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1.
Nat Plants ; 9(12): 2085-2094, 2023 12.
Article in English | MEDLINE | ID: mdl-38049516

ABSTRACT

Plant signalling peptides are typically released from larger precursors by proteolytic cleavage to regulate plant growth, development and stress responses. Recent studies reported the characterization of a divergent family of Brassicaceae-specific peptides, SERINE RICH ENDOGENOUS PEPTIDES (SCOOPs), and their perception by the leucine-rich repeat receptor kinase MALE DISCOVERER 1-INTERACTING RECEPTOR-LIKE KINASE 2 (MIK2). Here, we reveal that the SCOOP family is highly expanded, containing at least 50 members in the Columbia-0 reference Arabidopsis thaliana genome. Notably, perception of these peptides is strictly MIK2-dependent. How bioactive SCOOP peptides are produced, and to what extent their perception is responsible for the multiple physiological roles associated with MIK2 are currently unclear. Using N-terminomics, we validate the N-terminal cleavage site of representative PROSCOOPs. The cleavage sites are determined by conserved motifs upstream of the minimal SCOOP bioactive epitope. We identified subtilases necessary and sufficient to process PROSCOOP peptides at conserved cleavage motifs. Mutation of these subtilases, or their recognition motifs, suppressed PROSCOOP cleavage and associated overexpression phenotypes. Furthermore, we show that higher-order mutants of these subtilases show phenotypes reminiscent of mik2 null mutant plants, consistent with impaired PROSCOOP biogenesis, and demonstrating biological relevance of SCOOP perception by MIK2. Together, this work provides insights into the molecular mechanisms underlying the functions of the recently identified SCOOP peptides and their receptor MIK2.


Subject(s)
Arabidopsis Proteins , Arabidopsis , Brassicaceae , Arabidopsis Proteins/genetics , Serine , Arabidopsis/physiology , Peptides , Protein Kinases/genetics , Receptors, Cell Surface/genetics
2.
PLoS Pathog ; 19(1): e1011072, 2023 01.
Article in English | MEDLINE | ID: mdl-36656837

ABSTRACT

Plants perceive the presence of insect eggs deposited on leaves as a cue of imminent herbivore attack. Consequential plant signaling events include the accumulation of salicylic acid and reactive oxygen species, transcriptional reprogramming, and cell death. Interestingly, egg-induced innate immunity shows similarities with immune responses triggered upon recognition of microbial pathogens, and in recent years, it became apparent that egg perception affects plant-microbe interactions. Here, we highlight recent findings on insect egg-induced innate immunity and how egg-mediated signaling impacts plant-microbe interactions. Ecological considerations beg the question: Who benefits from egg perception in these complex interactions?


Subject(s)
Insecta , Plants , Animals , Insecta/physiology , Immunity, Innate , Plant Immunity
3.
J Exp Bot ; 73(16): 5358-5360, 2022 09 12.
Article in English | MEDLINE | ID: mdl-36095661

ABSTRACT

This article comments on: Batyrshina ZS, Shavit R, Yaakov B, Bocobza S, Tzin V. 2022. The transcription factor gene TaMYB31 regulates the benzoxazinoid biosynthetic pathway in wheat. Journal of Experimental Botany73, 5634-5649. Benzoxazinoids (BXDs) are abundant indole-derived specialized metabolites in several monocot crop species, such as wheat, maize, and rye. They function in plant immunity against herbivorous arthropods and fungal pathogens, but also as iron chelators, in metal tolerance, and as allelochemicals. Although BXD biosynthetic pathways have been studied extensively and are well described, information about the transcriptional regulation of BXD biosynthesis is scarce. In the current issue of JXB, Batyrshina et al. (2022) identified the transcription factor gene TaMYB31 in the tetraploid wheat Triticum turgidum and verified its function as a component of BXD metabolism in the hexaploid wheat Triticum aestivum, where it regulates constitutive and stress-inducible BXD biosynthesis.


Subject(s)
Benzoxazines , Triticum , Benzoxazines/metabolism , Gene Expression Regulation, Plant , Tetraploidy , Transcription Factors/genetics , Transcription Factors/metabolism , Triticum/physiology
4.
Front Plant Sci ; 13: 852808, 2022.
Article in English | MEDLINE | ID: mdl-35401621

ABSTRACT

Initiation of plant immune signaling requires recognition of conserved molecular patterns from microbes and herbivores by plasma membrane-localized pattern recognition receptors. Additionally, plants produce and secrete numerous small peptide hormones, termed phytocytokines, which act as secondary danger signals to modulate immunity. In Arabidopsis, the Brassicae-specific SERINE RICH ENDOGENOUS PEPTIDE (SCOOP) family consists of 14 members that are perceived by the leucine-rich repeat receptor kinase MALE DISCOVERER 1-INTERACTING RECEPTOR LIKE KINASE 2 (MIK2). Recognition of SCOOP peptides elicits generic early signaling responses but knowledge on how and if SCOOPs modulate specific downstream immune defenses is limited. We report here that depletion of MIK2 or the single PROSCOOP12 precursor results in decreased Arabidopsis resistance against the generalist herbivore Spodoptera littoralis but not the specialist Pieris brassicae. Increased performance of S. littoralis on mik2-1 and proscoop12 is accompanied by a diminished accumulation of jasmonic acid, jasmonate-isoleucine and indolic glucosinolates. Additionally, we show transcriptional activation of the PROSCOOP gene family in response to insect herbivory. Our data therefore indicate that perception of endogenous SCOOP peptides by MIK2 modulates the jasmonate pathway and thereby contributes to enhanced defense against a generalist herbivore.

5.
New Phytol ; 232(6): 2491-2505, 2021 12.
Article in English | MEDLINE | ID: mdl-34510462

ABSTRACT

Plants are able to detect insect eggs deposited on leaves. In Arabidopsis, eggs of the butterfly species Pieris brassicae (common name large white) induce plant defenses and activate the salicylic acid (SA) pathway. We previously discovered that oviposition triggers a systemic acquired resistance (SAR) against the bacterial hemibiotroph pathogen Pseudomonas syringae. Here, we show that insect eggs or treatment with egg extract (EE) induce SAR against the fungal necrotroph Botrytis cinerea BMM and the oomycete pathogen Hyaloperonospora arabidopsidis Noco2. This response is abolished in ics1, ald1 and fmo1, indicating that the SA pathway and the N-hydroxypipecolic acid (NHP) pathway are involved. Establishment of EE-induced SAR in distal leaves potentially involves tryptophan-derived metabolites, including camalexin. Indeed, SAR is abolished in the biosynthesis mutants cyp79B2 cyp79B3, cyp71a12 cyp71a13 and pad3-1, and camalexin is toxic to B. cinerea in vitro. This study reveals an interesting mechanism by which lepidopteran eggs interfere with plant-pathogen interactions.


Subject(s)
Arabidopsis Proteins , Oomycetes , Animals , Arabidopsis Proteins/metabolism , Gene Expression Regulation, Plant , Insecta/metabolism , Oomycetes/metabolism , Plant Diseases , Pseudomonas syringae/metabolism , Salicylic Acid
6.
Plant Physiol ; 185(1): 240-255, 2021 02 25.
Article in English | MEDLINE | ID: mdl-33631806

ABSTRACT

In Arabidopsis (Arabidopsis thaliana), a hypersensitive-like response (HR-like response) is triggered underneath the eggs of the large white butterfly Pieris brassicae (P. brassicae), and this response is dependent on salicylic acid (SA) accumulation and signaling. Previous reports indicate that the clade I L-type LECTIN RECEPTOR KINASE-I.8 (LecRK-I.8) is involved in early steps of egg recognition. A genome-wide association study was used to better characterize the genetic structure of the HR-like response and discover loci that contribute to this response. We report here the identification of LecRK-I.1, a close homolog of LecRK-I.8, and show that two main haplotypes that explain part of the variation in HR-like response segregate among natural Arabidopsis accessions. Besides, signatures of balancing selection at this locus suggest that it may be ecologically important. Disruption of LecRK-I.1 results in decreased HR-like response and SA signaling, indicating that this protein is important for the observed responses. Furthermore, we provide evidence that LecRK-I.1 functions in the same signaling pathway as LecRK-I.8. Altogether, our results show that the response to eggs of P. brassicae is controlled by multiple LecRKs.


Subject(s)
Arabidopsis Proteins/genetics , Arabidopsis Proteins/immunology , Cell Death/genetics , Cell Death/immunology , Plant Immunity/genetics , Plant Immunity/immunology , Protein Serine-Threonine Kinases/immunology , Animals , Arabidopsis/genetics , Arabidopsis/immunology , Gene Expression Regulation, Plant , Genes, Plant , Insecta/parasitology , Ovum
7.
Elife ; 92020 09 28.
Article in English | MEDLINE | ID: mdl-32985977

ABSTRACT

Recognition of conserved microbial molecules activates immune responses in plants, a process termed pattern-triggered immunity (PTI). Similarly, insect eggs trigger defenses that impede egg development or attract predators, but information on the nature of egg-associated elicitors is scarce. We performed an unbiased bioactivity-guided fractionation of eggs of the butterfly Pieris brassicae. Nuclear magnetic resonance (NMR) spectroscopy and mass spectrometry of active fractions led to the identification of phosphatidylcholines (PCs). PCs are released from insect eggs, and they induce salicylic acid and H2O2 accumulation, defense gene expression and cell death in Arabidopsis, all of which constitute a hallmark of PTI. Active PCs contain primarily C16 to C18-fatty acyl chains with various levels of desaturation, suggesting a relatively broad ligand specificity of cell-surface receptor(s). The finding of PCs as egg-associated molecular patterns (EAMPs) illustrates the acute ability of plants to detect conserved immunogenic patterns from their enemies, even from seemingly passive structures such as eggs.


Subject(s)
Arabidopsis , Butterflies/metabolism , Ovum/chemistry , Phosphatidylcholines , Animals , Arabidopsis/drug effects , Arabidopsis/immunology , Larva/chemistry , Phosphatidylcholines/immunology , Phosphatidylcholines/metabolism , Phosphatidylcholines/pharmacology
8.
Plant Physiol ; 181(3): 1008-1028, 2019 11.
Article in English | MEDLINE | ID: mdl-31515446

ABSTRACT

Tocopherols are lipid-soluble antioxidants synthesized in plastids of plants and other photosynthetic organisms. The four known tocopherols, α-, ß-, γ-, and δ-tocopherol, differ in number and position of methyl groups on their chromanol head group. In unstressed Arabidopsis (Arabidopsis thaliana) leaves, α-tocopherol constitutes the main tocopherol form, whereas seeds predominantly contain γ-tocopherol. Here, we show that inoculation of Arabidopsis leaves with the bacterial pathogen Pseudomonas syringae induces the expression of genes involved in early steps of tocopherol biosynthesis and triggers strong accumulation of γ-tocopherol, moderate production of δ-tocopherol, and generation of the benzoquinol precursors of tocopherols. The pathogen-inducible biosynthesis of tocopherols is promoted by the immune regulators ENHANCED DISEASE SUSCEPTIBILITY1 and PHYTOALEXIN-DEFICIENT4. In addition, tocopherols accumulate in response to bacterial flagellin and reactive oxygen species. By quantifying tocopherol forms in inoculated wild-type plants and biosynthetic pathway mutants, we provide biochemical insights into the pathogen-inducible tocopherol pathway. Notably, vitamin E deficient2 (vte2) mutant plants, which are compromised in both tocopherol and benzoquinol precursor accumulation, exhibit increased susceptibility toward compatible P. syringae and possess heightened levels of markers of lipid peroxidation after bacterial infection. The deficiency of triunsaturated fatty acids in vte2-1 fatty acid desaturase3-2 (fad3-2) fad7-2 fad8 quadruple mutants prevents increased lipid peroxidation in the vte2 background and restores pathogen resistance to wild-type levels. Therefore, the tocopherol biosynthetic pathway positively influences salicylic acid accumulation and guarantees effective basal resistance of Arabidopsis against compatible P. syringae, possibly by protecting leaves from the pathogen-induced oxidation of trienoic fatty acid-containing lipids.


Subject(s)
Arabidopsis Proteins/metabolism , Arabidopsis/metabolism , Tocopherols/metabolism , Arabidopsis/microbiology , Arabidopsis Proteins/genetics , Carboxylic Ester Hydrolases/genetics , Carboxylic Ester Hydrolases/metabolism , DNA-Binding Proteins/genetics , DNA-Binding Proteins/metabolism , Gene Expression Regulation, Plant/genetics , Gene Expression Regulation, Plant/physiology , Plant Immunity/genetics , Plant Immunity/physiology , Plant Leaves/genetics , Plant Leaves/metabolism , Pseudomonas syringae/pathogenicity
9.
Front Plant Sci ; 10: 623, 2019.
Article in English | MEDLINE | ID: mdl-31134123

ABSTRACT

Plants induce defense responses after insect egg deposition, but very little is known about the perception mechanisms. In Arabidopsis thaliana, eggs of the specialist insect Pieris brassicae trigger accumulation of reactive oxygen species (ROS) and salicylic acid (SA), followed by induction of defense genes and localized necrosis. Here, the involvement of the clade I L-type lectin receptor kinase LecRK-I.8 in these responses was studied. Expression of LecRK-I.8 was upregulated at the site of P. brassicae oviposition and egg extract (EE) treatment. ROS, SA, cell death, and expression of PR1 were substantially reduced in the Arabidopsis knock-out mutant lecrk-I.8 after EE treatment. In addition, EE-induced systemic resistance against Pseudomonas syringae was abolished in lecrk-I.8. Expression of ten clade I homologs of LecRK-I.8 was also induced by EE treatment, but single mutants displayed only weak alteration of EE-induced PR1 expression. These results demonstrate that LecRK-I.8 is an early component of egg perception.

10.
Mol Plant Microbe Interact ; 31(3): 344-355, 2018 03.
Article in English | MEDLINE | ID: mdl-29130376

ABSTRACT

We isolated previously several Arabidopsis thaliana mutants with constitutive expression of the early microbe-associated molecular pattern-induced gene ATL2, named eca (expresión constitutiva de ATL2). Here, we further explored the interaction of eca mutants with pest and pathogens. Of all eca mutants, eca2 was more resistant to a fungal pathogen (Botrytis cinerea) and a bacterial pathogen (Pseudomonas syringae) as well as to a generalist herbivorous insect (Spodoptera littoralis). Permeability of the cuticle is increased in eca2; chemical characterization shows that eca2 has a significant reduction of both cuticular wax and cutin. Additionally, we determined that eca2 did not display a similar compensatory transcriptional response, compared with a previously characterized cuticular mutant, and that resistance to B. cinerea is mediated by the priming of the early and late induced defense responses, including salicylic acid- and jasmonic acid-induced genes. These results suggest that ECA2-dependent responses are involved in the nonhost defense mechanism against biotrophic and necrotrophic pathogens and against a generalist insect by modulation and priming of innate immunity and late defense responses. Making eca2 an interesting model to characterize the molecular basis for plant defenses against different biotic interactions and to study the initial events that take place in the cuticle surface of the aerial organs.


Subject(s)
Arabidopsis Proteins/genetics , Arabidopsis/immunology , Arabidopsis/microbiology , DNA-Binding Proteins/genetics , Herbivory , Insecta/physiology , Mutation/genetics , Plant Epidermis/metabolism , Animals , Arabidopsis/genetics , Arabidopsis/parasitology , Arabidopsis Proteins/metabolism , Botrytis/physiology , Cyclopentanes , DNA, Plant/metabolism , DNA-Binding Proteins/metabolism , Disease Resistance , Gene Expression Profiling , Gene Expression Regulation, Plant , Genome, Plant , Membrane Lipids , Models, Biological , Oxylipins , Plant Diseases/genetics , Plant Diseases/immunology , Plant Diseases/microbiology , Plant Diseases/parasitology , Pseudomonas syringae/physiology , Waxes
11.
Plant J ; 93(4): 703-728, 2018 02.
Article in English | MEDLINE | ID: mdl-29160609

ABSTRACT

Herbivorous arthropods have interacted with plants for millions of years. During feeding they release chemical cues that allow plants to detect the attack and mount an efficient defense response. A signaling cascade triggers the expression of hundreds of genes, which encode defensive proteins and enzymes for synthesis of toxic metabolites. This direct defense is often complemented by emission of volatiles that attract beneficial parasitoids. In return, arthropods have evolved strategies to interfere with plant defenses, either by producing effectors to inhibit detection and downstream signaling steps, or by adapting to their detrimental effect. In this review, we address the current knowledge on the molecular and chemical dialog between plants and herbivores, with an emphasis on co-evolutionary aspects.


Subject(s)
Arthropods/physiology , Herbivory/physiology , Plant Physiological Phenomena , Animals , Biological Evolution , Insecta/physiology , Phytoplasma/virology , Plant Proteins/metabolism , Plants/chemistry , Plants/metabolism , Receptors, Pattern Recognition/metabolism
12.
Mol Plant ; 9(5): 662-681, 2016 05 02.
Article in English | MEDLINE | ID: mdl-26802249

ABSTRACT

Tryptophan-derived, indolic metabolites possess diverse functions in Arabidopsis innate immunity to microbial pathogen infection. Here, we investigate the functional role and regulatory characteristics of indolic metabolism in Arabidopsis systemic acquired resistance (SAR) triggered by the bacterial pathogen Pseudomonas syringae. Indolic metabolism is broadly activated in both P. syringae-inoculated and distant, non-inoculated leaves. At inoculation sites, camalexin, indol-3-ylmethylamine (I3A), and indole-3-carboxylic acid (ICA) are the major accumulating compounds. Camalexin accumulation is positively affected by MYB122, and the cytochrome P450 genes CYP81F1 and CYP81F2. Local I3A production, by contrast, occurs via indole glucosinolate breakdown by PEN2- dependent and independent pathways. Moreover, exogenous application of the defense hormone salicylic acid stimulates I3A generation at the expense of its precursor indol-3-ylmethylglucosinolate (I3M), and the SAR regulator pipecolic acid primes plants for enhanced P. syringae-induced activation of distinct branches of indolic metabolism. In uninfected systemic tissue, the metabolic response is more specific and associated with enhanced levels of the indolics I3A, ICA, and indole-3-carbaldehyde (ICC). Systemic indole accumulation fully depends on functional CYP79B2/3, PEN2, and MYB34/51/122, and requires functional SAR signaling. Genetic analyses suggest that systemically elevated indoles are dispensable for SAR and associated systemic increases of salicylic acid. However, soil-grown but not hydroponically -cultivated cyp79b2/3 and pen2 plants, both defective in indolic secondary metabolism, exhibit pre-induced immunity, which abrogates their intrinsic ability to induce SAR.


Subject(s)
Plant Diseases/microbiology , Arabidopsis/metabolism , Arabidopsis/microbiology , Disease Resistance/genetics , Disease Resistance/physiology , Gene Expression Regulation, Plant/genetics , Gene Expression Regulation, Plant/physiology , Immunity, Innate/genetics , Immunity, Innate/physiology , Indoles/metabolism , Plant Diseases/genetics , Pseudomonas syringae/pathogenicity , Thiazoles/metabolism
13.
Mol Plant ; 7(7): 1191-210, 2014 Jul.
Article in English | MEDLINE | ID: mdl-24908268

ABSTRACT

Hydrogen peroxide (H2O2) operates as a signaling molecule in eukaryotes, but the specificity of its signaling capacities remains largely unrevealed. Here, we analyzed whether a moderate production of H2O2 from two different plant cellular compartments has divergent effects on the plant transcriptome. Arabidopsis thaliana overexpressing glycolate oxidase in the chloroplast (Fahnenstich et al., 2008; Balazadeh et al., 2012) and plants deficient in peroxisomal catalase (Queval et al., 2007; Inzé et al., 2012) were grown under non-photorespiratory conditions and then transferred to photorespiratory conditions to foster the production of H2O2 in both organelles. We show that H2O2 originating in a specific organelle induces two types of responses: one that integrates signals independently from the subcellular site of H2O2 production and another that is dependent on the H2O2 production site. H2O2 produced in peroxisomes induces transcripts involved in protein repair responses, while H2O2 produced in chloroplasts induces early signaling responses, including transcription factors and biosynthetic genes involved in production of secondary signaling messengers. There is a significant bias towards the induction of genes involved in responses to wounding and pathogen attack by chloroplastic-produced H2O2, including indolic glucosinolates-, camalexin-, and stigmasterol-biosynthetic genes. These transcriptional responses were accompanied by the accumulation of 4-methoxy-indol-3-ylmethyl glucosinolate and stigmasterol.


Subject(s)
Arabidopsis/cytology , Arabidopsis/metabolism , Chloroplasts/metabolism , Hydrogen Peroxide/metabolism , Peroxisomes/metabolism , Transcriptome , Arabidopsis/drug effects , Arabidopsis/genetics , Carbon Dioxide/pharmacology , Chloroplasts/drug effects , Genome, Plant/genetics , Kinetics , Metabolomics , Peroxisomes/drug effects , Plants, Genetically Modified , Stigmasterol/metabolism , Transcriptome/drug effects , Tryptophan/metabolism
14.
Plant Signal Behav ; 8(11): e26366, 2013 Nov.
Article in English | MEDLINE | ID: mdl-24025239

ABSTRACT

Distinct amino acid metabolic pathways constitute integral parts of the plant immune system. We have recently identified pipecolic acid (Pip), a lysine-derived non-protein amino acid, as a critical regulator of systemic acquired resistance (SAR) and basal immunity to bacterial infection in Arabidopsis thaliana. In Arabidopsis, Pip acts as an endogenous mediator of defense amplification and priming. For instance, Pip conditions plants for effective biosynthesis of the phenolic defense signal salicylic acid (SA), accumulation of the phytoalexin camalexin, and expression of defense-related genes. Here, we show that tobacco plants respond to leaf infection by the compatible bacterial pathogen Pseudomonas syringae pv tabaci (Pstb) with a significant accumulation of several amino acids, including Lys, branched-chain, aromatic, and amide group amino acids. Moreover, Pstb strongly triggers, alongside the biosynthesis of SA and increases in the defensive alkaloid nicotine, the production of the Lys catabolites Pip and α-aminoadipic acid. Exogenous application of Pip to tobacco plants provides significant protection to infection by adapted Pstb or by non-adapted, hypersensitive cell death-inducing P. syringae pv maculicola. Pip thereby primes tobacco for rapid and strong accumulation of SA and nicotine following bacterial infection. Thus, our study indicates that the role of Pip as an amplifier of immune responses is conserved between members of the rosid and asterid groups of eudicot plants and suggests a broad practical applicability for Pip as a natural enhancer of plant disease resistance.


Subject(s)
Disease Resistance/drug effects , Nicotiana/immunology , Nicotine/metabolism , Pipecolic Acids/pharmacology , Plant Diseases/microbiology , Pseudomonas syringae/physiology , Salicylic Acid/metabolism , 2-Aminoadipic Acid/metabolism , Amines/metabolism , Amino Acids/metabolism , Plant Diseases/immunology , Plant Leaves/drug effects , Plant Leaves/metabolism , Plant Leaves/microbiology , Plant Roots/drug effects , Plant Roots/metabolism , Pseudomonas syringae/drug effects , Time Factors , Nicotiana/drug effects , Nicotiana/microbiology
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