Herbivore induced plant volatiles: Their role in plant defense for pest management

Plants respond to herbivory through different defensive mechanisms. The induction of volatile emission is one of the important and immediate response of plants to herbivory. Herbivore-induced plant volatiles (HIPVs) are involved in plant communication with natural enemies of the insect herbivores, neighboring plants, and different parts of the damaged plant. Release of a wide variety of HIPVs in response to herbivore damage and their role in plant-plant, plant-carnivore and intraplant communications represents a new facet of the complex interactions among different trophic levels. HIPVs are released from leaves, flowers, and fruits into the atmosphere or into the soil from roots in response to herbivore attack. Moreover, HIPVs act as feeding and/or oviposition deterrents to insect pests. HIPVs also mediate the interactions between the plants and the microorganisms. This review presents an overview of HIPVs emitted by plants, their role in plant defense against herbivores and their implications for pest management.     

Mechanisms of plant defense against insect herbivores

Plants respond to herbivory through various morphological, biochemicals, and molecular mechanisms to counter/offset the effects of herbivore attack. The biochemical mechanisms of defense against the herbivores are wide-ranging, highly dynamic, and are mediated both by direct and indirect defenses. The defensive compounds are either produced constitutively or in response to plant damage, and affect feeding, growth, and survival of herbivores. In addition, plants also release volatile organic compounds that attract the natural enemies of the herbivores. These strategies either act independently or in conjunction with each other. However, our understanding of these defensive mechanisms is still limited. Induced resistance could be exploited as an important tool for the pest management to minimize the amounts of insecticides used for pest control. Host plant resistance to insects, particularly, induced resistance, can also be manipulated with the use of chemical elicitors of secondary metabolites, which confer resistance to insects. By understanding the mechanisms of induced resistance, we can predict the herbivores that are likely to be affected by induced responses. The elicitors of induced responses can be sprayed on crop plants to build up the natural defense system against damage caused by herbivores. The induced responses can also be engineered genetically, so that the defensive compounds are constitutively produced in plants against are challenged by the herbivory. Induced resistance can be exploited for developing crop cultivars, which readily produce the inducible response upon mild infestation, and can act as one of components of integrated pest management for sustainable crop production.     

Avoidance and suppression of plant defenses by herbivores and pathogens

Plants are nutritious and hence herbivores and phytopathogens have specialized to attack and consume them. In turn, plants have evolved adaptations to detect and withstand these attacks. Such adaptations we call ‘defenses’ and they can operate either directly between the plant and the plant consumer or indirectly i.e. when taking effect via other organisms such as predators and parasitoids of herbivores. Plant defenses put selection pressure on plant-consumers and, as a result, herbivores and pathogens have evolved counter-adaptations to avoid, resist, or manipulate plant defenses. Here we review how plant consumers have adapted to cope with plant defenses and we will put special emphasis on the phenomenon of suppression of plant defenses.     

Jasmonic acid signalling and herbivore resistance traits constrain regrowth after herbivore attack in Nicotiana attenuata

Because traits conferring resistance on herbivores can reduce fitness-associated traits, trade-offs may occur between tolerance and resistance responses. We examined these trade-offs in genotypes of Nicotiana attenuata that were transformed to silence trypsin proteinase inhibitor (TPI) production (AS-Natpi), an antiherbivore defense associated with (14%) reductions in seed production, and the jasmonate signal cascade that elicits these defenses (AS-Nalox3), by measuring stalk and axillary branch growth and seed production after two defoliation regimes and Manduca sexta larval attack to bottom or middle and top stalk leaves. Larval attack and defoliation at middle and top leaves depressed seed production and increased axillary branching more than at bottom leaves. AS-Nalox3 and AS-Natpi plants produced significantly longer (two- to fourfold) branches than did wild-type (WT) plants, results that are consistent with resource-based trade-offs between resistance and regrowth. Methyl jasmonate (MeJA) treatment of AS-Nalox3 plants restored WT branch growth, suggesting that jasmonic acid (JA) signalling suppresses regrowth and contributes to apical dominance. These results are consistent with the existence of JA- and resource-mediated trade-offs between regrowth and herbivore resistance traits.     

Will plant vigor and tolerance be genetically correlated? Effects of intrinsic growth rate and self-limitation on regrowth

Plants are known to maintain fitness despite herbivore attack by a variety of damage-induced mechanisms. These mechanisms are said to confer tolerance, which can be measured as the slope of fitness over the proportion of plant biomass removed by herbivore damage. It was recently supposed by Stowe et al. (2000) that another plant property, general vigor, has little effect on tolerance. We developed simple models of annual monocarpic plants to determine if a genetic change in components of growth vigor will also change the fitness reaction to damage. We examined the impact of intrinsic growth rate on the tolerance reaction norm slope assuming plants grow geometrically, i.e., without self-limitation. In this case an increase in intrinsic growth rate decreases tolerance (the reaction norm slope becomes more negative). A logistic growth model was used to examine the impact of self-limiting growth on the relationship between intrinsic growth rate and the tolerance reaction norm slope. With self-limitation, the relationship is sensitive to the timing of attack. When attack is early and there is time for regrowth, increasing growth rate increases tolerance (slope becomes less negative). The time limitations imposed by late attack prevent appreciable regrowth and induce a negative relationship between growth rate and tolerance. In neither of these simple cases will the correlation between vigor and tolerance constrain selection on either trait. However, a positive correlation between growth rate and self-limitation will favor fast growth/strong self-limitation in a high-damage environment, but slow growth/weak self-limitation in a low-damage environment. Thus, fundamental growth rules that determine vigor have constitutive effects on tolerance. The net costs and benefits of damage-induced tolerance mechanisms will thus be influenced by the background imposed by fundamental growth rules. This revised version was published online in July 2006 with corrections to the Cover Date.     

Interactions among fungal endophytes,grasses and herbivores

The interaction between two species often depends on the presence or absence of a third species. One widespread three-species interaction involves fungal endophytes infecting grasses and the herbivores that feed upon them. The endophytes are allied with the fungal family Clavicipitaceae and grow systemically in intercellular spaces in above-ground plant tissues including seeds. Like relatedClaviceps species, the endophytes produce a variety of alkaloids that make the host plants toxic or distasteful to herbivores. A large number of grass species are infected, especially cool-season grasses in temperate areas. Field and laboratory studies have shown that herbivores avoid infected plants in choice trials and suffer increased mortality and decreased growth on infected grasses in feeding experiments. Resistance to herbivores may provide a selective advantage to infected plants in competitive interactions with noninfected plants. Recent studies have shown that differential herbivory can reverse competitive hierarchies among plant species. Both endophyte-infected and noninfected tall fescue grass (Festuca arundinacea) are outcompeted by orchardgrass (Dactylis glomerata) in the absence of insect herbivory. However, when herbivores are present infected tall fescue outcompetes orchardgrass. These results suggest that the frequency of infection in grass species and grassland communities will increase over time. Several studies are reviewed illustrating increases in infection frequency within grass populations subject to herbivore pressure. Endophytic fungi may be important regulators of plant-herbivore interactions and so indirectly affect the structure and dynamics of plant communities.     

Molecular analysis of herbivore-induced condensed tannin synthesis: cloning and expression of dihydroflavonol reductase from trembling aspen (Populus tremuloides)

In order to study condensed tannin synthesis and its induction by herbivory, a dihydroflavonol reductase (DFR) cDNA was isolated from trembling aspen (Populus tremuloides). Bacterial overexpression demonstrated that this cDNA encodes a functional DFR enzyme, and Southern analysis revealed that DFR likely is a single-copy gene in the aspen genome. Aspen plants that were mechanically wounded showed a dramatic increase in DFR expression after 24 h in both wounded leaves and unwounded leaves on wounded trees. Feeding by forest tent caterpillar (Malacosoma disstria) and satin moth (Leucoma salicis) larvae, and treatment with methyl jasmonate, all strongly induced DFR expression. DFR enzyme activity was also induced in wounded aspen leaves, and phytochemical assays revealed that condensed tannin concentrations significantly increased in wounded and systemic leaves. The expression of other genes involved in the phenylpropanoid pathway were also induced by wounding. Our findings suggest that the induction of condensed tannins, compounds known to be important for defense against herbivores, is mediated by increased expression of DFR and other phenylpropanoid genes.     

Increased reproductive capacity and physical defense but decreased tannin content in an invasive plant

Abstract Plant invasions create novel plant–insect interactions. The EICA (evolution of increased competitive ability) hypothesis proposes that invasive plants will reallocate resources from defense to growth and/or reproduction because they have escaped from their co‐evolved insect natural enemies. Testing multiple herbivory by monophagous and oligophagous herbivores and simultaneous measurement of various plant traits will provide new insights into the evolutionary change of invasive plants. In this context, we conducted a common garden experiment to compare plant growth and reproduction, chemical and physical defense, and plant responses to herbivory by different types of herbivores between invasive North American populations and native East Asian populations of mile‐a‐minute weed, Persicaria perfoliata. We found that invasive mile‐a‐minute exhibited lower biomass, flowered earlier and had greater reproductive output than plants from the native range. Compared with native populations, plants from invasive populations had lower tannin content, but exhibited higher prickle density on nodes and leaves. Thus our results partially support the EICA hypothesis. When exposed to the monophagous insect, Rhinoncomimus latipes and the oligophagous insects, Gallerucida grisescens and Smaragdina nigrifrons, more damage by herbivory was found on invasive plants than on natives. R. latipes, G. grisescens and S. nigrifrons had strong, moderate and weak impacts on the growth and reproduction of mile‐a‐minute, respectively. The results indicate that mile‐a‐minute may have evolved a higher reproductive capacity in the introduced range, and this along with a lack of oligophagous and monophagous herbivores in the new range may have contributed to its invasiveness in North America.     

Arabidopsis myrosinases TGG1 and TGG2 have redundant function in glucosinolate breakdown and insect defense

In Arabidopsis and other Brassicaceae, the enzyme myrosinase (beta-thioglucoside glucohydrolase, TGG) degrades glucosinolates to produce toxins that deter herbivory. A broadly applicable selection for meiotic recombination between tightly linked T-DNA insertions was developed to generate Arabidopsis tgg1tgg2 double mutants and study myrosinase function. Glucosinolate breakdown in crushed leaves of tgg1 or tgg2 single mutants was comparable to that of wild-type, indicating redundant enzyme function. In contrast, leaf extracts of tgg1tgg2 double mutants had undetectable myrosinase activity in vitro, and damage-induced breakdown of endogenous glucosinolates was apparently absent for aliphatic and greatly slowed for indole glucosinolates. Maturing leaves of myrosinase mutants had significantly increased glucosinolate levels. However, developmental decreases in glucosinolate content during senescence and germination were unaffected, showing that these processes occur independently of TGG1 and TGG2. Insect herbivores with different host plant preferences and feeding styles varied in their responses to myrosinase mutations. Weight gain of two Lepidoptera, the generalist Trichoplusia ni and the facultative Solanaceae-specialist Manduca sexta, was significantly increased on tgg1tgg2 double mutants. Two crucifer-specialist Lepidoptera had differing responses. Whereas Plutella xylostella was unaffected by myrosinase mutations, Pieris rapae performed better on wild-type, perhaps due to reduced feeding stimulants in tgg1tgg2 mutants. Reproduction of two Homoptera, Myzus persicae and Brevicoryne brassicae, was unaffected by myrosinase mutations.     

Direct benefits of genetic mosaicism and intraorganismal selection: modeling coevolution between a long-lived tree and a short-lived herbivore

We model direct fitness benefits of genetic mosaicism for a long-lived tree in coevolution with a short-lived herbivore to test four hypotheses: that mosaicism reduces selection on the herbivore for resistance to plant defenses; that module-level selection allows the individual tree to adapt to its herbivore; and that this benefits the tree population, increasing average tree fitness and reducing local adaptation of the herbivore. We show that: mosaicism does not sufficiently reduce selection for resistance in the herbivore to benefit the tree; that individual trees do benefit from module-level selection when somatic mutation introduces new defenses; and that mosaicism does reduce local adaptation in the herbivore, which increases average tree fitness. These results are robust to varying genetic assumptions of dominance and the somatic mutation rate, but only hold for sufficiently long-lived trees with relatively strong selection. We also show that a mixed reproductive strategy of primarily asexual reproduction interspersed with occasional sexual reproduction is effective in coevolving with the herbivore, as it maintains beneficial allele combinations. Finally, we argue that intraorganismal genetic heterogeneity need not threaten the integrity of the individual and may be adaptive when selection acts concordantly between levels.     

Molecular and genomic basis of volatile-mediated indirect defense against insects in rice

Rice plants fed on by fall armyworm ( Spodoptera frugiperda , FAW) caterpillars emit a blend of volatiles dominated by terpenoids. These volatiles were highly attractive to females of the parasitoid Cotesia marginiventris . Microarray analysis identified 196 rice genes whose expression was significantly upregulated by FAW feeding, 18 of which encode metabolic enzymes potentially involved in volatile biosynthesis. Significant induction of expression of seven of the 11 terpene synthase ( TPS ) genes identified through the microarray experiments was confirmd using real-time RT-PCR. Enzymes encoded by three TPS genes, Os02g02930, Os08g07100 and Os08g04500, were biochemically characterized. Os02g02930 was found to encode a monoterpene synthase producing the single product S- linalool, which is the most abundant volatile emitted from FAW-damaged rice plants. Both Os08g07100 and Os08g04500 were found to encode sesquiterpene synthases, each producing multiple products. These three enzymes are responsible for production of the majority of the terpenes released from FAW-damaged rice plants. In addition to TPS genes, several key genes in the upstream terpenoid pathways were also found to be upregulated by FAW feeding. This paper provides a comprehensive analysis of FAW-induced volatiles and the corresponding volatile biosynthetic genes potentially involved in indirect defense in rice. Evolution of the genetic basis governing volatile terpenoid biosynthesis for indirect defense is discussed.     

Chemical variation within and between individuals of the lichenized ascomycete Tephromela atra

HPLC-analysis was used to determine the concentrations of the lichen compounds alectoronic acid (depsidon), -collatolic acid (depsidon) and atranorin (depsid) in the lichenized ascomycete Tephromela atra (syn. Lecanon atra) (Hudson) Hafeliner from limestone walls on the Baltic island of Öland, Sweden. In 24 individuals of T. atra sampled on a stone wall, the pre-reproductive and reproductive tissue did not differ in the concentrations of alectoronic acid, collatolic acid and atranorin. The concentrations of the three lichen compounds were inter-correlated in the reproductive tissue, but not in the pre-reproductive tissue. Single individuals of T. atra ranged in area covered from 10.1 to 147.4 cm² (mean: 38.5 cm²; N=24); 38.6% of this area was pre-reproductive tissue. However, the concentrations of the three lichen compounds were correlated neither with the total area covered by the lichen nor with the percentage of pre-reproductive tissue. This suggests that the concentrations of the lichen compounds do not change with increasing size (age) of the lichen. Analysis of specimens of T. atra from eight localities revealed a significant variation in lichen compounds (range between localities: alectoronic acid 0.60–3.26 μg/mg lichen dry weight (DW); collatolic acid 2.14–11.59 μg/mg lichen DW; atranorin 0.58–4.16 μg/mg lichen DW). The level of grazing observed in the lichens differed significantly among localities. However, no correlations between the concentrations of the three lichen compounds and the grazing damage to the lichens were found.     

TRANSPORT AND DEFENSIVE ROLE OF ELATOL AT THE SURFACE OF THE RED SEAWEED LAURENCIA OBTUSA (CERAMIALES,RHODOPHYTA)1

Natural within‐thallus concentrations of elatol produced by Laurencia obtusa (Huds.) J. V. Lamour. inhibit herbivory and prevent fouling. However, elatol occurs in larger amounts within the thallus compared with the quantities from the surface of this alga. We evaluated whether the surface elatol concentrations inhibit both herbivory and fouling and whether the content of corps en cerise can be transferred to the external cell walls. Surface elatol concentrations did not inhibit herbivory by sea urchins, settlement of barnacle larvae, or mussel attachment. Evidence of a connection between the corps en cerise, where elatol is probably stored, and the cell wall of L. obtusa was based on channel‐like membranous connections that transport vesicles from the corps to the cell wall region. Therefore, L. obtusa presents a specific process of chemical transport between the cell storage structures and the plant surface. We hypothesized that if high amounts of elatol are capable of inhibiting herbivory and fouling, if the tested organisms are ecologically relevant, and if elatol really occurs on the surface of L. obtusa and this seaweed can transport this compound to its surface, the low natural concentration of defensive chemicals on the surface of L. obtusa is probably not absolute but may be variable according to environmental conditions. We also hypothesized that herbivory and fouling would not exert the same selective force for the production of defensive chemicals on L. obtusa’s surface since the low concentrations of elatol were inefficient to inhibit either processes or distinguish selective pressures.     

Environmental dependency in the expression of costs of tolerance to deer herbivory

Plant tolerance to natural enemy damage is a defense strategy that minimizes the effects of damage on fitness. Despite the apparent benefits of tolerance, many populations exhibit intermediate levels of tolerance, indicating that constraints on the evolution of tolerance are likely. In a field experiment with the ivyleaf morning glory, costs of tolerance to deer herbivory in the form of negative genetic correlations between deer tolerance and fitness in the absence of damage were detected. However, these costs were detected only in the presence of insect herbivores. Such environmental dependency in the expression of costs of tolerance may facilitate the maintenance of tolerance at intermediate levels.     

Holey Aroids: Circular Trenching Behavior by a Leaf Beetle in Vietnam

The leaf beetle Aplosonyx ancora cuts circular trenches on the underside of leaves of their aroid host plants before feeding. Latex is exuded from these cuts and the beetles feed intermittently on these isolated tissues, apparently avoiding the latex. Circular feeding holes occur only in Araceae in which latex is contained in cells or vessels with cells bridging adjacent files ("anastomosing laticifers"). The phylogeny of Araceae and the restricted host records suggest a coevolutionary arms race and parallel phylogenesis between Aplosonyx and its aroid hosts.     

Metal accumulation and its effect on leaf herbivory in an allopolyploid species Arabidopsis kamchatica inherited from a diploid hyperaccumulator A. halleri

Excessive amounts of metal ions in soil are toxic for most plant species, yet metal can also facilitate plant survival by elemental defense against herbivores and pathogens. Zinc and cadmium hyperaccumulation in Arabidopsis halleri is known to be effective for the defense against natural enemies. The allotetraploid species A. kamchatica, derived from A. halleri and a non-hyperaccumulator A. lyrata, has a lower hyperaccumulation level of zinc than A. halleri, but its significance for elemental defense remains unknown. In this study, we evaluated the accumulation levels of zinc and cadmium in the allotetraploid compared with its diploid progenitors, and evaluated the contribution of metal treatments to anti-herbivore resistance under field conditions. The accumulation level of zinc in A. kamchatica was intermediate between the progenitors, but that of cadmium was lower than in both diploid progenitors. The elemental defense of A. kamchatica and A. halleri was supported by a field experiment comparing the herbivory level between a control group and metal-supplemented plants. Moreover, the effect of elemental defense was lower in A. kamchatica than in the hyperaccumulator progenitor A. halleri, which is consistent with the metal accumulation level. This result reveals that the allotetraploid plant inherited its hyperaccumulating ability from one progenitor as an advantageous trait but at an intermediate level.     

Nonglandular silicified trichomes are essential for rice defense against chewing herbivores

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

CHEMICAL DEFENSE AGAINST HERBIVORY IN THE ANTARCTIC MARINE MACROALGAE IRIDAEA CORDATA AND PHYLLOPHORA ANTARCTICA (RHODOPHYCEAE)

Iridaea cordata (Turner) Bory and Phyllophora antarctica A. et E. S. Gepp (Gigartinales, Rhodophyceae) are common in many high-latitude, shallow benthic marine communities in Antarctica, but previous observations have indicated little or no exploitation by potential herbivores. We have measured retention of test disks over the mouths of the common Antarctic sea urchin Sterechinus neumayeri Meissner, and we have used this assay to examine potential chemical defenses in I. cordata and P. antarctica. Thallus disks of both macroalgal species were retained by the urchins for significantly shorter times than inert filter paper disks and much shorter times than paper disks with a feeding stimulant. Both nonpolar and polar extracts of each macroalgal species added to disks with a feeding stimulant significantly decreased retention times relative to controls. These results support the hypothesis that chemical defenses in I. cordata and P. antarctica play a role in deterring potential herbivores.     

Partly transparent young legume pods: Do they mimic caterpillars for defense and simultaneously enable better photosynthesis?

Being partly or fully transparent as a defense from predation is mostly known in various groups of aquatic animals and various terrestrial arthropods. Plants, being photosynthetic and having cell walls made of various polymers, cannot be wholly transparent. In spite of these inherent limitations, some succulent plant species of arid zones have partially transparent “windows” in order to perform photosynthesis in their below-ground leaves, as defense from herbivores as well as for protection from harsh environmental conditions. Similarly, transparent “windows” or even wholly transparent leaves are found in certain thick or thin, above-ground organs irrespective of aridity. The young pods of various wild annual Mediterranean legume species belonging to the genera Lathyrus, Pisum and Vicia are partly transparent and may therefore look like caterpillars when viewed with back illumination. I propose that this character serves 2 functions: (1) being a type of defensive caterpillar mimicry that may reduce their consumption by various herbivores in that very sensitive stage, and (2) simultaneously allowing better photosynthesis in the rapidly growing seeds and pods. Unlike animals that are transparent for either defensive or aggressive crypsis, in the case of young legume pods it allows them to visually mimic caterpillars for defense.