Nanocarrier-mediated RNAi of CYP9A306 and CYB5R enhances susceptibility of invasive tomato pest, Tuta absoluta to cyantraniliprole
Cyantraniliprole, a second-generation anthranilic diamide, is widely used to manage lepidopteran pests, including the invasive tomato pinworm Tuta absoluta (Meyrick). However, cyantraniliprole’s resistance mechanisms and associated fitness costs in T. absoluta remain underexplored. Here, we investig...
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Frontiers Media S.A.
2025-04-01
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| Series: | Frontiers in Plant Science |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fpls.2025.1573634/full |
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| author | Farman Ullah Guru-Pirasanna-Pandi G Hina Gul Rudra Madhab Panda Ghulam Murtaza Zhijun Zhang Jun Huang Xiaowei Li Nicolas Desneux Yaobin Lu |
| author_facet | Farman Ullah Guru-Pirasanna-Pandi G Hina Gul Rudra Madhab Panda Ghulam Murtaza Zhijun Zhang Jun Huang Xiaowei Li Nicolas Desneux Yaobin Lu |
| author_sort | Farman Ullah |
| collection | DOAJ |
| description | Cyantraniliprole, a second-generation anthranilic diamide, is widely used to manage lepidopteran pests, including the invasive tomato pinworm Tuta absoluta (Meyrick). However, cyantraniliprole’s resistance mechanisms and associated fitness costs in T. absoluta remain underexplored. Here, we investigated the fitness costs and resistance mechanisms of cyantraniliprole-resistant strain (CyanRS) via nanocarrier-mediated RNA interference (RNAi). Results showed that the egg incubation period and developmental durations of larval and pupal stages were significantly prolonged in the CyanRS population of T. absoluta compared to the susceptible strain (SS). Further, the adult emergence, longevities of male and female, fecundity, and hatching rate were significantly reduced in CyanRS individuals. The mRNA expression levels of cytochrome b5 reductase (CYB5R) and cytochrome P450 (CYP9A306) were analyzed using RT-qPCR to explore their potential involvement in cyantraniliprole resistance in T. absoluta. Phylogenetic and motif analysis of CYB5R and CYP9A306 indicated their evolutionary and functional conservation with other insect species, especially Lepidopterans. Notably, nanocarrier-encapsulated dsRNA targeting CYB5R and CYP9A306 genes significantly reduced their expression levels. Further, the activity of cytochrome P450 was substantially decreased after the knockdown of the CYB5R and CYP9A306 genes. This increased susceptibility of the resistant population of T. absoluta to cyantraniliprole, leading to a higher mortality rate than the controls. These findings show that CYB5R and CYP9A306 might play a key role in cyantraniliprole resistance evolution in T. absoluta. The current study provides in-depth insights to understand the underlying mechanisms of cyantraniliprole resistance in this key invasive herbivore. |
| format | Article |
| id | doaj-art-09d4af0d4cf24ce8bf8cbb7d0a2d58b9 |
| institution | Kabale University |
| issn | 1664-462X |
| language | English |
| publishDate | 2025-04-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Plant Science |
| spelling | doaj-art-09d4af0d4cf24ce8bf8cbb7d0a2d58b92025-08-20T03:29:23ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2025-04-011610.3389/fpls.2025.15736341573634Nanocarrier-mediated RNAi of CYP9A306 and CYB5R enhances susceptibility of invasive tomato pest, Tuta absoluta to cyantraniliproleFarman Ullah0Guru-Pirasanna-Pandi G1Hina Gul2Rudra Madhab Panda3Ghulam Murtaza4Zhijun Zhang5Jun Huang6Xiaowei Li7Nicolas Desneux8Yaobin Lu9State Key Laboratory for Quality and Safety of Agro-Products, Key Laboratory of Biotechnology in Plant Protection of MOA of China and Zhejiang Province, Institute of Plant Protection and Microbiology, Zhejiang Academy of Agricultural Sciences, Hangzhou, ChinaProtection Division, ICAR-National Rice Research Institute, Cuttack, Odisha, IndiaState Key Laboratory for Quality and Safety of Agro-Products, Key Laboratory of Biotechnology in Plant Protection of MOA of China and Zhejiang Province, Institute of Plant Protection and Microbiology, Zhejiang Academy of Agricultural Sciences, Hangzhou, ChinaProtection Division, ICAR-National Rice Research Institute, Cuttack, Odisha, IndiaMARA Key Laboratory of Surveillance and Management for Plant Quarantine Pests, College of Plant Protection, China Agricultural University, Beijing, ChinaState Key Laboratory for Quality and Safety of Agro-Products, Key Laboratory of Biotechnology in Plant Protection of MOA of China and Zhejiang Province, Institute of Plant Protection and Microbiology, Zhejiang Academy of Agricultural Sciences, Hangzhou, ChinaState Key Laboratory for Quality and Safety of Agro-Products, Key Laboratory of Biotechnology in Plant Protection of MOA of China and Zhejiang Province, Institute of Plant Protection and Microbiology, Zhejiang Academy of Agricultural Sciences, Hangzhou, ChinaState Key Laboratory for Quality and Safety of Agro-Products, Key Laboratory of Biotechnology in Plant Protection of MOA of China and Zhejiang Province, Institute of Plant Protection and Microbiology, Zhejiang Academy of Agricultural Sciences, Hangzhou, ChinaUniversité Côte d’Azur, INRAE, CNRS, UMR ISA, Nice, FranceState Key Laboratory for Quality and Safety of Agro-Products, Key Laboratory of Biotechnology in Plant Protection of MOA of China and Zhejiang Province, Institute of Plant Protection and Microbiology, Zhejiang Academy of Agricultural Sciences, Hangzhou, ChinaCyantraniliprole, a second-generation anthranilic diamide, is widely used to manage lepidopteran pests, including the invasive tomato pinworm Tuta absoluta (Meyrick). However, cyantraniliprole’s resistance mechanisms and associated fitness costs in T. absoluta remain underexplored. Here, we investigated the fitness costs and resistance mechanisms of cyantraniliprole-resistant strain (CyanRS) via nanocarrier-mediated RNA interference (RNAi). Results showed that the egg incubation period and developmental durations of larval and pupal stages were significantly prolonged in the CyanRS population of T. absoluta compared to the susceptible strain (SS). Further, the adult emergence, longevities of male and female, fecundity, and hatching rate were significantly reduced in CyanRS individuals. The mRNA expression levels of cytochrome b5 reductase (CYB5R) and cytochrome P450 (CYP9A306) were analyzed using RT-qPCR to explore their potential involvement in cyantraniliprole resistance in T. absoluta. Phylogenetic and motif analysis of CYB5R and CYP9A306 indicated their evolutionary and functional conservation with other insect species, especially Lepidopterans. Notably, nanocarrier-encapsulated dsRNA targeting CYB5R and CYP9A306 genes significantly reduced their expression levels. Further, the activity of cytochrome P450 was substantially decreased after the knockdown of the CYB5R and CYP9A306 genes. This increased susceptibility of the resistant population of T. absoluta to cyantraniliprole, leading to a higher mortality rate than the controls. These findings show that CYB5R and CYP9A306 might play a key role in cyantraniliprole resistance evolution in T. absoluta. The current study provides in-depth insights to understand the underlying mechanisms of cyantraniliprole resistance in this key invasive herbivore.https://www.frontiersin.org/articles/10.3389/fpls.2025.1573634/fullresistance evolutionRNA interferencebiological traitslepidopteragene expression |
| spellingShingle | Farman Ullah Guru-Pirasanna-Pandi G Hina Gul Rudra Madhab Panda Ghulam Murtaza Zhijun Zhang Jun Huang Xiaowei Li Nicolas Desneux Yaobin Lu Nanocarrier-mediated RNAi of CYP9A306 and CYB5R enhances susceptibility of invasive tomato pest, Tuta absoluta to cyantraniliprole Frontiers in Plant Science resistance evolution RNA interference biological traits lepidoptera gene expression |
| title | Nanocarrier-mediated RNAi of CYP9A306 and CYB5R enhances susceptibility of invasive tomato pest, Tuta absoluta to cyantraniliprole |
| title_full | Nanocarrier-mediated RNAi of CYP9A306 and CYB5R enhances susceptibility of invasive tomato pest, Tuta absoluta to cyantraniliprole |
| title_fullStr | Nanocarrier-mediated RNAi of CYP9A306 and CYB5R enhances susceptibility of invasive tomato pest, Tuta absoluta to cyantraniliprole |
| title_full_unstemmed | Nanocarrier-mediated RNAi of CYP9A306 and CYB5R enhances susceptibility of invasive tomato pest, Tuta absoluta to cyantraniliprole |
| title_short | Nanocarrier-mediated RNAi of CYP9A306 and CYB5R enhances susceptibility of invasive tomato pest, Tuta absoluta to cyantraniliprole |
| title_sort | nanocarrier mediated rnai of cyp9a306 and cyb5r enhances susceptibility of invasive tomato pest tuta absoluta to cyantraniliprole |
| topic | resistance evolution RNA interference biological traits lepidoptera gene expression |
| url | https://www.frontiersin.org/articles/10.3389/fpls.2025.1573634/full |
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