The Tomato Kinase Pti1 Contributes to Production of Reactive Oxygen Species in Response to Two Flagellin-Derived Peptides and Promotes Resistance to <i>Pseudomonas syringae</i> Infection

Schwizer, Simon; Kraus, Christine M.; Dunham, Diane; Zheng, Yanyan; Fernandez-Pozo, Noé; Pombo, Marina A.; Fei, Zhangjun; Chakravarthy, Suma; Martin, Gregory B.

doi:10.1094/mpmi-03-17-0056-r

Cited by 23 publications

(32 citation statements)

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“…While leaf morphology may play a role in resistance (e.g., waxy cuticles, dense trichomes, and complex leaf topography), we showed that the recognition of flagellin is the major resistance determinant in the accessions tested in Fig 3b. Interestingly, while previous studies have found PTI results in a moderate inhibition of pathogen growth (~10-fold) (Zipfel et al ., 2004; Lacombe et al ., 2010; Schwizer et al ., 2017), our screen revealed a much stronger inhibition of pathogen growth (~150-fold) when plants recognize the pathogen on the leaf surface (Fig. 3), which is more similar to the degree of growth inhibition expected from NTI.…”

Section: Discussionmentioning

confidence: 99%

Natural variation for unusual host responses and flagellin-mediated immunity againstPseudomonas syringaein genetically diverse tomato accessions

Roberts

Mainiero

Powell

et al. 2019

Preprint

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The interaction between tomato and Pseudomonas syringae pv. tomato (Pst) is a well-developed model for investigating the molecular basis of the plant immune system. There is extensive natural variation in Solanum lycopersicum (tomato) but it has not been fully leveraged to enhance our understanding of the tomato-Pst pathosystem. We screened 216 genetically diverse accessions of cultivated tomato and a wild tomato species for natural variation in their response to three strains of Pst. The screen uncovered a broad range of previously unseen host symptoms in response to Pst, and one of these, stem galls, was found to be simply inherited. The screen also identified tomato accessions that showed enhanced responses to flagellin in bacterial population assays and in reactive oxygen species assays upon exposure to flagellin-derived peptides, flg22 and flgII-28. Reporter genes confirmed that the host responses were due primarily to pattern recognition receptor-immunity. This study revealed extensive natural variation in tomato for susceptibility and resistance to Pst and will enable elucidation of the molecular mechanisms underlying these host responses.Key Words: Bacterial speck disease, flagellin, natural variation, NLR-triggered immunity, patterntriggered immunity, plant immunity, PRR-triggered immunity Abramovitch RB, Janjusevic R, Stebbins CE, Martin GB. 2006. Type III effector AvrPtoB requires intrinsic E3 ubiquitin ligase activity to suppress plant cell death and immunity. Proc Natl Acad Sci USA 103: 2851-2856. Abramovitch RB, Kim Y-J, Chen S, Dickman MB, Martin GB. 2003. Pseudomonas type III effector AvrPtoB induces plant disease susceptibility by inhibition of host programmed cell death. EMBO J 22: 60-69. Arredondo CR, Davis RM. 2000. First report of Pseudomonas syringae pv. tomato race 1 on tomato in California. Plant Disease 84: 371. Bao Z, Meng F, Strickler SR, Dunham DM, Munkvold KR, Martin GB. 2015. Identification of a candidate gene in Solanum habrochaites for resistance to a race 1 strain of Pseudomonas syringae pv. tomato. The Plant Genome 8: 10.3835/plantgenome2015.3802.0006. Buell CR, Joardar V, Lindeberg M, Selengut J, Paulsen IT, Gwinn ML, Dodson RJ, Deboy RT, Durkin AS, Kolonay JF, et al. 2003. The complete genome sequence of the Arabidopsis and tomato pathogen Pseudomonas syringae pv. tomato DC3000.

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Section: Discussionmentioning

confidence: 99%

Natural variation for unusual host responses and flagellin-mediated immunity againstPseudomonas syringaein genetically diverse tomato accessions

Roberts

Mainiero

Powell

et al. 2019

Preprint

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“…Upon recognition of these and other MAMPs, a suite of molecular events occurs to promote defense, including the production of reactive oxygen species (ROS), activation of a mitogen-activated protein kinase (MAPK) cascade, transcriptional reprogramming, callose deposition at the cell wall, stomatal closure, and calcium fluxes (Couto and Zipfel, 2016;Li et al, 2016). While PTI has generally been associated with a moderate inhibition of bacterial pathogen growth in Arabidopsis (Arabidopsis thaliana) and tomato (;10fold; Zipfel et al, 2004;Lacombe et al, 2010;Schwizer et al, 2017), a recent study shows that flagellinmediated PTI plays a major role in immunity on the leaf surface for some tomato accessions, decreasing bacterial populations by ;150-fold (Roberts et al, 2019b).…”

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confidence: 99%

Molecular Characterization of Differences between the Tomato Immune Receptors Flagellin Sensing 3 and Flagellin Sensing 2

et al. 2020

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Plants mount defense responses by recognizing indicators of pathogen invasion, including microbe-associated molecular patterns (MAMPs). Flagellin, from the bacterial pathogen Pseudomonas syringae pv. tomato (Pst), contains two MAMPs, flg22 and flgII-28, that are recognized by tomato (Solanum lycopersicum) receptors Flagellin sensing2 (Fls2) and Fls3, respectively, but to what degree each receptor contributes to immunity and whether they promote immune responses using the same molecular mechanisms are unknown. Here, we characterized CRISPR/Cas9-generated Fls2 and Fls3 tomato mutants and found that the two receptors contribute equally to disease resistance both on the leaf surface and in the apoplast. However, we observed striking differences in certain host responses mediated by the two receptors. Compared to Fls2, Fls3 mediated a more sustained production of reactive oxygen species and an increase in transcript abundance of 44 tomato genes, with two genes serving as specific reporters for the Fls3 pathway. Fls3 had greater in vitro kinase activity than Fls2 and could transphosphorylate a substrate. Using chimeric Fls2/Fls3 proteins, we found no evidence that a single receptor domain is responsible for the Fls3sustained reactive oxygen species, suggesting involvement of multiple structural features or a nullified function of the chimeric construct. This work reveals differences in certain immunity outputs between Fls2 and Fls3, suggesting that they might use distinct molecular mechanisms to activate pattern-triggered immunity in response to flagellin-derived MAMPs.

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“…In tomato, PTO-INTERACTIN 1 (PTI1) was reported to be a positive regulator of PTI activation in response to FLS2 and FLS3 activation upon bacterial MAMPs (Schwizer et al, 2017). Further, CERK1 also interacts with PBS1-LIKE 27 (PBL27) to regulate PTI activation induced by chitin (Shinya et al, 2014;Yamada et al, 2016).…”

Section: Co-regulatory Rlksmentioning

confidence: 99%

Plant plasma membrane‐resident receptors: Surveillance for infections and coordination for growth and development

Manhães

Ortiz-Morea

et al. 2021

JIPB

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As sessile organisms, plants are exposed to pathogen invasions and environmental fluctuations. To overcome the challenges of their surroundings, plants acquire the potential to sense endogenous and exogenous cues, resulting in their adaptability. Hence, plants have evolved a large collection of plasma membrane-resident receptors, including RECEPTOR-LIKE KINASEs (RLKs) and RECEPTOR-LIKE PROTEINs (RLPs) to perceive those signals and regulate plant growth, development, and immunity. The ability of RLKs and RLPs to recognize distinct ligands relies on diverse categories of extracellular domains evolved. Co-regulatory receptors are often required to associate with RLKs and RLPs to facilitate cellular signal transduction. RECEPTOR-LIKE CYTOPLASMIC KINASEs (RLCKs) also associate with the complex, bifurcating the signal to key signaling hubs, such as MITOGEN-ACTIVATED PROTEIN KINASE (MAPK) cascades, to regulate diverse biological processes. Here, we discuss recent knowledge advances in understanding the roles of RLKs and RLPs in plant growth, development, and immunity, and their connection with co-regulatory receptors, leading to activation of diverse intracellular signaling pathways.

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The Tomato Kinase Pti1 Contributes to Production of Reactive Oxygen Species in Response to Two Flagellin-Derived Peptides and Promotes Resistance to Pseudomonas syringae Infection

Cited by 23 publications

References 106 publications

Natural variation for unusual host responses and flagellin-mediated immunity againstPseudomonas syringaein genetically diverse tomato accessions

Natural variation for unusual host responses and flagellin-mediated immunity againstPseudomonas syringaein genetically diverse tomato accessions

Molecular Characterization of Differences between the Tomato Immune Receptors Flagellin Sensing 3 and Flagellin Sensing 2

Plant plasma membrane‐resident receptors: Surveillance for infections and coordination for growth and development

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