Asymmetric effects of a leaf‐chewing herbivore on aphid population growth

1. Plant responses to herbivory are often specific to the feeding guild of the attacking herbivore. These phytochemical responses to herbivore damage can affect herbivore performance and activity. Comprehensive studies on the ecological consequences of multi‐herbivore plant interactions are key to understanding plant–herbivore community dynamics. 2. This study examined how feeding damage by co‐occurring herbivores from separate feeding guilds, Myzus persicae (Sulzer), a sucking herbivore, and Leptinotarsa decemlineata (Say), a chewing herbivore, alter plant chemistry and indirectly affect herbivore performance. Performance was measured when each insect fed on plants individually, sequentially, or simultaneously in laboratory and field experiments. Phytohormone and glycoalkaloid content were measured for each feeding sequence to evaluate plant responses to herbivory by each guild. Mid‐season and end‐of‐season tuber yield were evaluated in the field study. 3. Damage by L. decemlineata negatively impacted M. persicae performance in both laboratory and field settings. Damage by M. persicae did not affect L. decemlineata performance in laboratory assays. However, L. decemlineata performance was positively affected by M. persicae herbivory in the field, but this effect was temporary. Although phytohormones and plant defences varied across treatments, they provide little resolution on interaction outcomes. 4. These results confirm that the presence of multiple feeding guilds on a single plant can affect these chewing and sucking herbivores differentially, but given the variability in our phytochemical analyses compared with other studies, the mechanism remains unclear. The study's findings show that aphids are negatively affected by chewing herbivores across systems, while aphids temporarily affected beetles positively.     

The role of the octadecanoid pathway in the production of terpenoid indole alkaloids in Catharanthus roseus hairy roots under normal and UV‐B stress conditions

The octadecanoid pathway is responsible for producing jasmonic acid an important signaling molecule in plants, which controls the production of a variety of secondary metabolites. Previously the exogenous addition of jasmonic acid to Catharanthus roseus hairy roots caused an increase in terpenoid indole alkaloid (TIA) accumulation. The role of the endogenous production of jasmonic acid by the octadecanoid pathway in the production of TIAs in C. roseus hairy roots is examined. Feeding of octadecanoid pathway inhibitors suggests that the octadecanoid pathway does not actively control TIA production under normal growth conditions or during the UV‐B stress response in C. roseus hairy roots. Biotechnol. Bioeng. 2009;103: 1248–1254. © 2009 Wiley Periodicals, Inc.     

Anthropogenic increase in carbon dioxide modifies plant–insect interactions

Industrialisation has elevated atmospheric levels of CO₂ from original 280 ppm to current levels at 400 ppm, which is estimated to double by 2050. Although high atmospheric CO₂ levels affect insect interactions with host plants, the impact of global change on plant defences in response to insect attack is not completely understood. Recent studies have made advances in elucidating the mechanisms of the effects of high CO₂ levels in plant–insect interactions. New studies have proposed that gene regulation and phytohormones regulate resource allocation from photosynthesis to plant defences against insects. Biochemical and molecular studies demonstrated that both defensive hormones jasmonic acid (JA) and ethylene (ET) participate in modulating chemical defences against herbivores in plants grown under elevated CO₂ atmosphere rather than changes in C:N ratio. High atmospheric CO₂ levels increase vulnerability to insect damage by down‐regulating both inducive and constitutive chemical defences regulated by JA and ET. However, elevated CO₂ levels increase the JA antagonistic hormone salicylic acid that increases other chemical defences. How plants grown under elevated CO₂ environment allocate primary metabolites from photosynthesis to secondary metabolism would help to understand innate defences and prevent future herbivory in field crops. We present evidence demonstrating that changes in chemical defences in plants grown under elevated CO₂ environment are hormonal regulated and reject the C:N hypothesis. In addition, we discuss current knowledge of the mechanisms that regulate plants defences against insects in elevated CO₂ atmospheres.     

Plant‐mediated species networks: the modulating role of herbivore density

1. When herbivores of distinct feeding guilds, such as phloem feeders and leaf chewers, interact, the outcome of these interactions often shows facilitation. However, whether this facilitation turns into competition at stronger herbivory pressure remains unknown. 2. Using an integrative approach that links ecological processes (behavioural choices of insects) with physiological plant mechanisms (nutrient and phytohormone levels) for the wild crucifer Brassica nigra (L.) Koch., this study evaluates preferences of leaf chewers for plants previously infested with several densities of the specialist aphid Brevicoryne brassicae L. (Hemiptera, Aphididae). As leaf chewers, four species of caterpillars (Lepidoptera) were selected that differ in their degree of specialisation in crucifers. 3. These results show that, whereas at low and medium aphid densities caterpillars displayed a preference for aphid‐infested plants or no preference, at high aphid infestation density, all four species of caterpillar preferred uninfested plants, with a significant difference for Pieris rapae and Mamestra brassicae. 4. In contrast to our expectation, the consistent preference for uninfested plants at a high aphid density could not be associated with a decrease in plant nutrition. However, while jasmonate concentrations [i.e. 12‐oxo‐phytodienoic acid and jasmonic acid (JA)] at medium aphid‐density infestation decreased compared with low levels of infestation, at high infestation level, the jasmonates JA as well as JA conjugated with the amino acid isoleucine were present at higher levels compared with low‐infestation treatments. 5. This work provides evidence that positive interactions observed in herbivore communities can be transient, leading to negative interactions mediated by changes in plant defences rather than in plant nutrition.     

The Elongator complex‐associated protein DRL1 plays a positive role in immune responses against necrotrophic fungal pathogens in Arabidopsis

DEFORMED ROOT AND LEAVES1 (DRL1) is an Arabidopsis homologue of the yeast TOXIN TARGET4 (TOT4)/KILLER TOXIN‐INSENSITIVE12 (KTI12) protein that is physically associated with the RNA polymerase II‐interacting protein complex named Elongator. Mutations in DRL1 and Elongator lead to similar morphological and molecular phenotypes, suggesting that DRL1 and Elongator may functionally overlap in Arabidopsis. We have shown previously that Elongator plays an important role in both salicylic acid (SA)‐ and jasmonic acid (JA)/ethylene (ET)‐mediated defence responses. Here, we tested whether DRL1 also plays a similar role as Elongator in plant immune responses. Our results show that, although DRL1 partially contributes to SA‐induced cytotoxicity, it does not play a significant role in SA‐mediated expression of PATHOGENESIS‐RELATED genes and resistance to the virulent bacterial pathogen Pseudomonas syringae pv. maculicola ES4326. In contrast, DRL1 is required for JA/ET‐ and necrotrophic fungal pathogen Botrytis cinerea‐induced defence gene expression and for resistance to B. cinerea and Alternaria brassicicola. Furthermore, unlike the TOT4/KTI12 gene which, when overexpressed in yeast, confers zymocin resistance, a phenotype of the tot4/kti12 mutant, overexpression of DRL1 does not change B. cinerea‐induced defence gene expression and resistance to this pathogen. Finally, DRL1 contains an N‐terminal P‐loop and a C‐terminal calmodulin (CaM)‐binding domain and is a CaM‐binding protein. We demonstrate that both the P‐loop and the CaM‐binding domain are essential for the function of DRL1 in B. cinerea‐induced expression of PDF1.2 and ORA59, and in resistance to B. cinerea, suggesting that the function of DRL1 in plant immunity may be regulated by ATP/GTP and CaM binding.     

UVB radiation and 17‐hydroxygeranyllinalool diterpene glycosides provide durable resistance against mirid (Tupiocoris notatus) attack in field‐grown Nicotiana attenuata plants

Depending on geographical location, plants are exposed to variable amounts of UVB radiation and herbivore attack. Because the role(s) of UVB in the priming and/or accumulation of plant defence metabolites against herbivores are not well understood, we used field‐grown Nicotiana attenuata plants to explore the effects of UVB on herbivore performance. Consistent with previous reports, UVB‐exposed plants accumulated higher levels of ultraviolet (UV)‐absorbing compounds (rutin, chlorogenic acid, crypto‐chlorogenic acid and dicaffeoylspermidine). Furthermore, UVB increased the accumulation of jasmonic acid, jasmonoyl‐L‐isoleucine and abscisic acid, all phytohormones which regulate plant defence against biotic and abiotic stress. In herbivore bioassays, N. attenuata plants experimentally protected from UVB were more infested by mirids in three consecutive field seasons. Among defence metabolites measured, 17‐hydroxygeranyllinalool diterpene glycosides (HGL‐DTGs) showed strongly altered accumulation patterns. While constitutive HGL‐DTGs levels were higher under UVB, N. attenuata plants exposed to mirid bugs (Tupiocoris notatus) had still more HGL‐DTGs under UVB, and mirids preferred to feed on HGL‐DTGs‐silenced plants when other UVB protecting factors were eliminated by UVB filters. We conclude that UVB exposure not only stimulates UV protective screens but also affects plant defence mechanisms, such as HGL‐DTGs accumulation, and modulates ecological interactions of N. attenuata with its herbivores in nature.     

Bidirectional plant‐mediated interactions between rhizobacteria and shoot‐feeding herbivorous insects: a community ecology perspective

1. Plants interact with various organisms, aboveground as well as belowground. Such interactions result in changes in plant traits with consequences for members of the plant‐associated community at different trophic levels. Research thus far focussed on interactions of plants with individual species. However, studying such interactions in a community context is needed to gain a better understanding.
2. Members of the aboveground insect community induce defences that systemically influence plant interactions with herbivorous as well as carnivorous insects. Plant roots are associated with a community of plant‐growth promoting rhizobacteria (PGPR). This PGPR community modulates insect‐induced defences of plants. Thus, PGPR and insects interact indirectly via plant‐mediated interactions.
3. Such plant‐mediated interactions between belowground PGPR and aboveground insects have usually been addressed unidirectionally from belowground to aboveground. Here, we take a bidirectional approach to these cross‐compartment plant‐mediated interactions.
4. Recent studies show that upon aboveground attack by insect herbivores, plants may recruit rhizobacteria that enhance plant defence against the attackers. This rearranging of the PGPR community in the rhizosphere has consequences for members of the aboveground insect community. This review focusses on the bidirectional nature of plant‐mediated interactions between the PGPR and insect communities associated with plants, including (a) effects of beneficial rhizobacteria via modification of plant defence traits on insects and (b) effects of plant defence against insects on the PGPR community in the rhizosphere. We discuss how such knowledge can be used in the development of sustainable crop‐protection strategies.

     

Mechanisms of optimal defense patterns in Nicotiana attenuata: flowering attenuates herbivory-elicited ethylene and jasmonate signaling

To defend themselves against herbivore attack, plants produce secondary metabolites, which are variously inducible and constitutively deployed, presumably to optimize their fitness benefits in light of their fitness costs. Three phytohormones, jasmonates (JA) and their active forms, the JA-isoleucine (JA-Ile) and ethylene (ET), are known to play central roles in the elicitation of induced defenses, but little is known about how this mediation changes over ontogeny. The Optimal Defense Theory (ODT) predicts changes in the costs and benefits of the different types of defenses and has been usefully extrapolated to their modes of deployment. Here we studied whether the herbivore-induced accumulation of JA, JA-Ile and ET changed over ontogeny in Nicotiana attenuata, a native tobacco in which inducible defenses are particularly well studied. Herbivore-elicited ET production changed dramatically during six developmental stages, from rosette through flowering, decreasing with the elongation of the first corollas during flower development. This decrease was largely recovered within a day after flower removal by decapitation. A similar pattern was found for the herbivore-induced accumulation of JA and JA-Ile. These results are consistent with ODT predictions and suggest that the last steps in floral development control the inducibility of at least three plant hormones, optimizing defense-growth tradeoffs.     

Integration and scaling of UV‐B radiation effects on plants: from molecular interactions to whole plant responses

A process based model integrating the effects of UV‐B radiation to molecular level processes and their consequences to whole plant growth and development was developed from key parameters in the published literature. Model simulations showed that UV‐B radiation induced changes in plant metabolic and/or photosynthesis rates can result in plant growth inhibitions. The costs of effective epidermal UV‐B radiation absorptive compounds did not result in any significant changes in plant growth, but any associated metabolic costs effectively reduced the potential plant biomass. The model showed significant interactions between UV‐B radiation effects and temperature and any factor leading to inhibition of photosynthetic production or plant growth during the midday, but the effects were not cumulative for all factors. Vegetative growth were significantly delayed in species that do not exhibit reproductive cycles during a growing season, but vegetative growth and reproductive yield in species completing their life cycle in one growing season did not appear to be delayed more than 2–5 days, probably within the natural variability of the life cycles for many species. This is the first model to integrate the effects of increased UV‐B radiation through molecular level processes and their consequences to whole plant growth and development.     

Effect of UV‐B radiation on the content of UV‐B absorbing compounds and photosynthetic parameters in Parmotrema austrosinense from two contrasting habitats

• We studied the resistance of Parmotrema austrosinense to UV‐B stress. We focused on the effects of a high dose UV‐B radiation on the content of chlorophylls, carotenoids and UV‐B screening compounds.
• Photosynthetic parameters were measured by chlorophyll fluorescence (potential and effective quantum yields, photochemical and non‐photochemical quenching) and evaluated in control and UV‐B‐treated lichens. Lichens from two different locations in Cordoba, Argentina, were selected: (i) high altitude and dry plots at (Los Gigantes) and (ii) lowland high salinity plots (Salinas Grandes).
• UV‐B treatment led to a decrease in the content of photosynthetic pigments and UV‐B screens (absorbance decrease in 220–350 nm) in the samples from Salinas Grandes, while in Los Gigantes samples, an increase in UV‐B screen content was observed. Chlorophyll fluorescence parameters showed a UV‐B‐induced decline in F_V/F_M, Φ_PSII and qP indicating limitation of primary photosynthetic processes in photosystem II (PSII) of symbiotic alga, more pronounced in Salinas Grandes samples. Protective mechanism of PSII were activated by the UV‐B treatment to a higher extent in samples from Salinas Grandes (NPQ 0.48) than in Los Gigantes samples (NPQ 0.26).
• We concluded that site‐related characteristics, and in particular different UV‐B radiation regimen, had a strong effect on resistance of the photosynthetic apparatus of P. austrosinense to UV‐B radiation.

     

The effects of drought and herbivory on plant–herbivore interactions across 16 soybean genotypes in a field experiment

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Jasmonic acid carboxyl methyltransferase regulates development and herbivory‐induced defense response in rice

Jasmonic acid(JA) and related metabolites play a key role in plant defense and growth. JA carboxyl methyltransferase(JMT) may be involved in plant defense and development by methylating JA to methyl jasmonate(Me JA) and thus influencing the concentrations of JA and related metabolites. However, no JMT gene has been well characterized in monocotyledon defense and development at the molecular level. After we cloned a rice JMT gene,Os JMT1, whose encoding protein was localized in the cytosol, we found that the recombinant Os JMT1 protein catalyzed JA to Me JA. Os JMT1 is up-regulated in response to infestation with the brown planthopper(BPH; Nilaparvata lugens). Plants in which Os JMT1 had been overexpressed(oeJMT plants) showed reduced height and yield. These oe-JMT plants also exhibited increased Me JA levels but reduced levels of herbivore-induced JA and jasmonoyl-isoleucine(JAIle). The oe-JMT plants were more attractive to BPH female adults but showed increased resistance to BPH nymphs,probably owing to the different responses of BPH female adults and nymphs to the changes in levels of H_2O_2 and Me JA in oe-JMT plants. These results indicate that Os JMT1,by altering levels of JA and related metabolites, plays a role in regulating plant development and herbivore-induced defense responses in rice.     

Different mechanisms of Trichoderma virens‐mediated resistance in tomato against Fusarium wilt involve the jasmonic and salicylic acid pathways

In the present study, we investigated the role of Trichoderma virens (TriV_JSB100) spores or cell‐free culture filtrate in the regulation of growth and activation of the defence responses of tomato (Solanum lycopersicum) plants against Fusarium oxysporum f. sp. lycopersici by the development of a biocontrol–plant–pathogen interaction system. Two‐week‐old tomato seedlings primed with TriV_JSB100 spores cultured on barley grains (BGS) or with cell‐free culture filtrate (CF) were inoculated with Fusarium pathogen under glasshouse conditions; this resulted in significantly lower disease incidence in tomato Oogata‐Fukuju plants treated with BGS than in those treated with CF. To dissect the pathways associated with this response, jasmonic acid (JA) and salicylic acid (SA) signalling in BGS‐ and CF‐induced resistance was evaluated using JA‐ and SA‐impaired tomato lines. We observed that JA‐deficient mutant def1 plants were susceptible to Fusarium pathogen when they were treated with BGS. However, wild‐type (WT) BGS‐treated tomato plants showed a higher JA level and significantly lower disease incidence. SA‐deficient mutant NahG plants treated with CF were also found to be susceptible to Fusarium pathogen and displayed low SA levels, whereas WT CF‐treated tomato plants exhibited moderately lower disease levels and substantially higher SA levels. Expression of the JA‐responsive defensin gene PDF1 was induced in WT tomato plants treated with BGS, whereas the SA‐inducible pathogenesis‐related protein 1 acidic (PR1a) gene was up‐regulated in WT tomato plants treated with CF. These results suggest that TriV_JSB100 BGS and CF differentially induce JA and SA signalling cascades for the elicitation of Fusarium oxysporum resistance in tomato.     

Ultraviolet‐C priming of strawberry leaves against subsequent Mycosphaerella fragariae infection involves the action of reactive oxygen species,plant hormones,and terpenes

Ultraviolet‐C (UV‐C) radiation has been reported to induce defence responses to pathogens in growing crops and described as a new environmentally friendly method for disease control. However, whether the effect of the induced defence mechanisms will persist after the stress imposed by UV‐C is alleviated and how these mechanisms interact with pathogen elicitors upon infection have not yet been investigated. Thus, we inoculated strawberry plants with Mycosphaerella fragariae, the causal agent of leaf spot disease, after 5 weeks of repeated UV‐C irradiation treatment (cumulative dose of 10.2 kJ m^?2) and investigated the alteration of gene expression and biochemical phenotypes. The results revealed that UV‐C treatment had a significant impact on gene expression in strawberry leaves and led to the overexpression of a set of genes involved in plant–pathogen interaction. UV‐C‐treated leaves displayed a stronger response to infection after inoculation, with reduced symptoms and increases in accumulation of total phenolics and volatile terpenes, higher expression of pathogenesis‐related proteins and the activity of several defence enzymes. This study presumptively describe, for the first time, the involvement of terpenes, reactive oxygen species, and abscisic acid, salicylic acid, jasmonic acid, and their transduction factors, in the network underpinning UV‐C priming of growing crops for improved protection against pathogens.     

ATR and MKP1 play distinct roles in response to UV‐B stress in Arabidopsis

Ultraviolet‐B (UV‐B) stress activates MAP kinases (MAPKs) MPK3 and MPK6 in Arabidopsis. MAPK activity must be tightly controlled in order to ensure an appropriate cellular outcome. MAPK phosphatases (MKPs) effectively control MAPKs by dephosphorylation of phosphothreonine and phosphotyrosine in their activation loops. Arabidopsis MKP1 is an important regulator of MPK3 and MPK6, and mkp1 knockout mutants are hypersensitive to UV‐B stress, which is associated with reduced inactivation of MPK3 and MPK6. Here, we demonstrate that MPK3 and MPK6 are hyperactivated in response to UV‐B in plants that are deficient in photorepair, suggesting that UV‐damaged DNA is a trigger of MAPK signaling. This is not due to a block in replication, as, in contrast to atr, the mkp1 mutant is not hypersensitive to the replication‐inhibiting drug hydroxyurea, hydroxyurea does not activate MPK3 and MPK6, and atr is not impaired in MPK3 and MPK6 activation in response to UV‐B. We further show that mkp1 leaves and roots are UV‐B hypersensitive, whereas atr is mainly affected at the root level. Tolerance to UV‐B stress has been previously associated with stem cell removal and CYCB1;1 accumulation. Although UV‐B‐induced stem cell death and CYCB1;1 expression are not altered in mkp1 roots, CYCB1;1 expression is reduced in mkp1 leaves. We conclude that the MKP1 and ATR pathways operate in parallel, with primary roles for ATR in roots and MKP1 in leaves.     

An incoherent feed‐forward loop mediates robustness and tunability in a plant immune network

Immune signaling networks must be tunable to alleviate fitness costs associated with immunity and, at the same time, robust against pathogen interferences. How these properties mechanistically emerge in plant immune signaling networks is poorly understood. Here, we discovered a molecular mechanism by which the model plant species Arabidopsis thaliana achieves robust and tunable immunity triggered by the microbe‐associated molecular pattern, flg22. Salicylic acid (SA) is a major plant immune signal molecule. Another signal molecule jasmonate (JA) induced expression of a gene essential for SA accumulation, EDS5. Paradoxically, JA inhibited expression of PAD4, a positive regulator of EDS5 expression. This incoherent type‐4 feed‐forward loop (I4‐FFL) enabled JA to mitigate SA accumulation in the intact network but to support it under perturbation of PAD4, thereby minimizing the negative impact of SA on fitness as well as conferring robust SA‐mediated immunity. We also present evidence for evolutionary conservation of these gene regulations in the family Brassicaceae. Our results highlight an I4‐FFL that simultaneously provides the immune network with robustness and tunability in A. thaliana and possibly in its relatives.     

Integration of two herbivore‐induced plant volatiles results in synergistic effects on plant defence and resistance

Plants can use induced volatiles to detect herbivore‐ and pathogen‐attacked neighbors and prime their defenses. Several individual volatile priming cues have been identified, but whether plants are able to integrate multiple cues from stress‐related volatile blends remains poorly understood. Here, we investigated how maize plants respond to two herbivore‐induced volatile priming cues with complementary information content, the green leaf volatile (Z)‐3‐hexenyl acetate (HAC) and the aromatic volatile indole. In the absence of herbivory, HAC directly induced defence gene expression, whereas indole had no effect. Upon induction by simulated herbivory, both volatiles increased jasmonate signalling, defence gene expression, and defensive secondary metabolite production and increased plant resistance. Plant resistance to caterpillars was more strongly induced in dual volatile‐exposed plants than plants exposed to single volatiles.. Induced defence levels in dual volatile‐exposed plants were significantly higher than predicted from the added effects of the individual volatiles, with the exception of induced plant volatile production, which showed no increase upon dual‐exposure relative to single exposure. Thus, plants can integrate different volatile cues into strong and specific responses that promote herbivore defence induction and resistance. Integrating multiple volatiles may be beneficial, as volatile blends are more reliable indicators of future stress than single cues.