More Like this

1. A physical model links structure and function in the plant immune system

   https://doi.org/10.1073/pnas.2502872122  

   Weiner, Benjamin G; Märkle, Hanna; Laderman, Eric; Demirjian, Choghag; Bergelson, Joy (June 2025, Proceedings of the National Academy of Sciences)

   Effector-Triggered Immunity (ETI) is an important part of the plant immune system, allowing plants to sense and respond to harmful pathogen proteins known as “effectors.” Effectors can be sensed directly or indirectly by NLR (Nucleotide-binding Leucine-rich Repeat) proteins, many of which “guard” the plant proteins targeted by effectors. Although a few effector–target–NLR interactions have been characterized, a general understanding of how these molecular interactions give rise to a functioning immune system is lacking. Here, we present a physics-based model of ETI based on protein–protein interactions. We show that the simplest physical model consistent with the biology gives rise to a robust immune sensor and explains the empirical phenomenon of effector interference as a generic consequence of molecules competing for binding partners. Using the evolutionarily conserved ZAR1 defense gene as a model, we explain how more complex interaction networks integrate multiple pathogen signals into a single response. We then examine alternatives to a guarding architecture, including direct sensing, decoys, and blended “integrated decoy” strategies, and reveal that these sensing architectures obey functional trade-offs between their sensitivity, target protection, and proteomic cost. This allows a quantitative analysis of the trade-offs between different forms of ETI. We discuss these findings in the context of the evolutionary forces shaping the plant immune system. 

   more » « less
2. Proteome-wide analysis of cysteine reactivity during effector-triggered immunity

   McConnell, Evan W. Berg (April 2019, Plant physiology)

   A surge in the accumulation of oxidants generates shifts in the cellular redox potential during early stages of plant infection with pathogens and activation of effector-triggered immunity (ETI). The redoxome, defined as the proteome-wide oxidative modifications of proteins caused by oxidants, has a well-known impact on stress responses in metazoans. However, the identity of proteins and the residues sensitive to oxidation during the plant immune response remain largely unknown. Previous studies of the thimet oligopeptidases TOP1 and TOP2 placed them in the salicylic acid dependent branch of ETI, with a current model wherein TOPs sustain interconnected organellar and cytosolic pathways that modulate the oxidative burst and development of cell death. Herein, we characterized the ETI redoxomes in Arabidopsis (Arabidopsis thaliana) wild-type Col-0 and top1top2 mutant plants using a differential alkylation-based enrichment technique coupled with label-free mass spectrometry-based quantification. We identified cysteines sensitive to oxidation in a wide range of protein families at multiple time points after pathogen infection. Differences were detected between Col-0 and top1top2 redoxomes regarding the identity and number of oxidized cysteines, and the amplitude of time-dependent fluctuations in protein oxidation. Our results support a determining role for TOPs in maintaining the proper level and dynamics of proteome oxidation during ETI. This study significantly expands the repertoire of oxidation-sensitive plant proteins and can guide future mechanistic studies. 

   more » « less
3. Bringing Plant Immunity to Light: A Genetically Encoded, Bioluminescent Reporter of Pattern-Triggered Immunity in Nicotiana benthamiana

   https://doi.org/10.1094/MPMI-07-22-0160-TA  

   Garcia, Anthony G.; Steinbrenner, Adam D. (March 2023, Molecular Plant-Microbe Interactions®)

   Plants rely on innate immune systems to defend against a wide variety of biotic attackers. Key components of innate immunity include cell-surface pattern-recognition receptors (PRRs), which recognize pest- and pathogen-associated molecular patterns (PAMPs). Unlike other classes of receptors that often have visible cell-death immune outputs upon activation, PRRs generally lack rapid methods for assessing function. Here, we describe a genetically encoded bioluminescent reporter of immune activation by heterologously expressed PRRs in the model organism Nicotiana benthamiana. We characterized N. benthamiana transcriptome changes in response to Agrobacterium tumefaciens and subsequent PAMP treatment to identify pattern-triggered immunity (PTI)-associated marker genes, which were then used to generate promoter-luciferase fusion fungal bioluminescence pathway (FBP) constructs. A reporter construct termed pFBP_2xNbLYS1::LUZ allows for robust detection of PTI activation by heterologously expressed PRRs. Consistent with known PTI signaling pathways, reporter activation by receptor-like protein (RLP) PRRs is dependent on the known adaptor of RLP PRRs, i.e., SOBIR1. The FBP reporter minimizes the amount of labor, reagents, and time needed to assay function of PRRs and displays robust sensitivity at biologically relevant PAMP concentrations, making it ideal for high throughput screens. The tools described in this paper will be powerful for investigations of PRR function and characterization of the structure-function of plant cell-surface receptors. [Formula: see text] The author(s) have dedicated the work to the public domain under the Creative Commons CC0 “No Rights Reserved” license by waiving all of his or her rights to the work worldwide under copyright law, including all related and neighboring rights, to the extent allowed by law, 2023. 

   more » « less
4. Reduction of the canonical function of a glycolytic enzyme enolase triggers immune responses that further affect metabolism and growth in Arabidopsis

   https://doi.org/10.1093/plcell/koab283  

   Yang, Leiyun; Wang, Zhixue; Zhang, Aiqin; Bhawal, Ruchika; Li, Chunlong; Zhang, Sheng; Cheng, Lailiang; Hua, Jian (November 2021, The Plant Cell)

   Abstract Primary metabolism provides energy for growth and development as well as secondary metabolites for diverse environmental responses. Here we describe an unexpected consequence of disruption of a glycolytic enzyme enolase named LOW EXPRESSION OF OSMOTICALLY RESPONSIVE GENE 2 (LOS2) in causing constitutive defense responses or autoimmunity in Arabidopsis thaliana. The autoimmunity in the los2 mutant is accompanied by a higher expression of about one-quarter of intracellular immune receptor nucleotide-binding leucine-rich repeat (NLR) genes in the genome and is partially dependent on one of these NLR genes. The LOS2 gene was hypothesized to produce an alternatively translated protein c-Myc Binding Protein (MBP-1) that functions as a transcriptional repressor. Complementation tests show that LOS2 executes its function in growth and immunity regulation through the canonical enolase activity but not the production of MBP-1. In addition, the autoimmunity in the los2 mutants leads to a higher accumulation of sugars and organic acids and a depletion of glycolytic metabolites. These findings indicate that LOS2 does not exert its function in immune responses through an alternatively translated protein MBP-1. Rather, they show that a perturbation of glycolysis from the reduction of the enolase activity results in activation of NLR-involved immune responses which further influences primary metabolism and plant growth, highlighting the complex interaction between primary metabolism and plant immunity. 

   more » « less
5. Temporal fruit microbiome and immunity dynamics in postharvest apple ( Malus x domestica )

   https://doi.org/10.1093/hr/uhaf063  

   Kithan-Lundquist, Roselane; McMillan, Hannah M; He, Sheng-Yang; Sundin, George W (April 2025, Horticulture Research)

   Abstract The plant immune response plays a central role in maintaining a well-balanced and healthy microbiome for plant health. However, insights into how the fruit immune response and the fruit microbiome influence fruit health after harvest are limited. We investigated the temporal dynamics of the fruit microbiota and host defense gene expression patterns during postharvest storage of apple fruits at room temperature. Our results demonstrate a temporal dynamic shift in both bacterial and fungal community composition during postharvest storage that coincides with a steep-decline in host defense response gene expression associated with pattern-triggered immunity. We observed the gradual appearance of putative pathogenic/spoilage microbes belonging to genera Alternaria (fungi) and Gluconobacter and Acetobacter (bacteria) at the expense of Sporobolomyces and other genera, which have been suggested to be beneficial for plant hosts. Moreover, artificial induction of pattern-triggered immunity in apple fruit with the flg22 peptide delayed the onset of fruit rot caused by the fungal pathogen Penicillium expansum. Our results suggest that the fruit immune response helps to orchestrate a microbiome and that the collapse of the immunity results in the proliferation of spoilage microbes and fruit rot. These findings hold implications for the development of strategies to increase fruit quality and prolong shelf life in fruits and vegetables. 

   more » « less