Priming by Timing: Arabidopsis thaliana Adjusts Its Priming Response to Lepidoptera Eggs to the Time of Larval Hatching.
TL;DR: The results show that larvae gained less biomass the longer the eggs had previously been on the plant, and Arabidopsis thaliana adjusts the kinetics of its egg-primed response to the time point of larval hatching, ensuring that the plant is optimally prepared just in time prior to larvals hatching.
Abstract: Plants can respond to eggs laid by herbivorous insects on their leaves by preparing (priming) their defense against the hatching larvae. Egg-mediated priming of defense is known for several plant species, including Brassicaceae. However, it is unknown yet for how long the eggs need to remain on a plant until a primed defense state is reached, which is ecologically manifested by reduced performance of the hatching larvae. To address this question, we used Arabidopsis thaliana, which carried eggs of the butterfly Pieris brassicae for 1-6 days prior to exposure to larval feeding. Our results show that larvae gained less biomass the longer the eggs had previously been on the plant. The strongest priming effect was obtained when eggs had been on the plant for 5 or 6 days, i.e., for (almost) the entire development time of the Pieris embryo inside the egg until larval hatching. Transcript levels of priming-responsive genes, levels of jasmonic acid-isoleucine (JA-Ile), and of the egg-inducible phytoalexin camalexin increased with the egg exposure time. Larval performance studies on mutant plants revealed that camalexin is dispensable for anti-herbivore defense against P. brassicae larvae, whereas JA-Ile - in concert with egg-induced salicylic acid (SA) - seems to be important for signaling egg-mediated primed defense. Thus, A. thaliana adjusts the kinetics of its egg-primed response to the time point of larval hatching. Hence, the plant is optimally prepared just in time prior to larval hatching.
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TL;DR: The findings suggest that the plants’ egg‐killing trait is a new front on the evolutionary arms‐race between Brassicaceae and pierid butterflies beyond the well‐studied plant toxins that have evolved against their caterpillars.
Abstract: Evolutionary arms-races between plants and insect herbivores have long been proposed to generate key innovations such as plant toxins and detoxification mechanisms that can drive diversification of the interacting species. A novel front-line of plant defence is the killing of herbivorous insect eggs. We test whether an egg-killing plant trait has an evolutionary basis in such a plant-insect arms-race. Within the crucifer family (Brassicaceae), some species express a hypersensitive response (HR)-like necrosis underneath butterfly eggs (Pieridae) that leads to eggs desiccating or falling off the plant. We studied the phylogenetic distribution of this trait, its egg-killing effect on and elicitation by butterflies, by screening 31 Brassicales species, and nine Pieridae species. We show a clade-specific induction of strong, egg-killing HR-like necrosis mainly in species of the Brassiceae tribe including Brassica crops and close relatives. The necrosis is strongly elicited by pierid butterflies that are specialists of crucifers. Furthermore, HR-like necrosis is linked to PR1 defence gene expression, accumulation of reactive oxygen species and cell death, eventually leading to egg-killing. Our findings suggest that the plants' egg-killing trait is a new front on the evolutionary arms-race between Brassicaceae and pierid butterflies beyond the well-studied plant toxins that have evolved against their caterpillars.
24 citations
TL;DR: In this article, the authors identified the defense-eliciting protein from D. pini egg-associated secretion by ultrafiltration and gel electrophoresis, which they named "diprionin".
Abstract: 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-associated 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.
11 citations
TL;DR: In this article , the authors show that the fitness costs of priming are lower than those of constitutively activated defences, suggesting that priming functions as an ecological adaptation of the plant to respond faster to a hostile environment.
10 citations
TL;DR: In this paper, it was shown that lepidopteran eggs interfere with plant-pathogen interactions and cause systemic acquired resistance (SAR) against the bacterial hemibiotroph pathogen Pseudomonas syringae.
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.
8 citations
TL;DR: In this paper , a MSN-based deltamethrin formulation was evaluated based on the laying-eggs number and oviposition behavior, and the results showed that there might be differences between the treatments (KIT-6, DELTAMETHIN@KIT6, deltAMethrin@K IT-6 and water as a control) in terms of the insect control via the lay-egg and next generation prevention.
Abstract: Abstract Background Wheat is one of the main food for around 2 billion people worldwide. Among the biological stressors, Eurygaster integriceps Puton is a damaging insect in wheat and barley fields, which harms them both quantitatively (by overwintered adults) and qualitatively (by instar nymphs). The ovipositional and the new generation’s production control are pivotal approaches to control the severe damages of Sunn-pest. Methods In this study, to enhance the deltamethrin effectiveness while reducing its required dosage and also reducing the adverse health and environmental impacts, a novel MSN-based deltamethrin formulation was prepared and evaluated based on the laying-eggs number and oviposition behavior. To this, deltamethrin was loaded on KIT-6 mesoporous silica nanoparticles and characterized using SEM, TEM, and TGA analysis, and the insect potential of deltametrin@KIT6 was then evaluated. Results The results showed that there might be differences between the treatments (KIT-6, deltamethrin@KIT-6, deltamethrin commercial formulation, and water as a control) in terms of the insect control via the laying-egg and next-generation prevention. The results showed that KIT-6 and deltamethrin@KIT-6 could reduce the oviposition rate compared to water as the control. Deltamethrin@KIT-6 not only caused the less oviposition done but the eggs were scattered and the batch of eggs did not have a uniform-shape similar to the control mode. The deltamethrin@KIT-6 nanopesticide could increase the pesticide effectiveness by reducing the Sunn-pest’s oviposition and nymphal population and subsequently decreasing the damage caused by them. So that the concentrations of 10, 25, and 125 mg L −1 of deltamethrin@KIT-6 reduced oviposition by 63.24%, 66.11%, and 67.62%, respectively, compared to the control group. On the other hand, descriptive observations showed that another possible tension is created through insect eggs deposition on the boundary layer of leaves. Conclusion The MSN-based nanoformulation could be effectively considered to control the next-generation population density of Sunn-pest. Graphical Abstract
5 citations
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TL;DR: The 2-Delta Delta C(T) method as mentioned in this paper was proposed to analyze the relative changes in gene expression from real-time quantitative PCR experiments, and it has been shown to be useful in the analysis of realtime, quantitative PCR data.
139,407 citations
TL;DR: In this article, a model is described in an lmer call by a formula, in this case including both fixed-and random-effects terms, and the formula and data together determine a numerical representation of the model from which the profiled deviance or the profeatured REML criterion can be evaluated as a function of some of model parameters.
Abstract: Maximum likelihood or restricted maximum likelihood (REML) estimates of the parameters in linear mixed-effects models can be determined using the lmer function in the lme4 package for R. As for most model-fitting functions in R, the model is described in an lmer call by a formula, in this case including both fixed- and random-effects terms. The formula and data together determine a numerical representation of the model from which the profiled deviance or the profiled REML criterion can be evaluated as a function of some of the model parameters. The appropriate criterion is optimized, using one of the constrained optimization functions in R, to provide the parameter estimates. We describe the structure of the model, the steps in evaluating the profiled deviance or REML criterion, and the structure of classes or types that represents such a model. Sufficient detail is included to allow specialization of these structures by users who wish to write functions to fit specialized linear mixed models, such as models incorporating pedigrees or smoothing splines, that are not easily expressible in the formula language used by lmer.
50,607 citations
Additional excerpts
...…4.0.0)” (R Development Core Team, 2016) and R Studio (version 1.2.5042, R Studio Team, 2020) with the packages “car” (Fox and Weisberg, 2019), “lme4” (Bates et al., 2015), “lmtest” (Zeileis and Hothorn, 2002), “multcomp” (Hothorn et al., 2008), “nlme” (Pinheiro et al., 2020), and “psych”…...
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TL;DR: This paper describes simultaneous inference procedures in general parametric models, where the experimental questions are specified through a linear combination of elemental model parameters, and extends the canonical theory of multiple comparison procedures in ANOVA models to linear regression problems, generalizedlinear models, linear mixed effects models, the Cox model, robust linear models, etc.
Abstract: Simultaneous inference is a common problem in many areas of application. If multiple null hypotheses are tested simultaneously, the probability of rejecting erroneously at least one of them increases beyond the pre-specified significance level. Simultaneous inference procedures have to be used which adjust for multiplicity and thus control the overall type I error rate. In this paper we describe simultaneous inference procedures in general parametric models, where the experimental questions are specified through a linear combination of elemental model parameters. The framework described here is quite general and extends the canonical theory of multiple comparison procedures in ANOVA models to linear regression problems, generalized linear models, linear mixed effects models, the Cox model, robust linear models, etc. Several examples using a variety of different statistical models illustrate the breadth
10,545 citations
Book•
29 Nov 2010
TL;DR: This tutorial jumps right in to the power of R without dragging you through the basic concepts of the programming language.
Abstract: Preface 1. Getting Started With R 2. Reading and Manipulating Data 3. Exploring and Transforming Data 4. Fitting Linear Models 5. Fitting Generalized Linear Models 6. Diagnosing Problems in Linear and Generalized Linear Models 7. Drawing Graphs 8. Writing Programs References Author Index Subject Index Command Index Data Set Index Package Index About the Authors
9,947 citations
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...5042, R Studio Team, 2020) with the packages “car” (Fox and Weisberg, 2019), “lme4” (Bates et al....
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...…with the software “R (version 4.0.0)” (R Development Core Team, 2016) and R Studio (version 1.2.5042, R Studio Team, 2020) with the packages “car” (Fox and Weisberg, 2019), “lme4” (Bates et al., 2015), “lmtest” (Zeileis and Hothorn, 2002), “multcomp” (Hothorn et al., 2008), “nlme” (Pinheiro…...
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TL;DR: This review summarizes results from Arabidopsis-pathogen systems regarding the contributions of various defense responses to resistance to several biotrophic and necrotrophic pathogens.
Abstract: It has been suggested that effective defense against biotrophic pathogens is largely due to programmed cell death in the host, and to associated activation of defense responses regulated by the salicylic acid-dependent pathway. In contrast, necrotrophic pathogens benefit from host cell death, so they are not limited by cell death and salicylic acid-dependent defenses, but rather by a different set of defense responses activated by jasmonic acid and ethylene signaling. This review summarizes results from Arabidopsis-pathogen systems regarding the contributions of various defense responses to resistance to several biotrophic and necrotrophic pathogens. While the model above seems generally correct, there are exceptions and additional complexities.
3,721 citations
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...The SA-dependent, egg-mediated priming effect on A. thaliana defense against P. brassicae larvae is also linked with enhanced expression of SA-responsive, pathogenesis-related (PR) genes and of a gene encoding a cation exchanger (CAX3) and a plant defensin (PDF1....
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...In contrast, the feeding-induced expression of CAX3, the SA-responsive PR genes and PDF1....
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...Indeed, our analysis of plant responses to eggs showed that transcript levels of several, especially SA-responsive genes significantly increased with increasing egg exposure time and reached a maximum shortly before larval hatching....
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...Response Pattern III of Arabidopsis thaliana to Pieris brassicae Eggs: Gradually Increasing Induced Response Traits representing response pattern III (Figure 7A) are the SA-responsive PR genes, PAD3, CAX3, and PDF1....
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...PAD3 expression is suggested to be both SA-responsive (Glazebrook, 2005; Glawischnig, 2007) and JA-responsive (Pangesti et al., 2016)....
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