Zhang Yue, Liu Shanlin, De Meyer Marc, Liao Zuxing, Zhao Yan, Virgilio Massimiliano, Feng Shiqian, Qin Yujia, Singh Sandeep, Wee Suk Ling, Jiang Fan, Guo Shaokun, Li Hu, Deschepper Pablo, Vanbergen Sam, Delatte Hélène, Van Sauers-Muller Aliès, Syamsudin Tati Suryati, Kawi Anastasia Priscilla, Kasina Muo, Badji Kemo, Said Fazal, Liu Lijun, Zhao Zihua, Li Zhihong. 2023. Genomes of the cosmopolitan fruit pest Bactrocera dorsalis (Diptera: Tephritidae) reveal its global invasion history and thermal adaptation. Journal of Advanced Research, 53 : 61-74.
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Résumé : Introduction: The oriental fruit fly Bactrocera dorsalis is one of the most destructive agricultural pests worldwide, with highly debated species delimitation, origin, and global spread routes. Objectives: Our study intended to (i) resolve the taxonomic uncertainties between B. dorsalis and B. carambolae, (ii) reveal the population structure and global invasion routes of B. dorsalis across Asia, Africa, and Oceania, and (iii) identify genomic regions that are responsible for the thermal adaptation of B. dorsalis. Methods: Based on a high-quality chromosome-level reference genome assembly, we explored the population relationship using a genome-scale single nucleotide polymorphism dataset generated from the resequencing data of 487 B. dorsalis genomes and 25 B. carambolae genomes. Genome-wide association studies and silencing using RNA interference were used to identify and verify the candidate genes associated with extreme thermal stress. Results: We showed that B. dorsalis originates from the Southern India region with three independent invasion and spread routes worldwide: (i) from Northern India to Northern Southeast Asia, then to Southern Southeast Asia; (ii) from Northern India to Northern Southeast Asian, then to China and Hawaii; and (iii) from Southern India toward the African mainland, then to Madagascar, which is mainly facilitated by human activities including trade and immigration. Twenty-seven genes were identified by a genome-wide association study to be associated with 11 temperature bioclimatic variables. The Cyp6a9 gene may enhance the thermal adaptation of B. dorsalis and thus boost its invasion, which tended to be upregulated at a hardening temperature of 38 °C. Functional verification using RNA interference silencing against Cyp6a9, led to the specific decrease in Cyp6a9 expression, reducing the survival rate of dsRNA-feeding larvae exposed to extreme thermal stress of 45 °C after heat hardening treatments in B. dorsalis. Conclusion: This study provides insights into the evolutionary history and genetic basis of temperature adaptation in B. dorsalis.
Mots-clés Agrovoc : Bactrocera dorsalis, espèce envahissante, provenance, génome, stress thermique, adaptation, génomique, Bactrocera, Tephritidae
Mots-clés géographiques Agrovoc : Chine, Asie du Sud-Est, Madagascar, Inde, Hawaï, Afrique
Mots-clés libres : Bactrocera dorsalis, Chromosome-level genome assembly, Invasion routes and history, Resequencing, Species delimitation, Thermal adaptation
Classification Agris : H10 - Ravageurs des plantes
Champ stratégique Cirad : CTS 4 (2019-) - Santé des plantes, des animaux et des écosystèmes
Agences de financement européennes : European Commission
Agences de financement hors UE : National Natural Science Foundation of China
Programme de financement européen : H2020
Projets sur financement : (EU) In-silico boosted, pest prevention and off-season focused IPM against new and emerging fruit flies ('OFF-Season' FF-IPM)
Auteurs et affiliations
- Zhang Yue, CAU [China Agricultural University] (CHN)
- Liu Shanlin, CAU [China Agricultural University] (CHN)
- De Meyer Marc, Musée royal de l'Afrique centrale (BEL)
- Liao Zuxing, CAU [China Agricultural University] (CHN)
- Zhao Yan, CAU [China Agricultural University] (CHN)
- Virgilio Massimiliano, Musée royal de l'Afrique centrale (BEL)
- Feng Shiqian, CAU [China Agricultural University] (CHN)
- Qin Yujia, CAU [China Agricultural University] (CHN)
- Singh Sandeep, Punjab Agricultural University (IND)
- Wee Suk Ling, Universiti Kebangsaan Malaysia (MYS)
- Jiang Fan, Chinese Academy of Inspection and Quarantine (CHN)
- Guo Shaokun, CAU [China Agricultural University] (CHN)
- Li Hu, CAU [China Agricultural University] (CHN)
- Deschepper Pablo, RMCA (BEL)
- Vanbergen Sam, RMCA (BEL)
- Delatte Hélène, CIRAD-BIOS-UMR PVBMT (MDG)
- Van Sauers-Muller Aliès, Ministry of Agriculture, Animal Husbandry and Fisheries (Suriname) (SUR)
- Syamsudin Tati Suryati, Bandung Institute of Technology (IDN)
- Kawi Anastasia Priscilla, National Agriculture Quarantine & Inspection Authority (PNG)
- Kasina Muo, Apiculture Research Institute (KEN)
- Badji Kemo, Direction de la protection des végétaux (SEN)
- Said Fazal, Abdul Wali Khan University Mardan (PAK)
- Liu Lijun, CAU [China Agricultural University] (CHN)
- Zhao Zihua, CAU [China Agricultural University] (CHN)
- Li Zhihong, CAU [China Agricultural University] (CHN) - auteur correspondant
Source : Cirad-Agritrop (https://agritrop.cirad.fr/603528/)
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