Can plants use an entomopathogenic virus as a defense against herbivores?

It is by now well established that plants use various strategies to defend themselves against herbivores. Besides conventional weapons such as spines and stinging hairs and sophisticated chemical defenses, plants can also involve the enemies of the herbivores in their defense. It has been suggested that plants could even use entomopathogens as part of their defense strategies. In this paper, we show that Brassica oleraceae plants that are attacked by Myzus persicae aphids infected with an entomopathogenic parvovirus (M. persicae densovirus) transport the virus through the phloem locally and systematically. Moreover, healthy aphids that fed on the same leaf, but separated from infected aphids were infected via the plant. Hence, this is proof of the principle that plants can be vectors of an insect virus and can possibly use this virus as a defense against herbivores.     

植物诱导性直接防御

众所周知,植物对植食性昆虫危害的反应表现在3个方面：直接防御,间接防御,和耐害性。直接防御是指植物自身所具有的能影响寄主植物感虫性的所有特性。植物对昆虫危害的直接防御包括：限制食物供给,降低营养价值,减少偏嗜程度,破坏组织结构和抑制害虫代谢途径。目前已知的防御化合物主要包括植物次生代谢物质、昆虫消化酶（蛋白）抑制剂、蛋白酶、凝集素、氨基酸脱氨酶和氧化酶。植物在防御某种昆虫为害时多个因素往往具有累加效应或协同作用,并且对一种昆虫起主导作用的因素在防御另一种昆虫时可能仅仅起次要作用甚至根本不起作用。因此,对寄主植物基因表达、蛋白水平和活性以及代谢物含量在不同时空条件下进行广泛的定量和定性的高通量分析,不仅可以促进对植物直接防御机制的全面理解,而且有助于在农业生产中加快对作物抗性的特定靶标的鉴定。     

Inducible direct plant defense against insect herbivores: A review

Plants respond to insect herbivory with responses broadly known as direct defenses, indirect defenses, and tolerance. Direct defenses include all plant traits that affect susceptibility of host plants by themselves. Overall categories of direct plant defenses against insect herbivores include limiting food supply, reducing nutrient value, reducing preference, disrupting physical structures, and inhibiting chemical pathways of the attacking insect. Major known defense chemicals include plant secondary metabolites, protein inhibitors of insect digestive enzymes, proteases, lectins, amino acid deaminases and oxidases. Multiple factors with additive or even synergistic impact are usually involved in defense against a specific insect species, and factors of major importance to one insect species may only be of secondary importance or not effective at all against another insect species. Extensive qualitative and quantitative high throughput analyses of temporal and spatial variations in gene expression, protein level and activity, and metabolite concentration will accelerate not only the understanding of the overall mechanisms of direct defense, but also accelerate the identification of specific targets for enhancement of plant resistance for agriculture.     

Colorado potato beetle manipulates plant defenses in local and systemic leaves

Herbivore microbial associates can affect diverse interactions between plants and insect herbivores. Some insect symbionts enable herbivores to expand host plant range or to facilitate host plant use by modifying plant physiology. However, little attention has been paid to the role of herbivore-associated microbes in manipulating plant defenses. We have recently shown that Colorado potato beetle secrete the symbiotic bacteria to suppress plant defenses. The bacteria in oral secretions from the beetle hijack defense signaling pathways of host plants and the suppression of induced plant defenses benefits the beetle’s performance. While the defense suppression by the beetle-associated bacteria has been investigated in local damaged leaves, little is known about the effects of the symbiotic bacteria on the manipulation of plant defenses in systemic undamaged leaves. Here, we demonstrate that the symbiotic bacteria suppress plant defenses in both local and systemic tissues when plants are attacked by antibiotic-untreated larvae.     

The defensive role of Ni hyperaccumulation by plants: a field experiment

Hyperaccumulation of Ni by plants is hypothesized to function as an elemental defense against herbivores and pathogens. Laboratory experiments have documented toxic effects to herbivores consuming high-Ni plant tissues, but this paper reports the first experiment to examine the defensive effectiveness of Ni hyperaccumulation under field conditions. The experiment was conducted at an ultramafic soil site naturally inhabited by the Ni hyperaccumulator Streptanthus polygaloides (Brassicaceae). Experimental treatments examined the response of herbivores to hyperaccumulated Ni, using exclosure and insecticide treatments to divide herbivores into groups based primarily upon herbivore size. Three soils (Ni-amended greenhouse soil, unamended greenhouse soil, ultramafic soil), three exclosure treatments (exclosure, control exclosure, no exclosure), and a systemic insecticide treatment were combined in a fractional factorial experimental design. Streptanthus polygaloides plants were grown in a greenhouse for 2 mo, transplanted into the field by inserting potted plants into holes dug on the experimental site, and periodically examined for herbivore damage during a 41-d period. Initial surveys showed greater amounts of insect damage to plants with low tissue Ni levels, confirming the defensive effect of Ni against some insect herbivores, but large herbivores (probably vertebrates) later consumed entire plants regardless of plant Ni status. We concluded that Ni was not an effective defense against these large herbivores, probably because their diets mix high-Ni S. polygaloides foliage with that of associated non-hyperaccumulating species. We suggest that such dietary dilution is one mechanism whereby some herbivores can circumvent elemental plant defenses.     

Physiological function and ecological aspects of fatty acid-amino acid conjugates in insects†

In tritrophic interactions, plants recognize herbivore-produced elicitors and release a blend of volatile compounds (VOCs), which work as chemical cues for parasitoids or predators to locate their hosts. From detection of elicitors to VOC emissions, plants utilize sophisticated systems that resemble the plant–microbe interaction system. Fatty acid–amino acid conjugates (FACs), a class of insect elicitors, resemble compounds synthesized by microbes in nature. Recent evidence suggests that the recognition of insect elicitors by an ancestral microbe-associated defense system may be the origin of tritrophic interactions mediated by FACs. Here we discuss our findings in light of how plants have customized this defense to be effective against insect herbivores, and how some insects have successfully adapted to these defenses.     

Nonglandular silicified trichomes are essential for rice defense against chewing herbivores

Interspecific New Rice for Africa (NERICA) varieties have been recently developed and used in Sub-Saharan Africa but herbivore resistance properties of these plants remain poorly understood. Here we report that, compared to a local Japanese cultivar Nipponbare, NERICA 1, 4 and 10 are significantly more damaged by insect herbivores in the paddy fields. In contrast to high levels of leaf damage from rice skippers and grasshoppers, constitutive and induced volatile organic compounds for indirect plant defense were higher or similar in NERICAs and Nipponbare. Accumulation of direct defense secondary metabolites, momilactones A and B, and p-coumaroylputrescine (CoP) was reduced in NERICAs, while feruloylputrescine accumulated at similar levels in all varieties. Finally, we found that Nipponbare leaves were covered with sharp nonglandular trichomes impregnated with silicon but comparable defense structures were virtually absent in herbivory-prone NERICA plants. As damage to the larval gut membranes by Nipponbare silicified trichomes that pass intact through the insect digestive system, occurs, and larval performance is enhanced by trichome removal from otherwise chemically defended Nipponbare plants, we propose that silicified trichomes work as an important defense mechanism of rice against chewing insect herbivores.     

Parasitism by Cuscuta pentagona attenuates host plant defenses against insect herbivores

Considerable research has examined plant responses to concurrent attack by herbivores and pathogens, but the effects of attack by parasitic plants, another important class of plant-feeding organisms, on plant defenses against other enemies has not been explored. We investigated how attack by the parasitic plant Cuscuta pentagona impacted tomato (Solanum lycopersicum) defenses against the chewing insect beet armyworm (Spodoptera exigua; BAW). In response to insect feeding, C. pentagona-infested (parasitized) tomato plants produced only one-third of the antiherbivore phytohormone jasmonic acid (JA) produced by unparasitized plants. Similarly, parasitized tomato, in contrast to unparasitized plants, failed to emit herbivore-induced volatiles after 3 d of BAW feeding. Although parasitism impaired antiherbivore defenses, BAW growth was slower on parasitized tomato leaves. Vines of C. pentagona did not translocate JA from BAW-infested plants: amounts of JA in parasite vines grown on caterpillar-fed and control plants were similar. Parasitized plants generally contained more salicylic acid (SA), which can inhibit JA in some systems. Parasitized mutant (NahG) tomato plants deficient in SA produced more JA in response to insect feeding than parasitized wild-type plants, further suggesting cross talk between the SA and JA defense signaling pathways. However, JA induction by BAW was still reduced in parasitized compared to unparasitized NahG, implying that other factors must be involved. We found that parasitized plants were capable of producing induced volatiles when experimentally treated with JA, indicating that resource depletion by the parasite does not fully explain the observed attenuation of volatile response to herbivore feeding. Collectively, these findings show that parasitic plants can have important consequences for host plant defense against herbivores.     

Comparative analysis of quantitative trait loci controlling glucosinolates,myrosinase and insect resistance in Arabidopsis thaliana

Evolutionary interactions among insect herbivores and plant chemical defenses have generated systems where plant compounds have opposing fitness consequences for host plants, depending on attack by various insect herbivores. This interplay complicates understanding of fitness costs and benefits of plant chemical defenses. We are studying the role of the glucosinolate-myrosinase chemical defense system in protecting Arabidopsis thaliana from specialist and generalist insect herbivory. We used two Arabidopsis recombinant inbred populations in which we had previously mapped QTL controlling variation in the glucosinolate-myrosinase system. In this study we mapped QTL controlling resistance to specialist (Plutella xylostella) and generalist (Trichoplusia ni) herbivores. We identified a number of QTL that are specific to one herbivore or the other, as well as a single QTL that controls resistance to both insects. Comparison of QTL for herbivory, glucosinolates, and myrosinase showed that T. ni herbivory is strongly deterred by higher glucosinolate levels, faster breakdown rates, and specific chemical structures. In contrast, P. xylostella herbivory is uncorrelated with variation in the glucosinolate-myrosinase system. This agrees with evolutionary theory stating that specialist insects may overcome host plant chemical defenses, whereas generalists will be sensitive to these same defenses.     

Plant latex and other exudates as plant defense systems: roles of various defense chemicals and proteins contained therein

Plant latex and other exudates are saps that are exuded from the points of plant damage caused either mechanically or by insect herbivory. Although many (ca. 10%) of plant species exude latex or exudates, and although the defensive roles of plant latex against herbivorous insects have long been suggested by several studies, the detailed roles and functions of various latex ingredients, proteins and chemicals, in anti-herbivore plant defenses have not been well documented despite the wide occurrence of latex in the plant kingdom. Recently, however, substantial progress has been made. Several latex proteins, including cysteine proteases and chitin-related proteins, have been shown to play important defensive roles against insect herbivory. In the mulberry (Morus spp.)-silkworm (Bombyx mori) interaction, an old and well-known model system of plant-insect interaction, plant latex and its ingredients - sugar-mimic alkaloids and defense protein MLX56 - are found to play key roles. Complicated molecular interactions between Apocynaceae species and its specialist herbivores, in which cardenolides and defense proteins in latex play key roles, are becoming more and more evident. Emerging observations suggested that plant latex, analogous to animal venom, is a treasury of useful defense proteins and chemicals that has evolved through interspecific interactions. On the other hand, specialist herbivores developed sophisticated adaptations, either molecular, physiological, or behavioral, against latex-borne defenses. The existence of various adaptations in specialist herbivores itself is evidence that latex and its ingredients function as defenses at least against generalists. Here, we review molecular and structural mechanisms, ecological roles, and evolutionary aspects of plant latex as a general defense against insect herbivory and we discuss, from recent studies, the unique characteristics of latex-borne defense systems as transport systems of defense substances are discussed based on recent studies.     

Plant silicon effects on insect feeding dynamics are influenced by plant nitrogen availability

Although there is growing evidence that silicon (Si)‐based plant defenses effectively reduce both the palatability and digestibility of leaves, and thus impact nutrient assimilation by insect herbivores, much less is known about how this is affected by extrinsic and intrinsic factors. For example, do herbivores exhibit compensatory feeding on poor‐quality diets with Si or are Si defenses less effective in agroecosystems where high N availability increases plant quality? To investigate the interactive effects of N and Si on insect feeding, we conducted insect performance and compensatory feeding bioassays using maize, Zea mays L. (Poaceae), and the true armyworm, Pseudeletia unipuncta Haworth (Lepidoptera: Noctuidae). In the performance assay, the addition of Si alone resulted in increased larval mortality compared with the controls, likely because early instars with poorly developed mandibles could not feed effectively. However, larvae fed on plants treated with both Si and N survived better than on plants treated with Si only, although pupal mass did not differ between treatments. In our compensatory assay, Si addition reduced maize consumption, but increased both armyworm approximate digestibility and N assimilation efficiency, suggesting that enhanced post‐ingestion feeding physiology, rather than compensatory food intake, could have accounted for the lack of Si effects on pupal weight. Overall, our results demonstrate that, similar to other chemical and mechanical defenses, the effectiveness of plant Si defense is influenced by plant nutrient status and consumer compensatory ability.     

昆虫取食诱导的植物防御反应

植物被昆虫取食后可产生直接防御或间接防御。直接防御通过增加有毒的次生代谢产物或防御蛋白对昆虫生理代谢产生不利的影响,但对植物的消耗较大。间接防御通过释放挥发性化合物吸引天敌昆虫,并以此控制植食性昆虫。特异性的昆虫激发子(insect specific elicitors)能够诱导挥发性化合物的释放。多种信号途径参与昆虫取食诱导的植物防御反应,它们之间的相互作用协同或拮抗。了解昆虫取食诱导的植物防御反应,对于害虫综合治理策略的完善具有重要的意义。     

Effects of different secondary metabolite profiles in plant defense syndromes on specialist and generalist herbivores

Plants defend themselves against herbivores not only by a single trait but also by diversified multiple defense strategies. It remains unclear how these multiple defense mechanisms are effectively organized against herbivores. In this study, we focused on Brassicaceae plants, which have one of the most diversified secondary metabolites, glucosinolates (GSLs), as a defense against herbivores. By analyzing various defense traits including GSL profiles among 12 species (11 genera) of Brassicaceae plants, it is revealed that their defense strategies can be divided into three categories as multiple defenses. The GSL profiles differed between these three categories: (i) high nutritional level with long‐chain aliphatic GSLs; (ii) low nutritional level and high physical defenses with short‐chain aliphatic GSLs; and (iii) high nutritional level and low defense. The feeding experiment was conducted using two types of herbivores, Pieris rapae (Lepidoptera: Pieridae) as a specialist herbivore and the Eri silkmoth Samia cynthia ricini (Lepidoptera: Saturniidae) as a generalist, to assess the ability of each plant in multiple defense strategy. It was observed that the Eri silkmoth's performance differed according to which defense strategy it was exposed to. However, the growth rate of P. rapae did not vary among the three categories of defense strategy. These results suggest that the diversified defense strategies of Brassicaceae species have evolved to cope with diversified herbivores.     

The function of small RNAs in plant biotic stress response

Small RNAs(s RNAs) play essential roles in plants upon biotic stress. Plants utilize RNA silencing machinery to facilitate pathogen-associated molecular pattern-triggered immunity and effector-triggered immunity to defend against pathogen attack or to facilitate defense against insect herbivores. Pathogens, on the other hand, are also able to generate effectors and s RNAs to counter the host immune response. The arms race between plants and pathogens/insect herbivores has triggered the evolution of s RNAs,RNA silencing machinery and pathogen effectors. A great number of studies have been performed to investigate the roles of s RNAs in plant defense, bringing in the opportunity to utilize s RNAs in plant protection. Transgenic plants with pathogen-derived resistance ability or transgenerational defense have been generated, which show promising potential as solutions for pathogen/insect herbivore problems in the field. Here we summarize the recent progress on the function of s RNAs in response to biotic stress, mainly in plant-pathogen/insect herbivore interaction,and the application of s RNAs in disease and insect herbivore control.     

Effector proteins that modulate plant--insect interactions

Insect herbivores have highly diverse life cycles and feeding behaviors. They establish close interactions with their plant hosts and suppress plant defenses. Chewing herbivores evoke characteristic defense responses distinguishable from general mechanical damage. In addition, piercing-sucking hemipteran insects display typical feeding behavior that suggests active suppression of plant defense responses. Effectors that modulate plant defenses have been identified in the saliva of these insects. Tools for high-throughput effector identification and functional characterization have been developed. In addition, in some insect species it is possible to silence gene expression by RNAi. Together, this technological progress has enabled the identification of insect herbivore effectors and their targets that will lead to the development of novel strategies for pest resistances in plants.     

Non-protein amino acids in plant defense against insect herbivores: representative cases and opportunities for further functional analysis

Chemical defense against herbivores is of utmost importance for plants. Primary and secondary metabolites, including non-protein amino acids, have been implicated in plant defense against insect pests. High levels of non-protein amino acids have been identified in certain plant families, including legumes and grasses, where they have been associated with resistance to insect herbivory. Non-protein amino acids can have direct toxic effects via several mechanisms, including misincorporation into proteins, obstruction of primary metabolism, and mimicking and interfering with insect neurological processes. Additionally, certain non-protein amino acids allow nitrogen to be stored in a form that is metabolically inaccessible to herbivores and, in some cases, may act as signals for further plant defense responses. Specialized insect herbivores often possess specific mechanisms to avoid or detoxify non-protein amino acids from their host plants. Although hundreds of non-protein amino acids have been found in nature, biosynthetic pathways and defensive functions have been elucidated in only a few cases. Next-generation sequencing technologies and the development of additional plant and insect model species will facilitate further research on the production of non-protein amino acids, a widespread but relatively uninvestigated plant defense mechanism.     

Induction and persistence of allelochemicals in the foliage of balsam fir seedlings following simulated browsing

The intensity, pattern, and timing of browsing disturbances influence the mobilization of chemical defenses (allelochemicals) and subsequent growth of conifers such as balsam fir, an important food source for various insect and mammalian herbivores. The objective of this study was to examine the induction and persistence of allelochemicals in foliage of balsam fir seedlings as affected by the pattern and timing of browsing disturbance. We conducted a simulated browsing study in a greenhouse environment using four browsing patterns and three persistence times. Total phenols were induced shortly after simulated browsing and persisted for at least 1 month, whereas condensed tannins exhibited a delayed induction but were more persistent, remaining above background levels 2 months after simulated browsing. The chemistry of non-browsed seedlings revealed that a seasonal pattern was evident for both total phenols and condensed tannins. As the experiment progressed through the growing season, background levels of total phenols decreased while those of condensed tannins increased with the two allelochemicals groups appearing to show a negative relationship. These trends suggest that total phenols, which are assumed to have a lower biosynthetic cost and are more quickly mobilized than condensed tannins, are a first line of herbivory defense followed by condensed tannins which take longer to mobilize but have a longer persistence time or that total phenols act as a primary defense against insect herbivores which disturb plants in the early growing season while condensed tannins are mobilized in the late season to defend against mammalian browsers of balsam fir in winter.