Plant elicitor peptides are conserved signals regulating direct and indirect antiherbivore defense (original) (raw)
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Phytohormone-based activity mapping of insect herbivore-produced elicitors
Proceedings of The National Academy of Sciences, 2009
In response to insect attack, many plants exhibit dynamic biochemical changes, resulting in the induced production of direct and indirect defenses. Elicitors present in herbivore oral secretions are believed to positively regulate many inducible plant defenses; however, little is known about the specificity of elicitor recognition in plants. To investigate the phylogenic distribution of elicitor activity, we tested representatives from three different elicitor classes on the time course of defense-related phytohormone production, including ethylene (E), jasmonic acid (JA), and salicylic acid, in a range of plant species spanning angiosperm diversity. All families examined responded to at least one elicitor class with significant increases in E and JA production within 1 to 2 h after treatment, yet elicitation activity among species was highly idiosyncratic. The fatty-acid amino acid conjugate volicitin exhibited the widest range of phytohormone and volatile inducing activity, which spanned maize (Zea mays), soybean (Glycine max), and eggplant (Solanum melongena). In contrast, the activity of inceptinrelated peptides, originally described in cowpea (Vigna unguiculata), was limited even within the Fabaceae. Similarly, caeliferin A16:0, a disulfooxy fatty acid from grasshoppers, was the only elicitor with demonstrable activity in Arabidopsis thaliana. Although precise mechanisms remain unknown, the unpredictable nature of elicitor activity between plant species supports the existence of specific receptor-ligand interactions mediating recognition. Despite the lack of an ideal plant model for studying the action of numerous elicitors, E and JA exist as highly conserved and readily quantifiable markers for future discoveries in this field. ethylene ͉ insect elicitor ͉ jasmonic acid ͉ plant defense ͉ volatile organic compound This article contains supporting information online at www.pnas.org/cgi/content/full/ 0811861106/DCSupplemental.
The Plant Journal, 2020
Plant Elicitor Peptides (Peps) are conserved regulators of defense responses and models for the study of Damage-Associated Molecular Pattern (DAMP)-induced immunity. Although present as multigene families in most species, the functional relevance of these multigene families remains largely undefined. While Arabidopsis Peps appear largely redundant in function, previous work examining Pep-induced responses in maize implied specificity of function. To better define function of individual ZmPeps and their cognate ZmPEPR receptors, activities were examined by assessing changes in defense-associated phytohormones, specialized metabolites and global gene expression patterns, in combination with heterologous expression assays and analyses of CRISPR/Cas9-generated knockout plants. Beyond simply delineating individual ZmPep and ZmPEPR activities, these experiments led to a number of new insights into Pep signaling mechanisms. ZmPROPEP and other Poaceous precursors were found to contain multiple active Peps, a phenomenon not previously observed for this family. In all, seven new ZmPeps were identified and the peptides were found to have specific activities defined by relative magnitude of response output rather than by uniqueness. A striking correlation between individual ZmPep-elicited changes in levels of jasmonic acid and ethylene and the magnitude of induced defense responses was observed, indicating that collectively ZmPeps may regulate immune output through rheostat-like tuning of phytohormone levels. Peptide structure-function studies and ligand-receptor modeling revealed structural features critical to ZmPep function and led to identification of ZmPep5a as a potential antagonist peptide able to competitively inhibit activity of other ZmPeps, a regulatory mechanism not previously observed for this family.
Insect herbivores selectively suppress the HPL branch of the oxylipin pathway in host plants
The Plant Journal, 2013
Insect herbivores have developed a myriad of strategies to manipulate the defense responses of their host plants. Here we provide evidence that chewing insects differentially alter the oxylipin profiles produced by the two main and competing branches of the plant defensive response pathway, the allene oxide synthase (AOS) and hydroperoxide lyase (HPL) branches, responsible for wound-inducible production of jasmonates (JAs), and Green Leafy Volatiles (GLVs) respectively. Specifically, we used three Arabidopsis genotypes damaged by mechanical wounding or by insects of different feeding guilds (piercing aphids, generalist chewing caterpillars and specialist chewing caterpillars). We established that emission of GLVs is stimulated by wounding incurred mechanically or by aphids, but the release of these volatiles is constitutively impaired by both generalist and specialist chewing insects. Simultaneously however, these chewing herbivores stimulated JA production, demonstrating targeted insectsuppression of the HPL branch of the oxylipin pathway. Employment of lines engineered to express HPL constitutively, in conjunction with qRT-PCR-based expression analyses, established a combination of transcriptional and posttranscriptional reprogramming of the HPLpathway genes as the mechanistic basis of insect-mediated suppression of the corresponding metabolites. Feeding studies alluded to potential evolutionary advantage of suppressing GLV production as caterpillars preferably consumed leaf tissue from plants that had not been primed by these volatile cues. Feussner, I. and Fauconnier, M.L. (2009) Attacks by a piercing-sucking insect (Myzus persicae Sultzer) or a chewing insect (Leptinotarsa decemlineata Say) on potato plants (Solanum tuberosum L.) induce differential changes in volatile compound release and oxylipin synthesis. Journal of experimental botany, 60, 1231-1240. Halitschke, R. and Baldwin, I.T. (2003) Antisense LOX expression increases herbivore performance by decreasing defense responses and inhibiting growth-related transcriptional reorganization in Nicotiana attenuata. Plant J, 36, 794-807. Halitschke, R., Schittko, U., Pohnert, G., Boland, W. and Baldwin, I.T. (2001) Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata. III. Fatty acid-amino acid conjugates in herbivore oral secretions are necessary and sufficient for herbivore-specific plant responses. Plant Physiol, 125, 711-717.
Role of phytohormones in insect-specific plant reactions
2012
The capacity to perceive and respond is integral to biological immune systems, but to what extent can plants specifically recognize and respond to insects? Recent findings suggest that plants possess surveillance systems that are able to detect general patterns of cellular damage as well as highly specific herbivore-associated cues. The jasmonate (JA) pathway has emerged as the major signaling cassette that integrates information perceived at the plant-insect interface into broadspectrum defense responses. Specificity can be achieved via JA-independent processes and spatiotemporal changes of JA-modulating hormones, including ethylene, salicylic acid, abscisic acid, auxin, cytokinins, brassinosteroids and gibberellins. The identification of receptors and ligands and an integrative view of hormone-mediated response systems are crucial to understand specificity in plant immunity to herbivores. Know your enemy-a golden rule of plant defense? "If you know your enemies and know yourself, you can win a hundred battles without a single loss", states Sun Tzu in his ancient military treatise The Art of War. Plants, as primary producers of organic matter in terrestrial ecosystems, must continuously resist a multitude of attackers and, unlike the armies of Sun Tzu, do not have the option of retreating to safe ground. Have plants nevertheless evolved the capacity to "know" the attacking enemies and adjust their defenses accordingly? In this review we use the paradigm of molecular specificity in plant-pathogen interactions as a framework to discuss potential mechanisms by which plants specifically recognize and respond to insect herbivores. Plants recognize herbivores via mechanical and chemical cues An appropriate defense response to a biotic threat requires initial recognition. Pathogens are recognized when conserved patterns of microbial molecules called microbe-or pathogenassociated molecular patterns (MAMPs or PAMPs) are detected by pattern recognition receptors (PRRs) on the surface of the host plant cell, leading to PAMP-triggered immunity (PTI; Figure 1). Damage-associated molecular patterns (DAMPs), which are endogenous
Identification of an insect-produced olfactory cue that primes plant defenses
Nature Communications, 2017
It is increasingly clear that plants perceive and respond to olfactory cues. Yet, knowledge about the specificity and sensitivity of such perception remains limited. We previously documented priming of anti-herbivore defenses in tall goldenrod plants (Solidago altissima) by volatile emissions from a specialist herbivore, the goldenrod gall fly (Eurosta solidaginis). Here, we explore the specific chemical cues mediating this interaction. We report that E,S-conophthorin, the most abundant component of the emission of male flies, elicits a priming response equivalent to that observed for the overall blend. Furthermore, while the strength of priming is dose dependent, plants respond even to very low concentrations of E,S-conophthorin relative to typical fly emissions. Evaluation of other blend components yields results consistent with the hypothesis that priming in this interaction is mediated by a single compound. These findings provide insights into the perceptual capabilities underly...
Signal Transduction in Plant–Insect Interactions: From Membrane Potential Variations to Metabolomics
2012
Upon herbivore attack plants react with a cascade of signals. Early events are represented by ion flux unbalances that eventually lead to plasma transmembrane potential (Vm) variations. These events are triggered by mechanical wounding implicated by chewing/piercing herbivores along with the injection of oral secretions (OS) containing plant response effectors and elicitors. Vm depolarization has been found to be a common event when plants interact with different biotrophs, and to vary depending on type and feeding habit of the biotroph. Here we show recent advances of internal and external signal trans duction in plant-insect interactions by analyzing the differential impact of mechanical and herbivore damage on plants. Vm variations, calcium signaling, and ROS production precede the late events represented by gene expression, proteomics, and metabolomics. Transcriptomics allows to decipher genomic expression following Vm variations and signaling upon herbivory; proteomics helps to understand. the biological function of expressed genes, whereas meta bolomics gives feedbacks on the combined action of gene expression and protein synthesis, by showing the complexity of plant responses through synthesis of direct and indirect plant defense molecules. The practical application of modem methods starting from signal transduction to metabolic responses to insect her bivory are discussed and documented.
Plant-to-plant communication triggered by systemin primes anti-herbivore resistance in tomato
Scientific reports, 2017
Plants actively respond to herbivory by inducing various defense mechanisms in both damaged (locally) and non-damaged tissues (systemically). In addition, it is currently widely accepted that plant-to-plant communication allows specific neighbors to be warned of likely incoming stress (defense priming). Systemin is a plant peptide hormone promoting the systemic response to herbivory in tomato. This 18-aa peptide is also able to induce the release of bioactive Volatile Organic Compounds, thus also promoting the interaction between the tomato and the third trophic level (e.g. predators and parasitoids of insect pests). In this work, using a combination of gene expression (RNA-Seq and qRT-PCR), behavioral and chemical approaches, we demonstrate that systemin triggers metabolic changes of the plant that are capable of inducing a primed state in neighboring unchallenged plants. At the molecular level, the primed state is mainly associated with an elevated transcription of pattern -recogn...
Stability of Plant Defense Proteins in the Gut of Insect Herbivores
PLANT PHYSIOLOGY, 2007
Plant defense against insect herbivores is mediated in part by enzymes that impair digestive processes in the insect gut. Little is known about the evolutionary origins of these enzymes, their distribution in the plant kingdom, or the mechanisms by which they act in the protease-rich environment of the animal digestive tract. One example of such an enzyme is threonine (Thr) deaminase (TD), which in tomato (Solanum lycopersicum) serves a dual role in isoleucine (Ile) biosynthesis in planta and Thr degradation in the insect midgut. Here, we report that tomato uses different TD isozymes to perform these functions. Whereas the constitutively expressed TD1 has a housekeeping role in Ile biosynthesis, expression of TD2 in leaves is activated by the jasmonate signaling pathway in response to herbivore attack. Ingestion of tomato foliage by specialist (Manduca sexta) and generalist (Trichoplusia ni) insect herbivores triggered proteolytic removal of TD2's C-terminal regulatory domain, r...
Transgenic Research, 2013
Plant-herbivore relationships are complex interactions encompassing elaborate networks of molecules, signals and strategies used to overcome defences developed by each other. Herbivores use multiple feeding strategies to obtain nutrients from host plants. In turn, plants respond by triggering defence mechanisms to inhibit, block or modify the metabolism of the pest. As part of these defences, herbivore-challenged plants emit volatiles to attract natural enemies and warn neighbouring plants of the imminent threat. In response, herbivores develop a variety of strategies to suppress plant-induced protection. Our understanding of the plant-herbivore interphase is limited, although recent molecular approaches have revealed the participation of a battery of genes, proteins and volatile metabolites in attack-defence processes. This review describes the intricate and dynamic defence systems governing plant-herbivore interactions by examining the diverse strategies plants employ to deny phytophagous arthropods the ability to breach newly developed mechanisms of plant resistance. A cornerstone of this understanding is the use of transgenic tools to unravel the complex networks that control these interactions.