Genome-Wide Identification, Evolution, and Female-Biased Expression Analysis of Odorant Receptors in Tuta absoluta (Lepidoptera: Gelechiidae)

The tomato leafminer, Tuta absoluta (Lepidoptera: Gelechiidae), is a highly destructive invasive pest targeting Solanaceae crops. Its olfactory system plays a crucial role in host location, mate finding, and other behavioral activities. However, there is a notable gap in the literature regarding the characterization of its chemosensory genes. In this study, we conducted a genome-wide identification of 58 odorant receptors (ORs) of T. absoluta. The identified ORs exhibit coding sequence (CDS) lengths ranging from 1062 bp to 1419 bp, encoding proteins of 354 to 473 amino acids. Gene structure analysis showed that the majority of these ORs consist of five, seven, eight, or nine exons, collectively representing 67% of the total ORs identified. Through chromosomal mapping, we identified several tandemly duplicate genes, including TabsOR12a, TabsOR12b, TabsOR12c, TabsOR21a, TabsOR21b, TabsOR34a, TabsOR34b, TabsOR34c, TabsOR62a, and TabsOR62b. The phylogenetic analysis indicated that six TabsORs were clustered within the lepidopteran sex pheromone receptor clade, while an expansion clade containing ten TabsORs resulted from tandem duplication events. Additionally, five TabsORs were classified into a specific OR clade in T. absoluta. Furthermore, through RNA-Seq and RT-qPCR analyses, we identified five TabsORs (TabsOR21a, TabsOR26a, TabsOR34a, TabsOR34c, and TabsOR36) exhibiting female-antennae-biased expression. Our study provides a valuable foundation to further investigations into the molecular and ecological functions of TabsORs, particularly in relation to oviposition behavior. These findings provide foundational data for the future exploration of the functions of female-biased expression OR genes in T. absoluta, thereby facilitating the further development of eco-friendly attract-and-kill techniques for the prevention and control of T. absoluta.

[1]  Szu-Chieh Wang,et al.  Decoding the genome of bloodsucking midge Forcipomyia taiwana (diptera: Ceratopogonidae): Insights into odorant receptor expansion. , 2024, Insect biochemistry and molecular biology.

[2]  Xiao-Jing Jiang,et al.  Identification of an adult attractant for Anomala corpulenta by the reverse chemical ecology approach , 2024, Journal of Pest Science.

[3]  Shuai Zhang,et al.  Circabidian rhythm of sex pheromone reception in a scarab beetle , 2024, Current Biology.

[4]  B. Berg,et al.  A female-specific odorant receptor mediates oviposition deterrence in the moth Helicoverpa armigera , 2023, Current Biology.

[5]  Yang Liu,et al.  Evolutionary shifts in pheromone receptors contribute to speciation in four Helicoverpa species , 2023, Cellular and Molecular Life Sciences.

[6]  Y. Liu,et al.  A chromosome-level genome assembly of tomato pinworm, Tuta absoluta , 2023, Scientific data.

[7]  Zhumei Ren,et al.  Genome-wide identification and characterization of the chemosensory relative protein genes in Rhus gall aphid Schlechtendalia chinensis , 2023, BMC Genomics.

[8]  Guirong Wang,et al.  Genome-Wide Analysis of the Odorant Receptor Gene Family in Solenopsis invicta, Ooceraea biroi, and Monomorium pharaonis (Hymenoptera: Formicidae) , 2023, International journal of molecular sciences.

[9]  Ling-Qiao Huang,et al.  Sex pheromone communication in an insect parasitoid, Campoletis chlorideae Uchida , 2022, Proceedings of the National Academy of Sciences of the United States of America.

[10]  B. Hansson,et al.  Sex- and tissue-specific expression of chemosensory receptor genes in a hawkmoth , 2022, Frontiers in Ecology and Evolution.

[11]  S. Mohamed,et al.  Electroantennogram and machine learning reveal a volatile blend mediating avoidance behavior by Tuta absoluta females to a wild tomato plant , 2022, Scientific Reports.

[12]  S. Dong,et al.  Identification and sex expression profiles of olfactory-related genes in Mythimna loreyi based on antennal transcriptome analysis , 2022, Journal of Asia-Pacific Entomology.

[13]  Bin Chen,et al.  Genome-wide identification and expression profiling of odorant receptor genes in the malaria vector Anophelessinensis , 2022, Parasites & vectors.

[14]  T. Zhao,et al.  Screening for odorant receptor genes expressed in Aedes aegypti involved in host-seeking, blood-feeding and oviposition behaviors , 2022, Parasites & Vectors.

[15]  J. Gershenzon,et al.  Competing beetles attract egg laying in a hawkmoth , 2022, Current Biology.

[16]  Jin-ming Zhang,et al.  Comprehensive Metabolome and Volatilome Analyses in Eggplant and Tomato Reveal Their Differential Responses to Tuta absoluta Infestation , 2021, Frontiers in Plant Science.

[17]  Zhen Tian,et al.  Reverse chemical ecology guides the screening for Grapholita molesta pheromone synergists. , 2021, Pest management science.

[18]  Wenjia Yang,et al.  Outbreak of the South American tomato leafminer, Tuta absoluta, in the Chinese mainland: geographic and potential host range expansion. , 2021, Pest management science.

[19]  Manqun Wang,et al.  Discovery of behaviorally active semiochemicals in Aenasius bambawalei using a reverse chemical ecology approach. , 2021, Pest management science.

[20]  Jinjun Wang,et al.  Comparative transcriptomic analysis reveals female-biased olfactory genes potentially involved in plant volatile-mediated oviposition behavior of Bactrocera dorsalis , 2021, BMC Genomics.

[21]  Jin Zhang,et al.  Odorant Receptors for Detecting Flowering Plant Cues Are Functionally Conserved across Moths and Butterflies , 2020, Molecular biology and evolution.

[22]  H. Machekano,et al.  Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) on the “Offensive” in Africa: Prospects for Integrated Management Initiatives , 2020, Insects.

[23]  M. Knaden,et al.  The Molecular Basis of Host Selection in a Crucifer-Specialized Moth , 2020, Current Biology.

[24]  Sara E. Miller,et al.  Expansion and Accelerated Evolution of 9-Exon Odorant Receptors in Polistes Paper Wasps , 2020, bioRxiv.

[25]  P. Neumann,et al.  Gene Expression and Functional Analyses of Odorant Receptors in Small Hive Beetles (Aethina tumida) , 2020, International journal of molecular sciences.

[26]  Jun-feng Dong,et al.  A moth odorant receptor highly expressed in the ovipositor is involved in detecting host-plant volatiles , 2020, eLife.

[27]  Xianru Guo,et al.  Nonanal modulates oviposition preference in female Helicoverpa assulta (Lepidoptera: Noctuidae) via the activation of peripheral neurons , 2020, Pest management science.

[28]  Youzhong Guo,et al.  Functional Characterization of Sex Pheromone Receptors in the Fall Armyworm (Spodoptera frugiperda) , 2020, Insects.

[29]  Han Wu,et al.  An odorant receptor and glomerulus responding to farnesene in Helicoverpa assulta (Lepidoptera: Noctuidae). , 2019, Insect biochemistry and molecular biology.

[30]  Qi Wang,et al.  Functional characterization of one sex pheromone receptor (AlucOR4) in Apolygus lucorum (Meyer-Dür). , 2019, Journal of insect physiology.

[31]  Wei Fan,et al.  A chromosome-level genome assembly of Cydia pomonella provides insights into chemical ecology and insecticide resistance , 2019, Nature Communications.

[32]  Steven L Salzberg,et al.  Graph-based genome alignment and genotyping with HISAT2 and HISAT-genotype , 2019, Nature Biotechnology.

[33]  R. Nauen,et al.  Insecticide resistance in the tomato pinworm Tuta absoluta: patterns, spread, mechanisms, management and outlook , 2019, Journal of Pest Science.

[34]  A. C. Melo,et al.  Reverse chemical ecology-based approach leading to the accidental discovery of repellents for Rhodnius prolixus, a vector of Chagas diseases refractory to DEET. , 2018, Insect biochemistry and molecular biology.

[35]  J.‐F. Dong,et al.  An odorant receptor mediates the attractiveness of cis‐jasmone to Campoletis chlorideae, the endoparasitoid of Helicoverpa armigera , 2018, Insect molecular biology.

[36]  P. Milonas,et al.  Electrophysiological and Oviposition Responses of Tuta absoluta Females to Herbivore-Induced Volatiles in Tomato Plants , 2018, Journal of Chemical Ecology.

[37]  P. Gregg,et al.  Advances in Attract-and-Kill for Agricultural Pests: Beyond Pheromones. , 2018, Annual review of entomology.

[38]  N. Desneux,et al.  Ecology, Worldwide Spread, and Management of the Invasive South American Tomato Pinworm, Tuta absoluta: Past, Present, and Future. , 2018, Annual review of entomology.

[39]  Y. Choo,et al.  Reverse chemical ecology approach for the identification of an oviposition attractant for Culex quinquefasciatus , 2018, Proceedings of the National Academy of Sciences.

[40]  Ming Wen,et al.  Molecular basis of peripheral olfactory sensing during oviposition in the behavior of the parasitic wasp Anastatus japonicus. , 2017, Insect biochemistry and molecular biology.

[41]  B. Hansson,et al.  Functional evolution of Lepidoptera olfactory receptors revealed by deorphanization of a moth repertoire , 2017, Nature Communications.

[42]  Martin N. Andersson,et al.  A Sex Pheromone Receptor in the Hessian Fly Mayetiola destructor (Diptera, Cecidomyiidae) , 2016, Front. Cell. Neurosci..

[43]  Peter Anderson,et al.  Insect host plant selection in complex environments. , 2015, Current opinion in insect science.

[44]  S. Salzberg,et al.  StringTie enables improved reconstruction of a transcriptome from RNA-seq reads , 2015, Nature Biotechnology.

[45]  Alexandros Stamatakis,et al.  RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies , 2014, Bioinform..

[46]  D. Heckel,et al.  Behavioral assays for studies of host plant choice and adaptation in herbivorous insects. , 2014, Annual review of entomology.

[47]  G. L. Taboada,et al.  ProtTest 3: fast selection of best-fit models of protein evolution , 2011, Bioinform..

[48]  R. Yamaoka,et al.  Highly Selective Tuning of a Silkworm Olfactory Receptor to a Key Mulberry Leaf Volatile , 2009, Current Biology.

[49]  Toni Gabaldón,et al.  trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses , 2009, Bioinform..

[50]  K. Katoh,et al.  MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. , 2002, Nucleic acids research.