Plant Manipulation by Insects: Galls, Green Islands, and More

A special issue of Insects (ISSN 2075-4450).

Deadline for manuscript submissions: closed (31 July 2024) | Viewed by 7273

Special Issue Editors


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Guest Editor
Department of Biology, San Francisco State University, San Francisco, CA 94132, USA
Interests: population and community ecology; quantitative ecology; plant–insect interactions; gall induction; host–plant manipulation by insects

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Guest Editor
Department of Food and Life Sciences, Ibaraki University, Ami, Ibaraki 300‑0393, Japan
Interests: phytohormones; bioactive substances; gall induction; biosynthesis

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Guest Editor
Institut de Recherche sur la Biologie de l’Insecte (IRBI), UMR 7261 CNRS-Université de Tours, Avenue Monge, Faculté des Sciences et Techniques, Parc Grandmont, 37200 Tours, France
Interests: plant–insect–microbe interactions; gall–inducing insects; leaf–miners; plant manipulation; effectors; symbionts

Special Issue Information

Dear Colleagues,

The induction of plant galls and green islands may be the most spectacular examples of how insects manipulate plants. Even processes as simple as insect feeding behaviors have also been shown to alter plants in ways that benefit insects. However, recent evidence suggests that broad-scale manipulation of plants by insects occurs in more subtle ways that can lead to modulation of plant defenses, manipulation of stomata leading to increased moisture content, higher leaf temperatures, and reduced emission of volatile organic compounds, and the alteration of nutrient partitioning within plants via the formation of mobilizing sinks. Small molecule effectors such as cytokinins (CKs) and indole-acetic acid (IAA), secreted effector proteins and peptides, and microbial symbionts have been shown to be used by insects to manipulate plants. Research to understand more comprehensively how insects and their secretions impact the physiology, biochemistry, and gene expression of plants is in its infancy but will require an expanded toolbox of biochemical, immunohistochemical, and molecular approaches along with increased genetic resources for non-model organisms to expand our understanding. Since some reprogramming species are important pests, discovering also how plant reprogramming impacts the ecology and evolution of biotic interactions and how they can be disrupted will benefit agriculture and forestry.

Prof. Dr. Edward F. Connor
Prof. Dr. Yoshihito Suzuki
Dr. David Giron
Guest Editors

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Keywords

  • modulation of plant defense by insects
  • secreted effectors
  • phytohormones
  • effector proteins
  • microbial symbionts
  • mobilizing sinks

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Published Papers (3 papers)

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Research

13 pages, 1666 KiB  
Article
New Gall-Forming Insect Model, Smicronyx madaranus: Critical Stages for Gall Formation, Phylogeny, and Effectiveness of Gene Functional Analysis
by Ryo Ushima, Ryoma Sugimoto, Yota Sano, Hinako Ogi, Ryuichiro Ino, Hiroshi Hayakawa, Keisuke Shimada and Tsutomu Tsuchida
Insects 2024, 15(1), 63; https://doi.org/10.3390/insects15010063 - 16 Jan 2024
Viewed by 2250
Abstract
The molecular mechanisms underlying insect gall formation remain unclear. A major reason for the inability to identify the responsible genes is that only a few systems can be experimentally validated in the laboratory. To overcome these problems, we established a new galling insect [...] Read more.
The molecular mechanisms underlying insect gall formation remain unclear. A major reason for the inability to identify the responsible genes is that only a few systems can be experimentally validated in the laboratory. To overcome these problems, we established a new galling insect model, Smicronyx madaranus. Our manipulation experiments using nail polish sealing and insecticide treatment revealed an age-dependent change in gall formation by S. madaranus; adult females and larvae are responsible for gall induction and enlargement, respectively. Furthermore, it has been suggested that substances released during oviposition and larval feeding are involved in each process. Phylogenetic analysis showed that gall-forming weevils, including S. madaranus, belong to two distinct lineages that utilize different host plants. This may indicate that gall-forming traits evolved independently in these Smicronyx lineages. The efficacy of RNA interference (RNAi) in S. madaranus was confirmed by targeting the multicopper oxidase 2 gene. It is expected that the mechanisms of gall formation will be elucidated by a comprehensive functional analysis of candidate genes using RNAi and the S. madaranus galling system in the near future. Full article
(This article belongs to the Special Issue Plant Manipulation by Insects: Galls, Green Islands, and More)
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14 pages, 3626 KiB  
Article
Conferring High IAA Productivity on Low-IAA-Producing Organisms with PonAAS2, an Aromatic Aldehyde Synthase of a Galling Sawfly, and Identification of Its Inhibitor
by Takeshi Hiura, Hibiki Yoshida, Umi Miyata, Tadao Asami and Yoshihito Suzuki
Insects 2023, 14(7), 598; https://doi.org/10.3390/insects14070598 - 2 Jul 2023
Cited by 1 | Viewed by 1331
Abstract
Gall-inducing insects often contain high concentrations of phytohormones, such as auxin and cytokinin, which are suggested to be involved in gall induction, but no conclusive evidence has yet been obtained. There are two possible approaches to investigating the importance of phytohormones in gall [...] Read more.
Gall-inducing insects often contain high concentrations of phytohormones, such as auxin and cytokinin, which are suggested to be involved in gall induction, but no conclusive evidence has yet been obtained. There are two possible approaches to investigating the importance of phytohormones in gall induction: demonstrating either that high phytohormone productivity can induce gall-inducing ability in non-gall-inducing insects or that the gall-inducing ability is inhibited when phytohormone productivity in galling insects is suppressed. In this study, we show that the overexpression of PonAAS2, which encodes an aromatic aldehyde synthase (AAS) responsible for the rate-limiting step in indoleacetic acid (IAA) biosynthesis in a galling sawfly (Pontania sp.) that contains high levels of endogenous IAA, conferred high IAA productivity on Caenorhabditis elegans, as the model system. This result strongly suggests that PonAAS2 can also confer high IAA productivity on low-IAA-producing insects. We also successfully identified an inhibitor of PonAAS2 in a chemical library. This highly selective inhibitor showed stronger inhibitory activity against AAS than against aromatic amino acid decarboxylase, which belongs to the same superfamily as AAS. We also confirm that this inhibitor clearly inhibited IAA productivity in the high-IAA-producing C. elegans engineered here. Full article
(This article belongs to the Special Issue Plant Manipulation by Insects: Galls, Green Islands, and More)
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15 pages, 1720 KiB  
Article
Abscisic Acid: A Potential Secreted Effector Synthesized by Phytophagous Insects for Host-Plant Manipulation
by Stephannie Seng, Gabriela E. Ponce, Peter Andreas, Anna Kisiala, Rosemarie De Clerck-Floate, Donald G. Miller III, Ming-Shun Chen, Peter W. Price, John F. Tooker, R. J. Neil Emery and Edward F. Connor
Insects 2023, 14(6), 489; https://doi.org/10.3390/insects14060489 - 24 May 2023
Cited by 3 | Viewed by 2788
Abstract
Abscisic acid (ABA) is an isoprenoid-derived plant signaling molecule involved in a wide variety of plant processes, including facets of growth and development as well as responses to abiotic and biotic stress. ABA had previously been reported in a wide variety of animals, [...] Read more.
Abscisic acid (ABA) is an isoprenoid-derived plant signaling molecule involved in a wide variety of plant processes, including facets of growth and development as well as responses to abiotic and biotic stress. ABA had previously been reported in a wide variety of animals, including insects and humans. We used high-performance liquid chromatography-electrospray ionization tandem mass spectrometry (HPLC-(ESI)-MS/MS) to examine concentrations of ABA in 17 species of phytophagous insects, including gall- and non-gall-inducing species from all insect orders with species known to induce plant galls: Thysanoptera, Hemiptera, Lepidoptera, Coleoptera, Diptera, and Hymenoptera. We found ABA in insect species in all six orders, in both gall-inducing and non-gall-inducing species, with no tendency for gall-inducing insects to have higher concentrations. The concentrations of ABA in insects often markedly exceeded those typically found in plants, suggesting it is highly improbable that insects obtain all their ABA from their host plant via consumption and sequestration. As a follow-up, we used immunohistochemistry to determine that ABA localizes to the salivary glands in the larvae of the gall-inducing Eurosta solidaginis (Diptera: Tephritidae). The high concentrations of ABA, combined with its localization to salivary glands, suggest that insects are synthesizing and secreting ABA to manipulate their host plants. The pervasiveness of ABA among both gall- and non-gall-inducing insects and our current knowledge of the role of ABA in plant processes suggest that insects are using ABA to manipulate source-sink mechanisms of nutrient allocation or to suppress host-plant defenses. ABA joins the triumvirate of phytohormones, along with cytokinins (CKs) and indole-3-acetic acid (IAA), that are abundant, widespread, and localized to glandular organs in insects and used to manipulate host plants. Full article
(This article belongs to the Special Issue Plant Manipulation by Insects: Galls, Green Islands, and More)
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