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Insects are associated with a plethora of different microbes of which we are only starting to understand their role in shaping insect–plant interactions. Besides directly benefitting from symbiotic microbial metabolism, insects obtain and transmit microbes within their environment, making them ideal vectors and potential beneficiaries of plant diseases and microbes that alter plant defenses. To prevent damage, plants elicit stress-specific defenses to ward off insects and their microbiota. However, both insects and microbes harbor a wealth of adaptations that allow them to circumvent effective plant defense activation. In the past decades, it has become apparent that the enormous diversity and metabolic potential of insect-associated microbes may play a far more important role in shaping insect–plant interactions than previously anticipated. The latter may have implications for the development of sustainable pest control strategies. Therefore, this review sheds light on the current knowledge on multitrophic insect–microbe–plant interactions in a rapidly expanding field of research. [ABSTRACT FROM AUTHOR]

Nitropropionic acid (NPA) is a widely distributed naturally occurring nitroaliphatic toxin produced by leguminous plants and fungi. The Southern green shield bug feeds on leguminous plants and shows no symptoms of intoxication. Likewise, its gutassociated microorganisms are subjected to high levels of this toxic compound. In this study, we isolated a bacterium from this insect's gut system, classified as Pseudomonas sp. strain Nvir, that was highly resistant to NPA and was fully degrading it to inorganic nitrogen compounds and carbon dioxide. In order to understand the metabolic fate of NPA, we traced the fate of all atoms of the NPA molecule using isotope tracing experiments with [15N]NPA and [1-13C]NPA, in addition to experiments with uniformly 13C-labeled biomass that was used to follow the incorporation of 12C atoms from [U-12C]NPA into tricarboxylic acid cycle intermediates. With the help of genomics and transcriptomics, we uncovered the isolate's NPA degradation pathway, which involves a putative propionate-3-nitronate monooxygenase responsible for the first step of NPA degradation. The discovered protein shares only 32% sequence identity with previously described propionate-3-nitronate monooxygenases. Finally, we advocate that NPA-degrading bacteria might find application in biotechnology, and their unique enzymes might be used in biosynthesis, bioremediation, and in dealing with postharvest NPA contamination in economically important products. IMPORTANCE Plants have evolved sophisticated chemical defense mechanisms, such as the production of plant toxins in order to deter herbivores. One example of such a plant toxin is nitropropionic acid (NPA), which is produced by leguminous plants and also by certain fungi. In this project, we have isolated a bacterium from the intestinal tract of a pest insect, the Southern green shield bug, that is able to degrade NPA. Through a multiomics approach, we identified the respective metabolic pathway and determined the metabolic fate of all atoms of the NPA molecule. In addition, we provide a new genetic marker that can be used for genome mining toward NPA degradation. The discovery of degradation pathways of plant toxins by environmental bacteria opens new possibilities for pretreatment of contaminated food and feed sources and characterization of understudied enzymes allows their broad application in biotechnology. [ABSTRACT FROM AUTHOR]

The Southern green shield bug, Nezara viridula, is an invasive piercing and sucking pest insect that feeds on crops and poses a threat to global food production. Insects live in close relationships with microorganisms providing their host with unique capabilities, such as resistance to toxic plant metabolites. In this study, we investigated the resistance to and detoxification of the plant metabolite 3-nitropropionic acid by core and transient members of the N. viridula microbial community. Microbial community members showed a different tolerance to the toxin and we determined that six out of eight strains detoxified 3-nitropropionic acid. Additionally, we determined that 3-nitropropionic acid might interfere with the biosynthesis and transport of L-leucine. Moreover, our study explored the influence of diet on the gut microbial composition of N. viridula, demonstrating that switching to a single-plant diet shifts the abundance of core microbes. In line with this, testing pairwise microbial interactions revealed that core microbiota members support each other and repress the growth of transient microorganisms. With this work, we provide novel insights into the factors shaping the insect gut microbial communities and demonstrate that N. viridula harbours many toxin-degrading bacteria that could support its resistance to plant defences., (© The Author(s) 2024. Published by Oxford University Press on behalf of FEMS.)

Insect herbivores are amongst the most destructive plant pests, damaging both naturally occurring and domesticated plants. As sessile organisms, plants make use of structural and chemical barriers to counteract herbivores. However, over 75% of herbivorous insect species are well adapted to their host's defenses and these specialists are generally difficult to ward off. By actively antagonizing the number of insect eggs deposited on plants, future damage by the herbivore's offspring can be limited. Therefore, it is important to understand which plant traits influence attractiveness for oviposition, especially for specialist insects that are well adapted to their host plants. In this study, we investigated the oviposition preference of Pieris butterflies (Lepidoptera: Pieridae) by offering them the choice between 350 different naturally occurring Arabidopsis accessions. Using a genome-wide association study of the oviposition data and subsequent fine mapping with full genome sequences of 164 accessions, we identified WRKY42 and AOC1 as candidate genes that are associated with the oviposition preference observed for Pieris butterflies. Host plant choice assays with Arabidopsis genotypes impaired in WRKY42 or AOC1 function confirmed a clear role for WRKY42 in oviposition preference of female Pieris butterflies, while for AOC1 the effect was mild. In contrast, WRKY42-impaired plants, which were preferred for oviposition by butterflies, negatively impacted offspring performance. These findings exemplify that plant genotype can have opposite effects on oviposition preference and caterpillar performance. This knowledge can be used for breeding trap crops or crops that are unattractive for oviposition by pest insects., (© The Author(s) 2022. Published by Oxford University Press on behalf of the Society for Experimental Biology.)

In nature, plants are exposed to biotic and abiotic stresses that often occur simultaneously. Therefore, plant responses to combinations of stresses are most representative of how plants respond to stresses. We used RNAseq to assess temporal changes in the transcriptome of Arabidopsis thaliana to herbivory by Pieris rapae caterpillars, either alone or in combination with prior exposure to drought or infection with the necrotrophic fungus Botrytis cinerea. Pre-exposure to drought stress or Botrytis infection resulted in a significantly different timing of the caterpillar-induced transcriptional changes. Additionally, the combination of drought and P. rapae induced an extensive downregulation of A. thaliana genes involved in defence against pathogens. Despite a more substantial growth reduction observed for plants exposed to drought plus P. rapae feeding compared with P. rapae feeding alone, this did not affect weight increase of this specialist caterpillar. Plants respond to combined stresses with phenotypic and transcriptional changes that differ from the single stress situation. The effect of a previous exposure to drought or B. cinerea infection on transcriptional changes to caterpillars is largely overridden by the stress imposed by caterpillars, indicating that plants shift their response to the most recent stress applied., (© 2016 The Authors. New Phytologist © 2016 New Phytologist Trust.)

In nature, plants have to cope with a wide range of stress conditions that often occur simultaneously or in sequence. To investigate how plants cope with multi-stress conditions, we analyzed the dynamics of whole-transcriptome profiles of Arabidopsis thaliana exposed to six sequential double stresses inflicted by combinations of: (i) infection by the necrotrophic fungus Botrytis cinerea, (ii) herbivory by chewing larvae of Pieris rapae, and (iii) drought stress. Each of these stresses induced specific expression profiles over time, in which one-third of all differentially expressed genes was shared by at least two single stresses. Of these, 394 genes were differentially expressed during all three stress conditions, albeit often in opposite directions. When two stresses were applied in sequence, plants displayed transcriptome profiles that were very similar to the second stress, irrespective of the nature of the first stress. Nevertheless, significant first-stress signatures could be identified in the sequential stress profiles. Bioinformatic analysis of the dynamics of co-expressed gene clusters highlighted specific clusters and biological processes of which the timing of activation or repression was altered by a prior stress. The first-stress signatures in second stress transcriptional profiles were remarkably often related to responses to phytohormones, strengthening the notion that hormones are global modulators of interactions between different types of stress. Because prior stresses can affect the level of tolerance against a subsequent stress (e.g. prior herbivory strongly affected resistance to B. cinerea), the first-stress signatures can provide important leads for the identification of molecular players that are decisive in the interactions between stress response pathways., (© 2016 The Authors The Plant Journal © 2016 John Wiley & Sons Ltd.)