Chaymaa Riahi

Plant-herbivore interactions are embedded within complex ecological networks in which microorganisms associated with either partner can reshape interactions across trophic levels. Yet how microbial infections of herbivorous insects alter the molecular signals they deliver to plants remains largely unexplored. Here, we identify REPAT proteins as key molecular mediators linking microbial infection in caterpillars to plant defense responses. Comparative genomic analyses revealed that REPATs comprise an insect protein family that has expanded in Lepidoptera, with a conserved β-REPAT lineage and rapidly diversifying α- and γ-REPAT lineages, the latter encompassing most REPATs previously implicated in plant interactions. Proteomic analyses of caterpillar oral secretions revealed that viruses with contrasting infection strategies exerted opposite effects on REPAT abundance. Infection with the lethal baculovirus Spodoptera exigua multiple nucleopolyhedrovirus (SeMNPV) increased the abundance of multiple REPAT proteins, whereas infection with the persistent, covert iflavirus Spodoptera exigua iflavirus 1 (SeIV1) consistently reduced REPAT abundance across dietary conditions. These changes were associated with reciprocal effects on plant defense: herbivory by SeMNPV-infected larvae attenuated jasmonate-associated responses in tomato, whereas SeIV1-infected larvae enhanced defense activation in pepper. Together, our findings reveal that viral infection of the herbivore can propagate across trophic levels and reshape plant responses to herbivory by altering the repertoire of effectors delivered during feeding, uncovering a mechanism through which insect-microbe interactions can influence plant defense.

Whitefly-transmitted viruses are one of the biggest threats to tomato ( Solanum lycopersicum) growing worldwide. Strategies based on the introgression of resistance traits from wild relatives are promoted to control tomato pests and diseases. Recently, a trichome-based resistance characterizing the wild species Solanum pimpinellifolium was introgressed into a cultivated tomato. An advanced backcross line (BC₅S₂) exhibiting the presence of acylsugar-associated type IV trichomes, which are lacking in cultivated tomatoes, was effective at controlling whiteflies (Hemiptera: Aleyrodidae) and limiting the spread of whitefly-transmitted viruses. However, at early growth stages, type IV trichome density and acylsugar production are limited; thus, protection against whiteflies and whitefly-transmitted viruses remains irrelevant. In this work, we demonstrate that young BC₅S₂ tomato plants feeding-punctured by the zoophytophagous predator Nesidiocoris tenuis (Hemiptera: Miridae) displayed an increase (above 50%) in type IV trichome density. Acylsugar production was consistently increased in N. tenuis-punctured BC₅S₂ plants, which was more likely associated with upregulated expression of the BCKD-E2 gene related to acylsugar biosynthesis. In addition, the infestation of BC₅S₂ plants with N. tenuis effectively induced the expression of defensive genes involved in the jasmonic acid signaling pathway, resulting in strong repellence to Bemisia tabaci and attractiveness to N. tenuis. Thus, through preplant release of N. tenuis in tomato nurseries carried out in some integrated pest management programs, type IV trichome-expressing plants can be prepared to control whiteflies and whitefly-transmitted viruses at early growth stages. This study emphasizes the advantage of reinforcing constitutive resistance using defense inducers to guarantee robust protection against pests and transmitted viruses.

Plant essential oils (PEOs) are being studied as a potential alternative to synthetic pesticides in agriculture. PEOs have the potential to control pests both directly, by being toxic or repellent to pests, and indirectly, by activating plant’s defense mechanisms. In this study, the effectiveness of five PEOs (Achillea millefolium, Allium sativum, Rosmarinus officinallis, Tagetes minuta, and Thymus zygis) on controlling Tuta absoluta and their impact on the predator Nesidiocoris tenuis was examined. The study revelead that PEOs from A. millefolium and A. sativum-sprayed plants significantly reduced the number of T. absoluta-infested leaflets and did not affect the establishment and reproduction of N. tenuis. Additionally, the spraying of A. millefolium and A. sativum increased the expression of defense genes in the plants, triggering the release of herbivory-induced plant volatiles (HIPVs), such as C6 green leaf volatiles, monoterpenes, and aldehydes, which can be messengers in tritrophic interactions. The results suggest that PEOs from A. millefolium and A. sativum can provide a dual benefit for controlling arthropod pests, as they can directly exhibit toxicity against these pests while also activating plant defense mechanisms. Overall, this study provides new insights into using PEOs as a sustainable solution for controlling pests and diseases in agriculture, by reducing synthetic pesticides and promoting the use of natural predators.

Insect herbivory activates plant defense mechanisms and releases a blend of herbivore-induced plant volatiles (HIPVs). These volatile compounds may be involved in plant-plant communication and induce defense response in undamaged plants. In this work, we investigated whether the exposure of sweet pepper plants to HIPVs [(Z)-3-hexenol, (Z)-3-hexenyl acetate, (Z)-3-hexenyl propanoate, (Z)-3-hexenyl butanoate, hexyl butanoate, methyl salicylate and methyl jasmonate] activates the sweet pepper immune defense system. For this, healthy sweet pepper plants were individually exposed to the each of the above mentioned HIPVs over 48 h. The expression of jasmonic acid and salicylic acid related genes was quantified. Here, we show that all the tested volatiles induced plant defenses by upregulating the jasmonic acid and salicylic acid signaling pathway. Additionally, the response of Frankliniella occidentalis, a key sweet pepper pest, and Orius laevigatus, the main natural enemy of F. occidentalis, to HIPV-exposed sweet pepper plants were studied in a Y-tube olfactometer. Only plants exposed to (Z)-3-hexenyl propanoate and methyl salicylate repelled F. occidentalis whereas O. laevigatus showed a strong preference to plants exposed to (Z)-3-hexenol, (Z)-3-hexenyl propanoate, (Z)-3-hexenyl butanoate, methyl salicylate and methyl jasmonate. Our results show that HIPVs act as elicitors to sweet pepper plant defenses by enhancing defensive signaling pathways. We anticipate our results to be a starting point for integrating HIPVs-based approaches in sweet pepper pest management systems which may provide a sustainable strategy to manage insect pests in horticultural plants.

In recent years, the use of predatory mirid bugs (Hemiptera: Miridae) in horticultural crops has increased considerably. Mirid bugs are zoophytophagous predators, that is, they display omnivorous behavior and feed on both plants and arthropods. Mirid bugs feed effectively on a wide range of prey, such as whiteflies, lepidopteran eggs and mites. In addition, the phytophagous behavior of mirid bugs can activate defenses in the plants on which they feed. Despite the positive biological attributes, their use still presents some constraints. Their establishment and retention on the crop is not always easy and economic plant damage can be caused by some mirid species. In this review, the current strategies for using zoophytophagous mirid bugs in horticultural crops, mainly Nesidiocoris tenuis, Macrolophus pygmaeus and Dicyphus hesperus, are reviewed. We discuss six different approaches which, in our opinion, can optimize the efficacy of mirids as biocontrol agents and help expand their use into more areas worldwide. In this review we (i) highlight the large number of species and biotypes which are yet to be described and explore their applicability, (ii) present how it is possible to take advantage of the mirid‐induced plant defenses to improve pest management, (iii) argue that genetic selection of improved mirid strains is feasible, (iv) explore the use of companion plants and the use of alternative foods to improve the mirid bug management, and finally (vi) discuss strategies for the expansion of mirid bugs as biological control agents to horticultural crops other than just tomatoes. © 2020 Society of Chemical Industry

Cultivated melon was domesticated from wild melons, which produce small fruits with non-edible fruit flesh. The increase in fruit flesh is one of the major domestication achievements in this species. In previous work, a quantitative trait locus (QTL) on chromosome 6 (paqt6.1) linked to fruit flesh content was detected in a cross between cultivated (“Piel de Sapo”, PS) and wild (Ames 24294, TRI) accessions. The QTL was introgressed into the PS background, generating the TRI_6-3 introgression line (IL) that confirmed the effects of paqt6.1. The primary objective of this work was to fine-map paqt6.1 as the first step for the map-based cloning. Two different approaches were carried out; however, the results were not consistent, precluding the fine mapping of paqt6.1. TRI_6-3 and other related ILs were genotyped by genotyping-by-sequencing, finding additional introgressions in other chromosomes. In an F₂ population from TRI_6-3-x-PS, we found an epistatic interaction between paqt6.1 and another locus on chromosome 11. The interaction was verified in advanced populations, suggesting that the effects of paqt6.1 are conditioned by the allelic composition at another locus in chromosome 11. Both loci should have TRI alleles to reduce the flesh content in the PS background. The implications on the history of melon domestication are discussed.