scholarly journals Responses to larval herbivory in the phenylpropanoid pathway of Ulmus minor are boosted by prior insect egg deposition

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.

2011 ◽  
Vol 279 (1726) ◽  
pp. 101-108 ◽  
Author(s):  
Ivo Beyaert ◽  
Diana Köpke ◽  
Josefin Stiller ◽  
Almuth Hammerbacher ◽  
Kinuyo Yoneya ◽  
...  

Plant anti-herbivore defence is inducible by both insect feeding and egg deposition. However, little is known about the ability of insect eggs to induce defences directed not against the eggs themselves, but against larvae that subsequently hatch from the eggs. We studied how oviposition (OP) by the sawfly Diprion pini on Pinus sylvestris foliage affects the plant's defensive potential against sawfly larvae. Larvae that initiated their development on P. sylvestris twigs on which they hatched from eggs gained less weight and suffered higher mortality than those fed on egg-free twigs. The poor performance of these larvae also affected the next herbivore generation since fecundity of resulting females was lower than that of females which spent their larval development on egg-free pine. Transcript levels of P. sylvestris sesquiterpene synthases ( Ps TPS1, Ps TPS2) were increased by D. pini OP, reached their highest levels just before larval hatching, and decreased when larvae started to feed. However, concentrations of terpenoid and phenolic metabolites presumed to act as feeding deterrents or toxins for herbivores did not change significantly after OP and feeding. Nevertheless, our performance data suggest that insect egg deposition may act to ‘warn’ a plant of upcoming feeding damage by larvae.


2019 ◽  
Author(s):  
Eddie Griese ◽  
Ana Pineda ◽  
Foteini G. Pashalidou ◽  
Eleonora Pizarro Iradi ◽  
Monika Hilker ◽  
...  

AbstractAccording to the preference-performance hypothesis (PPH), also known as ‘mother-knows-best hypothesis’, herbivorous insects prefer those plants for oviposition, which yield the best offspring performance. Yet, most studies testing the PPH neglect the possibility that plant responses to insect eggs may affect both egg survival and larval performance. Here, we tested the PPH by studying responses of seven Brassicaceae plant species to oviposition by two cabbage white species. When including the egg phase, our study supports the ‘mother-knows-best hypothesis’: larvae of Pieris rapae (solitary) or P. brassicae (gregarious) gained most weight on those plant species which had received most eggs (B. nigra or B. montana, respectively). However, our experiments did not reveal any relationship between oviposition preference and egg survival. Brassicaceous species are known to respond to these butterfly eggs with a hypersensitive response (HR)-like necrosis, which can lower egg survival. Pieris eggs frequently induced necrosis in five of the tested plant species. Survival of clustered P. brassicae eggs was unaffected by HR-like in four of the five species. Therefore, our experiments did not reveal any relationship between P. brassicae egg survival and oviposition preference. Females of P. rapae preferred oviposition on plant species which most frequently showed HR-like necrosis. Remarkably, although egg survival was lower on HR-like plants, larval biomass was higher compared to plants without a necrosis. We conclude that egg survival does not seem to be a deciding factor for oviposition choices. However, egg-mediated plant responses might be important to explain the PPH of the two Pieris species.Lay summaryEgg-laying preferences of herbivorous insects can often be linked to offspring performance. Commonly, the fate of insect eggs and the plant responses to the eggs have been ignored when studying the link between preference and performance. By including the egg phase, our study supports the ‘mother-knows-best hypothesis’, explained by butterfly oviposition and associated egg and larval performances on different plant species. We especially found that egg-mediated responses seem a deciding factor for butterfly oviposition choices.


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.


2018 ◽  
Vol 42 (3) ◽  
pp. 1019-1032 ◽  
Author(s):  
Vivien Lortzing ◽  
Jana Oberländer ◽  
Tobias Lortzing ◽  
Takayuki Tohge ◽  
Anke Steppuhn ◽  
...  

2015 ◽  
Vol 60 (1) ◽  
pp. 493-515 ◽  
Author(s):  
Monika Hilker ◽  
Nina E. Fatouros

2021 ◽  
Vol 21 (1) ◽  
Author(s):  
Ganyu Zhang ◽  
Wenjuan Guo ◽  
Xiaoyi Wang ◽  
Qian Wang ◽  
Jin Cui ◽  
...  

Abstract Background Elongated rostra play an important role in the egg-laying of weevils, and its emergence plays a key role in the adaptive radiation of weevils. Eucryptorrhynchus scrobiculatus Motschulsky and E. brandti Harold co-occur on the same only host Ailanthus altissima, while their oviposition sites are different. In order to understand the adaptation between the rostra of the two weevils and their oviposition sites, the structural differentiation of the rostra in E. scrobiculatus and E. brandti was compared. Results The present study reveals that: (1) The rostra length of E. scrobiculatus and E. brandti was found to be correlated with body size, larger weevils have a correspondingly longer rostrum. The increase of rostra length may be a byproduct of larger weevils. (2) There were significant differences in the external shape of the two rostra, especially the shape of the mandibles of the mouthparts at the apex of the rostra used to excavate an oviposition cavity. (3) There was no difference in the size of the abductor muscles that control the extension of the mandibles, but there were significant differences in the size of the adductor muscles that control the contraction of the mandibles. Conclusions These structural differences reflect the functional potential ovipositional tactics of rostra, which is considered to be a response to the ecological demands of egg deposition, and also provide new insights into the coexistence of two weevil species in the same host A. altissima.


2018 ◽  
Vol 19 (11) ◽  
pp. 3519 ◽  
Author(s):  
Agustina Bernal-Vicente ◽  
Daniel Cantabella ◽  
Cesar Petri ◽  
José Hernández ◽  
Pedro Diaz-Vivancos

Salinity is considered as one of the most important abiotic challenges that affect crop productivity. Plant hormones, including salicylic acid (SA), are key factors in the defence signalling output triggered during plant responses against environmental stresses. We have previously reported in peach a new SA biosynthetic pathway from mandelonitrile (MD), the molecule at the hub of the cyanogenic glucoside turnover in Prunus sp. In this work, we have studied whether this new SA biosynthetic pathway is also present in plum and the possible role this pathway plays in plant plasticity under salinity, focusing on the transgenic plum line J8-1, which displays stress tolerance via an enhanced antioxidant capacity. The SA biosynthesis from MD in non-transgenic and J8-1 micropropagated plum shoots was studied by metabolomics. Then the response of J8-1 to salt stress in presence of MD or Phe (MD precursor) was assayed by measuring: chlorophyll content and fluorescence parameters, stress related hormones, levels of non-enzymatic antioxidants, the expression of two genes coding redox-related proteins, and the content of soluble nutrients. The results from in vitro assays suggest that the SA synthesis from the MD pathway demonstrated in peach is not clearly present in plum, at least under the tested conditions. Nevertheless, in J8-1 NaCl-stressed seedlings, an increase in SA was recorded as a result of the MD treatment, suggesting that MD could be involved in the SA biosynthesis under NaCl stress conditions in plum plants. We have also shown that the plum line J8-1 was tolerant to NaCl under greenhouse conditions, and this response was quite similar in MD-treated plants. Nevertheless, the MD treatment produced an increase in SA, jasmonic acid (JA) and reduced ascorbate (ASC) contents, as well as in the coefficient of non-photochemical quenching (qN) and the gene expression of Non-Expressor of Pathogenesis-Related 1 (NPR1) and thioredoxin H (TrxH) under salinity conditions. This response suggested a crosstalk between different signalling pathways (NPR1/Trx and SA/JA) leading to salinity tolerance in the transgenic plum line J8-1.


Author(s):  
José A. Hernández ◽  
Pedro Diaz-Vivancos ◽  
Gregorio Barba-Espín ◽  
María José Clemente-Moreno

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