated bacterioferritin comigratory protein (BCP), putative nitroreductase, IlvD, LeuC, D (branched-chain amino acid proteins), and chaperonin proteins GroEL2. Identification offered new insights into the metabolome of the legume-cereal intercrop and proteome of NGR234-Z. mays interactions that underline the new molecular candidates likely to be involved in the fitness of rhizobium in the intercropping system.

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Data availability

The raw files for proteomics are available on Massive reference- MassIVE MSV000086912.

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Acknowledgements

The authors are grateful to Pulse Research Station (Vadodara) and Dr. S. K. Singh from Main Maize Research Station (Godhra) of Anand Agricultural University, India for providing C. cajan and Z. mays seeds. We acknowledge Dr. Murali Sharaff, PDPIAS, CHARUSAT, Changa for providing needful suggestions to the manuscript. We gratefully acknowledge the Metabolomics facility, the School of Life Sciences, the University of Hyderabad for GC-MS/MS analysis, and the Centre for Cellular and Molecular Platforms (C-CAMP), Bangalore for LC-MS/MS facility.

Funding

SMV is grateful to the University Grant Commission, New Delhi, India for the UGC-BSR fellowship. ARP thanks the Science and Engineering Research Board, Department of Science and Technology, Govt. of India for the JC Bose Fellowship (Grant No. JCB/2017/000053). The infrastructure support to the Department of Microbiology and Biotechnology Centre at The M.S. University of Baroda, Vadodara under the DST-FIST program of Govt. of India is acknowledged.

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SMV performed the research and interpreted the data; GA and SMV designed the experiments, analyzed the data, and wrote the manuscript. SA and ARP standardized the method and analyzed metabolomics (GC–MS/MS) data. SA and ARP also provided critical comments on the write-up of the manuscript. CP performed label-free quantitative proteomics (LC/MS/MS) and also carried out data analysis. All authors gave final approval of the version to be submitted and any revised version.

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Correspondence to G. Archana.

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Vora, S.M., Ankati, S., Patole, C. et al. Alterations of Primary Metabolites in Root Exudates of Intercropped Cajanus cajan–Zea mays Modulate the Adaptation and Proteome of Ensifer (Sinorhizobium) fredii NGR234. Microb Ecol 83, 1008–1025 (2022). https://doi.org/10.1007/s00248-021-01818-4

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  • DOI: https://doi.org/10.1007/s00248-021-01818-4

Keywords

  • Ensifer fredii NGR234
  • Root exudates (RE)
  • Cajanus cajan
  • Zea mays
  • Metabolomics
  • Proteomics