Indirect plant defense against insect herbivores: a review

Plants respond to herbivore attack by launching 2 types of defenses: direct defense and indirect defense. Direct defense includes all plant traits that increase the resistance of host plants to insect herbivores by affecting the physiology and/or behavior of the attackers. Indirect defense includes all traits that by themselves do not have significant direct impact on the attacking herbivores, but can attract natural enemies of the herbivores and thus reduce plant loss. When plants recognize herbivore‐associated elicitors, they produce and release a blend of volatiles that can attract predators, parasites, and other natural enemies. Known herbivore‐associated elicitors include fatty acid–amino acid conjugates, sulfur‐containing fatty acids, fragments of cell walls, peptides, esters, and enzymes. Identified plant volatiles include terpenes, nitrogenous compounds, and indoles. In addition, constitive traits including extrafloral nectars, food bodies, and domatia can be further induced to higher levels and attract natural enemies as well as provide food and shelter to carnivores. A better understanding of indirect plant defense at global and componential levels via advanced high throughput technologies may lead to utilization of indirect defense in suppression of herbivore damage to plants.     

转基因抗虫作物对非靶标昆虫的影响

转基因抗虫作物自 1996年被批准商业化种植以来 ,它的抗虫性和经济效益已得到了普遍肯定 ,同时 ,转基因抗虫作物对非靶标生物的影响 ,如转基因抗虫作物的长期种植 ,是否会导致次要害虫上升为主要害虫 ,是否会影响有益昆虫 ,包括重要经济昆虫、捕食性和寄生性天敌以及重要蝶类的种类及种群数量 ,已成为转基因抗虫作物生态风险评估的重要内容。一些研究结果表明 ,转基因抗虫作物在对靶标害虫有效控制的同时 ,一些对杀虫蛋白不敏感的非靶标害虫有加重危害的趋势 ,由于种植转基因抗虫作物 ,减少了化学农药的使用 ,客观上也使非靶标害虫种群数量上升 ,这对转基因抗虫作物害虫综合治理提出了新的要求。靶标害虫数量的减少直接影响了害虫天敌种群数量 ,靶标害虫取食转基因抗虫作物后发育迟缓 ,也间接影响了天敌昆虫的生长发育 ,转基因抗虫作物的花粉或花蜜是一些重要经济昆虫如蜜蜂、熊蜂和一些寄生蜂 ,甚至捕食性天敌的食物来源 ,或花粉飘落到一些鳞翅目昆虫如家蚕或重要蝶类昆虫的寄主植物上 ,直接或间接对这些昆虫造成一定影响。目前大多数研究表明转基因抗虫作物对非靶标昆虫 ,特别是对有益昆虫没有明显的不利影响 ,也有研究报道认为对某些有益昆虫有一定的不良影响。这为深入开展转基因抗虫作物的生态安全     

Vitamin C content in plants is modified by insects and influences susceptibility to herbivory

Analysis of a diverse cross‐sample of plant‐insect interactions suggests that the abundance of vitamin C (L ‐ascorbic acid, ascorbate or AsA) in plants influences their susceptibility to insect feeding. These effects may be mediated by AsAs roles as an essential dietary nutrient, as an antioxidant in the insect midgut, or as a substrate for plant‐derived ascorbate oxidase, which can lead to generation of toxic reactive oxygen species. Ascorbate can also influence the efficacy of plant defenses such as myrosinases and tannins, and alter insects' susceptibility to natural enemies. Conversely, herbivores appear to influence both de novo synthesis and redox cycling of AsA in their host plants, thereby potentially altering the nutritional value of crops and their susceptibility to pests. The recent development of genetically modified crops with enhanced AsA content provides both an impetus and a tool set for further studies on the role of AsA in plant‐insect interactions.     

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.     

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。     

Consumptive and nonconsumptive effect ratios depend on interaction between plant quality and hunting behavior of omnivorous predators

Predators not only consume prey but exert nonconsumptive effects in form of scaring, consequently disturbing feeding or reproduction. However, how alternative food sources and hunting mode interactively affect consumptive and nonconsumptive effects with implications for prey fitness have not been addressed, impending functional understanding of such tritrophic interactions. With a herbivorous beetle, two omnivorous predatory bugs (plant sap as alternative food, contrasting hunting modes), and four willow genotypes (contrasting suitability for beetle/omnivore), we investigated direct and indirect effects of plant quality on the beetles key reproductive traits (oviposition rate, clutch size). Using combinations of either or both omnivores on different plant genotypes, we calculated the contribution of c onsumptive (eggs predated) and n onc onsumptive (fewer eggs laid) effect on beetle fitness, including a prey density‐independent measure (c:nc ratio). We found that larger clutches increase egg survival in presence of the omnivore not immediately consuming all eggs. However, rather than lowering mean, the beetles generally responded with a frequency shift toward smaller clutches. However, female beetles decreased mean and changed clutch size frequency with decreasing plant quality, therefore reducing intraspecific exploitative competition among larvae. More importantly, variation in host plant quality (to omnivore) led to nonconsumptive effects between one‐third and twice as strong as the consumptive effects. Increased egg consumption on plants less suitable to the omnivore may therefore be accompanied by less searching and disturbing the beetle, representing a “cost” to the indirect plant defense in the form of a lower nonconsumptive effect. Many predators are omnivores and altering c:nc ratios (with egg retention as the most direct link to prey fitness) via plant quality and hunting behavior should be fundamental to advance ecological theory and applications. Furthermore, exploring modulation of fitness traits by bottom‐up and top‐down effects will help to explain how and why species aggregate.     

Phylloplane bacteria increase the negative impact of food limitation on insect fitness

1. When populations of herbivorous insects increase in density, they can alter the quantity or quality of their food. The impacts of diet‐related stressors on insect fitness have been investigated singly, but not simultaneously. 2. Foliage quantity and quality of red alder, Alnus rubra, were manipulated together with the presence of non‐entomopathogenic phylloplane bacteria to investigate their impacts, singly and in combination, on survival, pupal mass, growth rate, fecundity and egg quality of a cyclic forest insect, the western tent caterpillar, Malacosoma californicum pluviale. 3. Food limitation (half food) had strong negative impacts on all life‐history traits. When the larvae were fed continuously, however, neither ingesting phylloplane bacteria nor eating leaves from damaged branches (induced foliage) affected survival. In the half‐food treatment, ingesting bacteria further increased mortality, while feeding on induced foliage improved survival. 4. Growth rate and pupal mass of both sexes were reduced for larvae with food limitation compared with continuously fed insects and this was exacerbated when the larvae also ate bacteria‐treated leaves. A combination of bacteria and induced foliage also reduced larval growth rate by 5% in the full‐food treatment. 5. Fecundity (eggs per egg mass) was 2.7 times greater in full‐food than in food‐limited treatments but neither phylloplane bacteria nor plant induction had an effect. Insects fed induced foliage produced smaller eggs. Overall, there was no evidence of a three‐way interaction between the three stressors, although there were negative synergistic effects, primarily between food limitation and the ingestion of phylloplane bacteria.     

Capturing the interaction types of two Bt toxins Cry1Ac and Cry2Ab on suppressing the cotton bollworm by using multi‐exponential equations

Transgenic crops are increasingly promoted for their practical effects on suppressing certain insect pests, but all transgenic crops are not equally successful. The insect pests can easily develop resistance against single Bacillus thuringiensis (Bt) toxin transgenic crops. Therefore, transgenic crops including two or more mixed Bt‐toxins can solve this problem by delaying the resistance development and killing the majority of targeted pests before the evolution of resistance. It is important to test the controlling effects of transgenic crops including multiple mixed toxins on a particular insect pest. Previous research has checked the cross‐resistance and interactions between Bt toxins Cry1Ac and Cry2Ab against one susceptible and four resistant strains of cotton bollworm. The results showed that independence was the main interaction type between two toxins for the susceptible strain, whereas synergism was the main interaction type for any one resistant strain. However, the optimal combinations of two toxins were not obtained. In the present study, we developed two multi‐exponential equations (namely bi‐ and tri‐exponential equations) to describe the combination effects of two Bt toxins. Importantly, the equations can provide predictions of combination effects of different continuous concentrations of two toxins. We compared these two multi‐exponential equations with the generalized linear model (GLM) in describing the combination effects, and found that the bi‐ and tri‐exponential equations are better than GLM. Moreover, the bi‐exponential equation can also provide the optimal dose combinations for two toxins.     

植物蛋白酶抑制素抗虫作用的研究进展

植物自身为抵抗昆虫等的为害,在长期进化过程中形成了复杂的化学防御体系,其中起主导作用的是一些植物化学物质。这些化合物能影响昆虫（或其它有机体）的生长、行为和群体生物学,因而又称为它感素（allelochemics）[1～3]。大多数它感素为植物的利己素,可以单一或协同对害虫起作用,构成植物的抗虫性。根据植物对昆虫取食的反应,可将植物的化学防御概括为两类：一类是组成型防御[4],即抗虫物质不依赖于昆虫的取食而存在于植物组织中;另一类是诱导型防御[5～9],即植物仅当昆虫取食时才大量合成抗虫物质。诱导型抗虫物质当然亦可以组…     

Molecular strategies of plant defense and insect counter-defense

The prediction of human population growth worldwide indicates there will be a need to substantially increase food production in order to meet the demand on food supply.This can be achieved in part by the effective management of insect pests. Since plants have co-evolved with herbivorous insects for millions of years, they have developed an array of defense genes to protect themselves against a wide variety of chewing and sucking insects.Using these naturally-occurring genes via genetic engineering represents an environmentally friendly insect pest-control measure. Insects, however, have been actively evolving adaptive mechanisms to evade natural plant defenses. Such evolved adaptability undoubtedly has helped insects during the last century to rapidly overcome a great many humanimposed management practices and agents, including chemical insecticides and genetically engineered plants. Thus, better understanding of the molecular and genetic basis of plant defense and insect counter-defense mechanisms is imperative, not only from a basic science perspective, but also for biotechnology-based pest control practice. In this review, we emphasize the recent advance and understanding of molecular strategies of attack-counterattack and defense-counter-defense between plants and their herbivores.     

Perception, signaling and molecular basis of oviposition-mediated plant responses

Eggs deposited on plants by herbivorous insects represent a threat as they develop into feeding larvae. Plants are not a passive substrate and have evolved sophisticated mechanisms to detect eggs and induce direct and indirect defenses. Recent years have seen exciting development in molecular aspects of egg-induced responses. Some egg-associated elicitors have been identified, and signaling pathways and egg-induced expression profiles are being uncovered. Depending on the mode of oviposition, both the jasmonic acid and salicylic acid pathways seem to play a role in the induction of defense responses. An emerging concept is that eggs are recognized like microbial pathogens and innate immune responses are triggered. In addition, some eggs contain elicitors that induce highly specific defenses in plants. Examples of egg-induced suppression of defense or, on the contrary, egg-induced resistance highlight the complexity of plant–egg interactions in an on-going arms race between herbivores and their hosts. A major challenge is to identify plant receptors for egg-associated elicitors, to assess the specificity of these elicitors and to identify molecular components that underlie various responses to oviposition.     

The broad-leaf herbicide 2,4-dichlorophenoxyacetic acid turns rice into a living trap for a major insect pest and a parasitic wasp

Synthetic chemical elicitors of plant defense have been touted as a powerful means for sustainable crop protection. Yet, they have never been successfully applied to control insect pests in the field. We developed a high-throughput chemical genetics screening system based on a herbivore-induced linalool synthase promoter fused to a β-glucuronidase (GUS) reporter construct to test synthetic compounds for their potential to induce rice defenses. We identified 2,4-dichlorophenoxyacetic acid (2,4-D), an auxin homolog and widely used herbicide in monocotyledonous crops, as a potent elicitor of rice defenses. Low doses of 2,4-D induced a strong defensive reaction upstream of the jasmonic acid and ethylene pathways, resulting in a marked increase in trypsin proteinase inhibitor activity and volatile production. Induced plants were more resistant to the striped stem borer Chilo suppressalis, but became highly attractive to the brown planthopper Nilaparvata lugens and its main egg parasitoid Anagrus nilaparvatae. In a field experiment, 2,4-D application turned rice plants into living traps for N. lugens by attracting parasitoids. Our findings demonstrate the potential of auxin homologs as defensive signals and show the potential of the herbicide to turn rice into a selective catch crop for an economically important pest.     

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.     

Defense strategies used by two sympatric vineyard moth pests

Natural enemies including parasitoids are the major biological cause of mortality among phytophagous insects. In response to parasitism, these insects have evolved a set of defenses to protect themselves, including behavioral, morphological, physiological and immunological barriers. According to life history theory, resources are partitioned to various functions including defense, implying trade-offs among defense mechanisms. In this study we characterized the relative investment in behavioral, physical and immunological defense systems in two sympatric species of Tortricidae (Eupoecilia ambiguella, Lobesia botrana) which are important grapevine moth pests. We also estimated the parasitism by parasitoids in natural populations of both species, to infer the relative success of the investment strategies used by each moth. We demonstrated that larvae invest differently in defense systems according to the species. Relative to L. botrana, E. ambiguella larvae invested more into morphological defenses and less into behavioral defenses, and exhibited lower basal levels of immune defense but strongly responded to immune challenge. L. botrana larvae in a natural population were more heavily parasitized by various parasitoid species than E. ambiguella, suggesting that the efficacy of defense strategies against parasitoids is not equal among species. These results have implications for understanding of regulation in communities, and in the development of biological control strategies for these two grapevine pests.     

Plant genotype affects the quality of oilseed rape (Brassica napus) for adults and larvae of the pollen beetle (Meligethes aeneus)

Plant quality is one of the main factors influencing the fitness of phytophagous insects. Plant quality can vary not only among genotypes of the same host plant species, but also relative to the insect sex or its life stage. In the present study, the performance of larvae and adults of the pollen beetle (Meligethes aeneus F., Coleoptera: Nitidulidae), a major insect pest of oilseed rape crops, is compared on six genotypes of oilseed rape (Brassica napus). All of the traits that are measured vary among genotypes, and comprise larval developmental duration, life span of unfed emerging adults and survival time of field‐sampled adults fed with pollen from the different genotypes. No correlation is found between insect performance and quantity of food available, showing that the quality of the food (i.e. pollen) is the fitness determinant for this insect species. Additionally, the performance of larvae and adults is also not correlated despite use of the same plant genotypes, suggesting that the determinants of pollen quality differ at least partially between both life stages. It is hypothesized that this may be a result of extensive differences in diet breadth between the life stages: larvae are specialists of brassicaceous plants, whereas adults are generalists. Finally, it is suggested that the manipulation of plant quality to increase pollen beetle development time may comprise a valuable strategy for favouring biological control by natural enemies of this pest; for example, as a result of extending the vulnerability window of larvae to attack by parasitoids.     

Host plant resistance for insect control in some important crop plants

Insect pests of cereal crop plants are among the most destructive and devastating factors limiting world food production. Insects often inflict losses of 15 to 50% of the yield of some crops in various parts of the world. Insects also provide infection courts for various pathogens that inflict even greater damage. The nature of these losses is especially tragic for poor farmers in the tropics since the insects consume dry matter already produced using limited resources. Reduction of these losses would enhance the world food supply available to man, even if actual production remains the same, by allotting to man and animals that proportion of production now consumed by insects. Control of insect‐inflicted damage on a world‐wide basis is a very difficult task. Chemical control is effective and readily available in some, but not all, countries. However, chemical control is often unavailable, ineffective, too expensive, and likely to create environmental and safety hazards that make it unsuitable for many parts of the world. Several excellent examples of biological control of insects also attest to the potential usefulness of this method of reducing insect‐inflicted losses, but this method also has been ineffective for certain major insect pests due to lack of effective identification, distribution, and maintenance of biological control agents. On the whole, host plant resistance (HPR) to insects has been the most successful and widely used method of control. HPR has been used successfully in a number of major crop species to help control damage inflicted by major insect pests. However, problems with identifying sources of resistance and transferring it to usable varieties have often been difficult to overcome. Also, once resistance is deployed, changes in insect populations which allow them to overcome the resistance sometimes eliminate the potential advantages of resistant varieties. However, methods to quantify host‐insect interactions have improved significantly over the past few years, and the prospects for developing and maintaining usable levels of resistance to several major insect pests of most major crops are good. Studies of the biochemical and biophysical mechanisms of insect resistance have added a new dimension to HPR work. Knowledge of specific factors that contribute to insect resistance can be extremely useful to plant breeders and entomologists. The ability to identify and select for one specific plant component or group of components can speed the development of resistant varieties. Studies of the effect of such resistance components on insect development and behavior can help determine the likelihood of insects being able to overcome the resistance factors. Studies of the effect of the resistance factors on host plant yield, performance, or quality may help plant breeders overcome the problems often associated with the development of high yielding and high quality resistant varieties. Identification of several different mechanisms of resistance could provide breeders the opportunity to adjust levels of several resistance components in order to arrive at a proper blend of resistance, quality, and yield. Furthermore, development of varieties with multiple mechanisms of resistance should slow the development of new biotypes of insects that could overcome the HPR since the insects would have to simultaneously or sequentially develop the ability to overcome several resistance factors. Therefore, knowledge of mechanisms of insect resistance could facilitate the development of more stable and long‐lasting types of resistance.     

Family matters: effect of host plant variation in chemical and mechanical defenses on a sequestering specialist herbivore

Insect herbivores contend with various plant traits that are presumed to function as feeding deterrents. Paradoxically, some specialist insect herbivores might benefit from some of these plant traits, for example by sequestering plant chemical defenses that herbivores then use as their own defense against natural enemies. Larvae of the butterfly species Battus philenor (L.) (Papilionidae) sequester toxic alkaloids (aristolochic acids) from their Aristolochia host plants, rendering larvae and adults unpalatable to a broad range of predators. We studied the importance of two putative defensive traits in Aristolochia erecta: leaf toughness and aristolochic acid content, and we examined the effect of intra- and interplant chemical variation on the chemical phenotype of B. philenor larvae. It has been proposed that genetic variation for sequestration ability is ??invisible to natural selection?? because intra- and interindividual variation in host-plant chemistry will largely eliminate a role for herbivore genetic variation in determining an herbivore??s chemical phenotype. We found substantial intra- and interplant variation in leaf toughness and in the aristolochic acid chemistry in A. erecta. Based on field observations and laboratory experiments, we showed that first-instar larvae preferentially fed on less tough, younger leaves and avoided tougher, older leaves, and we found no evidence that aristolochic acid content influenced first-instar larval foraging. We found that the majority of variation in the amount of aristolochic acid sequestered by larvae was explained by larval family, not by host-plant aristolochic acid content. Heritable variation for sequestration is the predominant determinant of larval, and likely adult, chemical phenotype. This study shows that for these highly specialized herbivores that sequester chemical defenses, traits that offer mechanical resistance, such as leaf toughness, might be more important determinants of early-instar larval foraging behavior and development compared to plant chemical defenses.     

Priming of antiherbivore defensive responses in plants

Defense priming is defined as increased readiness of defense induction. A growing body of literature indicates that plants (or intact parts of a plant) are primed in anticipation of impending environmental stresses, both biotic and abiotic, and upon the following stimulus, induce defenses more quickly and strongly. For instance, some plants previously exposed to herbivore‐inducible plant volatiles (HIPVs) from neighboring plants under herbivore attack show faster or stronger defense activation and enhanced insect resistance when challenged with secondary insect feeding. Research on priming of antiherbivore defense has been limited to the HIPV‐mediated mechanism until recently, but significant advances were made in the past three years, including non‐HIPV‐mediated defense priming, epigenetic modifications as the molecular mechanism of priming, and others. It is timely to consider the advances in research on defense priming in the plant–insect interactions.