Plant Defense Theory Research Articles

Phytochemical drivers of insect herbivory: a functional toolbox to support agroecological diversification.

Plant metabolism is a key feature of biodiversity that remains underexploited in functional frameworks used in agroecology. Here, we study how phytochemical diversity considered at three organizational levels can promote pest control. In a factorial field experiment, we manipulated plant diversity in three monocultures and three mixed crops of oilseed rape to explore how intra- and interspecific phytochemical diversity affects pest infestation. We combined recent progress in metabolomics with classic metrics used in ecology to test a box of hypotheses grounded in plant defence theory. According to the hypothesis of 'phytochemically mediated coevolution', our study stresses the relationships between herbivore infestation and particular classes of specialized metabolites like glucosinolates. Among 178 significant relationships between metabolites and herbivory rates, only 20% were negative. At the plant level, phytochemical abundance and richness had poor predictive power on pest regulation. This challenges the hypothesis of 'synergistic effects'. At the crop cover level, in line with the hypothesis of 'associational resistance', the phytochemical dissimilarity between neighbouring plants limited pest infestation. We discuss the intricate links between associational resistance and bottom-up pest control. Bridging different levels of organization in agroecosystems helps to dissect the multi-scale relationships between phytochemistry and insect herbivory.

Evolutionary signatures of a trade-off in direct and indirect defenses across the wild grape genus Vitis.

Evolutionary correlations between chemical defense and protection by mutualist bodyguards have been long predicted, but tests of these pattern remain rare. We use a phylogenetic framework to test for evolutionary correlations indicative of trade-offs or synergisms between direct defense in the form of plant secondary metabolism, and indirect defense in the form of leaf domatia, across 33 species in the wild grape genus, Vitis. We also performed a bioassay with a generalist herbivore to associate our chemical phenotypes with herbivore palatability. Finally, we tested whether defensive traits correlate with the average abiotic characteristics of each species' contemporary range and whether these correlations were consistent with plant defense theory. We found a negative evolutionary correlation between domatia size and the diversity of secondary metabolites in Vitis leaf tissue across the genus, and also that leaves with a higher diversity and richness of secondary metabolites were less palatable to a generalist herbivore, consistent with a trade-off in chemical and mutualistic defense investment. Predictions from plant defense theory were not supported by associations between investment in defense phenotypes and abiotic variables. Our work demonstrates an evolutionary pattern indicative of a trade-off between indirect and direct defense strategies across the Vitis genus.

Cotton plants as ideal models for teaching and research on inducible direct plant defenses

Cotton (Gossypium hirsutum) stores defensive compounds in glands covering its leaves and other tissues. The density and the chemical filling of these glands increase systematically in developing leaves in response to herbivory on older leaves. Cotton seedlings are known to respond more strongly to actual caterpillar herbivory than to mere physical damage. It is not clear whether this amplified response is linked to insect-derived elicitors or difference in damage properties. To investigate this, we assessed the effect of repeated artificial damage without and with application of regurgitant from Spodoptera exigua caterpillars. Repeated mechanical damage led to a systemic increase of gland density, gland size, and content of defensive terpenes, with no detectable additional elicitation upon regurgitant treatment. Dual choice feeding assays further showed that defense induction triggered by just physical damage made newly developing leaves far less palatable to S. exigua larvae as compared to leaves from undamaged seedlings, whereas they did not distinguish between leaves from damaged plants treated with or without regurgitant. Our study confirms that the systemic induction of cotton glands is an unspecific response to physical damage, although cotton is known to respond to caterpillar-associated elicitors for other defensive traits. Cotton glands induction can be readily visualized under modest magnification, making the experiments described in this study highly suited to teach chemical ecology and aspects of plant defense theory in practical classes.

Using biological invasions to improve plant defense theory

AbstractTheory to explain how plants defend themselves against herbivorous insects is rich, but can be difficult to test. Biological invasions provide unique opportunities to test and improve upon plant defense theory, as plants experience predictable shifts in insect herbivory after introduction to a new range. Here, we use an invasion to evaluate the power of three cornerstone hypotheses to predict the evolution of defense against herbivorous insects. These three hypotheses represent increasing refinements of classic plant‐insect theory regarding optimal defense, and each rests on the same three assumptions: that introduced plant populations escape natural enemies, that insect herbivory reduces plant fitness, and that putative defenses decrease herbivory. These assumptions remain untested in most invasions, which likely contributes to conflicting support for many plant defense hypotheses. We provide evidence that these assumptions are met in common mullein, Verbascum thapsus L. (Scrophulariaceae), which we propose can thus be used as a model system to test plant defense theory. We find that the hypothesis that integrates predictions of within‐plant optimal defense theory and the evolutionary dilemma model (i.e., the ‘shifting defense allocation’ hypothesis) provides strong insights into both invasion and evolution of plant defense. Specifically, we show that introduced populations that escape important specialist herbivores increase the concentration of secondary compounds in high‐quality tissue in particular, in this case protecting valuable young leaves from generalist herbivores that dominate in the introduced range. We would not have detected this shift without exploring within‐plant defense allocation across native and introduced populations, a task rarely undertaken when assessing evolutionary change in plant defenses. This finding provides broad insight into how native and introduced plant populations alike may respond to shifts in herbivore pressure. We close by highlighting future directions of inquiry using introduced plant populations to develop and test plant defense theory more generally.

Distributing Defenses: How Resource Defendability Shapes the Optimal Response to Risk.

AbstractMany organisms divide limited defenses among heterogeneous assets. Plants allocate defensive chemicals among tissues differing in value, cost of defense, and risk of herbivory. Some ant colonies allocate specialized defenders among multiple nests differing in volume, entrance size, and risk of attack. We develop a general mathematical model to determine the optimal strategy for dividing defenses among assets depending on their value, defendability, and risk of attack. We build on plant defense theory by focusing on defendability, which we define as the functional relationship between defensive investment and successful defense. We show that if hard-to-defend assets cost more to defend, as assumed in resource defense theory, the optimal strategy allocates more defenses to those assets, regardless of risk. Inspired by cavity-nesting ants, we also consider the possibility that hard-to-defend assets have a lower chance to be successfully defended, even when defensive investment is high. Under this assumption, the optimal response to elevated risk is to reduce defensive allocation to hard-to-defend assets, a conservative strategy previously observed in turtle ants (Cephalotes). This new perspective on defendability suggests that in systems where assets differ in the chance of successful defense, defensive strategies may evolve to be sensitive to risk in surprising ways.

Effects of Magnetized, Chelated Iron Foliage Treatments on Foliar Physiology, Plant Growth and Drought Tolerance for Two Legume Species

A greenhouse study was conducted to determine the effects of foliar applications of magnetized, chelated liquid iron fertilizer for increasing the drought tolerance of two legumes. Study objectives were to determine the drought tolerance effects of four treatments on foliar gas exchange, soil moisture, and plant growth for velvet bean (Mucuns pruriens) and soybean (Gylcine max) plants. The four foliage treatments included applications with chelated liquid iron fertilizer (2.5 and 5%) with a conventional boom sprayer, with and without magnets in the spray lines. Physiological measurements were collected before foliar treatments and again after a 24-day deficit irrigation schedule. Physicochemical water properties were measured for each of the foliar treatments. Photosynthesis rates were 5.98, 2.04 and 3.19 µmol/m2/s for the control, non-magnetized and magnetized fertilizer treatments (2.5%), respectively, after completing the deficit irrigation schedule. Instantaneous water use efficiency (IWUE) was 0.60, 0.28 and 1.02 for the control, non-magnetized and magnetized fertilizer treatments (2.5%), respectively, after completing the deficit irrigation schedule. Photosynthesis and IWUE increased 56 and 263% for the magnetized fertilizer treatment (2.5%) compared to the non-magnetized foliar treatment, when averaged across both legume species. Photosynthesis and IWUE increased as electrical conductivity increased and oxidation reduction potential (ORP) decreased in absolute terms. A single foliar application resulted in aberrant physiological responses that are contrary to very widely held plant defense theories involving abiotic stressors. The single application improved the photosynthesis and water use efficiency for water stressed legumes emphasizing the need to better understand the relationships between water quality, plant bioenergetics, and stress physiology. Improved drought tolerance in row crops such as dry beans and soybeans, with a single magnetized fertilizer application, would be cost effective and easily adapted into current cropping systems. Interactions among physicochemical water properties, bioenergetics, plant metabolism, and crop stress physiology need to be further investigated in order to improve the quality of irrigation water to enhance drought tolerance of field crops.

A preliminary evaluation of the environmental toxicology of road salts on plant root dynamics

Although critical for the deicing of roads and bridges throughout the winter season in North America, road salts continue to have yearlong negative impacts on both anthropogenic and biological systems. Our objective was to measure the impact of four commonly used road salt ingredients on the dynamics of plant growth and development. Using onions as a model system, we hypothesized that exposing plants to different concentrations of sodium chloride, calcium chloride, potassium chloride, and magnesium chloride treatments would allow us to calculate the environmental concentration at which root development is halted by each road salt. We found that root growth decreased with sodium chloride, calcium chloride, and potassium chloride treatments, but increased with magnesium chloride. We used a linear model of root growth rates and concentrations to calculate the level at which each road salt becomes toxic to plants in the surrounding environment. We also apply the ecological theory of the principle of allocation to discuss how the chemical induction of root growth by magnesium chloride road salts may result in a life history trade-off that reduces investment toward plant-defense. The predicted trade-off in plant defense suggests that crop species in urban environments would be more susceptible to herbivory and as such would rely more on agricultural pesticides to sustain food security. We propose further studies to evaluate applications of plant defense theory in an urban context.

Phytochemistry reflects different evolutionary history in traditional classes versus specialized structural motifs

Foundational hypotheses addressing plant–insect codiversification and plant defense theory typically assume a macroevolutionary pattern whereby closely related plants have similar chemical profiles. However, numerous studies have documented variation in the degree of phytochemical trait lability, raising the possibility that phytochemical evolution is more nuanced than initially assumed. We utilize proton nuclear magnetic resonance (1H NMR) data, chemical classification, and double digest restriction-site associated DNA sequencing (ddRADseq) to resolve evolutionary relationships and characterize the evolution of secondary chemistry in the Neotropical plant clade Radula (Piper; Piperaceae). Sequencing data substantially improved phylogenetic resolution relative to past studies, and spectroscopic characterization revealed the presence of 35 metabolite classes. Metabolite classes displayed phylogenetic signal, whereas the crude 1H NMR spectra featured little evidence of phylogenetic signal in multivariate tests of chemical resonances. Evolutionary correlations were detected in two pairs of compound classes (flavonoids with chalcones; p-alkenyl phenols with kavalactones), where the gain or loss of a class was dependent on the other’s state. Overall, the evolution of secondary chemistry in Radula is characterized by strong phylogenetic signal of traditional compound classes and weak phylogenetic signal of specialized chemical motifs, consistent with both classic evolutionary hypotheses and recent examinations of phytochemical evolution in young lineages.

Herbivore-induced defenses are not under phylogenetic constraints in the genus Quercus (oak): Phylogenetic patterns of growth, defense, and storage.

The evolution of plant defenses is often constrained by phylogeny. Many of the differences between competing plant defense theories hinge upon the differences in the location of meristem damage (apical versus auxiliary) and the amount of tissue removed. We analyzed the growth and defense responses of 12 Quercus (oak) species from a well‐resolved molecular phylogeny using phylogenetically independent contrasts. Access to light is paramount for forest‐dwelling tree species, such as many members of the genus Quercus. We therefore predicted a greater investment in defense when apical meristem tissue was removed. We also predicted a greater investment in defense when large amounts of tissue were removed and a greater investment in growth when less tissues were removed. We conducted five simulated herbivory treatments including a control with no damage and alterations of the location of meristem damage (apical versus auxiliary shoots) and intensity (25% versus 75% tissue removal). We measured growth, defense, and nutrient re‐allocation traits in response to simulated herbivory. Phylomorphospace models were used to demonstrate the phylogenetic nature of trade‐offs between characteristics of growth, chemical defenses, and nutrient re‐allocation. We found that growth–defense trade‐offs in control treatments were under phylogenetic constraints, but phylogenetic constraints and growth–defense trade‐offs were not common in the simulated herbivory treatments. Growth–defense constraints exist within the Quercus genus, although there are adaptations to herbivory that vary among species.

Extending Plant Defense Theory to Seeds

Plant defense theory explores how plants invest in defenses against natural enemies but has focused primarily on the traits expressed by juvenile and mature plants. Here we describe the diverse ways in which seeds are chemically and physically defended. We suggest that through associations with other traits, seeds are likely to exhibit defense syndromes that reflect constraints or trade-offs imposed by selection to attract dispersers, enable effective dispersal, ensure appropriate timing of seed germination, and enhance seedling performance. We draw attention to seed and reproductive traits that are analogous to defense traits in mature plants and describe how the effectiveness of defenses is likely to differ at pre- and postdispersal stages. We also highlight recent insights into the mutualistic and antagonistic interactions between seeds and microbial communities, including fungi and endohyphal bacteria, that can influence seed survival in the soil and subsequent seedling vigor.

Information theory tests critical predictions of plant defense theory for specialized metabolism.

Different plant defense theories have provided important theoretical guidance in explaining patterns in plant specialized metabolism, but their critical predictions remain to be tested. Here, we systematically explored the metabolomes of Nicotiana attenuata, from single plants to populations, as well as of closely related species, using unbiased tandem mass spectrometry (MS/MS) analyses and processed the abundances of compound spectrum-based MS features within an information theory framework to test critical predictions of optimal defense (OD) and moving target (MT) theories. Information components of plant metabolomes were consistent with the OD theory but contradicted the main prediction of the MT theory for herbivory-induced dynamics of metabolome compositions. From micro- to macroevolutionary scales, jasmonate signaling was confirmed as the master determinant of OD, while ethylene signaling provided fine-tuning for herbivore-specific responses annotated via MS/MS molecular networks.

Resin ducts as resistance traits in conifers: linking dendrochronology and resin-based defences.

Conifers have evolved different chemical and anatomical defences against a wide range of antagonists. Resin ducts produce, store and translocate oleoresin, a complex terpenoid mixture that acts as both a physical and a chemical defence. Although resin duct characteristics (e.g., number, density, area) have been positively related to biotic resistance in several conifer species, the literature reporting this association remains inconclusive. Axial resin ducts recorded in annual growth rings are an archive of annual defensive investment in trees. This whole-life record of defence investment can be analysed using standard dendrochronological procedures, which allows us to assess interannual variability and the effect of understudied drivers of phenotypic variation on resin-based defences. Understanding the sources of phenotypic variation in defences, such as genetic differentiation and environmental plasticity, is essential for assessing the adaptive potential of forest tree populations to resist pests under climate change. Here, we reviewed the evidence supporting the importance of resin ducts in conifer resistance, and summarized current knowledge about the sources of variation in resin duct production. We propose a standardized methodology to measure resin duct production by means of dendrochronological procedures. This approach will illuminate the roles of resin ducts in tree defence across species, while helping to fill pivotal knowledge gaps in plant defence theory, and leading to a robust understanding of the patterns of variation in resin-based defences throughout the tree's lifespan.

Trade-offs between growth, reproduction and defense in response to resource availability manipulations.

The Brazilian Cerrado is one of the most endangered biomes in the world. We evaluated the sustainability of leaf harvest in one of the most important Cerrado tree species, Stryphnodendron adstringens. The bark of this tree is used as a source of medicinal tannin. Harvesting bark, however, often kills the tree. In a manipulative field experiment, we tested the hypothesis that harvesting leaves, which might serve as an alternative source of tannin, would be less detrimental for tree survival, growth, reproduction, and defense than harvesting bark. In a two-way crossed experimental design, we either clipped 100% of a plant’s leaves or applied NPK fertilizer to the soil. Our predictions of the experimental outcomes were based on plant resource and defense theory. Growth was determined by total leaf dry mass production, reproduction by inflorescence and fruit production traits, and defense by total phenolics, hydrolyzable tannins, and condensed tannins. Fertilization had a marginally positive effect on total leaf dry mass. Defoliation had no effect on subsequent leaf production, and most importantly, no plants died as a result of defoliation. We found high tannin amounts in leaves of S. adstringens produced both prior to and subsequent to clipping, further suggesting that leaves could serve as a sustainable alternative source of tannin. After clipping, plants invested more in tannin production and less in reproduction. Our results suggest that leaf harvest may be more sustainable than harvesting of bark in S. adstringens. We suggest the need for further investigation of the medicinal properties of leaf tannins to formulate a viable sustainable management plan for the exploitation of this plant species.

Effects of long-term nitrogen and phosphorus addition on plant defence compounds in a freshwater wetland

Prominent theories of plant defence have predicted that alleviating nutrient limitation will result in decreased production of defence compounds. Yet effects of nutrient addition on plant defence compounds have been found to vary, and research on plant resource allocation in different organs in response to long-term nutrient addition is limited. In this study, we aimed to elucidate effects of 12-yr nitrogen (N) addition and 10-yr phosphorus (P) addition on plant defence compounds (total polyphenols, condensed tannins, cellulose and lignin) in both leaves and stems of dominant specie Glyceria spiculosa in a freshwater wetland in the Sanjiang Plain, Northeast China. Both N addition and P addition reduced the production of defence compounds in plant leaves, but increased the production of lignin in the stems. Notably, the concentrations of plant secondary metabolites closely correlated with the plant C:N:P stoichiometric ratios. The results suggest that long-term nutrient addition can alter plant carbon allocation to C-based defence compounds, and thus potentially exert influences on nutrient cycling and ecological processes in freshwater wetlands.

Plant physical and chemical defence variation along elevation gradients: a functional trait-based approach.

Predicting variation in plant functional traits related to anti-herbivore defences remains a major challenge in ecological research, considering that multiple traits have evolved in response to both abiotic and biotic conditions. Therefore, understanding variation in plant anti-herbivore defence traits requires studyingtheir expression along steep environmental gradients, such as along elevation,where multiple biotic and abiotic factors co-vary. We expand on plant defence theory and propose a novel conceptual framework to address the sources of variations of plant resistance traits at the community level. We analysed elevation patterns of within-community trait dissimilarity using the RaoQ index, and the community-weighted-mean (CWM) index, on several plant functional traits: plant height, specific leaf area (SLA), leaf-dry-matter-content (LDMC), silicium content, presence of trichomes, carbon-to-nitrogen ratio (CN) and total secondary metabolite richness. We found that at high elevation, where harsh environmental conditions persist, community functional convergence is dictated by traits relating to plant growth (plant height and SLA), while divergence arises for traits relating resource-use (LDMC). At low elevation, where greater biotic pressure occurs, we found a combination of random (plant height), convergence (metabolite richness) and divergence patterns (silicium content). This framework thus combines community assembly rules of ecological filtering and niche partition with plant defence hypotheses to unravel the relationship between environmental variations, biotic pressure and the average phenotype of plants within a community.

The Effects of Artificial Selection for Rapid Cycling in Brassica rapa on Herbivore Preference and Performance

Premise of research. The assumption of a trade-off between growth and defense is a major tenet of plant defense theory, though not all prior research has supported this trade-off. If this trade-off...

Breaching Plant Defence Theories:Growth Rates of Plants Directly Impact the Evolution of Consumption Rates of Herbivorous Insects

Independent of the nature and extent of plant defences, the growth rates of plants could solely influence the consumption rates of herbivorous insects in a manner that allows insects feeding on slower growing plants to have lower consumption rates. Further, there may be diverse links between defences and growth rates of plants that are yet to be discovered.

Regulation of Fatty Acid Production and Release in Benthic Algae: Could Parallel Allelopathy Be Explained with Plant Defence Theories?

Many organisms produce chemical compounds, generally referred as secondary metabolites, to defend against predators and competitors (allelopathic compounds). Several hypotheses have been proposed to explain the interaction between environmental factors and secondary metabolites production. However, microalgae commonly use simple metabolites having a role in primary metabolism as allelopathic compounds. The aim of this study was to determine whether classical theories of plant chemical defences could be applied to microalgae producing allelochemicals derived from the primary metabolism. Our study was designed to investigate how growth phase, algal population density, nutrient limitation and carbon assimilation affect the production and release of allelopathic free fatty acids (FFAs) among other FFAs. The model species used was Uronema confervicolum, a benthic filamentous green alga that produces two allelopathic FFAs (linoleic and α-linolenic acids) inhibiting diatom growth. FFAs have been quantified in algal biomass and in culture medium. Our results were analysed according to two classical plant defence theories: the growth-differentiation balance hypothesis (GDBH) and the optimal defence theory (ODT), based on the metabolic capacities for defence production and on the need for defence, respectively. While a higher production of allelopathic compounds under increased light conditions supports the use of GDBH with this microalga, the observation of a negative feedback mechanism mostly supports ODT. Therefore, both theories were insufficient to explain all the observed effects of environmental factors on the production of these allelochemicals. This highlights the needs of new theories and models to better describe chemical interactions of microalgae.

Recent advances in plant-herbivore interactions

Plant-herbivore interactions shape community dynamics across marine, freshwater, and terrestrial habitats. From amphipods to elephants and from algae to trees, plant-herbivore relationships are the crucial link generating animal biomass (and human societies) from mere sunlight. These interactions are, thus, pivotal to understanding the ecology and evolution of virtually any ecosystem. Here, we briefly highlight recent advances in four areas of plant-herbivore interactions: (1) plant defense theory, (2) herbivore diversity and ecosystem function, (3) predation risk aversion and herbivory, and (4) how a changing climate impacts plant-herbivore interactions. Recent advances in plant defense theory, for example, highlight how plant life history and defense traits affect and are affected by multiple drivers, including enemy pressure, resource availability, and the local plant neighborhood, resulting in trait-mediated feedback loops linking trophic interactions with ecosystem nutrient dynamics. Similarly, although the positive effect of consumer diversity on ecosystem function has long been recognized, recent advances using DNA barcoding to elucidate diet, and Global Positioning System/remote sensing to determine habitat selection and impact, have shown that herbivore communities are probably even more functionally diverse than currently realized. Moreover, although most diversity-function studies continue to emphasize plant diversity, herbivore diversity may have even stronger impacts on ecosystem multifunctionality. Recent studies also highlight the role of risk in plant-herbivore interactions, and risk-driven trophic cascades have emerged as landscape-scale patterns in a variety of ecosystems. Perhaps not surprisingly, many plant-herbivore interactions are currently being altered by climate change, which affects plant growth rates and resource allocation, expression of chemical defenses, plant phenology, and herbivore metabolism and behavior. Finally, we conclude by noting that although the field is advancing rapidly, the world is changing even more rapidly, challenging our ability to manage these pivotal links in the food chain.

Nutrient supply alters goldenrod's induced response to herbivory

SummaryRecent interest in using trait‐based approaches to understand and predict ecosystem processes and evolutionary responses to environmental change highlights the need to understand the relative importance of genetic and environmental sources of intraspecific trait variation within local populations of dominant species.Here, I combine plant defence theory with functional approaches to quantify genetic trait variation and phenotypic trait plasticity of nine goldenrod (Solidago altissima) genotypes derived from a local field population in Connecticut, USA, to herbivory along a nutrient supply gradient.I found that increasing nutrient supply changed the dominant plant defence strategy from tolerance to induced resistance. Induced resistance was detected through decreased herbivore growth rates and a behavioural feeding shift of grasshoppers to older leaf tissue. This could not be fully accounted for through stoichiometric changes in leaf tissue quality.A multidimensional phenotype approach revealed that abiotic and biotic environments (nutrients and herbivory) accounted for almost as much whole‐plant trait variation (31%) as did plant genotype (36%). Increasing nutrient supply and herbivory resulted in independent and differential effects on whole‐plant trait expression. Increasing both treatments concurrently produced a unique plant phenotype with increased leaf carbon content and allocation to asexual reproduction (E × E).Notably, individual genotypes exhibited different magnitudes of multivariate trait plasticity to nutrient and herbivory gradients. However, the population of genotypes as a whole within a given environment expressed an approximately equal magnitude of trait variation across both permissive (high nutrient, no herbivory) and stressful (low nutrient, high herbivory) environments.Quantifying plasticity in defensive strategy in concert with correlated whole‐plant trait expression changes across multiple abiotic and biotic factors may be key to providing a mechanistic understanding of how heterogeneous landscapes impact community interactions and ecosystem processes.Alay summaryis available for this article.