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Amino acid availability determines plant immune homeostasis in the rhizosphere microbiome

View ORCID ProfileYang Liu, Jiatong Han, Andrew J. Wilson, Lucy O’Sullivan, View ORCID ProfileCara H. Haney
doi: https://doi.org/10.1101/2021.12.20.473424
Yang Liu
1Department of Microbiology and Immunology, The University of British Columbia, Vancouver, Canada V6T 1Z3
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Jiatong Han
1Department of Microbiology and Immunology, The University of British Columbia, Vancouver, Canada V6T 1Z3
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Andrew J. Wilson
1Department of Microbiology and Immunology, The University of British Columbia, Vancouver, Canada V6T 1Z3
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Lucy O’Sullivan
2Department of Molecular Biology, Massachusetts General Hospital, Boston, MA 02114
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Cara H. Haney
1Department of Microbiology and Immunology, The University of British Columbia, Vancouver, Canada V6T 1Z3
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  • ORCID record for Cara H. Haney
  • For correspondence: cara.haney@ubc.ca
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Abstract

Microbes possess conserved microbe-associated molecular patterns (MAMPs) such as flagellin that are recognized by plant receptors to induce immunity. Despite containing the same MAMPs as pathogens, commensals thrive in the plant rhizosphere microbiome indicating they must suppress or evade host immunity. The beneficial bacteria Pseudomonas capeferrum WCS358 can suppress Arabidopsis root immunity via acidification by secreting gluconic acid. While gluconic acid is sufficient to suppress immunity, we found that it is not necessary in a second beneficial strain Pseudomonas simiae WCS417, which produces more gluconic acid than WCS358. To uncover mechanisms that contribute to the suppression of Arabidopsis immunity, we performed a forward genetic screen in EMS-mutagenized P. simiae WCS417 using a flagellin-inducible CYP71A12pro:GUS reporter as an Arabidopsis immune readout. We identified a mutant that cannot suppress flagellin-elicited CYP71A12pro:GUS expression or acidify the rhizosphere. Next generation sequencing revealed a mutation in the catabolic site of an ornithine carbamoyltransferase argF, which is required for arginine biosynthesis. The mutant could be complemented by expression of argF from a plasmid, and a ΔargF mutant could not suppress immunity. Fungal pathogens can use alkalization through production of ammonia and glutamate, the arginine biosynthetic precursors, to promote their own growth and virulence. Therefore, we hypothesized that the biosynthesis of specific amino acids may be necessary to reduce levels of ammonia and glutamate to prevent rhizosphere alkalization and bacterial overgrowth. Genetically blocking arginine, glutamine, or proline biosynthesis, or by adding corresponding exogenous amino acids, resulted in rhizosphere alkalization. Interestingly, exogenous amino acids caused bacterial overgrowth in a gluconic acid-deficient mutants. Our findings show that bacterial amino acid biosynthesis contributes to acidification by preventing accumulation of glutamate precursors and the resulting alkalization. Collectively this work shows that by regulating nutrient availability, plants have the potential to regulate their immune homeostasis in the rhizosphere microbiome.

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY 4.0 International license.
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Posted December 21, 2021.
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Amino acid availability determines plant immune homeostasis in the rhizosphere microbiome
Yang Liu, Jiatong Han, Andrew J. Wilson, Lucy O’Sullivan, Cara H. Haney
bioRxiv 2021.12.20.473424; doi: https://doi.org/10.1101/2021.12.20.473424
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Amino acid availability determines plant immune homeostasis in the rhizosphere microbiome
Yang Liu, Jiatong Han, Andrew J. Wilson, Lucy O’Sullivan, Cara H. Haney
bioRxiv 2021.12.20.473424; doi: https://doi.org/10.1101/2021.12.20.473424

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