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7. Drosophila suzukii (Diptera: Drosophilidae): A Decade of Research Towards a Sustainable Integrated Pest Management Program

Author

Tait, Gabriella, primary, Mermer, Serhan, additional, Stockton, Dara, additional, Lee, Jana, additional, Avosani, Sabina, additional, Abrieux, Antoine, additional, Anfora, Gianfranco, additional, Beers, Elizabeth, additional, Biondi, Antonio, additional, Burrack, Hannah, additional, Cha, Dong, additional, Chiu, Joanna C, additional, Choi, Man-Yeon, additional, Cloonan, Kevin, additional, Crava, Cristina M, additional, Daane, Kent M, additional, Dalton, Daniel T, additional, Diepenbrock, Lauren, additional, Fanning, Phillip, additional, Ganjisaffar, Fatemeh, additional, Gómez, Miguel I, additional, Gut, Larry, additional, Grassi, Alberto, additional, Hamby, Kelly, additional, Hoelmer, Kim A, additional, Ioriatti, Claudio, additional, Isaacs, Rufus, additional, Klick, Jimmy, additional, Kraft, Laura, additional, Loeb, Gregory, additional, Rossi-Stacconi, Marco Valerio, additional, Nieri, Rachele, additional, Pfab, Ferdinand, additional, Puppato, Simone, additional, Rendon, Dalila, additional, Renkema, Justin, additional, Rodriguez-Saona, Cesar, additional, Rogers, Mary, additional, Sassù, Fabiana, additional, Schöneberg, Torsten, additional, Scott, Maxwell J, additional, Seagraves, Michael, additional, Sial, Ashfaq, additional, Van Timmeren, Steven, additional, Wallingford, Anna, additional, Wang, Xingeng, additional, Yeh, D Adeline, additional, Zalom, Frank G, additional, and Walton, Vaughn M, additional

Published
2021
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8. Population genomics in the arboviral vectorAedes aegyptireveals the genomic architecture and evolution of endogenous viral elements

Author

Crava, Cristina M., primary, Varghese, Finny S., additional, Pischedda, Elisa, additional, Halbach, Rebecca, additional, Palatini, Umberto, additional, Marconcini, Michele, additional, Gasmi, Leila, additional, Redmond, Seth, additional, Afrane, Yaw, additional, Ayala, Diego, additional, Paupy, Christophe, additional, Carballar‐Lejarazu, Rebeca, additional, Miesen, Pascal, additional, Rij, Ronald P., additional, and Bonizzoni, Mariangela, additional

Published
2021
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11. Population genomics in the arboviral vector Aedes aegypti reveals the genomic architecture and evolution of endogenous viral elements.

Author

Crava, Cristina M., Varghese, Finny S., Pischedda, Elisa, Halbach, Rebecca, Palatini, Umberto, Marconcini, Michele, Gasmi, Leila, Redmond, Seth, Afrane, Yaw, Ayala, Diego, Paupy, Christophe, Carballar‐Lejarazu, Rebeca, Miesen, Pascal, Rij, Ronald P., and Bonizzoni, Mariangela

Subjects
*AEDES aegypti, *RETROVIRUS diseases, *HORIZONTAL gene transfer, *GENOMICS, *MOSQUITOES, *VIRUS diseases
Abstract

Horizontal gene transfer from viruses to eukaryotic cells is a pervasive phenomenon. Somatic viral integrations are linked to persistent viral infection whereas integrations into germline cells are maintained in host genomes by vertical transmission and may be co‐opted for host functions. In the arboviral vector Aedes aegypti, an endogenous viral element from a nonretroviral RNA virus (nrEVE) was shown to produce PIWI‐interacting RNAs (piRNAs) to limit infection with a cognate virus. Thus, nrEVEs may constitute a heritable, sequence‐specific mechanism for antiviral immunity, analogous to piRNA‐mediated silencing of transposable elements. Here, we combine population genomics and evolutionary approaches to analyse the genomic architecture of nrEVEs in A. aegypti. We conducted a genome‐wide screen for adaptive nrEVEs and searched for novel population‐specific nrEVEs in the genomes of 80 individual wild‐caught mosquitoes from five geographical populations. We show a dynamic landscape of nrEVEs in mosquito genomes and identified five novel nrEVEs derived from two currently circulating viruses, providing evidence of the environmental‐dependent modification of a piRNA cluster. Overall, our results show that virus endogenization events are complex with only a few nrEVEs contributing to adaptive evolution in A. aegypti. [ABSTRACT FROM AUTHOR]

Published
2021
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12. Drosophila suzukii(Diptera: Drosophilidae): A Decade of Research Towards a Sustainable Integrated Pest Management Program

Author

Tait, Gabriella, Mermer, Serhan, Stockton, Dara, Lee, Jana, Avosani, Sabina, Abrieux, Antoine, Anfora, Gianfranco, Beers, Elizabeth, Biondi, Antonio, Burrack, Hannah, Cha, Dong, Chiu, Joanna C, Choi, Man-Yeon, Cloonan, Kevin, Crava, Cristina M, Daane, Kent M, Dalton, Daniel T, Diepenbrock, Lauren, Fanning, Phillip, Ganjisaffar, Fatemeh, Gómez, Miguel I, Gut, Larry, Grassi, Alberto, Hamby, Kelly, Hoelmer, Kim A, Ioriatti, Claudio, Isaacs, Rufus, Klick, Jimmy, Kraft, Laura, Loeb, Gregory, Rossi-Stacconi, Marco Valerio, Nieri, Rachele, Pfab, Ferdinand, Puppato, Simone, Rendon, Dalila, Renkema, Justin, Rodriguez-Saona, Cesar, Rogers, Mary, Sassù, Fabiana, Schöneberg, Torsten, Scott, Maxwell J, Seagraves, Michael, Sial, Ashfaq, Van Timmeren, Steven, Wallingford, Anna, Wang, Xingeng, Yeh, D Adeline, Zalom, Frank G, and Walton, Vaughn M

Abstract

Drosophila suzukii(Matsumura) (Diptera: Drosophilidae) also known as spotted-wing drosophila (SWD), is a pest native to Southeast Asia. In the last few decades, the pest has expanded its range to affect all major European and American fruit production regions. SWD is a highly adaptive insect that is able to disperse, survive, and flourish under a range of environmental conditions. Infestation by SWD generates both direct and indirect economic impacts through yield losses, shorter shelf life of infested fruit, and increased production costs. Fresh markets, frozen berries, and fruit export programs have been impacted by the pest due to zero tolerance for fruit infestation. As SWD control programs rely heavily on insecticides, exceedance of maximum residue levels (MRLs) has also resulted in crop rejections. The economic impact of SWD has been particularly severe for organic operations, mainly due to the limited availability of effective insecticides. Integrated pest management (IPM) of SWD could significantly reduce chemical inputs but would require substantial changes to horticultural management practices. This review evaluates the most promising methods studied as part of an IPM strategy against SWD across the world. For each of the considered techniques, the effectiveness, impact, sustainability, and stage of development are discussed.Graphical Abstract

Published
2021
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13. Transcriptome profiling reveals differential gene expression of detoxification enzymes in a hemimetabolous tobacco pest after feeding on jasmonate-silenced Nicotiana attenuata plants

Author

Crava, Cristina M., Brütting, Christoph, and Baldwin, Ian T.

Subjects
Bedbugs, Monosaccharide Transport Proteins, Down-Regulation, Cyclopentanes, Heteroptera, Contig Mapping, Cytochrome P-450 Enzyme System, Plant Growth Regulators, Tobacco, Genetics, Animals, Gene Silencing, Herbivory, Oxylipins, Coyote tobacco, Phylogeny, Glutathione Transferase, Sequence Analysis, RNA, Gene Expression Profiling, Plants, Genetically Modified, Up-Regulation, Inactivation, Metabolic, RNA, Trophic interactions, Piercing-sucking herbivory, Detoxification, Settore AGR/12 - PATOLOGIA VEGETALE, Biotechnology, Research Article
Abstract

Background The evolutionary arms race between plants and insects has driven the co-evolution of sophisticated defense mechanisms used by plants to deter herbivores and equally sophisticated strategies that enable phytophagous insects to rapidly detoxify the plant’s defense metabolites. In this study, we identify the genetic determinants that enable the mirid, Tupiocoris notatus, to feed on its well-defended host plant, Nicotiana attenuata, an outstanding model for plant-insect interaction studies. Results We used an RNAseq approach to evaluate the global gene expression of T. notatus after feeding on a transgenic N. attenuata line which does not accumulate jasmonic acid (JA) after herbivory, and consequently accumulates very low levels of defense metabolites. Using Illumina sequencing, we generated a de novo assembled transcriptome which resulted in 63,062 contigs (putative transcript isoforms) contained in 42,610 isotigs (putative identified genes). Differential expression analysis based on RSEM-estimated transcript abundances identified 82 differentially expressed (DE) transcripts between T. notatus fed on wild-type and the defenseless plants. The same analysis conducted with Corset-estimated transcript abundances identified 59 DE clusters containing 85 transcripts. In both analyses, a larger number of DE transcripts were found down-regulated in mirids feeding on JA-silenced plants (around 70%). Among these down-regulated transcripts we identified seven transcripts possibly involved in the detoxification of N. attenuata defense metabolite, specifically, one glutathione-S-transferase (GST), one UDP-glucosyltransferase (UGT), five cytochrome P450 (P450s), and six serine proteases. Real-time quantitative PCR confirmed the down-regulation for six transcripts (encoding GST, UGT and four P450s) and revealed that their expression was only slightly decreased in mirids feeding on another N. attenuata transgenic line specifically silenced in the accumulation of diterpene glycosides, one of the many classes of JA-mediated defenses in N. attenuata. Conclusions The results provide a transcriptional overview of the changes in a specialist hemimetabolous insect associated with feeding on host plants depleted in chemical defenses. Overall, the analysis reveals that T. notatus responses to host plant defenses are narrow and engages P450 detoxification pathways. It further identifies candidate genes which can be tested in future experiments to understand their role in shaping the T. notatus-N. attenuata interaction. Electronic supplementary material The online version of this article (doi:10.1186/s12864-016-3348-0) contains supplementary material, which is available to authorized users.

Published
2016

19. RNA interference in Lepidoptera : An overview of successful and unsuccessful studies and implications for experimental design

Author

Terenius, Olle, Papanicolaou, Alexie, Garbutt, Jennie S., Eleftherianos, Ioannis, Huvenne, Hanneke, Kanginakudru, Sriramana, Albrechtsen, Merete, An, Chunju, Aymeric, Jean-Luc, Barthel, Andrea, Bebas, Piotr, Bitra, Kavita, Bravo, Alejandra, Chevalier, François, Collinge, Derek P., Crava, Cristina M., de Maagd, Ruud A., Duvic, Bernard, Erlandson, Martin, Faye, Ingrid, Felföldi, Gabriella, Fujiwara, Haruhiko, Futahashi, Ryo, Gandhe, Archana S., Gatehouse, Heather S., Gatehouse, Laurence N., Giebultowicz, Jadwiga M., Gómez, Isabel, Grimmelikhuijzen, Cornelis J. P., Groot, Astrid T., Hauser, Frank, Heckel, David G., Hegedus, Dwayne D., Hrycaj, Steven, Huang, Lihua, Hull, J. Joe, Iatrou, Kostas, Iga, Masatoshi, Kanost, Michael R., Kotwica, Joanna, Li, Changyou, Li, Jianghong, Liu, Jisheng, Lundmark, Magnus, Matsumoto, Shogo, Meyering-Vos, Martina, Millichap, Peter J., Monteiro, Antónia, Mrinal, Nirotpal, Niimi, Teruyuki, Nowara, Daniela, Ohnishi, Atsushi, Oostra, Vicencio, Ozaki, Katsuhisa, Papakonstantinou, Maria, Popadic, Aleksandar, Rajam, Manchikatla V., Saenko, Suzanne, Simpson, Robert M., Soberón, Mario, Strand, Michael R., Tomita, Shuichiro, Toprak, Umut, Wang, Ping, Wee, Choon Wei, Whyard, Steven, Zhang, Wenqing, Nagaraju, Javaregowda, Ffrench-Constant, Richard H., Herrero, Salvador, Gordon, Karl, Swevers, Luc, Smagghe, Guy, Terenius, Olle, Papanicolaou, Alexie, Garbutt, Jennie S., Eleftherianos, Ioannis, Huvenne, Hanneke, Kanginakudru, Sriramana, Albrechtsen, Merete, An, Chunju, Aymeric, Jean-Luc, Barthel, Andrea, Bebas, Piotr, Bitra, Kavita, Bravo, Alejandra, Chevalier, François, Collinge, Derek P., Crava, Cristina M., de Maagd, Ruud A., Duvic, Bernard, Erlandson, Martin, Faye, Ingrid, Felföldi, Gabriella, Fujiwara, Haruhiko, Futahashi, Ryo, Gandhe, Archana S., Gatehouse, Heather S., Gatehouse, Laurence N., Giebultowicz, Jadwiga M., Gómez, Isabel, Grimmelikhuijzen, Cornelis J. P., Groot, Astrid T., Hauser, Frank, Heckel, David G., Hegedus, Dwayne D., Hrycaj, Steven, Huang, Lihua, Hull, J. Joe, Iatrou, Kostas, Iga, Masatoshi, Kanost, Michael R., Kotwica, Joanna, Li, Changyou, Li, Jianghong, Liu, Jisheng, Lundmark, Magnus, Matsumoto, Shogo, Meyering-Vos, Martina, Millichap, Peter J., Monteiro, Antónia, Mrinal, Nirotpal, Niimi, Teruyuki, Nowara, Daniela, Ohnishi, Atsushi, Oostra, Vicencio, Ozaki, Katsuhisa, Papakonstantinou, Maria, Popadic, Aleksandar, Rajam, Manchikatla V., Saenko, Suzanne, Simpson, Robert M., Soberón, Mario, Strand, Michael R., Tomita, Shuichiro, Toprak, Umut, Wang, Ping, Wee, Choon Wei, Whyard, Steven, Zhang, Wenqing, Nagaraju, Javaregowda, Ffrench-Constant, Richard H., Herrero, Salvador, Gordon, Karl, Swevers, Luc, and Smagghe, Guy

Abstract

Gene silencing through RNA interference (RNAi) has revolutionized the study of gene function, particularly in non-model insects. However, in Lepidoptera (moths and butterflies) RNAi has many times proven to be difficult to achieve. Most of the negative results have been anecdotal and the positive experiments have not been collected in such a way that they are possible to analyze. In this review, we have collected detailed data from more than 150 experiments including all to date published and many unpublished experiments. Despite a large variation in the data, trends that are found are that RNAi is particularly successful in the family Saturniidae and in genes involved in immunity. On the contrary, gene expression in epidermal tissues seems to be most difficult to silence. In addition, gene silencing by feeding dsRNA requires high concentrations for success. Possible causes for the variability of success in RNAi experiments in Lepidoptera are discussed. The review also points to a need to further investigate the mechanism of RNAi in lepidopteran insects and its possible connection to the innate immune response. Our general understanding of RNAi in Lepidoptera will be further aided in the future as our public database at http://insectacentral.org/RNAi will continue to gather information on RNAi experiments.

Published
2011
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22. The Evolution of Olfactory Gene Families in Drosophila and the Genomic Basis of chemical-Ecological Adaptation in Drosophila suzukii.

Author

Ramasamy, Sukanya, Ometto, Lino, Crava, Cristina M., Revadi, Santosh, Kaur, Rupinder, Horner, David S., Pisani, Davide, Dekker, Teun, Anfora, Gianfranco, and Rota-Stabelli, Omar

Subjects
INSECT olfactory receptors, DROSOPHILA evolution, DROSOPHILA genetics, INSECT phylogeny, DROSOPHILA suzukii
Abstract

How the evolution of olfactory genes correlates with adaption to new ecological niches is still a debated topic. We explored this issue in Drosophila suzukii, an emerging model that reproduces on fresh fruit rather than in fermenting substrates like most other Drosophila. We first annotated the repertoire of odorant receptors (ORs), odorant binding proteins (OBPs), and antennal ionotropic receptors (aIRs) in the genomes of two strains of D. suzukii and of its close relative Drosophila biarmipes. We then analyzed these genes on the phylogeny of 14 Drosophila species: whereas ORs and OBPs are characterized by higher turnover rates in some lineages including D. suzukii, aIRs are conserved throughout the genus. Drosophila suzukii is further characterized by a non-random distribution of OR turnover on the gene phylogeny, consistent with a change in selective pressures. In D. suzukii, we found duplications and signs of positive selection in ORs with affinity for short-chain esters, and loss of function of ORs with affinity for volatiles produced during fermentation. These receptors--Or85a and Or22a--are characterized by divergent alleles in the European and American genomes, and we hypothesize that they may have been replaced by some of the duplicated ORs in corresponding neurons, a hypothesis reciprocally confirmed by electrophysiological recordings. Our study quantifies the evolution of olfactory genes in Drosophila and reveals an array of genomic events that can be associated with the ecological adaptations of D. suzukii. [ABSTRACT FROM AUTHOR]

Published
2016
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23. RNA interference in Lepidoptera: An overview of successful and unsuccessful studies and implications for experimental design

Author

Terenius, Olle, primary, Papanicolaou, Alexie, additional, Garbutt, Jennie S., additional, Eleftherianos, Ioannis, additional, Huvenne, Hanneke, additional, Kanginakudru, Sriramana, additional, Albrechtsen, Merete, additional, An, Chunju, additional, Aymeric, Jean-Luc, additional, Barthel, Andrea, additional, Bebas, Piotr, additional, Bitra, Kavita, additional, Bravo, Alejandra, additional, Chevalier, François, additional, Collinge, Derek P., additional, Crava, Cristina M., additional, de Maagd, Ruud A., additional, Duvic, Bernard, additional, Erlandson, Martin, additional, Faye, Ingrid, additional, Felföldi, Gabriella, additional, Fujiwara, Haruhiko, additional, Futahashi, Ryo, additional, Gandhe, Archana S., additional, Gatehouse, Heather S., additional, Gatehouse, Laurence N., additional, Giebultowicz, Jadwiga M., additional, Gómez, Isabel, additional, Grimmelikhuijzen, Cornelis J.P., additional, Groot, Astrid T., additional, Hauser, Frank, additional, Heckel, David G., additional, Hegedus, Dwayne D., additional, Hrycaj, Steven, additional, Huang, Lihua, additional, Hull, J. Joe, additional, Iatrou, Kostas, additional, Iga, Masatoshi, additional, Kanost, Michael R., additional, Kotwica, Joanna, additional, Li, Changyou, additional, Li, Jianghong, additional, Liu, Jisheng, additional, Lundmark, Magnus, additional, Matsumoto, Shogo, additional, Meyering-Vos, Martina, additional, Millichap, Peter J., additional, Monteiro, Antónia, additional, Mrinal, Nirotpal, additional, Niimi, Teruyuki, additional, Nowara, Daniela, additional, Ohnishi, Atsushi, additional, Oostra, Vicencio, additional, Ozaki, Katsuhisa, additional, Papakonstantinou, Maria, additional, Popadic, Aleksandar, additional, Rajam, Manchikatla V., additional, Saenko, Suzanne, additional, Simpson, Robert M., additional, Soberón, Mario, additional, Strand, Michael R., additional, Tomita, Shuichiro, additional, Toprak, Umut, additional, Wang, Ping, additional, Wee, Choon Wei, additional, Whyard, Steven, additional, Zhang, Wenqing, additional, Nagaraju, Javaregowda, additional, ffrench-Constant, Richard H., additional, Herrero, Salvador, additional, Gordon, Karl, additional, Swevers, Luc, additional, and Smagghe, Guy, additional

Published
2011
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25. Non-retroviral Endogenous Viral Elements in Tephritid Fruit Flies Reveal Former Viral Infections Not Related to Known Circulating Viruses.

Author

Hernández-Pelegrín L, Ros VID, Herrero S, and Crava CM

Subjects
Animals, RNA, Small Interfering genetics, RNA, Small Interfering metabolism, Viruses genetics, RNA Viruses genetics, Virus Diseases, Diptera
Abstract

A wide variety of insect-specific non-retroviral RNA viruses specifically infect insects. During viral infection, fragments of viral sequences can integrate into the host genomes creating non-retroviral endogenous viral elements (nrEVEs). Although the exact function of nrEVEs is so far unknown, some studies suggest that nrEVEs may interfere with virus replication by producing PIWI-interacting RNAs (piRNAs) that recognize and degrade viral RNAs through sequence complementarity. In this article, we identified the nrEVEs repertoire of ten species within the dipteran family Tephritidae (true fruit flies), which are considered a major threat to agriculture worldwide. Our results suggest that each of these species contains nrEVEs, although in limited numbers, and that nrEVE integration may have occurred both before and after speciation. Furthermore, the majority of nrEVEs originated from viruses with negative single-stranded RNA genomes and represent structural viral functions. Notably, these nrEVEs exhibit low similarity to currently known circulating viruses. To explore the potential role of nrEVEs, we investigated their transcription pattern and the production of piRNAs in different tissues of Ceratitis capitata. We successfully identified piRNAs that are complementary to the sequence of one nrEVE in C. capitata, thereby highlighting a potential link between nrEVEs and the piRNA pathway. Overall, our results provide valuable insights into the comparative landscape of nrEVEs in true fruit flies, contributing to the understanding of the intimate relation between fruit flies and their past and present viral pathogens., (© 2023. The Author(s).)

Published
2023
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26. Evolutionary Insights into Taste Perception of the Invasive Pest Drosophila suzukii.

Author

Crava CM, Ramasamy S, Ometto L, Anfora G, and Rota-Stabelli O

Subjects
Animals, Computational Biology methods, Drosophila classification, Drosophila Proteins genetics, Gene Duplication, Gene Expression Regulation, Genome, Insect, Genomics methods, Molecular Sequence Annotation, Phylogeny, Selection, Genetic, Biological Evolution, Drosophila physiology, Taste Perception genetics
Abstract

Chemosensory perception allows insects to interact with the environment by perceiving odorant or tastant molecules; genes encoding chemoreceptors are the molecular interface between the environment and the insect, and play a central role in mediating its chemosensory behavior. Here, we explore how the evolution of these genes in the emerging pest Drosophila suzukii correlates with the peculiar ecology of this species. We annotated approximately 130 genes coding for gustatory receptors (GRs) and divergent ionotropic receptors (dIRs) in D. suzukii and in its close relative D. biarmipes We then analyzed the evolution, in terms of size, of each gene family as well of the molecular evolution of the genes in a 14 Drosophila species phylogenetic framework. We show that the overall evolution of GRs parallels that of dIRs not only in D. suzukii, but also in all other analyzed Drosophila Our results reveal an unprecedented burst of gene family size in the lineage leading to the suzukii subgroup, as well as genomic changes that characterize D. suzukii, particularly duplications and strong signs of positive selection in the putative bitter-taste receptor GR59d. Expression studies of duplicate genes in D. suzukii support a spatio-temporal subfunctionalization of the duplicate isoforms. Our results suggest that D. suzukii is not characterized by gene loss, as observed in other specialist Drosophila species, but rather by a dramatic acceleration of gene gains, compatible with a highly generalist feeding behavior. Overall, our analyses provide candidate taste receptors specific for D. suzukii that may correlate with its specific behavior, and which may be tested in functional studies to ultimately enhance its control in the field., (Copyright © 2016 Crava et al.)

Published
2016
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