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1.
Plant Physiol ; 192(1): 601-615, 2023 05 02.
Artigo em Inglês | MEDLINE | ID: mdl-36715647

RESUMO

Plant immunity relies on the perception of microbe-associated 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.


Assuntos
Proteínas de Arabidopsis , Arabidopsis , Aminoácidos/metabolismo , Virulência/genética , Glutamina/metabolismo , Arabidopsis/metabolismo , Proteínas de Arabidopsis/genética , Proteínas de Arabidopsis/metabolismo , Imunidade Vegetal , Serina/metabolismo , Pseudomonas syringae , Doenças das Plantas/microbiologia , Ácido Salicílico/metabolismo , Regulação da Expressão Gênica de Plantas
2.
PLoS Comput Biol ; 19(12): e1011651, 2023 Dec.
Artigo em Inglês | MEDLINE | ID: mdl-38150474

RESUMO

Bacterial pathogens adapt their metabolism to the plant environment to successfully colonize their hosts. In our efforts to uncover the metabolic pathways that contribute to the colonization of Arabidopsis thaliana leaves by Pseudomonas syringae pv tomato DC3000 (Pst DC3000), we created iPst19, an ensemble of 100 genome-scale network reconstructions of Pst DC3000 metabolism. We developed a novel approach for gene essentiality screens, leveraging the predictive power of iPst19 to identify core and ancillary condition-specific essential genes. Constraining the metabolic flux of iPst19 with Pst DC3000 gene expression data obtained from naïve-infected or pre-immunized-infected plants, revealed changes in bacterial metabolism imposed by plant immunity. Machine learning analysis revealed that among other amino acids, branched-chain amino acids (BCAAs) metabolism significantly contributed to the overall metabolic status of each gene-expression-contextualized iPst19 simulation. These predictions were tested and confirmed experimentally. Pst DC3000 growth and gene expression analysis showed that BCAAs suppress virulence gene expression in vitro without affecting bacterial growth. In planta, however, an excess of BCAAs suppress the expression of virulence genes at the early stages of infection and significantly impair the colonization of Arabidopsis leaves. Our findings suggesting that BCAAs catabolism is necessary to express virulence and colonize the host. Overall, this study provides valuable insights into how plant immunity impacts Pst DC3000 metabolism, and how bacterial metabolism impacts the expression of virulence.


Assuntos
Arabidopsis , Arabidopsis/genética , Arabidopsis/metabolismo , Pseudomonas syringae/genética , Aminoácidos de Cadeia Ramificada/metabolismo , Folhas de Planta/genética , Virulência/genética , Doenças das Plantas/genética , Doenças das Plantas/microbiologia
3.
Plant Physiol ; 189(4): 2315-2331, 2022 08 01.
Artigo em Inglês | MEDLINE | ID: mdl-35579373

RESUMO

Plants live under the constant challenge of microbes that probe the environment in search of potential hosts. Plant cells perceive microbe-associated molecular patterns (MAMPs) from incoming microbes and activate defense responses that suppress attempted infections. Despite the substantial progress made in understanding MAMP-triggered signaling pathways, the downstream mechanisms that suppress bacterial growth and disease remain poorly understood. Here, we uncover how MAMP perception in Arabidopsis (Arabidopsis thaliana) elicits dynamic changes in extracellular concentrations of free L-amino acids (AA). Within the first 3 h of MAMP perception, a fast and transient inhibition of AA uptake produces a transient increase in extracellular AA concentrations. Within 4 and 12 h of MAMP perception, a sustained enhanced uptake activity decreases the extracellular concentrations of AA. Gene expression analysis showed that salicylic acid-mediated signaling contributes to inducing the expression of AA/H+ symporters responsible for the MAMP-induced enhanced uptake. A screening of loss-of-function mutants identified the AA/H+ symporter lysin/histidine transporter-1 as an important contributor to MAMP-induced enhanced uptake of AA. Infection assays in lht1-1 seedlings revealed that high concentrations of extracellular AA promote bacterial growth in the absence of induced defense elicitation but contribute to suppressing bacterial growth upon MAMP perception. Overall, the data presented in this study reveal a mechanistic connection between MAMP-induced plant defense and suppression of bacterial growth through the modulation of AA transport activity.


Assuntos
Proteínas de Arabidopsis , Arabidopsis , Aminoácidos/metabolismo , Arabidopsis/metabolismo , Proteínas de Arabidopsis/genética , Proteínas de Arabidopsis/metabolismo , Regulação da Expressão Gênica de Plantas , Doenças das Plantas/microbiologia , Ácido Salicílico/metabolismo , Plântula/genética , Plântula/metabolismo
4.
J Immunol ; 202(12): 3370-3380, 2019 06 15.
Artigo em Inglês | MEDLINE | ID: mdl-31092636

RESUMO

The importance of antiviral CD8+ T cell recognition of alternative reading frame (ARF)-derived peptides is uncertain. In this study, we describe an epitope (NS1-ARF21-8) present in a predicted 14-residue peptide encoded by the +1 register of NS1 mRNA in the influenza A virus (IAV). NS1-ARF21-8 elicits a robust, highly functional CD8+ T cell response in IAV-infected BALB/c mice. NS1-ARF21-8 is presented from unspliced NS mRNA, likely from downstream initiation on a Met residue that comprises the P1 position of NS1-ARF21-8 Derived from a 14-residue peptide with no apparent biological function and negligible impacts on IAV infection, infectivity, and pathogenicity, NS1-ARF21-8 provides a clear demonstration of how immunosurveillance exploits natural errors in protein translation to provide antiviral immunity. We further show that IAV infection enhances a model cellular ARF translation, which potentially has important implications for virus-induced autoimmunity.


Assuntos
Linfócitos T CD8-Positivos/imunologia , Epitopos de Linfócito T/metabolismo , Vírus da Influenza A/fisiologia , Influenza Humana/imunologia , Infecções por Orthomyxoviridae/imunologia , Proteínas não Estruturais Virais/metabolismo , Processamento Alternativo , Animais , Modelos Animais de Doenças , Epitopos de Linfócito T/genética , Epitopos de Linfócito T/imunologia , Células HEK293 , Interações Hospedeiro-Patógeno , Humanos , Vigilância Imunológica , Camundongos , Camundongos Endogâmicos BALB C , Fases de Leitura Aberta/genética , Proteínas não Estruturais Virais/genética , Proteínas não Estruturais Virais/imunologia
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