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1.
Cell ; 173(2): 456-469.e16, 2018 04 05.
Article in English | MEDLINE | ID: mdl-29576453

ABSTRACT

Following a previous microbial inoculation, plants can induce broad-spectrum immunity to pathogen infection, a phenomenon known as systemic acquired resistance (SAR). SAR establishment in Arabidopsis thaliana is regulated by the Lys catabolite pipecolic acid (Pip) and flavin-dependent-monooxygenase1 (FMO1). Here, we show that elevated Pip is sufficient to induce an FMO1-dependent transcriptional reprogramming of leaves that is reminiscent of SAR. In planta and in vitro analyses demonstrate that FMO1 functions as a pipecolate N-hydroxylase, catalyzing the biochemical conversion of Pip to N-hydroxypipecolic acid (NHP). NHP systemically accumulates in plants after microbial attack. When exogenously applied, it overrides the defect of NHP-deficient fmo1 in acquired resistance and acts as a potent inducer of plant immunity to bacterial and oomycete infection. Our work has identified a pathogen-inducible L-Lys catabolic pathway in plants that generates the N-hydroxylated amino acid NHP as a critical regulator of systemic acquired resistance to pathogen infection.


Subject(s)
Arabidopsis Proteins/metabolism , Arabidopsis/metabolism , Oxygenases/metabolism , Pipecolic Acids/metabolism , Plant Immunity/drug effects , Arabidopsis/enzymology , Arabidopsis/immunology , Arabidopsis Proteins/genetics , Gas Chromatography-Mass Spectrometry , Lysine/metabolism , Oomycetes/pathogenicity , Oxygenases/genetics , Pipecolic Acids/analysis , Pipecolic Acids/pharmacology , Plant Leaves/enzymology , Plant Leaves/immunology , Plant Leaves/metabolism , Pseudomonas syringae/pathogenicity , Transaminases/genetics , Transaminases/metabolism
2.
EMBO J ; 39(2): e102602, 2020 01 15.
Article in English | MEDLINE | ID: mdl-31802519

ABSTRACT

Plants establish mutualistic associations with beneficial microbes while deploying the immune system to defend against pathogenic ones. Little is known about the interplay between mutualism and immunity and the mediator molecules enabling such crosstalk. Here, we show that plants respond differentially to a volatile bacterial compound through integral modulation of the immune system and the phosphate-starvation response (PSR) system, resulting in either mutualism or immunity. We found that exposure of Arabidopsis thaliana to a known plant growth-promoting rhizobacterium can unexpectedly have either beneficial or deleterious effects to plants. The beneficial-to-deleterious transition is dependent on availability of phosphate to the plants and is mediated by diacetyl, a bacterial volatile compound. Under phosphate-sufficient conditions, diacetyl partially suppresses plant production of reactive oxygen species (ROS) and enhances symbiont colonization without compromising disease resistance. Under phosphate-deficient conditions, diacetyl enhances phytohormone-mediated immunity and consequently causes plant hyper-sensitivity to phosphate deficiency. Therefore, diacetyl affects the type of relation between plant hosts and certain rhizobacteria in a way that depends on the plant's phosphate-starvation response system and phytohormone-mediated immunity.


Subject(s)
Arabidopsis/immunology , Diacetyl/pharmacology , Phosphates/metabolism , Plant Diseases/immunology , Plant Immunity/immunology , Plant Roots/immunology , Arabidopsis/drug effects , Arabidopsis/growth & development , Arabidopsis/metabolism , Bacteria/immunology , Bacteria/metabolism , Plant Diseases/microbiology , Plant Immunity/drug effects , Plant Roots/drug effects , Plant Roots/growth & development , Plant Roots/metabolism , Rhizosphere , Symbiosis , Volatile Organic Compounds/pharmacology
3.
New Phytol ; 242(5): 2163-2179, 2024 Jun.
Article in English | MEDLINE | ID: mdl-38532564

ABSTRACT

The S-domain-type receptor-like kinase (SD-RLK) LIPOOLIGOSACCHARIDE-SPECIFIC REDUCED ELICITATION (LORE) from Arabidopsis thaliana is a pattern recognition receptor that senses medium-chain 3-hydroxy fatty acids, such as 3-hydroxydecanoic acid (3-OH-C10:0), to activate pattern-triggered immunity. Here, we show that LORE homomerization is required to activate 3-OH-C10:0-induced immune signaling. Fluorescence lifetime imaging in Nicotiana benthamiana demonstrates that AtLORE homomerizes via the extracellular and transmembrane domains. Co-expression of AtLORE truncations lacking the intracellular domain exerts a dominant negative effect on AtLORE signaling in both N. benthamiana and A. thaliana, highlighting that homomerization is essential for signaling. Screening for 3-OH-C10:0-induced reactive oxygen species production revealed natural variation within the Arabidopsis genus. Arabidopsis lyrata and Arabidopsis halleri do not respond to 3-OH-C10:0, although both possess a putative LORE ortholog. Both LORE orthologs have defective extracellular domains that bind 3-OH-C10:0 to a similar level as AtLORE, but lack the ability to homomerize. Thus, ligand binding is independent of LORE homomerization. Analysis of AtLORE and AlyrLORE chimera suggests that the loss of AlyrLORE homomerization is caused by several amino acid polymorphisms across the extracellular domain. Our findings shed light on the activation mechanism of LORE and the loss of 3-OH-C10:0 perception within the Arabidopsis genus.


Subject(s)
Arabidopsis Proteins , Arabidopsis , Protein Multimerization , Signal Transduction , Arabidopsis/immunology , Arabidopsis/genetics , Arabidopsis/metabolism , Arabidopsis Proteins/metabolism , Arabidopsis Proteins/genetics , Arabidopsis Proteins/chemistry , Decanoic Acids/metabolism , Decanoic Acids/pharmacology , Nicotiana/genetics , Nicotiana/immunology , Nicotiana/metabolism , Plant Immunity/drug effects , Protein Domains , Reactive Oxygen Species/metabolism , Receptors, Pattern Recognition/metabolism
4.
New Phytol ; 243(1): 362-380, 2024 Jul.
Article in English | MEDLINE | ID: mdl-38730437

ABSTRACT

Plants typically activate distinct defense pathways against various pathogens. Heightened resistance to one pathogen often coincides with increased susceptibility to another pathogen. However, the underlying molecular basis of this antagonistic response remains unclear. Here, we demonstrate that mutants defective in the transcription factor ETHYLENE-INSENSITIVE 3-LIKE 2 (OsEIL2) exhibited enhanced resistance to the biotrophic bacterial pathogen Xanthomonas oryzae pv oryzae and to the hemibiotrophic fungal pathogen Magnaporthe oryzae, but enhanced susceptibility to the necrotrophic fungal pathogen Rhizoctonia solani. Furthermore, necrotroph-induced OsEIL2 binds to the promoter of OsWRKY67 with high affinity, leading to the upregulation of salicylic acid (SA)/jasmonic acid (JA) pathway genes and increased SA/JA levels, ultimately resulting in enhanced resistance. However, biotroph- and hemibiotroph-induced OsEIL2 targets OsERF083, resulting in the inhibition of SA/JA pathway genes and decreased SA/JA levels, ultimately leading to reduced resistance. Our findings unveil a previously uncharacterized defense mechanism wherein two distinct transcriptional regulatory modules differentially mediate immunity against pathogens with different lifestyles through the transcriptional reprogramming of phytohormone pathway genes.


Subject(s)
Cyclopentanes , Gene Expression Regulation, Plant , Oryza , Oxylipins , Plant Diseases , Plant Immunity , Plant Proteins , Rhizoctonia , Salicylic Acid , Xanthomonas , Oxylipins/metabolism , Salicylic Acid/metabolism , Cyclopentanes/metabolism , Oryza/microbiology , Oryza/genetics , Oryza/immunology , Plant Diseases/microbiology , Plant Diseases/immunology , Xanthomonas/physiology , Plant Proteins/metabolism , Plant Proteins/genetics , Rhizoctonia/physiology , Plant Immunity/drug effects , Mutation/genetics , Disease Resistance/genetics , Promoter Regions, Genetic/genetics , Transcription Factors/metabolism , Transcription Factors/genetics , Protein Binding/drug effects
5.
Physiol Plant ; 176(3): e14324, 2024.
Article in English | MEDLINE | ID: mdl-38705866

ABSTRACT

Broomrape (Orobanche cumana) negatively affects sunflower, causing severe yield losses, and thus, there is a need to control O. cumana infestation. Brassinosteroids (BRs) play key roles in plant growth and provide resilience to weed infection. This study aims to evaluate the mechanisms by which BRs ameliorate O. cumana infection in sunflower (Helianthus annuus). Seeds were pretreated with BRs (1, 10, and 100 nM) and O. cumana inoculation for 4 weeks under soil conditions. O. cumana infection significantly reduced plant growth traits, photosynthesis, endogenous BRs and regulated the plant defence (POX, GST), BRs signalling (BAK1, BSK1 to BSK4) and synthesis (BRI1, BR6OX2) genes. O. cumana also elevated the levels of malondialdehyde (MDA), hydroxyl radical (OH-), hydrogen peroxide (H2O2) and superoxide (O2 •-) in leaves/roots by 77/112, 63/103, 56/97 and 54/89%, as well as caused ultrastructural cellular damages in both leaves and roots. In response, plants activated a few enzymes, superoxide dismutase (SOD), peroxidase (POD) and reduced glutathione but were unable to stimulate the activity of ascorbate peroxidase (APX) and catalase (CAT) enzymes. The addition of BRs (especially at 10 nM) notably recovered the ultrastructural cellular damages, lowered the production of oxidative stress, activated the key enzymatic antioxidants and induced the phenolic and lignin contents. The downregulation in the particular genes by BRs is attributed to the increased resilience of sunflower via a susceptible reaction. In a nutshell, BRs notably enhanced the sunflower resistance to O. cumana infection by escalating the plant immunity responses, inducing systemic acquired resistance, reducing oxidative or cellular damages, and modulating the expression of BR synthesis or signalling genes.


Subject(s)
Brassinosteroids , Helianthus , Orobanche , Seeds , Helianthus/drug effects , Helianthus/immunology , Helianthus/physiology , Brassinosteroids/pharmacology , Brassinosteroids/metabolism , Orobanche/physiology , Orobanche/drug effects , Seeds/drug effects , Seeds/immunology , Plant Weeds/drug effects , Plant Weeds/physiology , Plant Diseases/parasitology , Plant Diseases/immunology , Plant Immunity/drug effects , Gene Expression Regulation, Plant/drug effects , Photosynthesis/drug effects , Plant Roots/immunology , Plant Roots/drug effects , Hydrogen Peroxide/metabolism , Plant Leaves/drug effects , Plant Leaves/immunology , Plant Proteins/metabolism , Plant Proteins/genetics , Malondialdehyde/metabolism
6.
J Nanobiotechnology ; 22(1): 617, 2024 Oct 12.
Article in English | MEDLINE | ID: mdl-39395991

ABSTRACT

BACKGROUND: Tomato (Solanum lycopersicum L.) production is severely threatened by bacterial wilt, caused by the phytopathogenic bacterium Ralstonia solanacearum. Recently, nano-enabled strategies have shown tremendous potential in crop disease management. OBJECTIVES: This study investigates the efficacy of biogenic nanoformulations (BNFs), comprising biogenic silica nanoparticles (SiNPs) and melatonin (MT), in controlling bacterial wilt in tomato. METHODS: SiNPs were synthesized using Zizania latifolia leaves extract. Further, MT containing BNFs were synthesized through the one-pot approach. Nanomaterials were characterized using standard characterization techniques. Greenhouse disease assays were conducted to assess the impact of SiNPs and BNFs on tomato plant immunity and resistance to bacterial wilt. RESULTS: The SiNPs and BNFs exhibited a spherical morphology, with particle sizes ranging from 13.02 nm to 22.33 nm for the SiNPs and 17.63 nm to 21.79 nm for the BNFs, indicating a relatively uniform size distribution and consistent shape across both materials. Greenhouse experiments revealed that soil application of BNFs outperformed SiNPs, significantly enhancing plant immunity and reducing bacterial wilt incidence by 78.29% in tomato plants by maintaining oxidative stress homeostasis via increasing the activities of antioxidant enzymes such as superoxide dismutase (31.81%), peroxidase (32.9%), catalase (32.65%), and ascorbate peroxidase (47.37%) compared to untreated infected plants. Additionally, BNFs induced disease resistance by enhancing the production of salicylic acid and activating defense-related genes (e.g., SlPAL1, SlICS1, SlNPR1, SlEDS, SlPD4, and SlSARD1) involved in phytohormones signaling in infected tomato plants. High-throughput 16 S rRNA sequencing revealed that BNFs promoted growth of beneficial rhizosphere bacteria (Gemmatimonadaceae, Ramlibacter, Microscillaceae, Anaerolineaceae, Chloroplast and Phormidium) in both healthy and diseased plants, while suppressing R. solanacearum abundance in infected plants. CONCLUSION: Overall, these findings suggest that BNFs offer a more promising and sustainable approach for managing bacterial wilt disease in tomato plants.


Subject(s)
Melatonin , Nanoparticles , Plant Diseases , Ralstonia solanacearum , Rhizosphere , Silicon Dioxide , Solanum lycopersicum , Solanum lycopersicum/microbiology , Ralstonia solanacearum/drug effects , Plant Diseases/microbiology , Plant Diseases/prevention & control , Nanoparticles/chemistry , Silicon Dioxide/chemistry , Silicon Dioxide/pharmacology , Melatonin/pharmacology , Disease Resistance/drug effects , Plant Immunity/drug effects , Immunomodulating Agents/pharmacology , Immunomodulating Agents/chemistry , Signal Transduction/drug effects , Plant Leaves/chemistry , Plant Leaves/microbiology
7.
Proc Natl Acad Sci U S A ; 118(47)2021 11 23.
Article in English | MEDLINE | ID: mdl-34799454

ABSTRACT

Pathogenic effector proteins use a variety of enzymatic activities to manipulate host cellular proteins and favor the infection process. However, these perturbations can be sensed by nucleotide-binding leucine-rich-repeat (NLR) proteins to activate effector-triggered immunity (ETI). Here we have identified a small molecule (Zaractin) that mimics the immune eliciting activity of the Pseudomonas syringae type III secreted effector (T3SE) HopF1r and show that both HopF1r and Zaractin activate the same NLR-mediated immune pathway in Arabidopsis Our results demonstrate that the ETI-inducing action of pathogenic effectors can be harnessed to identify synthetic activators of the eukaryotic immune system.


Subject(s)
Arabidopsis Proteins/metabolism , Arabidopsis/drug effects , Carrier Proteins/metabolism , Plant Immunity/drug effects , Small Molecule Libraries/pharmacology , Arabidopsis/microbiology , Bacterial Proteins/metabolism , NLR Proteins/metabolism , Plant Diseases/microbiology , Protein Binding/drug effects , Pseudomonas syringae/pathogenicity
8.
Pestic Biochem Physiol ; 204: 106071, 2024 Sep.
Article in English | MEDLINE | ID: mdl-39277416

ABSTRACT

Synthetic plant activators represent a promising novel class of green pesticides that can triggering endogenous plant immunity against pathogen invasion. In our previous study, we developed a series of fluorinated compounds capable of eliciting disease resistance in plants; however, the underlying regulatory mechanisms remained unclear. In this study, we systematically investigated the mechanism of plant immune activation using four synthetic plant activators in Arabidopsis thaliana (A. thaliana), including two fluorine-substituted and two non­fluorine-substituted molecules. Our findings revealed that the fluorinated compounds exhibited superior disease resistance activity compared to the non-fluorinated molecules. Gene expression analysis in systemic acquired resistance (SAR)- and induced systemic resistance (ISR)-related pathways demonstrated that fluorine substitution effectively regulated both SAR- and ISR-pathway activation, highlighting the distinct roles of fluorine in modulating the plant immune system. Notably, the prolonged ROS burst was observed in chloroplasts following treatment with all four plant activators, contrasting with the transient ROS burst induced by natural elicitors. These results provide insights into the unique mechanisms underlying synthetic plant activator-induced plant immunity. Furthermore, comprehensive proteomic analysis revealed a robust immune response mediated by fluorine-substituted plant activators. These findings offer novel insights into the role of fluorine substitution in SAR- and ISR-associated immune signaling pathways and their distinct impact on ROS production within chloroplasts.


Subject(s)
Arabidopsis , Chloroplasts , Reactive Oxygen Species , Signal Transduction , Signal Transduction/drug effects , Reactive Oxygen Species/metabolism , Chloroplasts/metabolism , Chloroplasts/drug effects , Arabidopsis/genetics , Arabidopsis/metabolism , Arabidopsis/drug effects , Arabidopsis/immunology , Plant Immunity/drug effects , Disease Resistance/drug effects , Halogenation , Plant Diseases/immunology
9.
Int J Mol Sci ; 25(15)2024 Aug 04.
Article in English | MEDLINE | ID: mdl-39126086

ABSTRACT

Strigolactones (SLs) are plant hormones that regulate diverse developmental processes and environmental responses in plants. It has been discovered that SLs play an important role in regulating plant immune resistance to pathogens but there are currently no reports on their role in the interaction between Nicotiana benthamiana and the tobacco mosaic virus (TMV). In this study, the exogenous application of SLs weakened the resistance of N. benthamiana to TMV, promoting TMV infection, whereas the exogenous application of Tis108, a SL inhibitor, resulted in the opposite effect. Virus-induced gene silencing (VIGS) inhibition of two key SL synthesis enzyme genes, NtCCD7 and NtCCD8, enhanced the resistance of N. benthamiana to TMV. Additionally, we conducted a screening of N. benthamiana related to TMV infection. TMV-infected plants treated with SLs were compared to the control by using RNA-seq. The KEGG enrichment analysis and weighted gene co-expression network analysis (WGCNA) of differentially expressed genes (DEGs) suggested that plant hormone signaling transduction may play a significant role in the SL-TMV-N. benthamiana interactions. This study reveals new functions of SLs in regulating plant immunity and provides a reference for controlling TMV diseases in production.


Subject(s)
Disease Resistance , Gene Expression Regulation, Plant , Lactones , Nicotiana , Plant Diseases , Tobacco Mosaic Virus , Nicotiana/virology , Nicotiana/genetics , Nicotiana/immunology , Tobacco Mosaic Virus/physiology , Lactones/pharmacology , Disease Resistance/genetics , Plant Diseases/virology , Plant Diseases/genetics , Plant Diseases/immunology , Plant Proteins/genetics , Plant Proteins/metabolism , Plant Growth Regulators/metabolism , Plant Growth Regulators/pharmacology , Plant Immunity/genetics , Plant Immunity/drug effects , Gene Silencing
10.
Int J Mol Sci ; 25(12)2024 Jun 07.
Article in English | MEDLINE | ID: mdl-38928022

ABSTRACT

Various metabolites, including phytohormones, phytoalexins, and amino acids, take part in the plant immune system. Herein, we analyzed the effects of L-methionine (Met), a sulfur-containing amino acid, on the plant immune system in tomato. Treatment with low concentrations of Met enhanced the resistance of tomato to a broad range of diseases caused by the hemi-biotrophic bacterial pathogen Pseudomonas syringae pv. tomato (Pst) and the necrotrophic fungal pathogen Botrytis cinerea (Bc), although it did not induce the production of any antimicrobial substances against these pathogens in tomato leaf tissues. Analyses of gene expression and phytohormone accumulation indicated that Met treatment alone did not activate the defense signals mediated by salicylic acid, jasmonic acid, and ethylene. However, the salicylic acid-responsive defense gene and the jasmonic acid-responsive gene were induced more rapidly in Met-treated plants after infection with Pst and Bc, respectively. These findings suggest that low concentrations of Met have a priming effect on the phytohormone-mediated immune system in tomato.


Subject(s)
Botrytis , Cyclopentanes , Gene Expression Regulation, Plant , Methionine , Plant Diseases , Plant Growth Regulators , Pseudomonas syringae , Solanum lycopersicum , Solanum lycopersicum/microbiology , Solanum lycopersicum/immunology , Solanum lycopersicum/genetics , Solanum lycopersicum/drug effects , Solanum lycopersicum/metabolism , Methionine/pharmacology , Gene Expression Regulation, Plant/drug effects , Plant Diseases/microbiology , Plant Diseases/immunology , Plant Diseases/genetics , Pseudomonas syringae/pathogenicity , Cyclopentanes/pharmacology , Cyclopentanes/metabolism , Plant Growth Regulators/pharmacology , Oxylipins/pharmacology , Oxylipins/metabolism , Plant Immunity/drug effects , Disease Resistance/drug effects , Disease Resistance/immunology , Salicylic Acid/pharmacology , Salicylic Acid/metabolism , Plant Leaves/immunology , Plant Leaves/microbiology , Plant Leaves/drug effects , Plant Proteins/genetics , Plant Proteins/metabolism , Ethylenes/metabolism
11.
Plant Cell ; 32(7): 2216-2236, 2020 07.
Article in English | MEDLINE | ID: mdl-32327536

ABSTRACT

Upon recognition of microbes, pattern recognition receptors (PRRs) activate pattern-triggered immunity. FLAGELLIN SENSING2 (FLS2) and BRASSINOSTEROID INSENSITIVE1-ASSOCIATED KINASE1 (BAK1) form a typical PRR complex that senses bacteria. Here, we report that the kinase activity of the malectin-like receptor-like kinase STRESS INDUCED FACTOR 2 (SIF2) is critical for Arabidopsis (Arabidopsis thaliana) resistance to bacteria by regulating stomatal immunity. SIF2 physically associates with the FLS2-BAK1 PRR complex and interacts with and phosphorylates the guard cell SLOW ANION CHANNEL1 (SLAC1), which is necessary for abscisic acid (ABA)-mediated stomatal closure. SIF2 is also required for the activation of ABA-induced S-type anion currents in Arabidopsis protoplasts, and SIF2 is sufficient to activate SLAC1 anion channels in Xenopus oocytes. SIF2-mediated activation of SLAC1 depends on specific phosphorylation of Ser 65. This work reveals that SIF2 functions between the FLS2-BAK1 initial immunity receptor complex and the final actuator SLAC1 in stomatal immunity.


Subject(s)
Arabidopsis Proteins/metabolism , Arabidopsis/physiology , Histone Deacetylases/metabolism , Membrane Proteins/metabolism , Plant Stomata/immunology , Repressor Proteins/metabolism , Abscisic Acid/metabolism , Abscisic Acid/pharmacology , Animals , Arabidopsis/microbiology , Arabidopsis Proteins/genetics , Arabidopsis Proteins/immunology , Disease Resistance/physiology , Female , Histone Deacetylases/genetics , Histone Deacetylases/immunology , Membrane Proteins/genetics , Membrane Proteins/immunology , Mutation , Oocytes/physiology , Phosphorylation , Plant Diseases/immunology , Plant Diseases/microbiology , Plant Immunity/drug effects , Plant Stomata/metabolism , Plants, Genetically Modified , Protein Kinases/metabolism , Protein Serine-Threonine Kinases/metabolism , Repressor Proteins/genetics , Repressor Proteins/immunology , Serine/metabolism , Xenopus
12.
Proc Natl Acad Sci U S A ; 117(22): 12017-12028, 2020 06 02.
Article in English | MEDLINE | ID: mdl-32434917

ABSTRACT

Synthetic chemical elicitors, so called plant strengtheners, can protect plants from pests and pathogens. Most plant strengtheners act by modifying defense signaling pathways, and little is known about other mechanisms by which they may increase plant resistance. Moreover, whether plant strengtheners that enhance insect resistance actually enhance crop yields is often unclear. Here, we uncover how a mechanism by which 4-fluorophenoxyacetic acid (4-FPA) protects cereals from piercing-sucking insects and thereby increases rice yield in the field. Four-FPA does not stimulate hormonal signaling, but modulates the production of peroxidases, H2O2, and flavonoids and directly triggers the formation of flavonoid polymers. The increased deposition of phenolic polymers in rice parenchyma cells of 4-FPA-treated plants is associated with a decreased capacity of the white-backed planthopper (WBPH) Sogatella furcifera to reach the plant phloem. We demonstrate that application of 4-PFA in the field enhances rice yield by reducing the abundance of, and damage caused by, insect pests. We demonstrate that 4-FPA also increases the resistance of other major cereals such as wheat and barley to piercing-sucking insect pests. This study unravels a mode of action by which plant strengtheners can suppress herbivores and increase crop yield. We postulate that this represents a conserved defense mechanism of plants against piercing-sucking insect pests, at least in cereals.


Subject(s)
Acetates/pharmacology , Feeding Behavior/drug effects , Flavonoids , Hemiptera , Plant Immunity/drug effects , Animals , Biological Assay , Crops, Agricultural/drug effects , Flavonoids/analysis , Flavonoids/metabolism , Herbivory , Hordeum/drug effects , Hydrogen Peroxide/analysis , Hydrogen Peroxide/metabolism , Oryza/drug effects , Peroxidases/analysis , Peroxidases/metabolism , Pest Control/methods , Plant Leaves/chemistry , Triticum/drug effects
13.
Plant Cell Environ ; 45(1): 236-247, 2022 01.
Article in English | MEDLINE | ID: mdl-34708407

ABSTRACT

Upon sensing attack by pathogens and insect herbivores, plants release complex mixtures of volatile compounds. Here, we show that the infection of lima bean (Phaseolus lunatus L.) plants with the non-host bacterial pathogen Pseudomonas syringae pv. tomato led to the production of microbe-induced plant volatiles (MIPVs). Surprisingly, the bacterial type III secretion system, which injects effector proteins directly into the plant cytosol to subvert host functions, was found to prime both intra- and inter-specific defense responses in neighbouring wild tobacco (Nicotiana benthamiana) plants. Screening of each of 16 effectors using the Pseudomonas fluorescens effector-to-host analyser revealed that an effector, HopP1, was responsible for immune activation in receiver tobacco plants. Further study demonstrated that 1-octen-3-ol, 3-octanone and 3-octanol are novel MIPVs emitted by the lima bean plant in a HopP1-dependent manner. Exposure to synthetic 1-octen-3-ol activated immunity in tobacco plants against a virulent pathogen Pseudomonas syringae pv. tabaci. Our results show for the first time that a bacterial type III effector can trigger the emission of C8 plant volatiles that mediate defense priming via plant-plant interactions. These results provide novel insights into the role of airborne chemicals in bacterial pathogen-induced inter-specific plant-plant interactions.


Subject(s)
Host-Pathogen Interactions/physiology , Plant Immunity , Pseudomonas syringae/pathogenicity , Type III Secretion Systems/physiology , Volatile Organic Compounds/metabolism , Air , Capsicum/physiology , Cucumis sativus/physiology , Gene Expression Regulation, Plant , Octanols/pharmacology , Phaseolus/physiology , Plant Immunity/drug effects , Signal Transduction , Nicotiana/physiology , Volatile Organic Compounds/pharmacology
14.
Int J Mol Sci ; 23(3)2022 Jan 25.
Article in English | MEDLINE | ID: mdl-35163275

ABSTRACT

Rice plants contain high basal levels of salicylic acid (SA), but some of their functions remain elusive. To elucidate the importance of SA homeostasis in rice immunity, we characterized four rice SA hydroxylase genes (OsSAHs) and verified their roles in SA metabolism and disease resistance. Recombinant OsSAH proteins catalyzed SA in vitro, while OsSAH3 protein showed only SA 5-hydroxylase (SA5H) activity, which was remarkably higher than that of other OsSAHs that presented both SA3H and SA5H activities. Amino acid substitutions revealed that three amino acids in the binding pocket affected SAH enzyme activity and/or specificity. Knockout OsSAH2 and OsSAH3 (sahKO) genes conferred enhanced resistance to both hemibiotrophic and necrotrophic pathogens, whereas overexpression of each OsSAH gene increased susceptibility to the pathogens. sahKO mutants showed increased SA and jasmonate levels compared to those of the wild type and OsSAH-overexpressing plants. Analysis of the OsSAH3 promoter indicated that its induction was mainly restricted around Magnaporthe oryzae infection sites. Taken together, our findings indicate that SA plays a vital role in immune signaling. Moreover, fine-tuning SA homeostasis through suppression of SA metabolism is an effective approach in studying broad-spectrum disease resistance in rice.


Subject(s)
Disease Resistance/physiology , Oryza/genetics , Salicylic Acid/metabolism , China , Cyclopentanes , Dioxygenases , Gene Expression/genetics , Gene Expression Regulation, Plant/drug effects , Gene Expression Regulation, Plant/genetics , Hydroxylation , Oryza/drug effects , Oryza/metabolism , Oxylipins , Plant Diseases/genetics , Plant Immunity/drug effects , Plant Immunity/physiology , Plant Proteins/genetics , Plants, Genetically Modified/metabolism , Salicylic Acid/pharmacology
15.
Plant Mol Biol ; 106(1-2): 123-143, 2021 May.
Article in English | MEDLINE | ID: mdl-33713297

ABSTRACT

Plants utilize a plethora of peptide signals to regulate their immune response. Peptide ligands and their cognate receptors involved in immune signaling share common motifs among many species of vascular plants. However, the origin and evolution of immune peptides is still poorly understood. Here, we searched for genes encoding small secreted peptides in the genomes of three bryophyte lineages-mosses, liverworts and hornworts-that occupy a critical position in the study of land plant evolution. We found that bryophytes shared common predicted small secreted peptides (SSPs) with vascular plants. The number of SSPs is higher in the genomes of mosses than in both the liverwort Marchantia polymorpha and the hornwort Anthoceros sp. The synthetic peptide elicitors-AtPEP and StPEP-specific for vascular plants, triggered ROS production in the protonema of the moss Physcomitrella patens, suggesting the possibility of recognizing peptide ligands from angiosperms by moss receptors. Mass spectrometry analysis of the moss Physcomitrella patens, both the wild type and the Δcerk mutant secretomes, revealed peptides that specifically responded to chitosan treatment, suggesting their role in immune signaling.


Subject(s)
Bryopsida/immunology , Bryopsida/metabolism , Peptides/metabolism , Plant Immunity , Signal Transduction , Amino Acid Sequence , Bryopsida/drug effects , Bryopsida/genetics , Chitosan/pharmacology , Genome, Plant , Peptides/chemistry , Plant Immunity/drug effects , Reactive Oxygen Species/metabolism , Signal Transduction/drug effects
16.
BMC Biotechnol ; 21(1): 12, 2021 02 03.
Article in English | MEDLINE | ID: mdl-33536000

ABSTRACT

BACKGROUND: Lyso-phosphatidylethanolamine (LPE) is a natural phospholipid that functions in the early stages of plant senescence. Plant innate immunity and early leaf senescence share molecular components. To reveal conserved mechanisms that link-up both processes, we tried to unravel to what extent LPE coordinates defense response and by what mode of action. RESULT: We found that LPE-treatment induces signaling and biosynthesis gene expression of the defensive hormone salicylic acid (SA). However, jasmonic acid and ethylene triggered gene induction levels are indistinguishable from the control. In accordance with gene induction for SA, oxidative stress, and reactive oxygen species (ROS) production, we detected raised in-situ hydrogen peroxide levels following LPE-application. Yet, ROS-burst assays of LPE-pretreated plants revealed a reduced release of ROS after PAMP-administration suggesting that LPE interferes with an oxidative burst. Our data refer to a priming effect of LPE on SA/ROS-associated genomic loci that encode pivotal factors in early senescence and considerably improve plant basal immunity. Thus, we challenged Arabidopsis thaliana with the hemibiotrophic pathogen Pseudomonas syringae. Consistently, we found an increased resistance in the LPE-pretreated Arabidopsis plants compared to the mock-pretreated control. CONCLUSIONS: Our results underscore a beneficial effect of LPE on plant innate immunity against hemibiotrophs. Given the resistance-promoting effect of exogenously applied LPE, this bio-agent bears the potential of being applied as a valuable tool for the genetic activation of defense-associated traits.


Subject(s)
Gene Expression Regulation, Plant/drug effects , Lysophospholipids/pharmacology , Plant Diseases/immunology , Plant Immunity/drug effects , Plant Immunity/genetics , Arabidopsis/genetics , Arabidopsis/immunology , Arabidopsis Proteins , Cyclopentanes , Ethylenes , Genes, Plant , Oxylipins , Pseudomonas syringae , Salicylic Acid/metabolism , Signal Transduction/drug effects , Signal Transduction/genetics
17.
Development ; 145(19)2018 10 01.
Article in English | MEDLINE | ID: mdl-30228101

ABSTRACT

The plant transmembrane receptor kinase FLAGELLIN SENSING 2 (FLS2) is crucial for innate immunity. Although previous studies have reported FLS2-mediated signal transduction and endocytosis via the clathrin-mediated pathway, whether additional endocytic pathways affect FLS2-mediated defense responses remains unclear. Here, we show that the Arabidopsis thaliana sterol-deficient mutant steroid methyltransferase 1 displays defects in immune responses induced by the flagellin-derived peptide flg22. Variable-angle total internal reflection fluorescence microscopy (VA-TIRFM) coupled with single-particle tracking showed that the spatiotemporal dynamics of FLS2-GFP changed on a millisecond time scale and that the FLS2-GFP dwell time at the plasma membrane increased in cells treated with a sterol-extracting reagent when compared with untreated counterparts. We further demonstrate that flg22-induced FLS2 clustering and endocytosis involves the sterol-associated endocytic pathway, which is distinct from the clathrin-mediated pathway. Moreover, flg22 enhanced the colocalization of FLS2-GFP with the membrane microdomain marker Flot 1-mCherry and FLS2 endocytosis via the sterol-associated pathway. This indicates that plants may respond to pathogen attacks by regulating two different endocytic pathways. Taken together, our results suggest the key role of sterol homeostasis in flg22-induced plant defense responses.


Subject(s)
Arabidopsis/cytology , Arabidopsis/immunology , Endocytosis , Flagellin/pharmacology , Sterols/metabolism , Arabidopsis/drug effects , Arabidopsis Proteins/metabolism , Cell Membrane/drug effects , Cell Membrane/metabolism , Clathrin/metabolism , Endocytosis/drug effects , Green Fluorescent Proteins/metabolism , Methyltransferases/metabolism , Mutation/genetics , Plant Epidermis/cytology , Plant Immunity/drug effects , Plants, Genetically Modified , Protein Aggregates , Protein Kinases/metabolism , Protein Multimerization
18.
Plant Physiol ; 182(2): 1052-1065, 2020 02.
Article in English | MEDLINE | ID: mdl-31806735

ABSTRACT

Plasma membrane (PM) depolarization functions as an initial step in plant defense signaling pathways. However, only a few ion channels/transporters have been characterized in the context of plant immunity. Here, we show that the Arabidopsis (Arabidopsis thaliana) Na+:K+:2Cl- (NKCC) cotransporter CCC1 has a dual function in plant immunity. CCC1 functions independently of PM depolarization and negatively regulates pathogen-associated molecular pattern-triggered immunity. However, CCC1 positively regulates plant basal and effector-triggered resistance to Pseudomonas syringae pv. tomato (Pst) DC3000. In line with the compromised immunity to Pst DC3000, ccc1 mutants show reduced expression of genes encoding enzymes involved in the biosynthesis of antimicrobial peptides, camalexin, and 4-OH-ICN, as well as pathogenesis-related proteins. Moreover, genes involved in cell wall and cuticle biosynthesis are constitutively down-regulated in ccc1 mutants, and the cell walls of these mutants exhibit major changes in monosaccharide composition. The role of CCC1 ion transporter activity in the regulation of plant immunity is corroborated by experiments using the specific NKCC inhibitor bumetanide. These results reveal a function for ion transporters in immunity-related cell wall fortification and antimicrobial biosynthesis.


Subject(s)
Arabidopsis Proteins/metabolism , Arabidopsis/immunology , Disease Resistance/genetics , Pseudomonas syringae/immunology , Solute Carrier Family 12, Member 2/genetics , Arabidopsis/drug effects , Arabidopsis/genetics , Arabidopsis/microbiology , Arabidopsis Proteins/genetics , Bumetanide/pharmacology , Cell Membrane/genetics , Cell Membrane/metabolism , Cell Membrane/physiology , Cell Wall/chemistry , Cell Wall/genetics , Cell Wall/metabolism , Disease Resistance/immunology , Gene Expression Profiling , Indoles/metabolism , Monosaccharides/chemistry , Monosaccharides/metabolism , Mutation , Pathogen-Associated Molecular Pattern Molecules/metabolism , Plant Diseases/genetics , Plant Diseases/immunology , Plant Diseases/microbiology , Plant Immunity/drug effects , Plant Immunity/genetics , Plant Leaves/drug effects , Plant Leaves/genetics , Plant Leaves/immunology , Plant Leaves/microbiology , Plants, Genetically Modified/metabolism , Pseudomonas syringae/drug effects , Pseudomonas syringae/pathogenicity , RNA-Seq , Sodium Potassium Chloride Symporter Inhibitors/pharmacology , Sodium-Potassium-Chloride Symporters/metabolism , Solute Carrier Family 12, Member 2/immunology , Solute Carrier Family 12, Member 2/metabolism , Thiazoles/metabolism
19.
Mar Drugs ; 19(2)2021 Jan 25.
Article in English | MEDLINE | ID: mdl-33504049

ABSTRACT

Sustainable agricultural practices increasingly demand novel, environmentally friendly compounds which induce plant immunity against pathogens. Stimulating plant immunity using seaweed extracts is a highly viable strategy, as these formulations contain many bio-elicitors (phyco-elicitors) which can significantly boost natural plant immunity. Certain bioactive elicitors present in a multitude of extracts of seaweeds (both commercially available and bench-scale laboratory formulations) activate pathogen-associated molecular patterns (PAMPs) due to their structural similarity (i.e., analogous structure) with pathogen-derived molecules. This is achieved via the priming and/or elicitation of the defense responses of the induced systemic resistance (ISR) and systemic acquired resistance (SAR) pathways. Knowledge accumulated over the past few decades is reviewed here, aiming to explain why certain seaweed-derived bioactives have such tremendous potential to elicit plant defense responses with considerable economic significance, particularly with increasing biotic stress impacts due to climate change and the concomitant move to sustainable agriculture and away from synthetic chemistry and environmental damage. Various extracts of seaweeds display remarkably different modes of action(s) which can manipulate the plant defense responses when applied. This review focuses on both the similarities and differences amongst the modes of actions of several different seaweed extracts, as well as their individual components. Novel biotechnological approaches for the development of new commercial products for crop protection, in a sustainable manner, are also suggested.


Subject(s)
Biological Products/pharmacology , Immunity, Innate/drug effects , Plant Diseases/prevention & control , Plant Immunity/drug effects , Seaweed , Animals , Biological Products/isolation & purification , Biological Products/therapeutic use , Humans , Immunity, Innate/physiology , Plant Diseases/immunology , Plant Immunity/physiology , Seaweed/isolation & purification
20.
Int J Mol Sci ; 22(21)2021 Oct 21.
Article in English | MEDLINE | ID: mdl-34768793

ABSTRACT

Botany-derived antimicrobial peptides (BAMPs), a class of small, cysteine-rich peptides produced in plants, are an important component of the plant immune system. Both in vivo and in vitro experiments have demonstrated their powerful antimicrobial activity. Besides in plants, BAMPs have cross-kingdom applications in human health, with toxic and/or inhibitory effects against a variety of tumor cells and viruses. With their diverse molecular structures, broad-spectrum antimicrobial activity, multiple mechanisms of action, and low cytotoxicity, BAMPs provide ideal backbones for drug design, and are potential candidates for plant protection and disease treatment. Lots of original research has elucidated the properties and antimicrobial mechanisms of BAMPs, and characterized their surface receptors and in vivo targets in pathogens. In this paper, we review and introduce five kinds of representative BAMPs belonging to the pathogenesis-related protein family, dissect their antifungal, antiviral, and anticancer mechanisms, and forecast their prospects in agriculture and global human health. Through the deeper understanding of BAMPs, we provide novel insights for their applications in broad-spectrum and durable plant disease prevention and control, and an outlook on the use of BAMPs in anticancer and antiviral drug design.


Subject(s)
Antimicrobial Peptides/genetics , Antimicrobial Peptides/metabolism , Antimicrobial Peptides/pharmacology , Agriculture , Anti-Infective Agents/pharmacology , Antimicrobial Cationic Peptides/pharmacology , Antiviral Agents/pharmacology , Drug Design/methods , Humans , Plant Immunity/drug effects , Plants/drug effects , Viruses/drug effects
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