Metabolomic analysis of the interaction between plants and herbivores

Insect herbivores by necessity have to deal with a large arsenal of plant defence metabolites. The levels of defence compounds may be increased by insect damage. These induced plant responses may also affect the metabolism and performance of successive insect herbivores. As the chemical nature of induced responses is largely unknown, global metabolomic analyses are a valuable tool to gain more insight into the metabolites possibly involved in such interactions. This study analyzed the interaction between feral cabbage (Brassica oleracea) and small cabbage white caterpillars (Pieris rapae) and how previous attacks to the plant affect the caterpillar metabolism. Because plants may be induced by shoot and root herbivory, we compared shoot and root induction by treating the plants on either plant part with jasmonic acid. Extracts of the plants and the caterpillars were chemically analysed using Ultra Performance Liquid Chromatography/Time of Flight Mass Spectrometry (UPLCT/MS). The study revealed that the levels of three structurally related coumaroylquinic acids were elevated in plants treated on the shoot. The levels of these compounds in plants and caterpillars were highly correlated: these compounds were defined as the ‘metabolic interface’. The role of these metabolites could only be discovered using simultaneous analysis of the plant and caterpillar metabolomes. We conclude that a metabolomics approach is useful in discovering unexpected bioactive compounds involved in ecological interactions between plants and their herbivores and higher trophic levels.     

Anthropogenic increase in carbon dioxide modifies plant–insect interactions

Industrialisation has elevated atmospheric levels of CO₂ from original 280 ppm to current levels at 400 ppm, which is estimated to double by 2050. Although high atmospheric CO₂ levels affect insect interactions with host plants, the impact of global change on plant defences in response to insect attack is not completely understood. Recent studies have made advances in elucidating the mechanisms of the effects of high CO₂ levels in plant–insect interactions. New studies have proposed that gene regulation and phytohormones regulate resource allocation from photosynthesis to plant defences against insects. Biochemical and molecular studies demonstrated that both defensive hormones jasmonic acid (JA) and ethylene (ET) participate in modulating chemical defences against herbivores in plants grown under elevated CO₂ atmosphere rather than changes in C:N ratio. High atmospheric CO₂ levels increase vulnerability to insect damage by down‐regulating both inducive and constitutive chemical defences regulated by JA and ET. However, elevated CO₂ levels increase the JA antagonistic hormone salicylic acid that increases other chemical defences. How plants grown under elevated CO₂ environment allocate primary metabolites from photosynthesis to secondary metabolism would help to understand innate defences and prevent future herbivory in field crops. We present evidence demonstrating that changes in chemical defences in plants grown under elevated CO₂ environment are hormonal regulated and reject the C:N hypothesis. In addition, we discuss current knowledge of the mechanisms that regulate plants defences against insects in elevated CO₂ atmospheres.     

大气CO2浓度升高对森林食叶昆虫的潜在影响

评述了大气CO₂浓度升高对森林食叶昆虫的影响,昆虫对森林取食为害水平的潜在变化,以及研究中的主要实验方法.大气CO₂浓度升高通过引起叶片化学变化进而影响食叶昆虫个体的取食和生长;但物种对环境变化反应的特异性、植物化学对高浓度CO₂的反应强度、昆虫对植物生理变化的敏感性和适应性、研究周期的长短、其它环境因子的协同效应以及不同实验中植物生长条件和研究方法的差异均将影响昆虫反应的方向和强度;CO₂气体浓度增高本身可能不足以对食叶昆虫个体的新陈代谢构成影响;大气CO₂浓度升高也可能影响森林食叶昆虫种群的大小.     

Phytochemical diversity impacts herbivory in a tropical rainforest tree community

Metabolomics provides an unprecedented window into diverse plant secondary metabolites that represent a potentially critical niche dimension in tropical forests underlying species coexistence. Here, we used untargeted metabolomics to evaluate chemical composition of 358 tree species and its relationship with phylogeny and variation in light environment, soil nutrients, and insect herbivore leaf damage in a tropical rainforest plot. We report no phylogenetic signal in most compound classes, indicating rapid diversification in tree metabolomes. We found that locally co-occurring species were more chemically dissimilar than random and that local chemical dispersion and metabolite diversity were associated with lower herbivory, especially that of specialist insect herbivores. Our results highlight the role of secondary metabolites in mediating plant–herbivore interactions and their potential to facilitate niche differentiation in a manner that contributes to species coexistence. Furthermore, our findings suggest that specialist herbivore pressure is an important mechanism promoting phytochemical diversity in tropical forests.     

Solar ultraviolet-B radiation and insect herbivory trigger partially overlapping phenolic responses in Nicotiana attenuata and Nicotiana longiflora

BACKGROUND AND AIMS: Plants exposed to solar ultraviolet-B radiation (UV-B, 280-315 nm) frequently suffer less insect herbivory than do plants that receive attenuated levels of UV-B. This anti-herbivore effect of solar UV-B exposure, which has been documented in several ecosystems, is in part mediated by changes in plant tissue quality. Exposure to UV-B can modify the abundance of a number of secondary metabolites, including phenolic compounds with potential impacts on insect herbivores. The aim of this study is to assess the potential anti-herbivore role of UV-B-induced phenolic compounds by comparing the phenolic profiles induced by UV-B and simulated insect herbivory in two wild species of the genus Nicotiana. METHODS: Plants grown under field and glasshouse conditions were exposed to contrasting levels of UV-B. Half of the plants of the attenuated UV-B treatment were given a simulated herbivory treatment, where leaves were mechanically damaged and immediately treated with oral secretions of Manduca sexta caterpillars. This treatment is known to mimic the impact of real herbivory on the expression of plant defences in Nicotiana. Phenolic profiles induced by UV-B and simulated herbivory were characterized using high-performance liquid chromatography-mass spectrometry (HPLC-MS). KEY RESULTS: UV-B induced the accumulation of several UV-absorbing phenolic compounds that are known to play a significant role in UV-B screening. Interestingly, there was a significant convergence in the phenolic profiles induced by UV-B and simulated herbivory: chlorogenic acid and dicaffeoylspermidine isomers, in particular, displayed a similar pattern of response to these stimuli. In contrast, rutin, the only flavonoid that accumulated in significant quantities in the experiments, was only induced by UV-B. CONCLUSIONS: The results suggest that the anti-herbivory effect induced by UV-B may be mediated at least in part by the accumulation of phenylpropanoid derivatives that are similar to those induced by the plant in response to insect herbivory.     

The effects of drought and herbivory on plant–herbivore interactions across 16 soybean genotypes in a field experiment

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Insect herbivory and plant adaptation in an early successional community*

To address the role of insect herbivores in adaptation of plant populations and the persistence of selection through succession, we manipulated herbivory in a long‐term field experiment. We suppressed insects in half of 16 plots over nine years and examined the genotypic structure and chemical defense of common dandelion (Taraxacum officinale), a naturally colonizing perennial apomictic plant. Insect suppression doubled dandelion abundance in the first few years, but had negligible effects thereafter. Using microsatellite DNA markers, we genotyped >2500 plants and demonstrate that insect suppression altered the genotypic composition of plots in both sampling years. Phenotypic and genotypic estimates of defensive terpenes and phenolics from the field plots allowed us to infer phenotypic plasticity and the response of dandelion populations to insect‐mediated natural selection. The effects of insect suppression on plant chemistry were, indeed, driven both by plasticity and plant genotypic identity. In particular, di‐phenolic inositol esters were more abundant in plots exposed to herbivory (due to the genotypic composition of the plots) and were also induced in response to herbivory. This field experiment thus demonstrates evolutionary sorting of plant genotypes in response to insect herbivores that was in same direction as the plastic defensive response within genotypes.     

Facilitation and inhibition: changes in plant nitrogen and secondary metabolites mediate interactions between above-ground and below-ground herbivores

To date, it remains unclear how herbivore-induced changes in plant primary and secondary metabolites impact above-ground and below-ground herbivore interactions. Here, we report effects of above-ground (adult) and below-ground (larval) feeding by Bikasha collaris on nitrogen and secondary chemicals in shoots and roots of Triadica sebifera to explain reciprocal above-ground and below-ground insect interactions. Plants increased root tannins with below-ground herbivory, but above-ground herbivory prevented this increase and larval survival doubled. Above-ground herbivory elevated root nitrogen, probably contributing to increased larval survival. However, plants increased foliar tannins with above-ground herbivory and below-ground herbivory amplified this increase, and adult survival decreased. As either foliar or root tannins increased, foliar flavonoids decreased, suggesting a trade-off between these chemicals. Together, these results show that plant chemicals mediate contrasting effects of conspecific larval and adult insects, whereas insects may take advantage of plant responses to facilitate their offspring performance, which may influence population dynamics.     

Secondary metabolites and plant/environment interactions: a view through Arabidopsis thaliana tinged glasses

Arabidopsis thaliana is a successful model plant for studying wide‐ranging topics including plant development, genetics and pathogen resistance. In addition, significant research has been conducted in the area of secondary metabolite biochemical genetics. The secondary metabolites in Arabidopsis include glucosinolates, terpenoids, phenylpropanoids, the alkaloid‐like camalexin, and other uncharacterized compounds. The genetic tools developed in studying secondary metabolite biochemistry are now being used to study how secondary metabolites control various biological processes. This includes compounds involved in plant/insect and plant/pathogen interactions, compounds preventing UV‐B damage, and compounds involved in hormone homeostasis. This review will describe what light Arabidopsis is shedding on the biological and ecological importance of specific secondary metabolites.     

Experimental climate warming alters aspen and birch phytochemistry and performance traits for an outbreak insect herbivore

Climate change and insect outbreaks are key factors contributing to regional and global patterns of increased tree mortality. While links between these environmental stressors have been established, our understanding of the mechanisms by which elevated temperature may affect tree–insect interactions is limited. Using a forest warming mesocosm, we investigated the influence of elevated temperature on phytochemistry, tree resistance traits, and insect performance. Specifically, we examined warming effects on forest tent caterpillar (Malacosoma disstria) and host trees aspen (Populus tremuloides) and birch (Betula papyrifera). Trees were grown under one of three temperature treatments (ambient, +1.7 °C, +3.4 °C) in a multiyear open‐air warming experiment. In the third and fourth years of warming (2011, 2012), we assessed foliar nutrients and defense chemistry. Elevated temperatures altered foliar nitrogen, carbohydrates, lignin, and condensed tannins, with differences in responses between species and years. In 2012, we performed bioassays using a common environment approach to evaluate plant‐mediated indirect warming effects on larval performance. Warming resulted in decreased food conversion efficiency and increased consumption, ultimately with minimal effect on larval development and biomass. These changes suggest that insects exhibited compensatory feeding due to reduced host quality. Within the context of observed phytochemical variation, primary metabolites were stronger predictors of insect performance than secondary metabolites. Between‐year differences in phytochemical shifts corresponded with substantially different weather conditions during these two years. By sampling across years within an ecologically realistic and environmentally open setting, our study demonstrates that plant and insect responses to warming can be temporally variable and context dependent. Results indicate that elevated temperatures can alter phytochemistry, tree resistance traits, and herbivore feeding, but that annual weather variability may modulate warming effects leading to uncertain consequences for plant–insect interactions with projected climate change.     

Weak latitudinal gradients in insect herbivory for dominant rangeland grasses of North America

Patterns of insect herbivory may follow predictable geographical gradients, with greater herbivory at low latitudes. However, biogeographic studies of insect herbivory often do not account for multiple abiotic factors (e.g., precipitation and soil nutrients) that could underlie gradients. We tested for latitudinal clines in insect herbivory as well as climatic, edaphic, and trait‐based drivers of herbivory. We quantified herbivory on five dominant grass species over 23 sites across the Great Plains, USA. We examined the importance of climate, edaphic factors, and traits as correlates of herbivory. Herbivory increased at low latitudes when all grass species were analyzed together and for two grass species individually, while two other grasses trended in this direction. Higher precipitation was related to more herbivory for two species but less herbivory for a different species, while higher specific root length was related to more herbivory for one species and less herbivory for a different species. Taken together, results highlight that climate and trait‐based correlates of herbivory can be highly contextual and species‐specific. Patterns of insect herbivory on dominant grasses support the hypothesis that herbivory increases toward lower latitudes, though weakly, and indicates that climate change may have species‐specific effects on plant–herbivore interactions.     

On the study of plant defence and herbivory using comparative approaches: how important are secondary plant compounds

Species comparisons are a cornerstone of biology and there is a long tradition of using the comparative framework to study the ecology and evolution of plant defensive traits. Early comparative studies led to the hypothesis that plant chemistry plays a central role in plant defence, and the evolution of plant secondary chemistry in response to insect herbivory remains a classic example of coevolution. However, recent comparative work has disagreed with this paradigm, reporting little connection between plant secondary chemicals and herbivory across distantly related plant taxa. One conclusion of this new work is that the importance of secondary chemistry in plant defence may have been generally overstated in earlier research. Here, we attempt to reconcile these contradicting viewpoints on the role of plant chemistry in defence by critically evaluating the use and interpretation of species correlations as a means to study defence–herbivory relationships. We conclude that the notion that plant primary metabolites (e.g. leaf nitrogen content) are the principal determinants of herbivory (or the target of natural selection by herbivores) is not likely to be correct. Despite the inference of recent community‐wide studies of herbivory, strong evidence remains for a prime role of secondary compounds in plant defence against herbivores.     

大气CO2浓度升高对植物、植食性昆虫及其天敌的影响研究进展

自世界工业革命以来,化石燃料的大量使用以及人类对自然环境的过度破坏,致使大气CO₂浓度不断升高.研究大气CO₂浓度升高介导的农业生态系统内植物、植食性昆虫及其天敌的适应机制,对于阐明气候变化下农业害虫爆发危害规律,指导防控与减排具有重要意义.本文综述了大气CO₂浓度升高对农业生态系统中植物、植食性昆虫及天敌的影响,主要包括：1)相关研究方法的改进;2)大气CO₂浓度升高介导的寄主植物营养和次生代谢物质的变化;3)大气CO₂浓度升高对以植物为食的昆虫的个体生长发育、种群数量、行为的影响;4)天敌昆虫的生物学及捕食量与寄生率变化.最后对今后的研究方向进行了展望.     

Leafhopper-induced plant resistance enhances predation risk in a phytophagous beetle

Many herbivores elicit biochemical, physiological, or morphological changes in their host plants that render them more resistant to co-occurring herbivores. Yet, despite the large number of studies that investigate how induced resistance affects herbivore preference and performance, very few have simultaneously explored the cascading effects of induction on higher trophic levels and consequences for prey suppression. In our study system, early-season herbivory by leafhoppers elevated plant resistance to subsequent attack by chrysomelid beetles sharing the same host plant. Notably, beetles feeding on leafhopper-damaged plants incurred developmental penalties (e.g., prolonged time in early larval instars) that rendered them more susceptible to predation by natural enemies. As a result, the combined bottom-up effect of leafhopper-induced resistance and the top-down effect of enhanced predation resulted in the synergistic suppression of beetle populations. These results emphasize that higher trophic level dynamics should be considered in conjunction with induced resistance to better understand how plants mediate interspecific interactions in phytophagous insect communities.     

Above‐ and belowground insect herbivores mediate the impact of nitrogen eutrophication on the soil food web in a grassland ecosystem

Insect herbivores are important drivers of ecosystem processes in grasslands, and can mediate the grassland's response to environmental change. For example, recent evidence shows that above‐ and belowground herbivory, individually and in combination, can modify how a plant community responds to nitrogen (N) eutrophication, an important driver of global change. However, knowledge about how such effects extend to the associated soil food web is lacking. In a mesocosm experiment, we investigated how communities of soil nematodes – an abundant and functionally important group of soil organisms – responded to above‐ and belowground insect herbivory at contrasting N levels. We found that the strongest influence of above‐ and belowground herbivory on the nematode community appeared at elevated N. The abundance of root‐feeding nematodes increased when either above‐ or belowground insect herbivores were present at elevated N, but when applied together the two herbivore types cancelled out one another's effect. Additionally, at elevated N aboveground herbivory increased the abundance of fungal‐feeders relative to bacterial‐feeders, which indicates changes in decomposition pathways induced by N and herbivory. Belowground herbivory increased the abundance of omnivorous nematodes. The shifts in both the herbivorous and detrital parts of the soil food web demonstrate that above‐ and belowground herbivory does not only mediate the response of the plant community to N eutrophication, but in extension also the soil food web sustained by the plant community. We conclude that feedbacks between effects of above‐ and belowground herbivory mediate the response of the grassland ecosystem to N eutrophication.     

昆虫唾液成分在昆虫与植物关系中的作用

近年来,人们对于植食性昆虫唾液的深入研究,揭示出其在昆虫与植物的相互关系和协同进化中起到非常重要的作用。植食性昆虫唾液中含有的酶类和各种有机成分,能诱导植物的一系列生化反应,而且这些反应有很强的特异性,与为害的昆虫种类甚至龄期有关。鳞翅目幼虫口腔分泌物（或反吐液）中含有的β-葡糖苷酶、葡萄糖氧化酶等酶类和挥发物诱导素等有机成分,已经证明可以诱导植物的反应; 刺吸式昆虫的取食也可以刺激植物产生反应,但其唾液内的酶类,如烟粉虱的碱性磷酸酶, 蚜虫的酚氧化酶、果胶酶和多聚半乳糖醛酸酶, 蝽类的寡聚半乳糖醛酸酶等是否发挥作用,目前还没有直接的证据。寄主植物对昆虫的唾液成分也有很大的影响,可能是昆虫对不同植物营养成分和毒性成分的适应方式。对昆虫唾液蛋白的分析表明,具有同样类型口器、食物类型接近的昆虫,唾液成分有更多的相似性。研究植食性昆虫的唾液成分,对于阐明昆虫和植物的协同进化关系、昆虫生物型的形成机理、害虫的致害机理,以及指导害虫防治等,有着一定的理论和实际意义。     

Potential effects of elevated carbon dioxide on leaf-feeding forest insects

The elevated concentration of atmospheric CO2 may result in a decline of leaf nutritional quality (especially N) and an increase in some kinds of defensive secondary components (such as phenolics). The changes in the phytochemistry of trees, combined with the effect of elevated CO2 per se, have a potential negative influence on insect herbivores. Here, we review the effect of elevated CO2 on the performance of leaf-feeding forest insects at individual-level and commu-nity-level. The elevated CO2 per se have little influence on the metabolism of insects. Over half of the tree-insect experimental systems show that the performance of individual insect become poorer under high-CO2 grown trees; but the others show that the insects have just little or no response to the treatments. The direction and magnitude of the changes in the performance of insects could be mediated by various factors. The effects of treatment are strongly species-dependent. The magni-tude of changes in the phytochemistry, the sensitivity and adaptive capacity of insects to the poorer leaf quality, the differences in plant growth conditions and experimental methods, and the mediated effects of other environmental factors (such as soil nutrient availability, light, temperature, O3) were all closely related to the final performance of insects. However, the larvae's consumption usually increased under enriched CO2 treatment, which was widely thought to be a compensa-tory response to poorer plant quality. The experiments on forest community-level found identically a reduction in herbivory, which was contrary to the results from small-scale experiments. The changes in insect popula-tion and the actual response of consumption by leaf-feeding forest insects under CO2 enrichment remain unclear, and more field-based experiments need to be conducted.     

植物次生代谢及其与环境的关系

人类对植物次生代谢产物（天然产物）的早期研究源于它们的应用价值,近些年来人们越来越认识到植物次生代谢产物广泛的生物学效应,开始重新评价这些化合物在植物生命活动以及生态系统中可能扮演的角色。植物的次生代谢是植物在长期进化中与环境（生物的和非生物的）相互作用的结果,次生代谢产物在植物提高自身保护和生存竞争能力、协调与环境关系上充当着重要的角色。介绍了植物次生代谢及其产物的特点,概述了植物次生代谢与温度、水分、光照、养分、CO2浓度、UV-B辐射、环境污染等非生物环境以及与化学防御、化感作用、菌根共生、微生物病害的关系。研究植物次生代谢与环境的关系,可以从更深的层次发掘植物与环境的内在联系,为全面、深入认识植物与环境的相互关系提供新的研究途径,同时也有利于人类更有效、合理地利用植物的次生代谢产物。     

Effects of insect attack to stems on plant survival,growth, reproduction and photosynthesis

Studies of insect herbivory have mostly focused on leaf‐feeding even though most woody plant biomass is stem tissue. Attack to stems has the potential to be more detrimental to plant performance than attack to leaves. Here we asked how severe is the impact of insect stem herbivory on plant performance. We quantify the effect of insect stem herbivory via a meta‐analysis of 119 papers in 100 studies (papers by the same authors were treated as the same study). These studies involved 92 plant species and 70 species of insect herbivore (including simulated herbivory). Attack to plant stems reduced plant performance by an average of approximately 22%. Stem herbivory had greatest impacts on plant and branch survival, which was reduced by 63%. Measures of plant reproduction and vegetative biomass were reduced by 33% and 16% respectively, while measurements of photosynthetic rate were not significantly different between plants with and without stem herbivore attack. Stem herbivory led to a decline in leader performance but an increase in performance of laterals, highlighting the importance of plant compensation. Juvenile plants were more severely affected by stem herbivory than adult plants, and studies conducted in greenhouses found more severe effects than studies conducted in the field. Stem herbivory did not have a significant effects on any of the non‐performance responses measured (defence compounds, SLA, root:shoot, phenology and plant carbon and nitrogen). We compare our results with results from various meta‐analyses considering herbivory on other plant parts. The impact of insect herbivory to stems on plant performance appears at least as severe as insect herbivory to roots and leaves, if not more.     

Herbivore‐induced plant responses in Brassica oleracea prevail over effects of constitutive resistance and result in enhanced herbivore attack

1. Plant responses to herbivore attack may have community‐wide effects on the composition of the plant‐associated insect community. Thereby, plant responses to an early‐season herbivore may have profound consequences for the amount and type of future attack. 2. Here we studied the effect of early‐season herbivory by caterpillars of Pieris rapae on the composition of the insect herbivore community on domesticated Brassica oleracea plants. We compared the effect of herbivory on two cultivars that differ in the degree of susceptibility to herbivores to analyse whether induced plant responses supersede differences caused by constitutive resistance. 3. Early‐season herbivory affected the herbivore community, having contrasting effects on different herbivore species, while these effects were similar on the two cultivars. Generalist insect herbivores avoided plants that had been induced, whereas these plants were colonised preferentially by specialist herbivores belonging to both leaf‐chewing and sap‐sucking guilds. 4. Our results show that community‐wide effects of early‐season herbivory may prevail over effects of constitutive plant resistance. Induced responses triggered by prior herbivory may lead to an increase in susceptibility to the dominant specialists in the herbivorous insect community. The outcome of the balance between contrasting responses of herbivorous community members to induced plants therefore determines whether induced plant responses result in enhanced plant resistance.