Rethinking the role of many plant phenolics – protection from photodamage not herbivores?

Phenolics have been considered classic defence compounds for protecting plants from herbivores, ever since plant secondary metabolites were suggested to have evolved for that reason. The resource availability and carbon-nutrient balance hypotheses proposed that variation in phenolic levels between and within plant species reflects environmental availability of nutrients and light, and represents a trade-off in allocation by plants to growth and defence against herbivores. In contrast to these concepts, we suggest that (1) the main role of many plant phenolics may be to protect leaves from photodamage, not herbivores; (2) they can achieve this by acting as antioxidants; and (3) their levels may vary with environmental conditions in order to counteract this potential photodamage. We therefore suggest that patterns in phenolic levels, often used to support the concept of trade-off between growth and herbivore defence in relation to resource availability, may actually reflect different risks of photodamage. We suggest that the level of many phenolics is low under some environmental conditions, not because resources to produce them are limited, but simply because the risk of photodamage is low and they are not required. If our photodamage hypothesis is correct, a reassessment of the ecological and evolutionary role of many phenolics in plant defence theory is required.     

The effects of season and water availability on chemical composition,secondary metabolites and biological activity in plants

Plants react towards changes in their environment, which can be a result of biotic or abiotic activities. Numerous studies have investigated the effects of abiotic stress on plants, and how it affects the primary as well as secondary metabolism. Generally it is accepted that plants react to environmental stress by increasing secondary metabolites. This is however a very broad and simplified explanation and often inaccurate. Various examples are provided where plants react positively, and often negatively towards seasonal variation and water availability, resulting in a lowering of certain secondary metabolites concentration, while others are increased. Furthermore species differences, cultivars and interaction of other environmental factors such as temperature complicates a simple conclusion from the effect of stress on plants. The differential expression of genes in different species and in different metabolic pathways ensures a complex and very specific reaction of a plant to environmental stress. Overall the paper provides support for a complex and intricate response system which differs for each plant species, and could be explained by understanding and studying the different metabolic pathways responsible for secondary metabolite production.     

短葶飞蓬黄酮及咖啡酸酯的含量与土壤氮供应量的关系

通过对短葶飞蓬(Erigeron breviscapus)不同产地的44个种群植株的总黄酮、灯盏乙素和总咖啡酸酯含量与产地土壤全氮(N)和速效N含量的相关分析, 探讨了产地间土壤N含量变化在药用植物短葶飞蓬植株次生代谢有效成分含量变化中的作用机制。结果显示: 土壤全N含量与种群植株中总黄酮含量呈显著的负相关(r=-0.391, p＜0.01), 而与总咖啡酸酯和灯盏乙素关系不显著; 土壤速效N含量与种群植株中总黄酮(r=-0.528, p＜0.01)、灯盏乙素(r=-0.490, p＜0.01)和总咖啡酸酯含量(r=-0.471, p＜0.01)都表现出更高的极显著负相关关系。全部44个种群中, 有效N供应量变化只能解释次生代谢产物含量的17%~30%的变化。非石灰土壤与石灰土壤的种群分开进行线性回归, 可解释总黄酮含量产地间约80%的变化, 以及灯盏乙素和总咖啡酸酯含量约60%的变化。植株总黄酮、灯盏乙素和总咖啡酸酯含量都与植株含N量存在显著的负相关关系。研究表明: 土壤丰富的有效N供应不利于黄酮和咖啡酸酯的合成积累, 与“碳素/营养平衡假说”的预测一致; 土壤有效N对植物次生代谢产物的影响会受到植物体内外因素的影响。不同产地的短葶飞蓬的黄酮等酚类次生代谢产物含量的差异, 可能是产地间不同的土壤N供应量和其他生态因子及遗传变异共同作用的结果。     

Tibor Jermy (1917–2014)

Throughout the course of their evolution, plants have acquired a wide range of chemical and mechanical defenses to protect against herbivores. Ehrlich & Raven's coevolutionary theory suggests that this diversification of defensive traits is driven by the strong impact of novel traits on insect herbivores. However, the impact of plant defenses on insects is difficult to compare between related plant species due to variation in environmental and biotic conditions. We standardized these factors as far as possible by analyzing the effects of chemical and mechanical defensive traits on insects in a local community of 11 Salicaceae species growing in sympatry, and their leaf‐chewing herbivores. Defensive traits (salicylates, flavonoids, tannins, trichomes, and leaf toughness) were generally not inter‐correlated, with the exception of a negative correlation between salicylates and trichomes. The content of salicylates, a novel group of defensive metabolites in the Salicaceae, was correlated with low herbivore diversity and high host specificity. Despite these effects, the phylogeny of the studied species shows loss of salicylates in some Salix species instead of their further diversification. This could be due to salicylates not decreasing the overall abundance of herbivores, despite accounting for up to 22% of the dry leaf mass and therefore being costly. The defense of low‐salicylate willow species is thus probably maintained by other defensive traits, such as trichomes. Our study shows that the balance between costs and benefits of defensive traits is not necessarily in favor of novel compounds and illustrates a process, which may lead to the reduction in a defensive trait.     

Within-plant variation in seaweed palatability and chemical defenses: optimal defense theory versus the growth-differentiation balance hypothesis

Within-plant variation in the concentration of secondary metabolites, nutritive value, toughness, and susceptibility to herbivory was assessed for the brown alga Dictyota ciliolata. When young apices and older tissue from the same plant were offered in equal abundance to the herbivorous amphipod Ampithoe longimana and the sea urchin Arbacia punctulata, young apices were consumed about 2 times more than older tissue. Compared to young apices, the less preferred older tissue had a less palatable lipophilic extract, significantly higher concentrations of two secondary metabolites (another secondary metabolite did not differ significantly), 33% more soluble protein, and was 233% tougher. Higher levels of chemical defenses in older tissues, and not tissue toughness or nutritive value, appear to be responsible for the preference of Ampithoe longimana for young apices. The pattern of lower levels of chemical defenses in young than older tissues of D. ciliolata is the opposite of the pattern observed in coenocytic seaweeds and most vascular terrestrial and marine plants, all of which have translocation systems for moving materials among plant portions. Unlike these other plants, which preferentially allocate chemical defenses to young tissues, D. ciliolata cannot readily translocate secondary metabolites. The growth-differentiation balance hypothesis suggests that actively dividing and expanding cells are less able to produce secondary metabolites. This hypothesis may help explain why older tissues are better defended than young, rapidly growing apices.     

Resource availability and the trichome defenses of tomato plants

We conducted two experiments to determine how resource availability influenced allocation by tomato (Lycopersicon esculentum) to trichomes, and how different patterns of trichome allocation by plants grown in different resource environments might then influence the behavior of tobacco hornworm (Manduca sexta) caterpillars. In the first experiment we used high and low levels of light and water, and then, using scanning electron microscopy, determined trichome densities on the leaves and stems. We sampled leaves and stems at several places throughout the plant to determine whether there were within-plant differences in allocation to trichomes. The results of the first experiment showed that resource availability influenced allocation to trichome growth. Patterns in high and low-light supported both the growth-differentiation balance hypothesis (GDBH) and the carbon-nutrient balance hypothesis (CNBH). However, the GDBH was not supported by differences among water treatments. Contrary, to predictions of the GDBH, plants with intermediate growth did not have the highest trichome densities, and plants with similar growth differed in trichome density. Possible biological and artifactual explanations are discussed. The first experiment also showed that there was within-plant variation in allocation to trichomes, and that plant resource availability may influence within-plant variation in allocation to trichomes. In the second experiment, we grew plants in high and low-light, and then monitored the behavior of tobacco hornworms on the stems of these plants in the laboratory. This experiment demonstrated that the light environment that tomato plants were grown in influenced the resting behavior of caterpillars. Furthermore, it demonstrated that both glandular and non-glandular trichomes impeded caterpillars from searching for food. Overall, this study indicated that plant resource availability can influence allocation to trichome defenses, and that these differences may affect insect herbivores.     

Ecological costs of biotrophic versus necrotrophic pathogen resistance, the hypersensitive response and signal transduction

Recent advances along numerous research avenues show that plant interactions with biotrophic and necrotrophic pathogens use similar pathways with opposing effects. The hypersensitive response is associated with increased biotroph resistance but decreased necrotroph resistance. In plant/herbivore interactions, opposing effects of defenses against specialist versus generalist herbivores are controlled by plant secondary metabolites, where a metabolite that provides resistance to generalist herbivores may stimulate specialist herbivores. This multi-trophic interaction is presented as an ecological cost of plant resistance, but similar concepts are rarely applied to plant interactions with different classes of pathogens. In this review, we begin to describe how necrotrophic pathogens may place an ecological cost upon plant resistance to biotrophic pathogens. We separate these potential ecological costs into three concepts: (1) the local cost of the hypersensitive response, (2) organismal cost of having machinery for a hypersensitive response and (3) antagonism between salicylate and jasmonate signaling. We describe the literature supporting these concepts and some predictions that they generate.     

Phenotypic variation and spatial structure of secondary chemistry in a natural population of a tropical tree species

To understand herbivore selection in natural plant populations, it is important to understand the landscape of plant chemical phenotypes that herbivores face and the sources of variation that will define this landscape. We studied the spatial patterns of variation in leaf secondary chemistry of the tropical tree Quararibea asterolepis , Pitt. (Bombacaceae) in a natural population on Barro Colorado Island, Panama, and used this background to discuss hypotheses of natural selection by herbivores. Quararibea plants collected from different sites had consistent differences in their chemical phenotypes. Some of these differences were explained by developmental and environmental sources of variation. Canopy trees had 13% lower yield of leaf extracts than gap seedlings, explained by 41% lower concentrations of the more abundant metabolites in the secondary compound profile. Also, plants growing in gaps had 25% higher yield than those in the understory, explained by two-fold increases in the concentration of some of the less polar secondary compounds in the profile. Differences in soil type did not affect the secondary chemistry of leaves, but sites with different topography had differences in the secondary compound profile that were not explained by any of the measured environmental sources of variation. Neighboring parent-offspring pairs and sibling/half sibling clusters displayed equal or higher variance among themselves than unrelated individuals at farther distances. Assuming that related plants should be more similar in their phenotypes, this pattern is consistent with local selection by herbivores overriding the similarity of related plants in a frequency- or distance-dependent manner.     

Can plant resistance to specialist herbivores be explained by plant chemistry or resource use strategy?

At both a macro- and micro-evolutionary level, selection of and performance on host plants by specialist herbivores are thought to be governed partially by host plant chemistry. Thus far, there is little evidence to suggest that specialists can detect small structural differences in secondary metabolites of their hosts, or that such differences affect host choice or performance of specialists. We tested whether phytochemical differences between closely related plant species are correlated with specialist host choice. We conducted no-choice feeding trials using 17 plant species of three genera of tribe Senecioneae (Jacobaea, Packera, and Senecio; Asteraceae) and a more distantly related species (Cynoglossum officinale; Boraginaceae) containing pyrrolizidine alkaloids (PAs), and four PA-sequestering specialist herbivores of the genus Longitarsus (Chrysomelidae). We also assessed whether variation in feeding by specialist herbivores is attributable to different resource use strategies of the tested plant species. Plant resource use strategy was quantified by measuring leaf dry matter content, which is related to both plant nutritive value and to plant investment in quantitative defences. We found no evidence that intra-generic differences in PA profiles affect feeding by specialist herbivores. Instead, our results indicate that decisions to begin feeding are related to plant resource use strategy, while decisions to continue feeding are not based on any plant characteristics measured in this study. These findings imply that PA composition does not significantly affect host choice by these specialist herbivores. Leaf dry matter content is somewhat phylogenetically conserved, indicating that plants may have difficulty altering resource use strategy in response to selection pressure by herbivores and other environmental factors on an evolutionary time scale.     

Interactions between plants and herbivores: A review of plant defense

Ecologists have long ignored or underestimated the importance of plant–herbivore interactions owing to the diversities of herbivores, plant defensive strategies and ecological systems. In this review, we briefly discussed the categories of herbivores. Then we reviewed the major types of plant defenses against herbivores. Selective forces of herbivore pressures have led to the evolution of various defensive mechanisms in plants, which can be classified into (i) resistance traits that reduce the amount of damage received, including physical, chemical, and biotic traits; (ii) tolerance mechanisms that decrease the impact of herbivore damage, and (iii) escape strategies that reduce the probability of plants to be found by herbivores. These strategies have been studied at different levels from molecular genetics and genomics, to chemistry and physiology, to community and ecosystem ecology. We summarized the development of the methodology for studying plant defenses against herbivores. Particularly, 24 of those hypotheses and models, which are influential in the international community concerning the relationship between plants and herbivores, including the defensive mimicry hypothesis, the compensatory continuum hypothesis, the slow-growth-high-mortality hypothesis, etc, were introduced and grouped into four categories according to plant defense strategies in the present review. Finally, we also reviewed the research progress of plant–herbivore interactions in China, and discussed the perspectives of studies on plant–herbivore interactions.     

Plant-mediated interactions between shoot-feeding aphids and root-feeding nematodes depend on nitrate fertilization

The plant metabolite composition is modulated by various abiotic and biotic factors including nutrient availability and herbivory. In turn, induced changes in plant quality can affect herbivore performance and mediate indirect interactions between spatially separated herbivores sharing a host. Studies on plant-mediated herbivore interactions have been carried out at single fertilization regimes only, but we hypothesized that nutrient availability modifies these interactions. Therefore, we studied the interactions between two vascular tissue herbivores, the aboveground feeding aphid Brevicoryne brassicae and the belowground infesting nematode Heterodera schachtii, on Arabidopsis thaliana grown under two nitrate fertilization conditions (varying by 33 %). Furthermore, we investigated plant growth and primary metabolic responses to fertilization and herbivore treatments, which could potentially mediate these interactions, as the herbivores may act as metabolic sinks. Whereas nematodes had no effects on aphids, aphid presence influenced nematodes in opposite directions, depending on fertilization: at low nitrate supply, aphids had a promoting effect on nematodes, whereas at high nitrate fertilization they lowered the nematode infestation compared to control plants. Plants produced significantly more biomass under high nitrate supply but C and N contents were not altered. Primary metabolite profiles differed only marginally between roots of both fertilization treatments in plants with and without aphids, indicating that nematodes may respond to these or other metabolic modifications, which are caused by minute environmental changes, in a sensitive way. Our results highlight the need to consider the importance of plant nutrient availability on the outcome of interactions between co-occurring herbivores in future studies.     

Advances in research of induced resistance to insects in cotton

Any change in a plant that occurs following herbivory or environmental factors is an induced response. These changes include phytochemical induction, increases in physical defenses, emission of volatiles that attract predators and parasitoids of herbivores, and reduction in plant nutritional quality for herbivores, which is termed induced resistance. Induced resistance has been demonstrated ubiquitously in plants. It is one of our goals to review what is known about the induced resistance to herbivorous insects in cotton, including three resistance secondary metabolites (terpenoid, tannin, and flavonoids) that are contained at any significant levels of resistance to herbivorous insects in cotton cultivates. In many cases, the quantities or quality of secondary metabolites in plant are changed after attacked by insects. This review focuses on induced plant resistance as quantitative or qualitative enhancement of defense mechanism against insect pests, especially on the abiotic-elicitors-induced resistance in cotton plants. The abiotic-elicitor of cupric chloride, an exogenous inorganic compound, may induce the secondary metabolites accumulation and is referred to as a copperinducible elicitor (CIE). Finally, we discuss how copperinducible elicitor may be used in the Integrated Pest Management (IPM) system for cotton resistance control.     

To grow and defend: lack of tradeoffs for brown algal phlorotannins

The concept of cost is an integral element of ecological theories, including optimal defense theory, resource availability theory, and growth-differentiation balance theory. Indeed most frameworks that attempt to explain within-plant patterns of secondary metabolites, as well as account for the evolution of induced defenses, presume that defenses are 'costly'. One way in which investigators have sought to quantify the cost of secondary metabolites is to examine growth/defense tradeoffs, which are predicted to occur wherever resources cannot be simultaneously allocated to both growth and defense. However, emerging evidence suggests that these critical assumptions may not be valid for brown algal phlorotannins, compounds that occur throughout the division Phaeophyta and have served as analogs to vascular plant tannins in numerous tests of terrestrial-derived ecological theories in the marine environment. Here we present a model of phlorotannins as metabolites with both primary and secondary roles and argue that apparent trade-offs between algal growth and phlorotannin content are not a reliable indicator for establishing a cost of defense. We suggest the ecological theories which presume that defenses are costly because resources allocated to defense cannot also be allocated to other 'primary' functions are unlikely to accurately predict the striking variations in algal phlorotannin concentrations that are observed in nature.     

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。     

Advances in research of induced resistance to insects in cotton

Any change in a plant that occurs following herbivory or environmental factors is an induced response. These changes include phytochemical induction, increases in physical defenses, emission of volatiles that attract predators and parasitoids of herbivores, and reduction in plant nutritional quality for herbivores, which is termed induced resistance. Induced resistance has been demon-strated ubiquitously in plants. It is one of our goals to review what is known about the induced resistance to herbivorous insects in cotton, including three resistance secondary metabolites (terpenoid, tannin, and flavonoids) that are contained at any significant levels of resistance to herbivorous insects in cotton cultivates. In many cases, the quantities or quality of secondary metabolites in plant are changed after attacked by insects. This review focuses on induced plant resistance as quantitative or qualitative enhancement of defense mechanism against insect pests, especially on the abiotic-elicitors-induced resistance in cotton plants. The abiotic-elicitor of cupric chloride, an exogenous inorganic compound, may induce the second-ary metabolites accumulation and is referred to as a copper-inducible elicitor (CIE). Finally, we discuss how copper-inducible elicitor may be used in the Integrated Pest Management (IPM) system for cotton resistance control.     

Phytochemical diversity and synergistic effects on herbivores

Synergistic effects of multiple plant secondary metabolites on upper trophic levels constitute an underexplored but potentially widespread component of coevolution and ecological interactions. Examples of plant secondary metabolites acting synergistically as insect deterrents are not common, and many studies focus on the pharmaceutical applications of natural products, where activity is serendipitous and not an evolved response. This review summarizes some systems that are ideal for testing synergistic plant defenses and utilizes a focused meta-analysis to examine studies that have tested effects of multiple compounds on insects. Due to a dearth of ecological synergy studies, one of the few patterns for synergy that we are able to report from the meta-analysis is that phytochemical mixtures have a larger overall effect on generalist herbivores than specialist herbivores. We recommend a focus on synergy in chemical ecology programs and suggest future hypothesis tests and methods. These approaches are not focused on techniques in molecular biology to examine mechanisms at the cellular level, rather we recommend uncovering the existence of synergy first, by combining the best methods in organic synthesis, isolation, chemical ecology, bioassays, and quantitative analyses. Data generated by our recommended methods should provide rigorous tests of important hypotheses on how intraclass and interclass compounds act synergistically to deter insects, disrupt the immune response, and ultimately contribute to diversification. Further synergy research should also contribute to determining if antiherbivore synergy is widespread among plant secondary metabolites, which would be consistent with the hypothesis that synergistic defenses are a key attribute of the evolved diverse chemical mixtures found in plants.     

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。     

Costs of Defense and a Test of the Carbon-Nutrient Balance and Growth-Differentiation Balance Hypotheses for Two Co-Occurring Classes of Plant Defense

One of the goals of chemical ecology is to assess costs of plant defenses. Intraspecific trade-offs between growth and defense are traditionally viewed in the context of the carbon-nutrient balance hypothesis (CNBH) and the growth-differentiation balance hypothesis (GDBH). Broadly, these hypotheses suggest that growth is limited by deficiencies in carbon or nitrogen while rates of photosynthesis remain unchanged, and the subsequent reduced growth results in the more abundant resource being invested in increased defense (mass-balance based allocation). The GDBH further predicts trade-offs in growth and defense should only be observed when resources are abundant. Most support for these hypotheses comes from work with phenolics. We examined trade-offs related to production of two classes of defenses, saponins (triterpenoids) and flavans (phenolics), in Pentaclethra macroloba (Fabaceae), an abundant tree in Costa Rican wet forests. We quantified physiological costs of plant defenses by measuring photosynthetic parameters (which are often assumed to be stable) in addition to biomass. Pentaclethra macroloba were grown in full sunlight or shade under three levels of nitrogen alone or with conspecific neighbors that could potentially alter nutrient availability via competition or facilitation. Biomass and photosynthesis were not affected by nitrogen or competition for seedlings in full sunlight, but they responded positively to nitrogen in shade-grown plants. The trade-off predicted by the GDBH between growth and metabolite production was only present between flavans and biomass in sun-grown plants (abundant resource conditions). Support was also only partial for the CNBH as flavans declined with nitrogen but saponins increased. This suggests saponin production should be considered in terms of detailed biosynthetic pathway models while phenolic production fits mass-balance based allocation models (such as the CNBH). Contrary to expectations based on the two defense hypotheses, trade-offs were found between defenses and photosynthesis, indicating that studies of plant defenses should include direct measures of physiological responses.