Chaoyang Zhao
Fang Zhu
Qian Sun
Xuguo Zhou- 1Center for Medical, Agricultural and Veterinary Entomology, United States Department of Agriculture, Agricultural Research Service, Gainesville, FL, United States
- 2Department of Entomology, Pennsylvania State University, University Park, PA, United States
- 3Department of Entomology, Louisiana State University, Baton Rouge, LA, United States
- 4Department of Entomology, University of Kentucky, Lexington, KY, United States
Editorial on the Research Topic
Mechanisms and Strategies of Arthropod Adaptation to the Chemical Environment
As one of the most successful groups of animals, arthropods have evolved a wide range of adaptive strategies that allow them to live in almost every habitat on Earth (Ledesma et al., 2020). These strategies largely involve in the capabilities of coping with the chemical stresses imposed by their environments, including both biotic and abiotic components, to help them survive and thrive (Korsloot et al., 2004). While the biotic components can be the hosts, predators, parasitoids, and competitors of arthropods, pesticides have become an increasingly prominent abiotic factor owing to their extensive/indispensable use in agricultural and urban environment (Sparks and Nauen, 2015; Gould et al., 2018). Nevertheless, both biotic and abiotic components have been some of the key drivers facilitating the evolution of stress management in arthropods, which include perceiving, processing, and responding to chemical signals at a variety of biological levels (Després et al., 2007; Vilcinskas, 2013; Liu, 2015; van Leeuwen and Dermauw, 2016; Alyokhin and Chen, 2017). This Research Topic is dedicated to this topic and the following four papers have advanced our understanding by examining pertinent hypotheses.
To defend against predators, certain herbivorous arthropods evolve the ability of utilizing toxic chemical compounds produced by their host plants as molecular weapons, a research field that has drawn growing attention in recent years (Petschenka and Agrawal, 2016). Instead of metabolizing them, some arthropods can absorb and accumulate these plant compounds in their body, thereby making themselves toxic or unpalatable to their predators, a phenomenon termed sequestration (Nishida, 2002; Beran and Petschenka, 2022). As one of the best-known examples, the horseradish flea beetle, Phyllotreta armoraciae, a monophagous insect feeding on brassicaceous plants, is able to sequester host-derived glucosinolates to protect itself against predators (Yang et al., 2020). In this Research Topic, Yang et al. further showed that the uptake of glucosinolates mainly occurred at the foregut of P. armoraciae, in contrast to the widely accepted notion that the endodermal midgut is the tissue for hydrophilic compound absorption. According to authors, and as far as we are aware, this is the first report that insects may use their foregut to absorb hydrophilic compounds, laying the ground for understanding the roles foregut may play in insects’ adaptation to the chemical environment.
The metabolism of toxic compounds is another way that arthropods use to survive the natural and synthetic chemicals (Li et al., 2007). Unlike sequestration whose research is still in its infancy, xenobiotic metabolism has been extensively studied, and multiple classes of detoxification enzymes have been identified and functionally characterized, including cytochrome P450 monooxygenases (P450s), glutathione S-transferases (GSTs), carboxylesterases (CarEs), UDP-glucosyltransferases (UGTs), sulfotransferases, and ATP-binding cassette (ABC) transporters (Feyereisen 2012; Zhu et al., 2014; van Leeuwen and Dermauw, 2016; Nauen et al., 2022). Two papers in this issue investigated the mechanisms underlying pesticide detoxifications using the insect pests of public health importance, the housefly, Musca domestica, and the southern house mosquito, Culex quinquefasciatus, respectively. While Gong et al. focused on the role of cytochrome P450 reductase (CPR) as a cofactor of P450s in pesticide metabolism, You et al. examined the diel rhythmic expression of several detoxification genes, including those encoding P450s, GSTs, and CarEs, and discussed how such expression scheme was associated with pesticide susceptibility in these insects.
RNA interference (RNAi) is a gene silencing mechanism that arthropods, as many other life forms, have evolved to circumvent viral infection (Fire et al., 1998; Wilson and Doudna, 2013). This mechanism has been used to develop the strategies for beneficial arthropod protection and pest control (Vogel et al., 2019). The Bayer “SmartStax Pro” maize (Mon87411), the first RNAi transgenic trait, has been recently deregulated in the US, China, and Canada, and this RNAi-based biocontrol product is commercially available to the US farmers, starting 2022 (De Schutter et al., 2022). By allowing the target arthropod pests to ingest double-stranded RNA (dsRNA) molecules that function to silence specific genes, pests are killed or their viability is impaired. However, the efficacy of RNAi can be affected by many factors including the instability of dsRNAs prior to their entry into host cells. The fourth paper by Lei et al. identified and characterized the sole dsRNase gene in the tawny crazy ant, Nylanderia fulva, to improve the silencing efficacy for this emerging invasive pest that spreads rapidly across the southern United States.
Lastly but certainly not least, we are grateful to all authors for contributing their articles and anonymous reviewers, as well as editorial staff for their constructive comments and suggestions. We hope this Research Topic will be of interest to the broad readership of Frontiers in Physiology.
Author Contributions
All authors listed have made a substantial, direct and intellectual contribution to the work, specifically CZ drafted, and FZ, QS, and XZ revised editorial. All authors have approved it for publication.
Author Disclaimer
Mention of trade names or commercial products in this publication is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the US Department of Agriculture.
Conflict of Interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Publisher’s Note
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors, and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.
References
Alyokhin A., Chen Y. H. (2017). Adaptation to Toxic Hosts as a Factor in the Evolution of Insecticide Resistance. Curr. Opin. Insect Sci. 21, 33–38. doi:10.1016/j.cois.2017.04.006
Beran F., Petschenka G. (2022). Sequestration of Plant Defense Compounds by Insects: From Mechanisms to Insect-Plant Coevolution. Annu. Rev. Entomol. 67, 163–180. doi:10.1146/annurev-ento-062821-062319
De Schutter K., Taning C. N. T., Van Daele L., Van Damme E. J. M., Dubruel P., Smagghe G. (2022). RNAi-Based Biocontrol Products: Market Status, Regulatory Aspects, and Risk Assessment. Front. Insect Sci. 1, 818037. doi:10.3389/finsc10.3389/finsc.2021.818037
Després L., David J.-P., Gallet C. (2007). The Evolutionary Ecology of Insect Resistance to Plant Chemicals. Trends Ecol. Evol. 22 (6), 298–307. doi:10.1016/j.tree.2007.02.010
Feyereisen R. (2012). “Insect CYP Genes and P450 Enzymes,” in Insect Molecular Biology and Biochemistry (West Bengal, INDIA: Academic Press), 236–316. doi:10.1016/b978-0-12-384747-8.10008-x
Fire A., Xu S., Montgomery M. K., Kostas S. A., Driver S. E., Mello C. C. (1998). Potent and Specific Genetic Interference by Double-Stranded RNA in Caenorhabditis elegans. nature 391 (6669), 806–811. doi:10.1038/35888
Gould F., Brown Z. S., Kuzma J. (2018). Wicked Evolution: Can We Address the Sociobiological Dilemma of Pesticide Resistance? Science 360 (6390), 728–732. doi:10.1126/science.aar3780
Korsloot A., van Gestel C. A., Van Straalen N. M. (2004). Environmental Stress and Cellular Response in Arthropods. Boca Raton, Florida: CRC Press.
Ledesma E., Jiménez-Valverde A., Baquero E., Jordana R., de Castro A., Ortuño V. M. (2020). Arthropod Biodiversity Patterns point to the Mesovoid Shallow Substratum (MSS) as a Climate Refugium. Zoology 141, 125771. doi:10.1016/j.zool.2020.125771
Li X., Schuler M. A., Berenbaum M. R. (2007). Molecular Mechanisms of Metabolic Resistance to Synthetic and Natural Xenobiotics. Annu. Rev. Entomol. 52, 231–253. doi:10.1146/annurev.ento.51.110104.151104
Liu N. (2015). Insecticide Resistance in Mosquitoes: Impact, Mechanisms, and Research Directions. Annu. Rev. Entomol. 60, 537–559. doi:10.1146/annurev-ento-010814-020828
Nauen R., Bass C., Feyereisen R., Vontas J. (2022). The Role of Cytochrome P450s in Insect Toxicology and Resistance. Annu. Rev. Entomol. 67, 105–124. doi:10.1146/annurev-ento-070621-061328
Nishida R. (2002). Sequestration of Defensive Substances from Plants by Lepidoptera. Annu. Rev. Entomol. 47 (1), 57–92. doi:10.1146/annurev.ento.47.091201.145121
Petschenka G., Agrawal A. A. (2016). How Herbivores Coopt Plant Defenses: Natural Selection, Specialization, and Sequestration. Curr. Opin. Insect Sci. 14, 17–24. doi:10.1016/j.cois.2015.12.004
Sparks T. C., Nauen R. (2015). IRAC: Mode of Action Classification and Insecticide Resistance Management. Pestic. Biochem. Physiol. 121, 122–128. doi:10.1016/j.pestbp.2014.11.014
Van Leeuwen T., Dermauw W. (2016). The Molecular Evolution of Xenobiotic Metabolism and Resistance in Chelicerate Mites. Annu. Rev. Entomol. 61, 475–498. doi:10.1146/annurev-ento-010715-023907
Vilcinskas A. (2013). Evolutionary Plasticity of Insect Immunity. J. Insect Physiol. 59 (2), 123–129. doi:10.1016/j.jinsphys.2012.08.018
Vogel E., Santos D., Mingels L., Verdonckt T. W., Broeck J. V. (2019). RNA Interference in Insects: Protecting Beneficials and Controlling Pests. Front. Physiol. 9, 1912. doi:10.3389/fphys.2018.01912
Wilson R. C., Doudna J. A. (2013). Molecular Mechanisms of RNA Interference. Annu. Rev. Biophys. 42, 217–239. doi:10.1146/annurev-biophys-083012-130404
Yang Z.-L., Kunert G., Sporer T., Körnig J., Beran F. (2020). Glucosinolate Abundance and Composition in Brassicaceae Influence Sequestration in a Specialist Flea Beetle. J. Chem. Ecol. 46 (2), 186–197. doi:10.1007/s10886-020-01144-y
Keywords: arthropod, adaptation, sequestration, pesticide, RNAi
Citation: Zhao C, Zhu F, Sun Q and Zhou X (2022) Editorial: Mechanisms and Strategies of Arthropod Adaptation to the Chemical Environment. Front. Physiol. 13:889757. doi: 10.3389/fphys.2022.889757
Received: 04 March 2022; Accepted: 08 March 2022;
Published: 25 March 2022.
Edited and reviewed by:
Sylvia Anton, Institut National de la Recherche Agronomique (INRA), FranceCopyright © 2022 Zhao, Zhu, Sun and Zhou. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Chaoyang Zhao, zhaochaoyang2009@gmail.com