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.     

Root growth dynamics of Nicotiana attenuata seedlings are affected by simulated herbivore attack

Many studies demonstrate resource-based trade-offs between growth and defence on a large timescale. Yet, the short-term dynamics of this growth reaction are still completely unclear, making it difficult to explain growth-defence trade-offs mechanistically. In this study, image-based non-destructive methods were used to quantify root growth reactions happening within hours following simulated herbivore attack. The induction of wound reactions in Nicotiana attenuata in the seedling stage led to transiently decreased root growth rates. Application of the oral secretion of the specialist herbivore Manduca sexta to the leaves led to a transient decrease in root growth that was more pronounced than if a mere mechanical wounding was imposed. Root growth reduction was more pronounced than leaf growth reduction. When fatty acid-amino acid conjugates (FACs) were applied to wounds, root growth reduction occurred in the same intensity as when oral secretion was applied. Timing of the transient growth reduction coincided with endogenous bursts of jasmonate (JA) and ethylene emissions reported in literature. Simulation of a wound response by applying methyl jasmonate (MeJA) led to more prolonged negative effects on root growth. Increased nicotine concentrations, trichome lengths and densities were observed within 72 h in seedlings that were treated with MeJA or that were mechanically wounded. Overall, these reactions indicate that even in a very early developmental stage, the diversion of plant metabolism from primary (growth-sustaining) to secondary (defence-related) metabolism can cause profound alterations of plant growth performance.     

Induced responses in Nicotiana attenuata affect behavior and growth of the specialist herbivore Manduca sexta

Many plants employ induced responses against generalist herbivores. Specialist herbivores, however, may employ several mechanisms to overcome the negative effects of induced plant defenses. Here we test how the behavior and development of specialist Manduca sexta larvae are affected by induced responses in their natural host plant Nicotiana attenuata. On a spatial scale relevant to both the plant and the herbivore, we first determined how methyl jasmonate (MeJA)-induced responses, such as increased nicotine production, affect the tendency of larvae to leave induced plants. When larvae were allowed to move between two plants planted in one pot, they left an MeJA-treated plant faster than a control plant. When both plants in the pot were MeJA-treated, the larvae developed more slowly than when both plants were uninduced, or when the larvae had the opportunity to move to an uninduced neighbor. The sooner larvae moved from an MeJA-treated plant to an untreated neighbor, the larger the body mass they attained. This demonstrates that M. sexta larvae can compensate behaviorally for the deleterious effects of induced plant responses. These effects were observed in plants grown under both low and high N supply rates, though the effects were more pronounced under high N. To examine the consequences of the timing and the direction of the host plant switching behavior for larval development, neonate larvae were fed leaves excised from induced and uninduced plants. Larvae confined to MeJA-treated leaves had higher mortality rates and grew slower than larvae fed only control leaves. This demonstrates that MeJA-induced responses decrease growth and development of specialist herbivores that do not have the behavioral option of moving to an uninduced plant. The sooner the larvae were switched to MeJA-treated leaves, the slower their development compared to larvae fed only uninduced leaves. In contrast, the sooner larvae fed MeJA-treated leaves were switched to control leaves, the faster they developed. Again the effects of MeJA treatment were stronger in plants grown under high N supply. We propose that induced plants growing in close competition with an uninduced conspecific may offset the fitness costs of these induced responses and perhaps obtain a fitness benefit by motivating herbivores to move to their neighboring competitors. Received: 25 March 1999 / Accepted: 8 October 1999     

Elm leaves ‘warned’ by insect egg deposition reduce survival of hatching larvae by a shift in their quantitative leaf metabolite pattern

Plants may take insect eggs on their leaves as a warning of future herbivory and intensify their defence against feeding larvae. Responsible agents are, however, largely unknown, and little knowledge is available on this phenomenon in perennial plants. We investigated how egg deposition affects the anti‐herbivore defence of elm against the multivoltine elm leaf beetle. Prior egg deposition caused changes in the quality of feeding‐damaged leaves that resulted in increased larval mortality and reduced reproductive capacity of the herbivore by harming especially female larvae. Chemical analyses of primary and secondary leaf metabolites in feeding‐damaged, egg‐free (F) and feeding‐damaged, egg‐deposited (EF)‐leaves revealed only small differences in concentrations when comparing metabolites singly. However, a pattern‐focused analysis showed clearly separable patterns of (F) and (EF)‐leaves because of concentration differences in especially nitrogen and phenolics, of which robinin was consumed in greater amounts by larvae on (EF) than on (F)‐leaves. Our study shows that insect egg deposition mediates a shift in the quantitative nutritional pattern of feeding‐damaged leaves, and thus might limit the herbivore's population growth by reducing the number of especially female herbivores. This may be a strategy that pays off in a long run particularly in perennial plants against multivoltine herbivores.     

Comparing the preferences of three herbivore species with resistance traits of 15 perennial dicots: the effects of phylogenetic constraints

Differences in palatability between 15 perennial dicotyledonous herbaceous plant species were investigated in a multiple choice test, involving three generalist herbivores. Palatability was compared with two categories of plant traits: defence characteristics and growth properties. On theoretical grounds, we expected a positive relationship between growth rate and palatability, and a negative relationship between palatability and defence traits. The possible effect of phylogeny on the outcome of the comparisons was investigated by analysing the data using phylogenetically independent contrasts. The three herbivores showed remarkably similar preferences, which indicates that the results of the choice experiment are a good representation of leaf palatability. The significant negative correlations found in a direct comparison between herbivore preference and relative growth rate, and between herbivore preference and lignin and dry matter content, did not hold after phylogenetic correction. On the other hand, one relationship emerged only when comparing phylogenetically independent contrasts: contrary to expectation, a negative relation was noted between juvenile growth rate and plant palatability. A possible explanation for the contradictory nature of this result is the uniformly ready availability of resources in our experiment.     

Trichomes of the seed fern Blanzyopteris praedentata: implications for plant–insect interactions in the Late Carboniferous

The fronds and compound tendrils of the Stephanian (Late Carboniferous) seed fern Blanzyopteris praedentata possess several types of trichomes, two of which may, based on their morphology, have functioned as deterrents against herbivores. Bands of upwardly curved trichomes, occurring on the adaxial surfaces of tendrils, frond- and pinna rachides, are also known from extant plants, where they create mechanical obstacles. Other trichomes that are glandular occur on most parts of the foliage and tendrils and represent a different form of defence mechanism. These trichomes apparently possessed a touch-sensitive mechanism that opened the secretory cell when touched. They are interpreted as functionally similar to the so-called 'explosive' trichomes of certain extant Cucurbitaceae and Solanaceae. Studies of living Oleander aphids ( Aphis nerii ) on Sicana odorifera (Cucurbitaceae) demonstrate the effectiveness of the physical component of this defence. When touched and ruptured by an aphid, the trichomes of S. odorifera rapidly release a sticky exudate, which adheres to the animal's legs; the accumulation of exudate on the legs eventually impedes the aphid. Based on these studies, hypotheses are presented on the types of animals that might have been deterred by the glandular trichomes of B. praedentata in the Late Carboniferous.  © 2003 The Linnean Society of London, Botanical Journal of the Linnean Society , 2003, 141 , 133–149.     

Alternative seed defence mechanisms in a palo verde (Fabaceae) hybrid zone: effects on bruchid beetle abundance

Abstract.

• 1 We asked three questions about the patterns of relative abundance of insect herbivores across host plant taxa at a palo verde hybrid zone. (1) What is the morphological structure of the hybrid zone and does this suggest a certain pattern of introgression? (2) How are putative parental seed defence mechanisms expressed in hybrid plants? (3) Do ovipositing females prefer host plant taxa on which their offspring have best survivorship?
• 2 Morphologically, hybrids were either intermediate or tended to resemble one parental species. Previous studies have suggested that unidirectional introgression results in loss of parental defence mechanisms against herbivores. Hybrid plants in general lacked seed coat resistance and early pod abscission which are known to act as plant defence mechanisms against bruchid beetles in the parental palo verde trees.
• 3 All other sources of bruchid mortality that we examined did not vary across parental and hybrid taxa, with the possible exception of egg parasitism which occurred at a lower frequency on one parental palo verde species.
• 4 Thus, survivorship of bruchid offspring should be greater on hybrid palo verdes.
• 5 Patterns of egg densities suggested that females may prefer hybrid hosts in some years but not others. An oviposition choice experiment conducted in the field, however, showed bruchids have no preference for hybrids over one of the parental species.
• 6 These results suggest that some insect herbivores may have higher densities on hybrid host plants because they are less resistant.

     

Genetic variation in herbivore resistance and tolerance: the role of plant life‐history stage and type of damage

Information of the patterns of genetic variation in plant resistance and tolerance against herbivores and genetic trade‐offs between these two defence strategies is central for our understanding of the evolution of plant defence. We found genetic variation in resistance to two specialist herbivores and in tolerance to artificial damage but not to a specialist leaf herbivore in a long‐lived perennial herb. Seedlings tended to have genetic variation in tolerance to artificial damage. Genetic variation in tolerance of adult plants to artificial damage was not consistent in time. Our results suggest that the level of genetic variation in tolerance and resistance depends on plant life‐history stage, type of damage and timing of estimating the tolerance relative to the occurrence of the damage, which might reflect the pattern of selection imposed by herbivory. Furthermore, we found no trade‐offs between resistance and tolerance, which suggests that the two defence strategies can evolve independently.     

Interaction between ants, extrafloral nectaries and insect herbivores in Neotropical coastal sand dunes: herbivore deterrence by visiting ants increases fruit set in Opuntia stricta (Cactaceae)

1. This study examines the anti-herbivore effect of ants visiting the extrafloral nectaries (EFNs) of Opuntia stricta (Cactaceae) and its possible influence on the plant's reproductive output in Mexican coastal sand dunes. Opuntia 's EFNs are located in the areoles of the developing tissue of emerging cladodes and flower buds.
2. Ants visited the EFNs of O . stricta on a round-the-clock basis. The associated ant assemblage was formed by nine species distributed in four subfamilies, and the species composition of the principal ant visitors changed markedly from day to night period.
3. Cladodes of control (ants present) and treatment (ants excluded) plants of Opuntia were equally infested by sucking bugs and mining dipterans. Damage to buds by a pyralid moth, however, was significantly higher on treatment than on control plants. Ant visitation to Opuntia 's EFNs translated into a 50% increase in the plant's reproductive output, as expressed by the number of fruits produced by experimental control and treatment branches. Moreover, fruit production by ant-visited branches was positively and significantly associated with the mean monthly rate of ant visitation to EFNs.
4. This is the first demonstration of ant protection leading to increased fruit set in the Cactaceae under natural conditions. Although the consequences of damage by sucking and mining insects remain unclear for Opuntia , the results show how the association of EFNs with vulnerable reproductive plant organs can result in a direct ant-derived benefit to plant fitness.     

斜纹夜蛾幼虫诱导的油菜抗虫性及其与茉莉酸信号途径的关系

植物在受植食性昆虫为害时能产生防御反应,并且植物的茉莉酸信号转导途径在这一过程中发挥着重要作用。然而, 迄今为止对于油菜Brassica campestris的诱导防御反应很少有研究报道。为此, 本实验通过测定油菜内茉莉酸和胰蛋白酶抑制剂含量研究了油菜在斜纹夜蛾Spodoptera litura幼虫为害后的抗虫性和胰蛋白酶抑制剂含量的变化,并分析这些变化在油菜诱导抗虫性与茉莉酸信号转导途径中的关系。结果表明：斜纹夜蛾幼虫取食能导致油菜体内茉莉酸和胰蛋白酶抑制剂含量系统性上升,外用茉莉酸甲酯处理也能系统性增加油菜的胰蛋白酶抑制剂含量,并且取食茉莉酸甲酯处理或斜纹夜蛾幼虫取食过的叶片能显著降低斜纹夜蛾幼虫的体重,两者的体重分别为对照植株上的67.5%和60.2%。机械损伤加斜纹夜蛾幼虫口腔分泌物处理能引起处理叶中茉莉酸和胰蛋白酶抑制剂含量的增加,但其诱导效果与机械损伤加水没有显著差异,并且两者明显低于虫害的诱导效果,两种处理的茉莉酸和胰蛋白酶抑制剂含量分别为虫害诱导的68.4%和24.4%及62.9%和36.9%;多次连续机械损伤的诱导效果与一次损伤的没有明显差异。结果说明斜纹夜蛾幼虫诱导的油菜抗虫性与茉莉酸信号转导途径有关,而其激活油菜抗虫反应的机理则可能与其特定的取食行为相关。     

Associational effects of plant defences in relation to within- and between-patch food choice by a mammalian herbivore: neighbour contrast susceptibility and defence

A basic idea of plant defences is that a plant should gain protection from its own defence. In addition, there is evidence that defence traits of the neighbouring plants can influence the degree of protection of an individual plant. These associational effects depend in part on the spatial scale of herbivore selectivity. A strong between-patch selectivity together with a weak within-patch selectivity leads to a situation where a palatable plant could avoid being grazed by growing in a patch with unpalatable plants, which is referred to as associational defence. Quite different associational effects will come about if the herbivore instead is unselective between patches and selective within a patch. We studied these effects in a manipulative experiment where we followed the food choice of fallow deer when they encountered two patches of overall different quality. One of the two patches consisted of pellets with low-tannin concentration in seven out of eight buckets and with high concentration in the remaining bucket. The other patch instead had seven high- and one low-tannin bucket. We performed the experiment both with individuals one at a time and with a group of 16–17 deer. We found that the deer were unselective between patches, but selective within a patch, and that the single low-tannin bucket among seven high-tannin buckets was used more than a low-tannin bucket among other low-tannin buckets. This corresponds to a situation where a palatable plant that grows among unpalatable plants is attacked more than if it was growing among its own kind, and for this effect we suggest the term neighbour contrast susceptibility, which is the opposite of associational defence. We also found that the high-tannin bucket in the less defended patch was less used than the high-tannin buckets in the other patch, which corresponds to neighbour contrast defence. The neighbour contrast susceptibility was present both for individual and group foraging, but the strength of the effect was somewhat weaker for groups due to weaker within-patch selectivity.     

Sex differences in nest defence by the red-backed shrike<Emphasis Type="Italic"> Lanius collurio</Emphasis>: effects of offspring age,brood size,and stage of breeding season

The red-backed shrike Lanius collurio is an open-cup nesting passerine bird, which protects its nest aggressively attacking predators near the nest. The response of parents to a human observer was investigated during the nesting period 1999–2001 in Poland. The intensity of nest defence increased as the breeding cycle progressed in accordance to the offspring value hypothesis. However, we did not find an increase in the level of aggression according to the number of offspring and the time of season. Contrary to previous predictions, we did not find gender differences in nest defence. More aggressive parents, both females and males, have significantly better breeding success than quieter individuals.     

Third generation of matrix metalloprotease inhibitors: Gain in selectivity by targeting the depth of the S1′ cavity

Following the disappointment of clinical trials with early broad-spectrum synthetic inhibitors of matrix metalloproteases (MMPs), the field is now resurging with a new focus on the development of more selective inhibitors. Compounds able to fully discriminate between different members of the MMP family are sorely needed for therapeutic applications. Chemical efforts over the past years have led to very few selective inhibitors of MMPs. The over-exploitation of the hydroxamate function, or other strong zinc-binding groups, might be responsible for this failure. By resorting to weaker zinc-chelating groups, like phosphoryl or carboxylic groups, inhibitors with improved selectivity profiles have been developed. However, the most encouraging results have been obtained with compounds that avoid targeting the zinc but gain their affinity from plunging deeper into the MMP S₁′ cavity. Analyses of the crystal structures of MMP-13 and MMP-8 complexes with such compounds provide novel insights for the design of more selective inhibitors for other members of the MMP family.