scholarly journals Defense of Scots pine against sawfly eggs (Diprion pini) is primed by exposure to sawfly sex pheromones

2019 ◽  
Vol 116 (49) ◽  
pp. 24668-24675 ◽  
Author(s):  
Norbert Bittner ◽  
Janik Hundacker ◽  
Ander Achotegui-Castells ◽  
Olle Anderbrant ◽  
Monika Hilker

Plants respond to insect infestation with defenses targeting insect eggs on their leaves and the feeding insects. Upon perceiving cues indicating imminent herbivory, such as damage-induced leaf odors emitted by neighboring plants, they are able to prime their defenses against feeding insects. Yet it remains unknown whether plants can amplify their defenses against insect eggs by responding to cues indicating imminent egg deposition. Here, we tested the hypothesis that a plant strengthens its defenses against insect eggs by responding to insect sex pheromones. Our study shows that preexposure of Pinus sylvestris to pine sawfly sex pheromones reduces the survival rate of subsequently laid sawfly eggs. Exposure to pheromones does not significantly affect the pine needle water content, but results in increased needle hydrogen peroxide concentrations and increased expression of defense-related pine genes such as SOD (superoxide dismutase), LOX (lipoxygenase), PAL (phenylalanine ammonia lyase), and PR-1 (pathogenesis related protein 1) after egg deposition. These results support our hypothesis that plant responses to sex pheromones emitted by an herbivorous insect can boost plant defensive responses to insect egg deposition, thus highlighting the ability of a plant to mobilize its defenses very early against an initial phase of insect attack, the egg deposition.

Author(s):  
Janik Hundacker ◽  
Norbert Bittner ◽  
Christoph Weise ◽  
Gunnar Bröhan ◽  
Martti Varama ◽  
...  

Known elicitors of plant defenses against eggs of herbivorous insects are low-molecular-weight organic compounds associated with the eggs. However, previous studies provided evidence that also proteinaceous compounds present in secretion associated with eggs of the herbivorous sawfly Diprion pini can elicit defensive responses in Pinus sylvestris. Pine responses induced by the proteinaceous secretion are known to result in enhanced emission of (E)-β-farnesene, which attracts egg parasitoids killing the eggs. Here, we aimed to identify the defense-eliciting protein and elucidate its function. After isolating the defense-eliciting protein from D. pini egg secretion by ultrafiltration and gel electrophoresis, we identified it by MALDI-ToF mass spectrometry as an annexin-like protein, which we named “diprionin”. Further GC-MS analyses showed that pine needles treated with heterologously expressed diprionin released enhanced quantities of (E)-β-farnesene. Our bioassays confirmed attractiveness of diprionin-treated pine to egg parasitoids. Expression of several pine candidate genes involved in terpene biosynthesis and regulation of ROS homeostasis was similarly affected by diprionin and natural sawfly egg deposition. However, the two treatments had different effects on expression of pathogenesis related genes (PR1, PR5). Diprionin is the first egg-associated proteinaceous elicitor of indirect plant defense against insect eggs described so far.


2002 ◽  
Vol 205 (4) ◽  
pp. 455-461 ◽  
Author(s):  
Monika Hilker ◽  
Carsten Kobs ◽  
Martti Varama ◽  
Kai Schrank

SUMMARY Plant volatiles released in response to feeding insects are known to attract enemies of the feeding herbivores. In this study, egg deposition by a herbivorous insect was shown to induce a gymnosperm plant to emit volatiles that attract egg parasitoids. Odour from twigs of Pinus sylvestris laden with egg masses of the pine sawfly Diprion pini attracts the eulophid egg parasitoid Chrysonotomyia ruforum. Volatiles released from pine twigs without diprionid eggs are not attractive. Oviposition by the sawfly onto pine needles induces not only a local response in pine needles laden with eggs but also a systemic reaction. Needles without eggs but adjacent to those bearing diprionid eggs also release the volatiles that attract the egg parasitoid. The elicitor of the attractive volatiles was shown to be present in the oviduct secretion coating the eggs of D. pini. When pine twigs are treated with jasmonic acid, a well-known plant wound signal, they emit volatiles that attract the egg parasitoid. These results show, for the first time, that a gymnosperm plant is able to attract parasitoids as soon as a herbivore has deposited its eggs on it. Thus, the plant appears to defend itself against herbivores prior to being damaged by feeding larvae.


Planta ◽  
2021 ◽  
Vol 255 (1) ◽  
Author(s):  
Johanna Schott ◽  
Benjamin Fuchs ◽  
Christoph Böttcher ◽  
Monika Hilker

Abstract Main conclusion Elms, which have received insect eggs as a ‘warning’ of larval herbivory, enhance their anti-herbivore defences by accumulating salicylic acid and amplifying phenylpropanoid-related transcriptional and metabolic responses to hatching larvae. Abstract Plant responses to insect eggs can result in intensified defences against hatching larvae. In annual plants, this egg-mediated effect is known to be associated with changes in leaf phenylpropanoid levels. However, little is known about how trees—long-living, perennial plants—improve their egg-mediated, anti-herbivore defences. The role of phytohormones and the phenylpropanoid pathway in egg-primed anti-herbivore defences of a tree species has until now been left unexplored. Using targeted and untargeted metabolome analyses we studied how the phenylpropanoid pathway of Ulmus minor responds to egg-laying by the elm leaf beetle and subsequent larval feeding. We found that when compared to untreated leaves, kaempferol and quercetin concentrations increased in feeding-damaged leaves with prior egg deposition, but not in feeding-damaged leaves without eggs. PCR analyses revealed that prior insect egg deposition intensified feeding-induced expression of phenylalanine ammonia lyase (PAL), encoding the gateway enzyme of the phenylpropanoid pathway. Salicylic acid (SA) concentrations were higher in egg-treated, feeding-damaged leaves than in egg-free, feeding-damaged leaves, but SA levels did not increase in response to egg deposition alone—in contrast to observations made of Arabidopsis thaliana. Our results indicate that prior egg deposition induces a SA-mediated response in elms to feeding damage. Furthermore, egg deposition boosts phenylpropanoid biosynthesis in subsequently feeding-damaged leaves by enhanced PAL expression, which results in the accumulation of phenylpropanoid derivatives. As such, the elm tree shows similar, yet distinct, responses to insect eggs and larval feeding as the annual model plant A. thaliana.


Genes ◽  
2021 ◽  
Vol 12 (7) ◽  
pp. 1007
Author(s):  
Divya Kattupalli ◽  
Asha Sreenivasan ◽  
Eppurathu Vasudevan Soniya

Black pepper (Piper nigrum L.) is a prominent spice that is an indispensable ingredient in cuisine and traditional medicine. Phytophthora capsici, the causative agent of footrot disease, causes a drastic constraint in P. nigrum cultivation and productivity. To counterattack various biotic and abiotic stresses, plants employ a broad array of mechanisms that includes the accumulation of pathogenesis-related (PR) proteins. Through a genome-wide survey, eleven PR-1 genes that belong to a CAP superfamily protein with a caveolin-binding motif (CBM) and a CAP-derived peptide (CAPE) were identified from P. nigrum. Despite the critical functional domains, PnPR-1 homologs differ in their signal peptide motifs and core amino acid composition in the functional protein domains. The conserved motifs of PnPR-1 proteins were identified using MEME. Most of the PnPR-1 proteins were basic in nature. Secondary and 3D structure analyses of the PnPR-1 proteins were also predicted, which may be linked to a functional role in P. nigrum. The GO and KEGG functional annotations predicted their function in the defense responses of plant-pathogen interactions. Furthermore, a transcriptome-assisted FPKM analysis revealed PnPR-1 genes mapped to the P. nigrum-P. capsici interaction pathway. An altered expression pattern was detected for PnPR-1 transcripts among which a significant upregulation was noted for basic PnPR-1 genes such as CL10113.C1 and Unigene17664. The drastic variation in the transcript levels of CL10113.C1 was further validated through qRT-PCR and it showed a significant upregulation in infected leaf samples compared with the control. A subsequent analysis revealed the structural details, phylogenetic relationships, conserved sequence motifs and critical cis-regulatory elements of PnPR-1 genes. This is the first genome-wide study that identified the role of PR-1 genes during P. nigrum-P. capsici interactions. The detailed in silico experimental analysis revealed the vital role of PnPR-1 genes in regulating the first layer of defense towards a P. capsici infection in Panniyur-1 plants.


2004 ◽  
Vol 85 (1) ◽  
pp. 33-37 ◽  
Author(s):  
Magali Merkx-Jacques ◽  
Jacqueline C. Bede

Abstract Plants exhibit remarkable plasticity in their ability to differentiate between herbivorous insect species and subtly adjust their defense responses to target distinct pests. One key mechanism used by plants to recognize herbivorous caterpillars is elicitors present in their oral secretions; however, these elicitors not only cause the induction of plant defenses but recent evidence suggests that they may also suppress plant responses. The absence of “expected changes” in induced defense responses of insect-infested plants has been attributed to hydrogen peroxide produced by caterpillar salivary glucose oxidase (GOX). Activity of this enzyme is variable among caterpillar species; it was detected in two generalist caterpillars, the beet armyworm (Spodoptera exigua) and the bertha armyworm (Mamestra configurata), but not in other generalist or specialist caterpillar species tested. In the beet armyworm, GOX activity fluctuated over larval development with high activity associated with the salivary glands of fourth instars. Larval salivary GOX activity of the beet armyworm and the bertha armyworm was observed to be significantly higher in caterpillars reared on artificial diet as compared with those reared on Medicago truncatula plants. This implies that a factor in the diet is involved in the regulation of caterpillar salivary enzyme activity. Therefore, plant diet may be regulating caterpillar oral elicitors that are involved in the regulation of plant defense responses: our goal is to understand these two processes.


2005 ◽  
Vol 24 (4) ◽  
pp. 216-224 ◽  
Author(s):  
Sujon Sarowar ◽  
Young Jin Kim ◽  
Eui Nam Kim ◽  
Ki Deok Kim ◽  
Byung Kook Hwang ◽  
...  

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