Elicitation of Jasmonate-Mediated Defense Responses by Mechanical Wounding and Insect Herbivory

Green leaf volatiles (GLVs) have long been associated with plant defense responses against insect herbivory. Although some of their biological activities appear to directly affect the attacking herbivore, one of the major functions of GLVs seems to be the priming of these defense responses. This priming is generally considered to impose low costs on the plant should no direct attack happen. Here, we demonstrate that priming of maize seedlings with GLVs is costly for the plants as it results in significantly reduced growth. We further demonstrate that priming very selectively affects growth responses after insect elicitor treatment and mechanical wounding depending on the age and/or the developmental stage of the treated plant. The differential growth response of maize seedlings to treatment with GLVs and subsequent herbivory-related damage sheds new light on the biological activity of these important plant volatile compounds and indicates consequences that go beyond defense.

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Induction of cell wall phenolic monomers as part of direct defense response in maize to pink stem borer (Sesamia inferens Walker) and non-insect interactions

Scientific Reports ◽

10.1038/s41598-021-93727-2 ◽

2021 ◽

Vol 11 (1) ◽

Author(s):

P. Lakshmi Soujanya ◽

J. C. Sekhar ◽

C. V. Ratnavathi ◽

Chikkappa G. Karjagi ◽

E. Shobha ◽

...

Keyword(s):

Induced Defense ◽

Stem Borer ◽

Defense Responses ◽

Short Term ◽

Mechanical Wounding ◽

Leaf Tissues ◽

Short And Long Term ◽

Insect Interactions ◽

Induced Defense Responses

AbstractPink stem borer (PSB) causes considerable yield losses to maize. Plant–insect interactions have significant implications for sustainable pest management. The present study demonstrated that PSB feeding, mechanical wounding, a combination of mechanical wounding and PSB regurgitation and exogenous application of methyl jasmonate have induced phenolic compound mediated defense responses both at short term (within 2 days of treatment) and long term (in 15 days of treatment) in leaf and stalk tissues of maize. The quantification of two major defense related phenolic compounds namely p-Coumaric acid (p-CA) and ferulic acid (FA) was carried out through ultra-fast liquid chromatography (UFLC) at 2 and 15 days after imposing the above treatments. The p-CA content induced in leaf tissues of maize genotypes were intrinsically higher when challenged by PSB attack at V3 and V6 stages in short- and long-term responses. Higher p-CA content was observed in stalk tissues upon wounding and regurgitation in short- and long-term responses at V3 and V6 stages. Significant accumulation of FA content was also observed in leaf tissues in response to PSB feeding at V3 stage in long-term response while at V6 stage it was observed both in short- and long-term responses. In stalk tissues, methyl jasmonate induced higher FA content in short-term response at V3 stage. However, at V6 stage PSB feeding induced FA accumulation in the short-term while, wounding and regurgitation treatment-induced defense responses in the long-term. In general, the resistant (DMRE 63, CM 500) and moderately resistant genotypes (WNZ ExoticPool) accumulated significantly higher contents of p-CA and FA content than susceptible ones (CM 202, BML 6) in most of the cases. The study indicates that phenolic mediated defense responses in maize are induced by PSB attack followed by wounding and regurgitation compared to the other induced treatments. Furthermore, the study confirmed that induced defense responses vary with plant genotype, stage of crop growth, plant tissue and short and long-term responses. The results of the study suggested that the Phenolic acids i.e. p-CA and FA may contribute to maize resistance mechanisms in the maize-PSB interaction system.

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SpitWorm, an herbivorous robot: Mechanical leaf wounding with simultaneous application of salivary components

10.1101/468702 ◽

2018 ◽

Cited By ~ 2

Author(s):

Guanjun Li ◽

Stefan Bartram ◽

Huijuan Guo ◽

Axel Mithöfer ◽

Maritta Kunert ◽

...

Keyword(s):

Plant Defense ◽

Insect Herbivory ◽

Lima Bean ◽

Phaseolus Lunatus ◽

Larval Feeding ◽

Insect Larvae ◽

Mechanical Wounding ◽

Simultaneous Application ◽

Biting Rate ◽

Chemical Factors

AbstractInduction of plant defense against insect herbivory is initiated by a combination of both, mechanical wounding and chemical factors. In order to study both effects independently on plant defense induction, SpitWorm, a computer controlled device which mimics the damage pattern of feeding insect larvae on leaves and can additionally apply oral secretions (OS) or other solutions to the ‘biting site’ during ‘feeding’, was developed and evaluated. The amount of OS left by a Spodoptera littoralis larva during feeding on Phaseolus lunatus (lima bean) leaves was estimated by combining larval foregut volume, biting rate, and quantification of a fluorescent dye injected into the larvae’s foregut prior to feeding. For providing OS amounts by SpitWorm equivalent to larval feeding, dilution and delivery rate were optimized. The effectiveness of SpitWorm was tested by comparing volatile organic compounds (VOC) emissions of P. lunatus leaves treated with either SpitWorm, MecWorm or S. littoralis larvae. Identification and quantification of emitted VOCs revealed that SpitWorm induced a volatile bouquet that is qualitatively and quantitatively similar to herbivory. Additionally, RT-qPCR of four jasmonic acid responsive genes showed that SpitWorm, in contrast to MecWorm, induces the same regulation pattern as insect feeding. Thus, SpitWorm mimics insect herbivory almost identical to real larvae feeding.

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Can herbivore-induced volatiles protect plants by increasing the herbivores’ susceptibility to natural pathogens?

10.1101/317560 ◽

2018 ◽

Cited By ~ 3

Author(s):

Laila Gasmi ◽

María Martínez-Solís ◽

Ada Frattini ◽

Meng Ye ◽

María Carmen Collado ◽

...

Keyword(s):

Gut Microbiota ◽

Spodoptera Exigua ◽

Negative Impact ◽

Insect Herbivory ◽

Defense Responses ◽

Hexenyl Acetate ◽

Induced Volatiles ◽

Herbivore Induced Plant Volatiles ◽

Herbivore Induced Volatiles ◽

Gut Microbiota Composition

AbstractIn response to insect herbivory, plants mobilize various defenses. Defense responses include the release of herbivore-induced plant volatiles (HIPVs) that can serve as signals to alert undamaged tissues and to attract natural enemies of the herbivores. It has also been shown that some HIPVs can have a direct negative impact on herbivore survival, but it is not yet understood by what mechanism. Here we tested the hypothesis that exposure to HIPVs renders insects more susceptible to natural pathogens. Exposing caterpillars of the noctuid Spodoptera exigua to indole and linalool, but not exposure to (Z)-3-hexenyl acetate increased the susceptibility to its nucleopolyhedrovirus (SeMNPV). We also found that exposure to indole, but not exposure to linalool or (Z)-3-hexenyl acetate, increased the pathogenicity of Bacillus thuringiensis. Additional experiments revealed significant changes on gut microbiota composition after forty-eight hours of larval exposure to indole. Overall, these results provide evidences that certain HIPVs can strongly enhance the susceptibility of caterpillars to pathogens, possibly through effects on the insects’ gut microbiota. These findings suggest a novel mechanism by which HIPVs can protect plants from herbivorous insects.

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Proteomic Analysis of MeJa-Induced Defense Responses in Rice against Wounding

International Journal of Molecular Sciences ◽

10.3390/ijms20102525 ◽

2019 ◽

Vol 20 (10) ◽

pp. 2525 ◽

Cited By ~ 8

Author(s):

Laura Bertini ◽

Luana Palazzi ◽

Silvia Proietti ◽

Susanna Pollastri ◽

Giorgio Arrigoni ◽

...

Keyword(s):

Oxidative Stress ◽

Induced Defense ◽

Defense Responses ◽

Mechanical Wounding ◽

Physiological Mechanisms ◽

Profiling Techniques ◽

Protein Classes ◽

Induced Defense Responses ◽

The Impact

The role of jasmonates in defense priming has been widely recognized. Priming is a physiological process by which a plant exposed to low doses of biotic or abiotic elicitors activates faster and/or stronger defense responses when subsequently challenged by a stress. In this work, we investigated the impact of MeJA-induced defense responses to mechanical wounding in rice (Oryza sativa). The proteome reprogramming of plants treated with MeJA, wounding or MeJA+wounding has been in-depth analyzed by using a combination of high throughput profiling techniques and bioinformatics tools. Gene Ontology analysis identified protein classes as defense/immunity proteins, hydrolases and oxidoreductases differentially enriched by the three treatments, although with different amplitude. Remarkably, proteins involved in photosynthesis or oxidative stress were significantly affected upon wounding in MeJA-primed plants. Although these identified proteins had been previously shown to play a role in defense responses, our study revealed that they are specifically associated with MeJA-priming. Additionally, we also showed that at the phenotypic level MeJA protects plants from oxidative stress and photosynthetic damage induced by wounding. Taken together, our results add novel insight into the molecular actors and physiological mechanisms orchestrated by MeJA in enhancing rice plants defenses after wounding.

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AaCOI1, Encoding a CORONATINE INSENSITIVE 1-Like Protein of Artemisia annua L., Is Involved in Development, Defense, and Anthocyanin Synthesis

Genes ◽

10.3390/genes11020221 ◽

2020 ◽

Vol 11 (2) ◽

pp. 221 ◽

Cited By ~ 1

Author(s):

Rong Liu ◽

Jinbiao Wang ◽

Mu Xiao ◽

Xiewang Gao ◽

Jin Chen ◽

...

Keyword(s):

Artemisia Annua ◽

Defense Responses ◽

Anthocyanin Synthesis ◽

Loss Of Function ◽

Mechanical Wounding ◽

Native Promoter ◽

Meja Treatment ◽

F Box Protein ◽

Ja Signaling ◽

Important Medicinal Plant

Artemisia annua is an important medicinal plant producing the majority of the antimalarial compound artemisinin. Jasmonates are potent inducers of artemisinin accumulation in Artemisisa annua plants. As the receptor of jasmonates, the F-box protein COI1 is critical to the JA signaling required for plant development, defense, and metabolic homeostasis. AaCOI1 from Artemisia annua, homologous to Arabidopsis AtCOI1, encodes a F-box protein located in the nuclei. Expressional profiles of the AaCOI1 in the root, stem, leaves, and inflorescence was investigated. The mRNA abundance of AaCOI1 was the highest in inflorescence, followed by in the leaves. Upon mechanical wounding or MeJA treatment, expression of AaCOI1 was upregulated after 6 h. When ectopically expressed, driven by the native promoter from Arabidopsis thaliana, AaCOI1 could partially complement the JA sensitivity and defense responses, but fully complemented the fertility, and the JA-induced anthocyanin accumulation in a coi1-16 loss-of-function mutant. Our study identifies the paralog of AtCOI1 in Artemisia annua, and revealed its implications in development, hormone signaling, defense, and metabolism. The results provide insight into JA perception in Artemisia annua, and pave the way for novel molecular breeding strategies in the canonical herbs to manipulate the anabolism of pharmaceutic compounds on the phytohormonal level.

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Insect herbivory antagonizes leaf cooling responses to elevated temperature in tomato

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1913885117 ◽

2020 ◽

Vol 117 (4) ◽

pp. 2211-2217 ◽

Cited By ~ 5

Author(s):

Nathan E. Havko ◽

Michael R. Das ◽

Alan M. McClain ◽

George Kapali ◽

Thomas D. Sharkey ◽

...

Keyword(s):

Climate Change ◽

Elevated Temperature ◽

Heat Waves ◽

Global Climate ◽

Feeding Activity ◽

Stomatal Closure ◽

Insect Herbivory ◽

Leaf Damage ◽

Extreme Weather Events ◽

Mechanical Wounding

As global climate change brings elevated average temperatures and more frequent and extreme weather events, pressure from biotic stresses will become increasingly compounded by harsh abiotic stress conditions. The plant hormone jasmonate (JA) promotes resilience to many environmental stresses, including attack by arthropod herbivores whose feeding activity is often stimulated by rising temperatures. How wound-induced JA signaling affects plant adaptive responses to elevated temperature (ET), however, remains largely unknown. In this study, we used the commercially important crop plant Solanum lycopersicum (cultivated tomato) to investigate the interaction between simulated heat waves and wound-inducible JA responses. We provide evidence that the heat shock protein HSP90 enhances wound responses at ET by increasing the accumulation of the JA receptor, COI1. Wound-induced JA responses directly interfered with short-term adaptation to ET by blocking leaf hyponasty and evaporative cooling. Specifically, leaf damage inflicted by insect herbivory or mechanical wounding at ET resulted in COI1-dependent stomatal closure, leading to increased leaf temperature, lower photosynthetic carbon assimilation rate, and growth inhibition. Pharmacological inhibition of HSP90 reversed these effects to recapitulate the phenotype of a JA-insensitive mutant lacking the COI1 receptor. As climate change is predicted to compound biotic stress with larger and more voracious arthropod pest populations, our results suggest that antagonistic responses resulting from a combination of insect herbivory and moderate heat stress may exacerbate crop losses.

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SpitWorm, an Herbivorous Robot: Mechanical Leaf Wounding with Simultaneous Application of Salivary Components

10.20944/preprints201907.0023.v1 ◽

2019 ◽

Author(s):

Guanjun Li ◽

Stefan Bartram ◽

Huijuan Guo ◽

Axel Mithoefer ◽

Maritta Kunert ◽

...

Keyword(s):

Plant Defense ◽

Insect Herbivory ◽

Lima Bean ◽

Phaseolus Lunatus ◽

Larval Feeding ◽

Insect Larvae ◽

Mechanical Wounding ◽

Simultaneous Application ◽

Biting Rate ◽

Chemical Factors

Induction of jasmonate-mediated plant defense against insect herbivory is initiated by a combination of both, mechanical wounding and chemical factors. In order to study both effects independently on plant defense induction, SpitWorm, a computer-controlled device which mimics the damage pattern of feeding insect larvae on leaves and, in addition, can apply oral secretions (OS) or other solutions to the ‘biting site’ during ‘feeding’, was developed and evaluated. The amount of OS left by a Spodoptera littoralis larva during feeding on Phaseolus lunatus (lima bean) leaves was estimated by combining larval foregut volume, biting rate, and quantification of a fluorescent dye injected into the larvae’s foregut prior to feeding. For providing OS amounts by SpitWorm equivalent to larval feeding, dilution and delivery rate were optimized. The effectiveness of SpitWorm was tested by comparing volatile organic compounds (VOC) emissions of P. lunatus leaves treated with either SpitWorm, MecWorm or S. littoralis larvae. Identification and quantification of emitted VOCs revealed that SpitWorm induced a volatile bouquet that is qualitatively and quantitatively similar to herbivory. Additionally, RT-qPCR of four jasmonic acid responsive genes showed that SpitWorm, in contrast to MecWorm, induces the same regulation pattern as insect feeding. Thus, SpitWorm mimics insect herbivory almost identical to real larvae feeding.

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Previous herbivory modulates aphid population growth and plant defense responses in a non-model plant, Carthamus tinctorius (Asteraceae)

Bulletin of Entomological Research ◽

10.1017/s0007485321000456 ◽

2021 ◽

pp. 1-11

Author(s):

Motahareh Amiri Domari ◽

Seyed Mozaffar Mansouri ◽

Mohsen Mehrparvar

Keyword(s):

Defense Mechanisms ◽

Induced Defense ◽

Defense Responses ◽

Carthamus Tinctorius ◽

Total Phenolic ◽

Plant Defense Responses ◽

Mechanical Wounding ◽

And Control ◽

Winged Aphid ◽

Wild Safflower

Abstract Plants have a variety of defense mechanisms that are often induced following attacks by herbivores; this benefits those plants by decreasing performance or preference of herbivores that attack the plants later. We investigated the effects of previous exposure of plants to the safflower aphid, Uroleucon carthami, cotton bollworm, Helicoverpa armigera, and mechanical wounding on subsequent safflower aphid infestations using commercial safflower (Carthamus tinctorius) cultivars and wild safflower species (C. oxyacantha). The experiments were conducted in a greenhouse with two treatments: previously induced plants via direct herbivory or mechanical wounding, and control plants that had never experienced herbivory. To test the performance of safflower aphid on different plant treatments, five unwinged aphids were placed on each plant and allowed to reproduce for 14 days. Finally, the total numbers of aphids on each plant were counted and the percentage of produced winged individuals was calculated. The number of aphids on plants that were previously infested or injured was significantly lower than in control plants. Percentage of winged aphids was significantly higher on induced plants, which is an indicator for unsuitable conditions. Also, significant increase in total phenolic content and hydrogen peroxide was observed in induced plants, showing that the levels of these compounds were either treatment, cultivar and/or genotype × treatment dependent, highlighting the specificity of these interactions. Overall, among the safflower cultivars the lowest number of aphids and the highest percentage of winged aphid individuals were observed on Mahali-Isfahan cultivar and wild safflower, showing that this cultivar is more sensitive to herbivory and/or responds to it more than other cultivars. These findings could contribute to a better utilization of induced defense in the integrated pest management of safflower fields.

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Shade suppresses wound-induced leaf repositioning through a mechanism involving PHYTOCHROME KINASE SUBSTRATE (PKS) genes

10.1101/2021.11.14.468560 ◽

2021 ◽

Author(s):

Anne-Sophie Fiorucci ◽

Olivier Michaud ◽

Emanuel Schmid-Siegert ◽

Martine Trevisan ◽

Laure Allenbach Petrolati ◽

...

Keyword(s):

Leaf Growth ◽

Expression Patterns ◽

Defense Responses ◽

Potential Interaction ◽

Shade Avoidance ◽

Mechanical Wounding ◽

Kinase Substrate ◽

Wound Signal ◽

The Relationship

Shaded plants challenged with herbivores or pathogens prioritize growth over defense. However, most experiments have focused on the effect of shading light cues on defense responses. To investigate the potential interaction between shade-avoidance and wounding-induced Jasmonate (JA)-mediated signaling on leaf growth and movement, we used repetitive mechanical wounding of leaf blades to mimic herbivore attacks. Phenotyping experiments with combined treatments on Arabidopsis thaliana rosettes revealed that shade strongly inhibits the wound effect on leaf elevation. By contrast, petiole length is reduced by wounding both in the sun and in the shade. Thus, the relationship between the shade and wounding/JA pathways varies depending on the physiological response, implying that leaf growth and movement can be uncoupled. Using RNA-sequencing, we identified genes with expression patterns matching the hyponastic response (opposite regulation by both stimuli, interaction between treatments with shade dominating the wound signal). Among them were genes from the PKS (Phytochrome Kinase Substrate) family, which was previously studied for its role in phototropism and leaf positioning. Interestingly, we observed reduced shade suppression of the wounding effect in pks2pks4 double mutants while a PKS4 overexpressing line showed constitutively elevated leaves and was less sensitive to wounding. Our results indicate a trait-specific interrelationship between shade and wounding cues on Arabidopsis leaf growth and positioning. Moreover, we identify PKS genes as integrators of external cues in the control of leaf hyponasty further emphasizing the role of these genes in aerial organ positioning.

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