Solar ultraviolet-B radiation alters the attractiveness of Arabidopsis plants to diamondback moths (Plutella xylostella L.): impacts on oviposition and involvement of the jasmonic acid pathway

Solar ultraviolet-B radiation (UV-B) can have large impacts on the interactions between plants and herbivorous insects. Several studies have documented effects of UV-B-induced changes in plant tissue quality on the feeding performance of insect larvae. In contrast, the effects of UV-B-induced plant responses on the behavior of adult insects have received little attention. We carried out a series of field and glasshouse experiments using the model plant Arabidopsis thaliana L. and the crucifer-specialist insect Plutella xylostella L. (diamondback moth) to investigate the effects of UV-B on natural herbivory and plant–insect interactions. Natural herbivory under field conditions was less severe on plants exposed to ambient UV-B than on plants grown under filters that attenuated the UV-B component of solar radiation. This reduced herbivory could not be accounted for by effects of UV-B on larval feeding preference and performance, as P. xylostella caterpillars did not respond to changes in plant quality induced by UV-B. In contrast, at the adult stage, the insects presented clear behavioral responses: P. xylostella moths deposited significantly more eggs on plants grown under attenuated UV-B levels than on plants exposed to ambient UV-B. The deterring effect of UV-B exposure on insect oviposition was absent in jar1-1, a mutant with impaired jasmonic acid (JA) sensitivity, but it was conserved in mutants with altered ethylene signaling. The jar1-1 mutant also presented reduced levels of UV-absorbing phenolic compounds than the other genotypes that we tested. Our results suggest that variations in UV-B exposure under natural conditions can have significant effects on insect herbivory by altering plant traits that female adults use as sources of information during the process of host selection for oviposition. These effects of natural UV-B on plant quality appear to be mediated by activation of signaling circuits in which the defense-related hormone JA plays a functional role.     

Plant‐mediated interactions between two herbivores differentially affect a subsequently arriving third herbivore in populations of wild cabbage

• Plants are part of biodiverse communities and frequently suffer from attack by multiple herbivorous insects. Plant responses to these herbivores are specific for insect feeding guilds: aphids and caterpillars induce different plant phenotypes. Moreover, plants respond differentially to single or dual herbivory, which may cascade into a chain of interactions in terms of resistance to other community members. Whether differential responses to single or dual herbivory have consequences for plant resistance to yet a third herbivore is unknown.
• We assessed the effects of single or dual herbivory by Brevicoryne brassicae aphids and/or Plutella xylostella caterpillars on resistance of plants from three natural populations of wild cabbage to feeding by caterpillars of Mamestra brassicae. We measured plant gene expression and phytohormone concentrations to illustrate mechanisms involved in induced responses.
• Performance of both B. brassicae and P. xylostella was reduced when feeding simultaneously with the other herbivore, compared to feeding alone. Gene expression and phytohormone concentrations in plants exposed to dual herbivory were different from those found in plants exposed to herbivory by either insect alone. Plants previously induced by both P. xylostella and B. brassicae negatively affected growth of the subsequently arriving M. brassicae. Furthermore, induced responses varied between wild cabbage populations.
• Feeding by multiple herbivores differentially activates plant defences, which has plant‐mediated negative consequences for a subsequently arriving herbivore. Plant population‐specific responses suggest that plant populations adapt to the specific communities of insect herbivores. Our study contributes to the understanding of plant defence plasticity in response to multiple insect attacks.

     

植物抗虫“防御警备”: 概念、机理与应用

植物抗虫“防御警备”是指受到某些生物或者非生物因子刺激警备后,植物会提前做好抗虫防御准备,之后当再次受到害虫袭击时,植物会产生更加快速和强烈的抗虫防御反应,从而使自身抗虫性显著提高.这是近年来新发现的植物防御害虫的一种策略,是一种特殊的诱导抗虫机制.植食性昆虫的取食、分泌物、产卵、为害诱导的植物挥发物(HIPVs)以及某些有益微生物、植物营养元素、重金属和一些化学物质均可以引起植物产生抗虫防御警备.防御警备具有抗性高效、持久、环境友好,甚至可以遗传到子代等优点.本文综述了近年来有关植物抗虫防御警备的研究,主要概括了植物抗虫防御警备的一般特征、刺激警备因子和形成机制,并对其在生产实践中的应用前景进行了简要分析,提出了这一领域尚未解决的问题和亟待深入的研究方向.通过合适的方法使植物产生抗虫防御警备可以大大减少杀虫剂的使用,成为害虫综合防治的重要手段.     

Field evidence for indirect interactions between foliar‐feeding insect and root‐feeding nematode communities on Nicotiana tabacum

Abstract 1. As herbivory often elicits systemic changes in plant traits, indirect interactions via induced plant responses may be a pervasive feature structuring herbivore communities. Although the importance of this phenomenon has been emphasised for herbivorous insects, it is unknown if and how induced responses contribute to the organisation of other major phytoparasitic taxa. 2. Survey and experimental field studies were used to investigate the role of plants in linking the dynamics of foliar‐feeding insects and root‐feeding nematodes on tobacco, Nicotiana tabacum. 3. Plant‐mediated interactions between insects and nematodes could largely be differentiated by insect feeding guild, with positive insect–nematode interactions predominating with leaf‐chewing insects (caterpillars) and negative interactions occurring with sap‐feeding insects (aphids). For example, insect defoliation was positively correlated with the abundance of root‐feeding nematodes, but aphids and nematodes were negatively correlated. Experimental field manipulations of foliar insect and nematode root herbivory also tended to support this outcome. 4. Overall, these results suggest that plants indirectly link the dynamics of divergent consumer taxa in spatially distinct ecosystems. This lends support to the growing perception that plants play a critical role in propagating indirect effects among a diverse assemblage of consumers.     

Interactions between above- and belowground insect herbivores as mediated by the plant defense system

Plants are frequently attacked by both above- and belowground arthropod herbivores. Nevertheless, studies rarely consider root and shoot herbivory in conjunction. Here we provide evidence that the root-feeding insect Agriotes lineatus reduces the performance of the foliage feeding insect Spodoptera exigua on cotton plants. In a bioassay, S. exigua larvae were allowed to feed on either undamaged plants, or on plants that had previously been exposed to root herbivory, foliar herbivory, or a combination of both. Previous root herbivory reduced the relative growth rates as well as the food consumption of S. exigua by more than 50% in comparison to larvae feeding on the undamaged controls. We found no effects in the opposite direction, as aboveground herbivory by S. exigua did not affect the relative growth rates of root-feeding A. lineatus . Remarkably, neither did the treatment with foliar herbivory affect the food consumption and relative growth rate of S. exigua in the bioassay. However, this treatment did result in a significant change in the distribution of S. exigua feeding. Plants that had been pre-exposed to foliar herbivory suffered significantly less damage on their young terminal leaves. While plant growth and foliar nitrogen levels were not affected by any of the treatments, we did find significant differences between treatments with respect to the level and distribution of plant defensive chemicals (terpenoids). Exposure to root herbivores resulted in an increase in terpenoid levels in both roots as well as in mature and immature foliage. Foliar damage, on the other hand, resulted in high terpenoid levels in young, terminal leaves only. Our results show that root-feeding herbivores may change the level and distribution of plant defenses aboveground. Our data suggest that the reported interactions between below- and aboveground insect herbivores are mediated by induced changes in plant secondary chemistry.     

Herbivore-specific plant volatiles prime neighboring plants for nonspecific defense responses

Plants produce species-specific herbivore-induced plant volatiles (HIPVs) after damage. We tested the hypothesis that herbivore-specific HIPVs prime neighboring plants to induce defenses specific to the priming herbivore. Since Manduca sexta (specialist) and Heliothis virescens (generalist) herbivory induced unique HIPV profiles in Nicotiana benthamiana, we used these HIPVs to prime receiver plants for defense responses to simulated herbivory (mechanical wounding and herbivore regurgitant application). Jasmonic acid (JA) accumulations and emitted volatile profiles were monitored as representative defense responses since JA is the major plant hormone involved in wound and defense signaling and HIPVs have been implicated as signals in tritrophic interactions. Herbivore species-specific HIPVs primed neighboring plants, which produced 2 to 4 times more volatiles and JA after simulated herbivory when compared to similarly treated constitutive volatile-exposed plants. However, HIPV-exposed plants accumulated similar amounts of volatiles and JA independent of the combination of priming or challenging herbivore. Furthermore, volatile profiles emitted by primed plants depended only on the challenging herbivore species but not on the species-specific HIPV profile of damaged emitter plants. This suggests that feeding by either herbivore species primed neighboring plants for increased HIPV emissions specific to the subsequently attacking herbivore and is probably controlled by JA.     

Leaf herbivory and drought stress affect floral attractive and defensive traits in Nicotiana quadrivalvis

Adaptive phenotypic plasticity allows sessile organisms such as plants to match trait expression to the particular environment they experience. Plasticity may be limited, however, by resources in the environment, by responses to prior environmental cues, or by previous interactions with other species, such as competition or herbivory. Thus, understanding the expression of plastic traits and their effects on plant performance requires evaluating trait expression in complex environments, rather than across levels of a single variable. In this study, we tested the independent and combined effects of two components of a plant’s environment, herbivory and water availability, on the expression of attractive and defensive traits in Nicotiana quadrivalvis in the greenhouse. Damage and drought did not affect leaf nicotine concentrations but had additive and non-additive effects on floral attractive and defensive traits. Plants in the high water treatment produced larger flowers with more nectar than in the low water treatment. Leaf damage induced greater nectar volumes in the high water treatment only, suggesting that low water limited plastic responses to herbivore damage. Leaf damage also tended to induce higher nicotine concentrations in nectar, consistent with other studies showing that leaf damage can induce floral defenses. Our results suggest that there are separate and synergistic effects of leaf herbivory and drought on floral trait expression, and thus plasticity in response to complex environments may influence plant fitness via effects on floral visitation and defense.     

Effects of elevated ultraviolet-B radiation on a plant–herbivore interaction

Enhanced ultraviolet-B (UV-B) radiation may have multiple effects on both plants and animals and affect plant–herbivore interactions directly and indirectly by inducing changes in host plant quality. In this study, we examined combined effects of UV-B and herbivory on the defence of the mountain birch (Betula pubescens ssp. czerepanovii) and also the effects of enhanced UV-B radiation on a geometrid with an outbreak cycle: the autumnal moth (Epirrita autumnata). We established an experiment mimicking ozone depletion of 30% (a relevant level when simulating ozone depletion above Northern Lapland). Both arctic species responded only slightly to the enhanced level of UV-B radiation, which may indicate that these species are already adapted to a broader range of UV-B radiation. UV-B exposure slightly induced the accumulation of myricetin glycosides but had no significant effect on the contents of quercetin or kaempferol derivatives. Mountain birch seedlings responded more efficiently to herbivory wounding than to enhanced UV-B exposure. Herbivory induced the activities of foliar oxidases that had earlier been shown to impair both feeding and growth of moth larvae. In contrast, the contents of foliar phenolics did not show the same response in different clones, except for a decrease in the contents of tannin precursors. The induction of foliar phenoloxidase activities is a specific defence response of mountain birches against insect herbivory. To conclude, our results do not support the hypothesis that the outbreak cycle of the autumnal moth can be explained by the cycles of solar activity and UV-B.     

Ecological and Evolutionary Interactions between Wild Crucifers and Their Herbivorous Insects

Abstract Insects feeding on ten species of wild crucifer were investigated. Differences in host plant range and insect community structure were examined with regard to anti-herbivore defense mechanisms. Most of the crucifer species deterred insect herbivory by disappearing in the summer or by lowering their intrinsic quality as food for insects. Species with these defense mechanisms were exploited by only a few specialized herbivorous insects that seemed to have counter defenses. The plants without these defense mechanisms were used by many herbivorous insect species. Rorippa indica lacked direct defenses, but supported a low total density of herbivore individuals. This crucifer has an indirect defense mechanism: ants attracted to floral nectar defended the plant from deleterious herbivores. Crucifers that disappeared seasonally lacked other anti-herbivore defense mechanisms. This suggests that the phonological response is an alternative other responses to herbivore attack.     

The effect of elevated UV-B radiation on herbivory of pea byAutographa gamma

Leaves exposed to above-ambient fluxes of ultraviolet-B (UV-B) radiation commonly contain increased concentrations of phenolic compounds which may influence herbivores. However, the hypothesis that elevated UV-B modifies herbivory, whether mediated by phenolics or other plant constituents, has rarely been studied experimentally. We investigated the responses of the mothAutographa gamma L. (Lepidoptera: Noctuidae) to pea (Pisum sativum L.) grown at a range of plant-effective UV-B fluxes. Although total phenolics did increase significantly with increasing UV-B, this change had little deleterious effect on the 5th instar larvae ofA. gamma. However, tissue nitrogen also increased with increasing UV-B. Increased nitrogen was correlated with an increase in the efficiency with which larvae utilized their food and in larval growth rate, but in a reduction in the amount of plant material consumed. The apparently major role of nitrogen in determining herbivore responses to changing UV-B demonstrates the risks in predicting such responses soley on the basis of changes in phenolics and other secondary metabolites.     

Ultraviolet-B radiation co-opts defense signaling pathways

Plants in the field exposed to ambient solar ultraviolet-B (UV-B) radiation (280-320 nm) often show an increased resistance to herbivorous insects compared with control plants grown under filters that exclude the UV-B component of solar radiation. This corresponds with a significant overlap in gene expression between the UV-B and the wounding/herbivory response. Furthermore, wound-responsive signaling components such as mitogen-activated protein kinases are activated by UV-B. A mechanistic explanation for these overlaps might be that UV-B co-opts cell surface receptors for defense signals such as systemin and oligosaccharide elicitors in a ligand-independent manner.     

Effects of amount and recurrence of leaf herbivory on the induction of direct and indirect defences in wild cotton

• The induction of defences in response to herbivory is a key mechanism of plant resistance. While a number of studies have investigated the time course and magnitude of plant induction in response to a single event of herbivory, few have looked at the effects of recurrent herbivory. Furthermore, studies measuring the effects of the total amount and recurrence of herbivory on both direct and indirect plant defences are lacking. To address this gap, here we asked whether insect leaf herbivory induced changes in the amount and concentration of extrafloral nectar (an indirect defence) and concentration of leaf phenolic compounds (a direct defence) in wild cotton (Gossypium hirsutum).
• We conducted a greenhouse experiment where we tested single event or recurrent herbivory effects on defence induction by applying mechanical leaf damage and caterpillar (Spodoptera frugiperda) regurgitant.
• Single events of 25% and 50% leaf damage did not significantly influence extrafloral nectar production or concentration. Extrafloral nectar traits did, however, increase significantly relative to controls when plants were exposed to recurrent herbivory (two episodes of 25% damage). In contrast, phenolic compounds increased significantly in response to single events of  leaf damage but not to recurrent damage. In addition, we found. that local induction of extrafloral nectar production was stronger than systemic induction, whereas the reverse pattern was observed for phenolics.
• Together, these results reveal seemingly inverse patterns of induction of direct and indirect defences in response to herbivory in wild cotton.

     

Polyphenol oxidase and herbivore defense in trembling aspen (Populus tremuloides): cDNA cloning, expression, and potential substrates

The biochemical anti-herbivore defense of trembling aspen ( Populus tremuloides Michx.) was investigated in a molecular analysis of polyphenol oxidase (PPO; EC 1.10.3.2). A PPO cDNA was isolated from a trembling aspen wounded leaf cDNA library and its nucleotide sequence determined. Southern analysis indicated the presence of two PPO genes in the trembling aspen genome. Expression of PPO was found to be induced after herbivory by forest tent caterpillar, by wounding, and by methyl jasmonate treatment. Wound induction was systemic, and occurred in unwounded leaves on wounded plants. This pattern of expression is consistent with a role of this enzyme in insect defense. A search for potential PPO substrates in ethanolic aspen leaf extracts using electron spin resonance (ESR) found no pre-existing diphenolic compounds. However, following a brief delay and several additions of oxygen, an ESR signal specific for catechol was detected. The source of this catechol was most likely the aspen phenolic glycosides tremulacin or salicortin which decomposed during ESR experiments. This was subsequently confirmed in experiments using pure salicortin.     

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.     

Global Change Effects on Plant Chemical Defenses against Insect Herbivores

This review focuses on individual effects of major global change factors, such as elevated CO2, Oa, UV light and temperature,on plant secondary chemistry. These secondary metabolites are well-known for their role in plant defense against insect herbivory. Global change effects on secondary chemicals appear to be plant species-specific and dependent on the chemical type. Even though plant chemical responses induced by these factors are highly variable, there seems to be some specificity in the response to different environmental stressors. For example, even though the production of phenolic compounds is enhanced by both elevated CO2 and UV light levels, the latter appears to primarily increase the concentrations of fiavonoids. Likewise, specific phenolic metabolites seem to be induced by O3 but not by other factors, and an increase in volatile organic compounds has been particularly detected under elevated temperature. More information is needed regarding how global change factors influence inducibility of plant chemical defenses as well as how their indirect and direct effects impact insect performance and behavior, herbivory rates and pathogen attack. This knowledge is crucial to better understand how plants and their associated natural enemies will be affected in future changing environments.