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Many parasites can interfere with their host’s defences tomaximize their fitness. Here, we investigated if there isheritable variation in the spider miteTetranychus evansifortraits associated with how they interact with their host plant.We also determined if this variation correlates with mitefecundity.Tetranychus evansican interfere with jasmonate (JA)defences which are the main determinant of anti-herbivoreimmunity in plants. We investigated (i) variation in fecundityin the presence and absence of JA defences, making use ofa wild-type tomato cultivar and a JA-deficient mutant(defenseless-1), and (ii) variation in the induction of JAdefences, in fourT. evansifield populations and 59 inbredlines created from an outbred population originating fromcontrolled crosses of the four field populations. We observed astrong positive genetic correlation between fecundity in thepresence (on wild-type) and the absence of JA defences (ondefenseless-1). However, fecundity did not correlate with themagnitude of induced JA defences in wild-type plants. Ourresults suggest that the performance of the specialistT. evansiis not related to their ability to manipulate plant defences,either because all lines can adequately reduce levels ofdefences, or because they are resistant to them.

Many parasites can interfere with their host's defences to maximize their fitness. Here, we investigated if there is a heritable variation in the spider mite, Tetranychus evansi for traits associated with how they interact with their host plant. We also determined if this variation correlates with mite fecundity. Tetranychus evansi can interfere with jasmonate (JA) defences which are the main determinant of anti-herbivore immunity in plants. We investigated (i) variation in fecundity in the presence and absence of JA defences, making use of a wild-type tomato cultivar and a JA-deficient mutant (defenseless-1), and (ii) variation in the induction of JA defences, in four T. evansi field populations and 59 inbred lines created from an outbred population originating from controlled crosses of the four-field populations. We observed a strong positive genetic correlation between fecundity in the presence (on WT) and the absence of JA defences (on def-1). However, fecundity did not correlate with the magnitude of induced JA defences in WT plants. Our results suggest that the performance of the specialist T. evansi is not related to their ability to manipulate plant defences, either because all lines can adequately reduce levels of defences, or because they are resistant to them.

Additional file 16: Figure S1. Chemical structures of the three products formed from funneling reactions utilized by microorganisms in the breakdown of organic compounds. Catechol and protocatechuic acid degradation proceeds via the β-ketoadipate pathway while hydroxyquinol is formed from protocatechuate and degraded in an alternative pathway found in some bacteria and fungi.

Additional file 18: Figure S3. Spectra of selected substrates and their metabolites as detected in negative mode by UPLC-MS. Black peaks represent the substrate while red peaks depict the metabolites. Structures of both the substrate and the metabolite are as shown with their mass to charge ratios. The DOG used in the assay is indicated in blue. A thunderbolt sign shows the ortho-cleavage position.

Additional file 19: Figure S4. PCR amplicons of TuDOG7, TuDOG10 and TuDOG11 and their neighboring intron containing eukaryotic genes.

Additional file 20: Figure S5.in situ localization of T. urticae DOG genes (TuDOG11 and TuDOG3). A DIG-labelled antisense probe was used for hybridization and the signal was developed using anti-DIG-AP and FastRed as substrate. The reaction product is visible as a red signal (the cuticle got red staining in both antisense and sense treatment so we consider that as false signals) while the spider mite body shows green auto fluorescence. Abbreviations: C, cuticle; PME, posterior midgut epithelium; PM, posterior midgut; V, ventriculus; VE, ventricular epithelium; Scale bars: 100 μm.

Additional file 17: Figure S2. Schematic of oxygen consumption assay with Clark-type electrode. (A) The Clark type electrode reaction chamber. The rubber seal replaces the microsyringe after injection of the various components into the system. It serves to seal the chamber from external oxygen. (B) A zoom into the electrode unit. The platinum cathode is surrounded by a well that serves as a reservoir for electrolyte solution (50% potassium chloride). During the reaction, the electrolyte is ionized and initiates a current flow from anode to cathode. The current is equivalent to the oxygen concentration in the media. (C) Typical oxygen consumption curve observed when there is substrate cleavage. (D) The curve observed in the absence of substrate cleavage. In the absence of substrate cleavage, catechol was added at the end of the reaction as a control for activity.

Additional file 4: File S3. Coverage plots of 17 T. urticae DOG genes and their surrounding regions in the genome of Tetranychus urticae. Gene models of DOG genes and their neighboring genes are depicted as follows: large and small orange boxes represent coding sequences and untranslated regions, respectively, whereas introns are shown as connecting lines between the boxes. (+) and (-) represent the forward and reverse strand, respectively. Underneath the gene models of TuDOG7, TuDOG10 and TuDOG11, the length and position of an amplicon obtained by PCR (Fig. S4) is indicated with a red line. Next, coverage plots of Illumina-reads (‘“Illu.’”) from adult T. urticae polyA selected RNA [13] and from genomic DNA sequencing of the EtoxR (‘“Etox’”) and London(‘“Lon’”) strain of T. urticae [13, 110] are shown below the gene models. The Illumina reads coverage plots are followed by a coverage plot of Sanger (‘“San.’”) reads from genomic DNA sequencing of the London strain [13] and by an alignment of these Sanger reads with the T. urticae genome of the London strain. Paired-end Sanger reads for which both reads are mapped in or extend nearby the indicated region are denoted by thin lines to show pair connections [13] (see [43], for mapping details).

Additional file 21: Figure S6. Stain-free SDS-PAGE (panel a) and western blot (panel b) of purified recombinant T. urticae DOGs. The 6x His tagged proteins are between 25-37 kDa.

Plants have developed diverse defence mechanisms to ward off herbivorous pests. However, agriculture still faces estimatedcrop yield losses ranging from 25% to 40% annually. These losses arise not only because of direct feeding damage,but also because many pests serve as vectors of plant viruses. Herbivorous thrips (Thysanoptera) are important pests ofvegetable and ornamental crops worldwide, and encompass virtually all general problems of pests: they are highly polyphagous,hard to control because of their complex lifestyle, and they are vectors of destructive viruses. Currently, controlmanagement of thrips mainly relies on the use of chemical pesticides. However, thrips rapidly develop resistance tothese pesticides. With the rising demand for more sustainable, safer, and healthier food production systems, we urgentlyneed to pinpoint the gaps in knowledge of plant defences against thrips to enable the future development of novel controlmethods. In this review, we summarize the current, rather scarce, knowledge of thrips-induced plant responses andthe role of phytohormonal signalling and chemical defences in these responses. We describe concrete opportunities forbreeding resistance against pests such as thrips as a prototype approach for next-generation resistance breeding.

Biological control is an important ecosystem service delivered by natural enemies. Together with breeding for plant defence, it constitutes one of the most promising alternatives to pesticides for controlling herbivores in sustainable crop production. Especially induced plant defences may be promising targets in plant breeding for resistance against arthropod pests. Because they are activated upon herbivore damage, costs are only incurred when defence is needed. Moreover, they can be more specific than constitutive defences. Nevertheless, inducible defence traits that are harming plant pest organisms may interfere with biological control agents, such as predators and parasitoids. Despite the vast fundamental knowledge on plant defence mechanisms and their effects on natural enemies, our understanding of the feasibility of combining biological control with induced plant defence in practice is relatively poor. In this review, we focus on arthropod pest control and present the most important features of biological control with natural enemies and of induced plant defence. Furthermore, we show potential synergies and conflicts among them and, finally, identify gaps and list opportunities for their combined use in crop protection. We suggest that breeders should focus on inducible resistance traits that are compatible with the natural enemies of arthropod pests, specifically traits that help communities of natural enemies to build up.

Biological control is an important ecosystem service delivered by natural enemies. Together with breeding for plant defence, it constitutes one of the most promising alternatives to pesticides for controlling herbivores in sustainable crop production. Especially induced plant defences may be promising targets in plant breeding for resistance against arthropod pests. Because they are activated upon herbivore damage, costs are only incurred when defence is needed. Moreover, they can be more specific than constitutive defences. Nevertheless, inducible defence traits that are harming plant pest organisms may interfere with biological control agents, such as predators and parasitoids. Despite the vast fundamental knowledge on plant defence mechanisms and their effects on natural enemies, our understanding of the feasibility of combining biological control with induced plant defence in practice is relatively poor. In this review, we focus on arthropod pest control and present the most important features of biological control with natural enemies and of induced plant defence. Furthermore, we show potential synergies and conflicts among them and, finally, identify gaps and list opportunities for their combined use in crop protection. We suggest that breeders should focus on inducible resistance traits that are compatible with the natural enemies of arthropod pests, specifically traits that help communities of natural enemies to build up.

Biological control is an important ecosystem service delivered by natural enemies. Together with breeding for plant defence, it constitutes one of the most promising alternatives to pesticides for controlling herbivores in sustainable crop production. Especially induced plant defences may be promising targets in plant breeding for resistance against arthropod pests. Because they are activated upon herbivore damage, costs are only incurred when defence is needed. Moreover, they can be more specific than constitutive defences. Nevertheless, inducible defence traits that are harming plant pest organisms may interfere with biological control agents, such as predators and parasitoids. Despite the vast fundamental knowledge on plant defence mechanisms and their effects on natural enemies, our understanding of the feasibility of combining biological control with induced plant defence in practice is relatively poor. In this review, we focus on arthropod pest control and present the most important features of biological control with natural enemies and of induced plant defence. Furthermore, we show potential synergies and conflicts among them and, finally, identify gaps and list opportunities for their combined use in crop protection. We suggest that breeders should focus on inducible resistance traits that are compatible with the natural enemies of arthropod pests, specifically traits that help communities of natural enemies to build up.

The tomato (Lycopersicon esculentum) mutant def-1, which is deficient in induced jasmonic acid (JA) accumulation upon wounding or herbivory, was used to study the role of JA in the direct and indirect defense responses to phytophagous mites (Tetranychus urticae). In contrast to earlier reports, spider mites laid as many eggs and caused as much damage on def-1 as on wild-type plants, even though def-1 lacked induction of proteinase inhibitor activity. However, the hatching-rate of eggs on def-1 was significantly higher, suggesting that JA-dependent direct defenses enhanced egg mortality or increased the time needed for embryonic development. As to gene expression, def-1 had lower levels of JA-related transcripts but higher levels of salicylic acid (SA) related transcripts after 1 d of spider mite infestation. Furthermore, the indirect defense response was absent in def-1, since the five typical spider mite-induced tomato-volatiles (methyl salicylate [MeSA], 4,8,12-trimethyltrideca-1,3,7,11-tetraene [TMTT], linalool, trans-nerolidol, and trans-beta-ocimene) were not induced and the predatory mite Phytoseiulus persimilis did not discriminate between infested and uninfested def-1 tomatoes as it did with wild-type tomatoes. Similarly, the expression of the MeSA biosynthetic gene salicylic acid methyltransferase (SAMT) was induced by spider mites in wild type but not in def-1. Exogenous application of JA to def-1 induced the accumulation of SAMT and putative geranylgeranyl diphosphate synthase transcripts and restored MeSA- and TMTT-emission upon herbivory. JA is therefore necessary to induce the enzymatic conversion of SA into MeSA. We conclude that JA is essential for establishing the spider mite-induced indirect defense response in tomato.

Herbivores have evolved several strategies to cope with plant defences. Some herbivores are able to resist toxic compounds, while others can manipulate host immunity. Previously it was found that spider mites collected from non-solanaceous wild host plants consist mostly of individuals that induce tomato defences, but also at low frequencies of individuals that can suppress these defences. Also, it has been shown that mites collected from non-solanaceous plants can adapt to tomato by evolving traits that allow them to suppress defences. Hence, we wanted to know if this trait is also common among mites naturally occurring on tomatoes. Here, we compared three T. urticae populations sampled from tomato at three field sites, and also an outbred population created from them through controlled crosses. We then assessed their fecundity on wild-type (WT) tomato plants and def-1 mutants impaired in inducible JA-defences. We also assessed the magnitude of JA defences they induce in WT plants to discriminate between resistant types (high induction and high performance) and those that can suppress defences (low induction, high performance). We then aligned these data with data on variation in mitochondrial DNA cytochrome oxidase I (COI) and effector 84 (a suppressor of JA-defences in planta), in order to compare genetic diversity patterns among mite lines that induce or suppress defences. We found that suppression is the dominant phenotype in mite strains collected from field-grown tomatoes and that inducers and suppressors predominantly cluster in distinct effector 84 clades. We speculate that effector allelic diversity may be subject to natural selection when these mites colonize a novel host plant, promoting traits to cope with plant resistance, such as defence suppression, which facilitates adaptation.