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Living deep in the ground and surrounded by darkness, soil insects must rely on the chemicals released by plants to find the roots they feed on. Carbon dioxide, for example, is a by-product of plant respiration, which, above ground, is thought to attract moths to flowers and flies to apples; underground, however, its role is still unclear. This gaseous compound can travel through soil and potentially act as a compass for root-eating insects. Yet, it is also produced by decaying plants or animals, which are not edible. It is therefore possible that insects use this signal as a long-range cue to orient themselves, but then switch to another chemical when closer to their target to narrow in on an actual food source. To test this idea, Arce et al. investigated whether carbon dioxide guides the larvae of Western corn rootworm to maize roots. First, the rootworm genes responsible for sensing carbon dioxide were identified and switched off, making the larvae unable to detect this gas. When the genetically engineered rootworms were further than 9cm from maize roots, they were less able to locate that food source; closer to the roots, however, the insects could orient themselves towards the plant. This suggests that the insects use carbon dioxide at long distances but rely on another chemicals to narrow down their search at close range. To confirm this finding, Arce et al. tried absorbing the carbon dioxide using soda lime, leading to similar effects: carbon dioxide sensitive insects stopped detecting the roots at long but not short distances. Additional experiments then revealed that the compound could help insects find the best roots to feed on. Indeed, eating plants that grow on rich terrain – for instance, fertilized soils – helps insects to grow bigger and faster. These roots also release more carbon dioxide, in turn attracting rootworms more frequently. In the United States and Eastern Europe, Western corn rootworms inflict major damage to crops, highlighting the need to understand and manage the link between fertilization regimes, carbon dioxide release and how these pests find their food.

Plant leaves that are exposed to herbivore‐induced plant volatiles (HIPVs) respond by increasing their defenses, a phenomenon referred to as priming. Whether this phenomenon also occurs in the roots is unknown. Using maize plants, Zea mays, whose leaves respond strongly to leaf HIPVs, we measured the impact of belowground HIPVs, emanating from roots infested by the banded cucumber beetle, Diabrotica balteata, on constitutive and herbivore‐induced levels of defense‐related gene expression, phytohormones, volatile and non‐volatile primary and secondary metabolites, growth and herbivore resistance in roots of neighbouring plants. HIPV exposure did not increase constitutive or induced levels of any of the measured root traits. Furthermore, HIPV exposure did not reduce the performance or survival of D. balteata on maize or its ancestor teosinte. Cross‐exposure experiments between HIPVs from roots and leaves revealed that maize roots, in contrast to maize leaves, neither emit nor respond strongly to defense‐regulating HIPVs. Together, these results demonstrate that volatile‐mediated defense regulation is restricted to the leaves of maize. This finding is in line with the lower diffusibility of volatiles in the soil and the availability of other, potentially more efficient, information conduits below ground., Exposure to herbivore‐induced volatiles from infested neighbours does not alter plant response and resistance to root herbivory in maize.

Plant leaves that are exposed to herbivore induced plant volatiles (HIPVs) respond by increasing their defenses, a phenomenon referred to as priming. Whether this phenomenon also occurs in the roots is unknown. Using maize plants, Zea mays, whose leaves respond strongly to leaf HIPVs, we measured the impact of belowground HIPVs, emanating from roots infested by the banded cucumber beetle, Diabrotica balteata, on constitutive and herbivore‐induced levels of defense‐related gene expression, phytohormones, volatile and non‐volatile primary and secondary metabolites, growth and herbivore resistance in roots of neighboring plants. HIPV exposure did not increase constitutive or induced levels of any of the measured root traits. Furthermore, HIPV exposure did not reduce the performance or survival of D. balteata on maize or its ancestor teosinte. Cross‐exposure experiments between HIPVs from roots and leaves revealed that maize roots, in contrast to maize leaves, neither emit nor respond strongly to defense‐regulating HIPVs. Together, these results demonstrate that volatile‐mediated defense regulation is restricted to the leaves of maize. This finding is in line with the lower diffusibility of volatiles in the soil and the availability of other, potentially more efficient information conduits below ground.

Plants produce complex mixtures of primary and secondary metabolites. Herbivores use these metabolites as behavioral cues to increase their fitness. However, how herbivores integrate different metabolite classes into fitness-relevant foraging decisions in planta is poorly understood. We developed a molecular manipulative approach to modulate the availability of sugars and benzoxazinoid secondary metabolites as foraging cues for a specialist maize herbivore, the western corn rootworm. By disrupting sugar perception in the western corn rootworm and benzoxazinoid production in maize, we show that sugars and benzoxazinoids act as distinct and dynamically integrated mediators of short-distance host finding and acceptance. While sugars improve the capacity of rootworm larvae to find a host plant and to distinguish post-embryonic from less nutritious embryonic roots, benzoxazinoids are specifically required for the latter. Host acceptance in the form of root damage is increased by benzoxazinoids and sugars in an additive manner. This pattern is driven by increasing damage to post-embryonic roots in the presence of benzoxazinoids and sugars. Benzoxazinoid- and sugar-mediated foraging directly improves western corn rootworm growth and survival. Interestingly, western corn rootworm larvae retain a substantial fraction of their capacity to feed and survive on maize plants even when both classes of chemical cues are almost completely absent. This study unravels fine-grained differentiation and integration of primary and secondary metabolites into herbivore foraging and documents how the capacity to compensate for the lack of important chemical cues enables a specialist herbivore to survive within unpredictable metabolic landscapes.

SummaryInsect herbivores can use volatile and visual cues to locate and select suitable host plants from a distance. The importance of CO2, arguable the most conserved volatile marker of metabolic activity, is not well understood in this context, even though many herbivores are known to respond to minute differences in CO2 concentrations. To address this gap of knowledge, we manipulated CO2 perception of the larvae of the western corn rootworm (Diabrotica virgifera virgifera; WCR) through RNA interference and studied how CO2 perception impacts their interaction with their host plant, maize (Zea mays). We show that the expression of a putative Group 2 carbon dioxide receptor, DvvGr2, is specifically required for dose-dependent larval responses to CO2 in the ppm range. Silencing DvvGr2 has no effect on the ability of WCR larvae to locate host plants at short distance (DvvGr2 silencing and CO2 scrubbing, we demonstrate that WCR larvae use CO2 as a long-range host plant finding cue, but employ other volatiles for short-range host location. We furthermore show that the larvae use CO2 as a fitness-relevant long-distance indicator of plant nutritional status: Maize plants that are well-fertilized emit more CO2 from their roots and are better hosts for WCR than plants that are nutrient-deficient, and the capacity of WCR larvae to distinguish between these plants depends exclusively on their capacity to perceive CO2 through DvvGr2. This study unravels how CO2 can mediate plant-herbivore interactions by serving as a distance-dependent host location and quality assessment cue.

SUMMARYPlant leaves that are exposed to herbivore induced plant volatiles (HIPVs) respond by increasing their defenses. Whether this phenomenon also occurs in the roots is unknown.Using maize (Zea mays), whose leaves respond strongly to leaf HIPVs, we measured the impact of root HIPVs, emanating from plants infested by the banded cucumber beetle (Diabrotica balteata), on constitutive and herbivore-induced levels of root soluble sugars, starch, total soluble proteins, free amino acids, volatile and non-volatile secondary metabolites, defense gene expression, growth and root herbivore resistance of neighboring plants.HIPV exposure did not alter constitutive or induced levels of any of the measured root traits. Furthermore, HIPV exposure did not reduce the performance and survival of banded cucumber beetle larvae on maize or teosinte. Cross-exposure experiments revealed that maize roots, in contrast to maize leaves, neither emit nor respond strongly to defense-regulating HIPVs.Together, these results demonstrate that volatile-mediated defense regulation is restricted to the leaves of maize and teosinte, a finding which is in line with the lower diffusibility of volatiles in the soil and the availability of other, potentially more efficient information conduits below ground.

Spider mites are destructive arthropod pests on many crops. The generalist herbivorous mite Tetranychus urticae induces defenses in tomato (Solanum lycopersicum) and this constrains its fitness. By contrast, the Solanaceae‐specialist Tetranychus evansi maintains a high reproductive performance by suppressing tomato defenses. Tetranychus evansi outcompetes T. urticae when infesting the same plant, but it is unknown whether this is facilitated by the defenses of the plant.We assessed the extent to which a secondary infestation by a competitor affects local plant defense responses (phytohormones and defense genes), mite gene expression and mite performance.We observed that T. evansi switches to hyper‐suppression of defenses after its tomato host is also invaded by its natural competitor T. urticae. Jasmonate (JA) and salicylate (SA) defenses were suppressed more strongly, albeit only locally at the feeding site of T. evansi, upon introduction of T. urticae to the infested leaflet. The hyper‐suppression of defenses coincided with increased expression of T. evansi genes coding for salivary defense‐suppressing effector proteins and was paralleled by an increased reproductive performance.Together, these observations suggest that T. evansi overcompensates its reproduction through hyper‐suppression of plant defenses in response to nearby competitors. We hypothesize that the competitor‐induced overcompensation promotes competitive population growth of T. evansi on tomato.

Plant defensive substances can affect the quality of herbivores as prey for predators either directly or indirectly. Directly when the prey has become toxic since it ingested toxic plant material and indirectly when these defences have affected the size and/or nutritional value (both quality parameters) of prey or their abundance. To disentangle direct and indirect effects of JA-defences on prey quality for predators, we used larvae of the omnivorous thrips Frankliniella occidentalis because these are not directly affected by the jasmonate-(JA)-regulated defences of tomato. We offered these thrips larvae the eggs of spider mites (Tetranychus urticae or T. evansi) that had been feeding from either normal tomato plants, JA-impaired plants, or plants treated with JA to artificially boost defences and assessed their performance. Thrips development and survival was reduced on the diet of T. evansi eggs relative to the diet of T. urticae eggs yet these effects were independent from the absence/presence of JA-defences. This indicates that the detrimental effects of tomato JA-defences on herbivores not necessarily also affects their quality as prey.

Plants produce complex mixtures of primary and secondary metabolites. Herbivores use these metabolites as behavioral cues to increase their fitness. However, how herbivores combine and integrate different metabolite classes into fitness-relevant foraging decisions in planta is poorly understood. We developed a molecular manipulative approach to modulate the availability of sugars and benzoxazinoid secondary metabolites as foraging cues for a specialist maize herbivore, the western corn rootworm. By disrupting sugar perception in the western corn rootworm and benzoxazinoid production in maize, we show that sugars and benzoxazinoids act as distinct and dynamically combined mediators of short-distance host finding and acceptance. While sugars improve the capacity of rootworm larvae to find a host plant and to distinguish postembryonic from less nutritious embryonic roots, benzoxazinoids are specifically required for the latter. Host acceptance in the form of root damage is increased by benzoxazinoids and sugars in an additive manner. This pattern is driven by increasing damage to postembryonic roots in the presence of benzoxazinoids and sugars. Benzoxazinoid- and sugar-mediated foraging directly improves western corn rootworm growth and survival. Interestingly, western corn rootworm larvae retain a substantial fraction of their capacity to feed and survive on maize plants even when both classes of chemical cues are almost completely absent. This study unravels fine-grained differentiation and combination of primary and secondary metabolites into herbivore foraging and documents how the capacity to compensate for the lack of important chemical cues enables a specialist herbivore to survive within unpredictable metabolic landscapes., This study shows how an important agricultural pest, the western corn rootworm, integrates nutrients (sugars) and plant defense compounds (benzoxazinoids) to navigate the maize rhizosphere and feed on the most nutritious roots.

Tomato plants are attacked by diverse herbivorous arthropods, including by cell-content-feeding mites, such as the extreme generalist Tetranychus urticae and specialists like Tetranychus evansi and Aculops lycopersici. Mite feeding induces plant defense responses that reduce mite performance. However, T. evansi and A. lycopersici suppress plant defenses via poorly understood mechanisms and, consequently, maintain a high performance on tomato. On a shared host, T. urticae can be facilitated by either of the specialist mites, likely due to the suppression of plant defenses. To better understand defense suppression and indirect plant-mediated interactions between herbivorous mites, we used gene-expression microarrays to analyze the transcriptomic changes in tomato after attack by either a single mite species (T. urticae, T. evansi, A. lycopersici) or two species simultaneously (T. urticae plus T. evansi or T. urticae plus A. lycopersici). Additionally, we assessed mite-induced changes in defense-associated phytohormones using LC-MS/MS. Compared to non-infested controls, jasmonates (JAs) and salicylate (SA) accumulated to higher amounts upon all mite-infestation treatments, but the response was attenuated after single infestations with defense-suppressors. Strikingly, whereas 8 to 10% of tomato genes were differentially expressed upon single infestations with T. urticae or A. lycopersici, respectively, only 0.1% was altered in T. evansi-infested plants. Transcriptome analysis of dual-infested leaves revealed that A. lycopersici primarily suppressed T. urticae-induced JA defenses, while T. evansi dampened T. urticae-triggered host responses on a transcriptome-wide scale. The latter suggests that T. evansi not solely down-regulates plant gene expression, but rather directs it back towards housekeeping levels. Our results provide valuable new insights into the mechanisms underlying host defense suppression and the plant-mediated facilitation of competing herbivores

Plants have evolved numerous defensive traits that enable them to resist herbivores. In turn, this resistance has selected for herbivores that can cope with defenses by either avoiding, resisting or suppressing them. Several species of herbivorous mites, such as the spider mites Tetranychus urticae and Tetranychus evansi, were found to maximize their performance by suppressing inducible plant defenses. At first glimpse it seems obvious why such a trait will be favored by natural selection. However, defense suppression appeared to readily backfire since mites that do so also make their host plant more suitable for competitors and their offspring more attractive for natural enemies. This, together with the fact that spider mites are infamous for their ability to resist (plant) toxins directly, justifies the question as to why traits that allow mites to suppress defenses nonetheless seem to be relatively common? We argue that this trait may facilitate generalist herbivores, like T. urticae, to colonize new host species. While specific detoxification mechanisms may, on average, be suitable only on a narrow range of similar hosts, defense suppression may be more broadly effective, provided it operates by targeting conserved plant signaling components. If so, resistance and suppression may be under frequency-dependent selection and be maintained as a polymorphism in generalist mite populations. In that case, the defense suppression trait may be under rapid positive selection in subpopulations that have recently colonized a new host but may erode in relatively isolated populations in which host-specific detoxification mechanisms emerge. Although there is empirical evidence to support these scenarios, it contradicts the observation that several of the mite species found to suppress plant defenses actually are relatively specialized. We argue that in these cases buffering traits may enable such mites to mitigate the negative side effects of suppression in natural communities and thus shield this trait from natural selection.

BACKGROUND: Plants are hotbeds for parasites such as arthropod herbivores, which acquire nutrients and energy from their hosts in order to grow and reproduce. Hence plants are selected to evolve resistance, which in turn selects for herbivores that can cope with this resistance. To preserve their fitness when attacked by herbivores, plants can employ complex strategies that include reallocation of resources and the production of defensive metabolites and structures. Plant defences can be either prefabricated or be produced only upon attack. Those that are ready-made are referred to as constitutive defences. Some constitutive defences are operational at any time while others require activation. Defences produced only when herbivores are present are referred to as induced defences. These can be established via de novo biosynthesis of defensive substances or via modifications of prefabricated substances and consequently these are active only when needed. Inducibility of defence may serve to save energy and to prevent self-intoxication but also implies that there is a delay in these defences becoming operational. Induced defences can be characterized by alterations in plant morphology and molecular chemistry and are associated with a decrease in herbivore performance. These alterations are set in motion by signals generated by herbivores. Finally, a subset of induced metabolites are released into the air as volatiles and function as a beacon for foraging natural enemies searching for prey, and this is referred to as induced indirect defence. SCOPE: The objective of this review is to evaluate (1) which strategies plants have evolved to cope with herbivores and (2) which traits herbivores have evolved that enable them to counter these defences. The primary focus is on the induction and suppression of plant defences and the review outlines how the palette of traits that determine induction/suppression of, and resistance/susceptibility of herbivores to, plant defences can give rise to exploitative competition and facilitation within ecological communities "inhabiting" a plant. CONCLUSIONS: Herbivores have evolved diverse strategies, which are not mutually exclusive, to decrease the negative effects of plant defences in order to maximize the conversion of plant material into offspring. Numerous adaptations have been found in herbivores, enabling them to dismantle or bypass defensive barriers, to avoid tissues with relatively high levels of defensive chemicals or to metabolize these chemicals once ingested. In addition, some herbivores interfere with the onset or completion of induced plant defences, resulting in the plant's resistance being partly or fully suppressed. The ability to suppress induced plant defences appears to occur across plant parasites from different kingdoms, including herbivorous arthropods, and there is remarkable diversity in suppression mechanisms. Suppression may strongly affect the structure of the food web, because the ability to suppress the activation of defences of a communal host may facilitate competitors, whereas the ability of a herbivore to cope with activated plant defences will not. Further characterization of the mechanisms and traits that give rise to suppression of plant defences will enable us to determine their role in shaping direct and indirect interactions in food webs and the extent to which these determine the coexistence and persistence of species.

When feeding from tomato (Solanum lycopersicum), the generalist spider mite Tetranychus urticae induces jasmonate (JA)- and salicylate (SA)-regulated defense responses that hamper its performance. The related T. evansi, a Solanaceae-specialist, suppresses these defenses, thereby upholding a high performance. On a shared leaf, T. urticae can be facilitated by T. evansi, likely via suppression of defenses by the latter. Yet, when infesting the same plant, T. evansi outcompetes T. urticae. Recently, we found that T. evansi intensifies suppression of defenses locally, i.e., at its feeding site, after T. urticae mites were introduced onto adjacent leaf tissue. This hyper-suppression is paralleled by an increased oviposition rate of T. evansi, probably promoting its competitive population growth. Here we present additional data that not only provide insight into the spatiotemporal dynamics of defense induction and suppression by mites, but that also suggest T. evansi to manipulate more than JA and SA defenses alone.

When two related species interbreed, their hybrid offspring frequently suffer from reduced fitness. The genetics of hybrid incompatibility are described by the Bateson-Dobzhansky-Muller (BDM) model, where fitness is reduced by epistatic interactions between alleles of heterospecific origin. Unfortunately, most empirical evidence for the BDM model comes from a few well-studied model organisms, restricting our genetic understanding of hybrid incompatibilities to limited taxa. These systems are predominantly diploid and incompatibility is often complete, which complicates the detection of recessive allelic interactions and excludes the possibility to study viable or intermediate stages. Here, we advocate research into non-model organisms with haploid or haplodiploid reproductive systems and incomplete hybrid incompatibility because (1) dominance is absent in haploids and (2) incomplete incompatibility allows comparing affected with unaffected individuals. We describe a novel two-locus statistic specifying the frequency of individuals for which two alleles co-occur. This approach to studying BDM incompatibilities requires genotypic characterization of hybrid individuals, but not genetic mapping or genome sequencing. To illustrate our approach, we investigated genetic causes for hybrid incompatibility between differentiated lineages of the haplodiploid spider mite Tetranychus evansi, and show that strong, but incomplete, hybrid breakdown occurs. In addition, by comparing the genotypes of viable hybrid males and inviable hybrid male eggs for eight microsatellite loci, we show that nuclear and cytonuclear BDM interactions constitute the basis of hybrid incompatibility in this species. Our approach opens up possibilities to study BDM interactions in non-model taxa, and may give further insight into the genetic mechanisms behind hybrid incompatibility.

It is well known that microbial pathogens and herbivores elicit defence responses in plants. Moreover, microorganisms associated with herbivores, such as bacteria or viruses, can modulate the plant's response to herbivores. Herbivorous spider mites can harbour different species of bacterial symbionts and exert a broad range of effects on host-plant defences. Hence, we tested the extent to which such symbionts affect the plant's defences induced by their mite host and assessed if this translates into changes in plant resistance. We assessed the bacterial communities of two strains of the common mite pest Tetranychus urticae. We found that these strains harboured distinct symbiotic bacteria and removed these using antibiotics. Subsequently, we tested to which extent mites with and without symbiotic bacteria induce plant defences in terms of phytohormone accumulation and defence gene expression, and assessed mite oviposition and survival as a measure for plant resistance. We observed that the absence/presence of these bacteria altered distinct plant defence parameters and affected mite performance but we did not find indications for a causal link between the two. We argue that although bacteria-related effects on host-induced plant defences may occur, these do not necessarily affect plant resistance concomitantly.

Plants respond to herbivory by mounting a defense. Some plant-eating spider mites (Tetranychus spp.) have adapted to plant defenses to maintain a high reproductive performance. From natural populations we selected three spider mite strains from two species, Tetranychus urticae and Tetranychus evansi, that can suppress plant defenses, using a fourth defense-inducing strain as a benchmark, to assess to which extent these strains suppress defenses differently. We characterized timing and magnitude of phytohormone accumulation and defense-gene expression, and determined if mites that cannot suppress defenses benefit from sharing a leaf with suppressors. The nonsuppressor strain induced a mixture of jasmonate- (JA) and salicylate (SA)-dependent defenses. Induced defense genes separated into three groups: 'early' (expression peak at 1 d postinfestation (dpi)); 'intermediate' (4 dpi); and 'late', whose expression increased until the leaf died. The T. evansi strains suppressed genes from all three groups, but the T. urticae strain only suppressed the late ones. Suppression occurred downstream of JA and SA accumulation, independently of the JA-SA antagonism, and was powerful enough to boost the reproductive performance of nonsuppressors up to 45%. Our results show that suppressing defenses not only brings benefits but, within herbivore communities, can also generate a considerable ecological cost when promoting the population growth of a competitor.

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.

R2R3-MYB transcription factors (TFs) are involved in diverse aspects of plant biology. Recently an R2R3-MYB was identified in Petunia x hybrida line P720 to have a role in the transcriptional regulation of floral volatile production. We propose a more foundational role for the R2R3-MYB TF EMISSION OF BENZENOIDS II (EOBII). The homolog of EOBII was isolated and characterized from P. x hybrida ‘Mitchell Diploid’ (MD) and Nicotiana attenuata. For both MD and N. attenuata, EOBII transcript accumulates to high levels in floral tissue with maximum accumulation at flower opening. When EOBII transcript levels are severely reduced using a stable RNAi (ir) approach in MD and N. attenuata, ir-EOBII flowers fail to enter anthesis and prematurely senesce. Transcript accumulation analysis demonstrated core phenylpropanoid pathway transcripts and cell wall modifier transcript levels are altered in ir-EOBII flowers. These flowers can be partially complemented by feeding with a sucrose, t-cinnamic acid, and gibberellic acid solution; presumably restoring cellular aspects sufficient for flower opening. Additionally, if ethylene sensitivity is blocked in either MD or N. attenuata, ir-EOBII flowers enter anthesis. These experiments demonstrate one R2R3-MYB TF can control a highly dynamic process fundamental to sexual reproduction in angiosperms: the opening of flowers.

Petunia (Petunia x hybrida cv 'Mitchell Diploid' [MD]) flowers emit high levels of multiple floral volatile benzenoid/phenylpropanoid (FVBP) compounds from anthesis to senescence in a concerted manner. Here we show seven genes responsible for the production of emitted FVBPs share similar transcript accumulation profiles through an analysis of four expression criteria. As a group, the FVBP gene transcripts accumulate to high levels in petal limb tissue of MD flowers from anthesis to senescence. Two to four hours of exogenous ethylene exposure reduces transcript levels of all FVBP genes examined, but 2h of treatment will not accelerate senescence or reduce volatile emissions in MD flowers. The FVBP genes show two obvious rhythmic patterns of transcript accumulation; however, corresponding enzyme activities of a subset of FVBP gene products do not. Together, these results depict floral volatile benzenoid/phenylpropanoid biosynthesis as a specific system with multiple regulatory features. One such feature is the highly regulated transcript accumulation of the FVBP genes. Additionally, ethylene may have a regulatory role in the FVBP system prior to a floral senescence program.

Highlight Here, a function for SlARF9, of the tomato ARF gene family, is defined and new insight provided into the mechanism by which auxin controls cell division and early fruit development., The transformation of the ovary into a fruit after successful completion of pollination and fertilization has been associated with many changes at transcriptomic level. These changes are part of a dynamic and complex regulatory network that is controlled by phytohormones, with a major role for auxin. One of the auxin-related genes differentially expressed upon fruit set and early fruit development in tomato is Solanum lycopersicum AUXIN RESPONSE FACTOR 9 (SlARF9). Here, the functional analysis of this ARF is described. SlARF9 expression was found to be auxin-responsive and SlARF9 mRNA levels were high in the ovules, placenta, and pericarp of pollinated ovaries, but also in other plant tissues with high cell division activity, such as the axillary meristems and root meristems. Transgenic plants with increased SlARF9 mRNA levels formed fruits that were smaller than wild-type fruits because of reduced cell division activity, whereas transgenic lines in which SlARF9 mRNA levels were reduced showed the opposite phenotype. The expression analysis, together with the phenotype of the transgenic lines, suggests that, in tomato, ARF9 negatively controls cell division during early fruit development.

Background Plants have inducible defenses to combat attacking organisms. Hence, some herbivores have adapted to suppress these defenses. Suppression of plant defenses has been shown to benefit herbivores by boosting their growth and reproductive performance. Results We observed in field-grown tomatoes that spider mites (Tetranychus urticae) establish larger colonies on plants already infested with the tomato russet mite (Aculops lycopersici). Using laboratory assays, we observed that spider mites have a much higher reproductive performance on russet mite-infested plants, similar to their performance on the jasmonic acid (JA)-biosynthesis mutant def-1. Hence, we tested if russet mites suppress JA-responses thereby facilitating spider mites. We found that russet mites manipulate defenses: they induce those mediated by salicylic acid (SA) but suppress those mediated by JA which would otherwise hinder growth. This suppression of JA-defenses occurs downstream of JA-accumulation and is independent from its natural antagonist SA. In contrast, spider mites induced both JA- and SA-responses while plants infested with the two mite species together display strongly reduced JA-responses, yet a doubled SA-response. The spider mite-induced JA-response in the presence of russet mites was restored on transgenic tomatoes unable to accumulate SA (nahG), but russet mites alone still did not induce JA-responses on nahG plants. Thus, indirect facilitation of spider mites by russet mites depends on the antagonistic action of SA on JA while suppression of JA-defenses by russet mites does not. Furthermore, russet mite-induced SA-responses inhibited secondary infection by Pseudomonas syringae (Pst) while not affecting the mite itself. Finally, while facilitating spider mites, russet mites experience reduced population growth. Conclusions Our results show that the benefits of suppressing plant defenses may diminish within communities with natural competitors. We show that suppression of defenses via the JA-SA antagonism can be a consequence, rather than the cause, of a primary suppression event and that its overall effect is determined by the presence of competing herbivores and the distinct palette of defenses these induce. Thus, whether or not host-defense manipulation improves an herbivore’s fitness depends on interactions with other herbivores via induced-host defenses, implicating bidirectional causation of community structure of herbivores sharing a plant. Electronic supplementary material The online version of this article (doi:10.1186/s12915-014-0098-9) contains supplementary material, which is available to authorized users.

Glandular trichomes are specialized hairs found on the surface of about 30% of all vascular plants and are responsible for a significant portion of a plant’s secondary chemistry. Glandular trichomes are an important source of essential oils, i.e., natural fragrances or products that can be used by the pharmaceutical industry, although many of these substances have evolved to provide the plant with protection against herbivores and pathogens. The storage compartment of glandular trichomes usually is located on the tip of the hair and is part of the glandular cell, or cells, which are metabolically active. Trichomes and their exudates can be harvested relatively easily, and this has permitted a detailed study of their metabolites, as well as the genes and proteins responsible for them. This knowledge now assists classical breeding programs, as well as targeted genetic engineering, aimed to optimize trichome density and physiology to facilitate customization of essential oil production or to tune biocide activity to enhance crop protection. We will provide an overview of the metabolic diversity found within plant glandular trichomes, with the emphasis on those of the Solanaceae, and of the tools available to manipulate their activities for enhancing the plant’s resistance to pests., JMA is funded via NWO Earth and Life Sciences (ALW) TOP (854.11.005) and BJCS via NWO Earth and Life Sciences (ALW) together with TTI Green Genetics (828.08.001).

Summary In Petunia × hybrida cv. ‘Mitchell Diploid’ floral fragrance is comprised of 13 volatile benzenoids/phenylpropanoids derived from the aromatic amino acid phenylalanine. Several genes involved in the direct synthesis of individual floral volatile benzenoid/phenylpropanoid (FVBP) compounds, i.e. at the end of the pathway, have been isolated and characterized in petunia through reverse genetic and biochemical approaches. In an effort to understand the regulation of ‘upstream’ components in the FVBP system, we have cloned and characterized two CHORISMATE MUTASE (PhCM1 and PhCM2) cDNAs from petunia. PhCM1 has a transcript accumulation profile consistent with known FVBP genes, while PhCM2 showed a constitutive transcript accumulation profile. The plastid-localized PhCM1 is allosterically regulated by tryptophan but not phenylalanine or tyrosine. The total FVBP emission in PhCM1 RNAi knockdown petunias is reduced by approximately 60–70%, and total chorismate mutase activity in corolla tissue is reduced by 80–85% compared to control plants. These results show that PhCM1 is the principal CHORISMATE MUTASE responsible for the coupling of metabolites from the shikimate pathway to the synthesis of FVBPs in the corolla of Petunia × hybrida cv. ‘Mitchell Diploid’.