No time for candy: passionfruit (Passiflora edulis) plants down-regulate damage-induced extra floral nectar production in response to light signals of competition

Plant fitness is often defined by the combined effects of herbivory and competition, and plants must strike a delicate balance between their ability to capture limiting resources and defend against herbivore attack. Many plants use indirect defenses, such as volatile compounds and extrafloral nectaries (EFN), to attract canopy arthropods that are natural enemies of herbivorous organisms. While recent evidence suggests that upon perception of low red to far-red (R:FR) ratios, which signal the proximity of competitors, plants down-regulate resource allocation to direct chemical defenses, it is unknown if a similar phytochrome-mediated response occurs for indirect defenses. We evaluated the interactive effects of R:FR ratio and simulated herbivory on nectar production by EFNs of passionfruit (Passiflora edulis f. flavicarpa). The activity of petiolar EFNs dramatically increased in response to simulated herbivory and hormonal treatment with methyl jasmonate (MeJA). Low R:FR ratios, which induced a classic “shade-avoidance” repertoire of increased stem elongation in P. edulis, strongly suppressed the EFN response triggered by simulated herbivory or MeJA application. Strikingly, the EFN response to wounding and light quality was localized to the branches that received the treatments. In vines like P. edulis, a local response would allow the plants to precisely adjust their light harvesting and defense phenotypes to the local conditions encountered by individual branches when foraging for resources in patchy canopies. Consistent with the emerging paradigm that phytochrome regulation of jasmonate signaling is a central modulator of adaptive phenotypic plasticity, our results demonstrate that light quality is a strong regulator of indirect defenses.     

Induction of extrafloral nectar depends on herbivore type in invasive and native Chinese tallow seedlings

Although induced defenses are widespread in nature, and a potentially important strategy used by invasive plants, it is unclear how induced defenses vary among populations and whether the intensity and duration of induced defenses depends on herbivore type. For invasive plants, low herbivore loads in their introduced ranges can lead to differences in herbivore defense compared to their native ranges, but we currently know little about how induced defenses vary among native and invasive populations. We conducted a greenhouse experiment to examine variation in one type of induced defense, extrafloral nectar (EFN) production, among native and invasive populations of Chinese tallow tree, Triadica sebifera. We experimentally manipulated herbivory from an exotic generalist scale insect, a native generalist caterpillar, both herbivores, or neither and then examined EFN production by Triadica. Damage from leaf-chewing caterpillars resulted in strongly induced EFN in both native and invasive populations while damage from phloem-feeding scales did not. Extrafloral nectar production and dissolved solute content peaked 4 days after caterpillar herbivory for both native and invasive populations. Number and proportion of leaves producing EFN, EFN volume and concentration of dissolved solutes were similar among native and invasive populations. These results suggest that selection for indirect defenses may be different than selection for other defenses in the introduced ranges of invasive plants, as constitutive and induced EFN production is retained in invasive populations.     

Decreased indirect defense in the invasive tree, Triadica sebifera

In the absence of coevolved natural enemies, plants are expected to experience selection away from costly herbivore defenses toward growth and reproduction [evolution of increased competitive ability hypothesis (EICA)], yet no one has demonstrated EICA for an indirect defense trait. Likewise, we have little understanding of how constitutive and induced levels of defense vary among native and invasive plant populations. We conducted a greenhouse experiment in the introduced range to test whether invasive populations have reduced constitutive and induced investment in an indirect defense trait, extrafloral nectar (EFN) production, compared to native populations of Chinese tallow tree, Triadica sebifera, through an experimental leaf damage treatment. Overall, native populations invested more in indirect defense: Native populations had a greater number (+16?%) and percentage of leaves producing EFN (35 vs. 28?%), produced more EFN (63?% greater volume), and produced more sugar (+33?%) compared to invasive populations, independent of damage treatment. Of these traits, number of leaves producing EFN and volume of EFN exhibited a trade-off between constitutive and induced investment but these did not depend on plant origin. Our results are the first to support the EICA hypothesis for an indirect defense trait. This suggests that tri-trophic interactions such as indirect defense are under similar selection as direct defense traits within introduced populations. Despite reduced investment in EFN production, invasive populations still retain the ability to produce EFN, which may enable invasive plants to defend against herbivores in the introduced range.     

Defensive effects of extrafloral nectaries in quaking aspen differ with scale

The effects of plant defenses on herbivory can differ among spatial scales. This may be particularly common with indirect defenses, such as extrafloral nectaries (EFNs), that attract predatory arthropods and are dependent on predator distribution, abundance, and behavior. We tested the defensive effects of EFNs in quaking aspen (Populus tremuloides Michx.) against damage by a specialist herbivore, the aspen leaf miner (Phyllocnistis populiella Cham.), at the scale of individual leaves and entire ramets (i.e., stems). Experiments excluding crawling arthropods revealed that the effects of aspen EFNs differed at the leaf and ramet scales. Crawling predators caused similar reductions in the percent leaf area mined on individual leaves with and without EFNs. However, the extent to which crawling predators increased leaf miner mortality and, consequently, reduced mining damage increased with EFN expression at the ramet scale. Thus, aspen EFNs provided a diffuse defense, reducing damage to leaves across a ramet regardless of leaf-scale EFN expression. We detected lower leaf miner damage and survival unassociated with crawling predators on EFN-bearing leaves, suggesting that direct defenses (e.g., chemical defenses) were stronger on leaves with than without EFNs. Greater direct defenses on EFN-bearing leaves may reduce the probability of losing these leaves and thus weakening ramet-scale EFN defense. Aspen growth was not related to EFN expression or the presence of crawling predators over the course of a single season. Different effects of aspen EFNs at the leaf and ramet scales suggest that future studies may benefit from examining indirect defenses simultaneously at multiple scales.     

Changing light conditions in pine rockland habitats affect the intensity and outcome of ant–plant interactions

Extrafloral nectar (EFN) mediates food‐for‐protection mutualisms between plants and ants. Such mutualisms exist within a complex web of biotic interactions, and in a framework provided by the abiotic environment. Both biotic and abiotic factors, therefore, affect the outcome of ant–plant interactions. We conducted an experiment to determine the effects of ant activity, and light intensity, on herbivory rates, growth, and reproductive fitness in Senna mexicana var. chapmanii, a perennial legume native to pine rockland habitats of south Florida. Forty plants were divided among four treatments in a factorial experimental design with two independent variables: ant activity and light intensity. Plants were divided equally between sunny and shady habitats, and ants were excluded from half of the plants in each habitat type. The presence of ants significantly reduced herbivory rates in S. chapmanii. In shaded habitats, the presence of ants had no effect on plant reproductive fitness, however, in sunny habitats plants with ants produced significantly more seeds over the duration of the 1‐yr study. Ants represent an important biotic defense against herbivores in S. chapmanii; however, their effects on plant fitness are dependent on light conditions. Pine rockland habitats in south Florida have been widely destroyed or mismanaged. In fragments that remain, suppression of fire has led to increased canopy closure and shading of the understory. These changes will likely negatively impact plants that rely on ants for defense. We highlight the importance of conservation efforts to preserve the pine rocklands and the fire regimes on which they rely.     

Intraspecific variation in defense against a generalist lepidopteran herbivore in populations of Eruca sativa (Mill.)

Populations of Eruca sativa (Brassicaceae) from desert and Mediterranean (Med) habitats in Israel differ in their defense against larvae of the generalist Spodoptera littoralis but not the specialist Pieris brassicae. Larvae of the generalist insect feeding on plants of the Med population gained significantly less weight than those feeding on the desert plants, and exogenous application of methyl jasmonate (MJ) on leaves of the Med plants significantly reduced the level of damage created by the generalist larvae. However, MJ treatment significantly induced resistance in plants of the desert population, whereas the generalist larvae caused similar damage to MJ‐induced and noninduced plants. Analyses of glucosinolates and expression of genes in their synthesis pathway indicated that defense in plants of the Med population against the generalist insect is governed by the accumulation of glucosinolates. In plants of the desert population, trypsin proteinase inhibitor activity was highly induced in response to herbivory by S. littoralis. Analysis of genes in the defense‐regulating signaling pathways suggested that in response to herbivory, differences between populations in the induced levels of jasmonic acid, ethylene, and salicylic acid mediate the differential defenses against the insect. In addition, expression analysis of myrosinase‐associated protein NSP2 suggested that in plants of the desert population, glucosinolates breakdown products were primarily directed to nitrile production. We suggest that proteinase inhibitors provide an effective defense in the desert plants, in which glucosinolate production is directed to the less toxic nitriles. The ecological role of nitrile production in preventing infestation by specialists is discussed.     

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。     

Changes in plant chemical defenses and nutritional quality as a function of ontogeny in <Emphasis Type="Italic">Plantago lanceolata</Emphasis> (Plantaginaceae)

Numerous empirical studies have examined ontogenetic trajectories in plant defenses but only a few have explored the potential mechanisms underlying those patterns. Furthermore, most documented ontogenetic trajectories in plant defenses have generally concentrated on aboveground tissues; thus, our knowledge regarding whole plant trends in plant defenses throughout development or potential allocation constraints between growth and defenses is limited. Here, we document changes in plant biomass, nutritional quality and chemical defenses for below- and aboveground tissues across seven age classes of Plantago lanceolata (Plantaginaceae) to evaluate: (1) partial and whole plant ontogenetic trajectories in constitutive chemical defenses and nutritional quality, and (2) the role of resource allocation constraints, namely root:shoot (R:S) ratios, in explaining whole plant investment in chemical defenses over time. Overall investment in iridoid glycosides (IGs) significantly increased, while water and nitrogen concentrations in shoot tissues decreased with plant age. Significant variation in IG content between shoot and root tissues across development was observed: allocation of IGs into root tissues linearly increased from younger to older plants, while non-linear shifts in allocation of IGs during ontogeny were observed for shoot tissues. Finally, R:S ratios only weakly explained overall allocation of resources into defenses, with young stages showing a positive relationship, while older stages showed a negative relationship between R:S ratios and IG concentrations. Ontogenetic trajectories in plant quality and defenses within and among plant tissues can strongly influence insect herbivores’ performance and/or predation risk; thus, they are likely to play a significant role in mediating species interactions.     

Pea aphids (Acyrthosiphon pisum Harris) reduce secretion of extrafloral nectar in broad bean (Vicia faba)

1. Herbivores sometimes suppress plant defences. This study tested whether the presence of pea aphids (Acyrthosiphon pisum Harris) on broad bean (Vicia faba) led to decreased secretion of extrafloral nectar (EFN) which functions as an indirect plant defence against herbivores. 2. To determine effects of aphid infestation on EFN secretion, a comparison was done between EFN secretion in uninfested plants and that in plants infested by A. pisum and another aphid species (Aphis craccivora Koch). 3. When broad bean plants were infested by A. pisum, they secreted significantly smaller amounts of EFN than did uninfested plants and A. craccivora‐infested plants. There was no significant difference in EFN secretion between uninfested plants and A. craccivora‐infested plants. The number of extrafloral nectaries did not differ among the three treatments. 4. These results suggest that A. pisum reduced EFN production in broad bean plants.     

Herbivory-induced overcompensation and resource-dependent production of extrafloral nectaries in Luffa cylindrica (Cucurbitaceae)

Extrafloral nectaries (EFNs) are nectar secretory structures involved in the indirect defense of plants. In the sponge gourd (Luffa cylindrica), EFNs commonly occur on the lower surface of leaf blades and stipules and remain functional until leaf senescence. To test the hypothesis that the development of EFNs is influenced by herbivore damage and resource availability, we grew Luffa cylindrica under different concentrations of Hoagland's nutrient solution (nutrient-poor conditions: 10%, 50%; and control condition: 100%) and two herbivory treatments (damaged and undamaged leaves). We collected ten leaves from treated plants to quantify leaf area and EFN density. Overall, leaf area increased and EFN decreased in damaged plants, but this significantly depended on nutritional status. In undamaged plants, EFN density tended to remain constant, whereas foliar area increased with nutrient input. Under herbivory, foliar area increased at 10% but decreased at 50 and 100% of nutrients in relation to undamaged plants, whereas EFN density tended to increase with nutrient availability to exceed undamaged plants under control concentrations. Plants under nutrient-poor conditions subjected to herbivory exhibited an increased foliar area, characterizing a compensatory mechanism. Our results suggest that herbivore-induced indirect defense is a damage- and resource-dependent response in Luffa cylindrica. These findings contribute to understanding the factors that modulate indirect defenses and plant-herbivore-environment interactions.     

Induced production of extrafloral nectar in intact lima bean plants in response to volatiles from spider mite-infested conspecific plants as a possible indirect defense against spider mites

We found that intact lima bean plants increased the secretion of extrafloral nectar (EFN) after exposure to Tetranychus urticae-induced plant volatiles. Predatory mites, Phytoseiulus persimilis, dispersed more slowly from an exposed intact plant than from a control plant (plant exposed to volatiles from intact conspecific). The predators also dispersed more slowly from those plants that were provided with extra EFN than from untreated plants. We further show that EFN was a potential alternative food source for P. persimilis. From these results, we concluded that increased EFN was involved in the slow dispersal of P. persimilis from the plants exposed to herbivore-induced plant volatiles. Our data suggest that the increase of EFN in an HIPV-exposed intact plant could be an induced indirect defense against spider mites.     

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。     

Physiological responses of spring rapeseed (Brassica napus) to red/far‐red ratios and irradiance during pre‐ and post‐flowering stages

Early shade signals promote the shade avoidance syndrome (SAS) which causes, among others, petiole and shoot elongation and upward leaf position. In spite of its relevance, these photomorphogenic responses have not been deeply studied in rapeseed (Brassica napus). In contrast to other crops like maize and wheat, rapeseed has a complex developmental phenotypic pattern as it evolves from an initial rosette to the main stem elongation and an indeterminate growth of floral raceme. In this work, we analyzed (1) morphological and physiological responses at individual level due to low red/far‐red (R/FR) ratio during plant development, and (2) changes in biomass allocation, grain yield and composition at crop level in response to high R/FR ratio and low irradiance in two modern spring rapeseed genotypes. We carried out pot and field experiments modifying R/FR ratios and irradiance at vegetative or reproductive stages. In pot experiments, low R/FR ratio increased the petiole and lamina length, upward leaf position and also accelerated leaf senescence. Furthermore, low R/FR ratio reduced main floral raceme and increased floral branching with higher remobilization of soluble carbohydrates from the stems. In field experiments, low irradiance during post‐flowering reduced grain yield, harvest index and grain oil content, and high R/FR ratio reaching the crop partially alleviated such effects. We conclude that photomorphogenic signals are integrated early during the vegetative growth, and irradiance has stronger effects than R/FR signals at rapeseed crop level.     

How to induce defense responses in wild plant populations? Using bilberry (Vaccinium myrtillus) as example

Inducible plant defense is a beneficial strategy for plants, which imply that plants should allocate resources from growth and reproduction to defense when herbivores attack. Plant ecologist has often studied defense responses in wild populations by biomass clipping experiments, whereas laboratory and greenhouse experiments in addition apply chemical elicitors to induce defense responses. To investigate whether field ecologists could benefit from methods used in laboratory and greenhouse studies, we established a randomized block‐design in a pine‐bilberry forest in Western Norway. We tested whether we could activate defense responses in bilberry (Vaccinium myrtillus) by nine different treatments using clipping (leaf tissue or branch removal) with or without chemical treatment by methyljasmonate (MeJA). We subsequently measured consequences of induced defenses through vegetative growth and insect herbivory during one growing season. Our results showed that only MeJA‐treated plants showed consistent defense responses through suppressed vegetative growth and reduced herbivory by leaf‐chewing insects, suggesting an allocation of resources from growth to defense. Leaf tissue removal reduced insect herbivory equal to the effect of the MeJa treatments, but had no negative impact on growth. Branch removal did not reduce insect herbivory or vegetative growth. MeJa treatment and clipping combined did not give an additional defense response. In this study, we investigated how to induce defense responses in wild plant populations under natural field conditions. Our results show that using the chemical elicitor MeJA, with or without biomass clipping, may be a better method to induce defense response in field experiments than clipping of leaves or branches that often has been used in ecological field studies.     

Differential response of Scots pine seedlings to variable intensity and ratio of red and far‐red light

We investigated the response to increasing intensity of red (R) and far‐R (FR) light and to a decrease in R:FR ratio in Pinus sylvestris L. (Scots pine) seedling. The results showed that FR high‐irradiance response for hypocotyl elongation may be present in Scots pine and that this response is enhanced by increasing light intensity. However, both hypocotyl inhibition and pigment accumulation were more strongly affected by the R light compared with FR light. This is in contrast to previous reports in Arabidopsis thaliana (L.) Heynh. In the angiosperm, A. thaliana R light shows an overall milder effect on inhibition of hypocotyl elongation and on pigment biosynthesis compared with FR suggesting conifers and angiosperms respond very differently to the different light regimes. Scots pine shade avoidance syndrome with longer hypocotyls, shorter cotyledons and lower chlorophyll content in response to shade conditions resembles the response observed in A. thaliana. However, anthocyanin accumulation increased with shade in Scots pine, which again differs from what is known in angiosperms. Overall, the response of seedling development and physiology to R and FR light in Scots pine indicates that the regulatory mechanism for light response may differ between gymnosperms and angiosperms.     

PHENOTYPIC PLASTICITY EARLY IN LIFE CONSTRAINS DEVELOPMENTAL RESPONSES LATER

Abstract.— Plastic stem‐elongation responses to the ratio of red:far‐red (R:FR) wavelengths enable plants to match their phenotype to local competitive conditions. However, elongation responses early in the life history may occur at the cost of reduced plasticity later in the life history, because elongation influences both allocation patterns and structural integrity. A common‐garden experiment was performed to test whether seedling responses to R:FR affect biomass allocation, biomass accumulation, and subsequent plasticity to the cue. Seedlings of Abutilon theophrasti were stimulated to elongate by low R:FR treatments, and subsequent growth and plasticity was compared with nonelongated individuals. Elongated seedlings were less responsive than nonelongated ones to a second bout of low R:FR. Thus, seedling plasticity to R:FR reduces subsequent responsiveness to this cue. This negative association across life‐history stages suggests an important constraint on the evolution of plastic stem responses, because selection in A. theophrasti has previously been shown to favor increases in early elongation in combination with increased later elongation. The reduced responsiveness of elongated seedlings to R:FR appeared to result from a structural feedback mechanism, indicating that the opportunity cost of early responses may be lower in environments providing structural support.     

Tree species diversity alters plant defense investment in an experimental forest plantation in southern Mexico

How plant species diversity affects traits conferring herbivore resistance (e.g., chemical defenses), as well as the mechanisms underlying such effects, has received little attention. One potential mechanism for the effect of diversity on plant defenses is that increased plant growth at high diversity could lead to reduced investment in defenses via growth–defense trade‐offs. We measured tree growth (diameter at breast height) and collected leaves to quantify total phenolics in 2.5‐year‐old plants of six tropical tree species (N = 597 plants) in a young experimental plantation in southern Mexico. Selected plants were classified as monocultures or as polycultures represented by mixtures of four of the six species examined. Tree species diversity had a significant negative effect on total phenolics, where polycultures exhibited a 13 percent lower mean concentration than monocultures. However, there was marked variation in the effects of diversity on defenses among tree species, with some species exhibiting strong reductions in phenolic levels in mixtures, whereas others were unresponsive. In addition, tree species diversity had no effect on growth, nor was the negative effect of diversity on chemical defenses mediated by a growth–defense trade‐off. These results demonstrate that tree diversity can alter investment in chemical defenses in long‐lived tree species but that such effect may not always be under strong control by plant endogenous resource allocation trade‐offs. Regardless of the underlying mechanism, these findings have important implications for predicting effects on consumers and ecosystem function.