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.

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 uncover that MAMP-perception in Arabidopsis induces the accumulation of free amino acids (AA) 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 suppressed bacterial virulence and bacterial growth directly without the need for MAMP-perception and SA-signaling, bypassing MAMP-elicited defense. 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 the direct suppressing effect of accumulating amino acids on the onset of bacterial virulence.

Leaf mesophyll-colonizing bacterial pathogens infect their plant hosts by adjusting their metabolism to the leaf mesophyll environment. Soon after the inoculation of naive, susceptible plants, the model bacterial pathogen Pseudomonas syringae pv. tomato DC3000 (PstDC3000) expresses virulence factors that suppress plant immunity, a requirement to produce robust infections. However, if plant immunity was elicited with Microbe-Associated Molecular-Patterns (MAMPs) prior to bacterial inoculation, PstDC3000 slows down virulence expression and only produces symptomless mild infections. To understand how bacterial metabolism adapts to these two contrasting conditions, we created iPst19, an in silico ensemble of genome-scale metabolic reconstructions. Constraining the in silico growth of iPst19 with in planta PstDC3000 gene expression data revealed that sugar catabolism is highly active in bacteria that have been inoculated in mock-treated plants. In contrast, branched-chain amino acids (BCAAs) catabolism is highly active in bacteria inoculated in MAMP-pretreated plants. Bacterial growth and gene expression analysis showed that BCAAs suppress virulence gene expression without affecting bacterial growth in vitro. In planta, however, BCAAs suppress the expression of virulence genes at the early stages of the infection and significantly impair leaf colonization of the host plant Arabidopsis thaliana. While the overexpression of the conserved bacterial leucine-responsive transcriptional regulator Lrp induced the expression of virulence genes, its downregulation had the opposite effect, suggesting that BCAA-free Lrp induces virulence while BCAA-Lrp does not. Overall, our data provide mechanistic connections to understand how plant immunity impacts PstDC3000 metabolism and virulence, furthering our understanding of bacterial pathogenesis and plant disease.

Many biological questions can benefit from the diverse perspectives of multiple disciplines, including engineering. In the last several decades, biological research has been advanced from engineering approaches to delineate processes including stem cell differentiation, optimizing cancer therapies, and building physical and genetic tools to manipulate cell function. The collaboration between fields necessitates a common language to bridge concepts that have historically been developed for engineering and emergent properties of biological systems. By utilizing the expertise of both fields, greater advances can be reached in biological research through the application of large data sets and modelling of biological processes. Parallels between cellular signalling and engineering process controls include feedback and feed‐forward loops, amplification and thresholds; in both fields, these subprocesses contribute widely to the overall function of the cell and engineered system. Feedback and feed‐forward loops, amplification and thresholds, along with their importance in biology and process controls and their contributions to overall function. Key Concepts Parallels exist between the structure and function of cellular signal transduction architectures and engineering process control concepts. Disruptions in signalling pathways and process control systems can have detrimental consequences, including health disorders and manufacturing casualties, respectively. Understanding cell signalling mechanisms in a process control context can provide a novel perspective for understanding treatments and therapies of diseases stemming from dysregulation of cellular controls. Similarities between everyday process controls like air conditioning can help unravel apparent complexities in cellular signaling. Using extended analogy between process controls and cellular signaling may provide insights into mechanisms of manipulation not previously explored.