Elicitor-induced plant immunity relies on amino acids accumulation to delay the onset of bacterial virulence

Abstract

Plant immunity relies on the perception of Microbe-Associate Molecular Patterns (MAMPs) from invading microbes to induce defense responses that suppress attempted infections. It has been proposed that MAMP-triggered immunity (MTI) suppresses bacterial infections by suppressing the onset of bacterial virulence. However, the mechanisms by which plants exert this action are poorly understood. Here, we showed that MAMP perception in Arabidopsis (Arabidopsis thaliana) induces the accumulation of free amino acids in a salicylic acid (SA)-dependent manner. When co-infiltrated with Glutamine and Serine, two of the MAMP-induced highly accumulating amino acids, Pseudomonas syringae pv. tomato DC3000 expressed low levels of virulence genes and failed to produce robust infections in otherwise susceptible plants. When applied exogenously, Glutamine and Serine directly suppressed bacterial virulence and growth, bypassing MAMP perception and SA-signaling. In addition, an increased level of endogenous Glutamine in the leaf apoplast of a gain-of-function mutant of Glutamine Dumper-1 rescued the partially compromised bacterial virulence- and growth-suppressing phenotype of the SA-induced deficient-2 (sid2) mutant. Our data suggest that MTI suppresses bacterial infections by delaying the onset of virulence with an excess of amino acids at the early stages of infection.

A computational model of Pseudomonas syringae metabolism unveils a role for branched-chain amino acids in Arabidopsis leaf colonization

“…Several amino acids and sugars produced significant growth over 60 hours of incubation ( Fig 1B ). Of special interest were plant metabolites previously shown to have an impact on Pst DC3000 infections [ 4 , 12 , 13 , 26 ]. GABA, a highly abundant amino acid in the LA of tomato plants, produced robust growth, as did L-glutamine, sucrose, and D-glucose ( Fig 1B ).…”

“…PRRs can be activated with purified synthetic MAMPs to elicit plant immunity prior to bacterial infection. Such activation of plant immunity elicits changes in the metabolite composition of the LA [ 12 ], which in turn, suppress the expression of Pst DC3000 T3SS and coronatine biosynthesis genes, thus compromising Pst DC3000 virulence and infectivity [ 12 – 14 ]. Altogether, these studies demonstrate that plant defense responses drive changes in the composition of LA metabolites that inhibit Pst DC3000 growth and prevent the onset of plant disease.…”

“…Nevertheless, amino acids and sugars present in the LA are emerging as important regulators of Pst DC3000 virulence within the LA. This seems especially true for Pst DC3000, as bacterial supplementation with glutamine, serine, or valine, decreased bacterial virulence and leaf colonization [ 12 ], while aspartate had the opposite effect [ 13 , 14 ]. Like aspartate and other organic acids, glucose was reported to have a positive impact in bacterial virulence gene expression and leaf colonization [ 14 ].…”

Transporter-mediated depletion of extracellular proline directly contributes to plant pattern-triggered immunity against a bacterial pathogen

“…Though, a caveat to this conclusion is that the single time point in our metabolomics analysis likely does not capture the full spectrum of PAMP-induced changes that occur. In this regard, a recent study reported that nine different amino acids significantly accumulated within the apoplast of Arabidopsis leaves 24 hours after flg22 treatment 53 . Because high concentrations of amino acids can repress T3SS genes in P. syringae , the authors concluded that increased amino acid levels within the apoplast contributes to flg22-induced T3SS repression and PTI 53 .…”

“…In this regard, a recent study reported that nine different amino acids significantly accumulated within the apoplast of Arabidopsis leaves 24 hours after flg22 treatment 53 . Because high concentrations of amino acids can repress T3SS genes in P. syringae , the authors concluded that increased amino acid levels within the apoplast contributes to flg22-induced T3SS repression and PTI 53 . However, these late-occurring changes are unlikely to be causal for T3SS repressive environment that is established within ten hours after PAMP perception ( Fig.…”