A comprehensive analysis of the defense responses of Odontotermes formosanus (Shiraki) provides insights into the changes during Serratia marcescens infection
Abstract Background Odontotermes formosanus (Shiraki) is a highly damaging agroforestry pest. Serratia marcescens is a broad-spectrum insecticidal pathogen and is highly lethal to O. formosanus. However, little is known about the mechanism between them. To improve the biological control of pests, a...
Saved in:
| Main Authors: | , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
BMC
2024-11-01
|
| Series: | BMC Genomics |
| Subjects: | |
| Online Access: | https://doi.org/10.1186/s12864-024-10955-2 |
| Tags: |
Add Tag
No Tags, Be the first to tag this record!
|
| _version_ | 1850062408166408192 |
|---|---|
| author | Zhiqiang Wang Mingyu Wang Yujingyun Zhou Kai Feng Fang Tang |
| author_facet | Zhiqiang Wang Mingyu Wang Yujingyun Zhou Kai Feng Fang Tang |
| author_sort | Zhiqiang Wang |
| collection | DOAJ |
| description | Abstract Background Odontotermes formosanus (Shiraki) is a highly damaging agroforestry pest. Serratia marcescens is a broad-spectrum insecticidal pathogen and is highly lethal to O. formosanus. However, little is known about the mechanism between them. To improve the biological control of pests, a more in-depth analysis of the interactions between the pests and the pathogens is essential. Results We used RNA-seq, enzyme activity assays and real-time fluorescent quantitative PCR (qPCR) to explore the defense responses of O. formosanus against SM1. RNA-seq results showed that 1,160, 2,531 and 4,536 genes were differentially expressed at 3, 6 and 12 h after SM1 infection, and Kyoto Encyclopedia of Genes and Genomes (KEGG) results indicated that immune response and energy metabolism were involved in the defense of O. formosanus against SM1. Reactive oxygen species (ROS) levels and ROS synthesis genes were significantly elevated, and the antioxidant system were induced in O. formosanus after SM1 infection. In addition, the cellular immune genes were affected, and the Toll, immune deficiency (Imd), Janus kinase/signal transducer and activator of transcription (JAK/STAT), c-Jun N-terminal Kinase (JNK) and melanization pathways were activated. In vitro, Oftermicin, an antimicrobial peptide, had a significantly inhibitory effect on SM1. Furthermore, the expression levels and enzyme activities of phosphofructokinase (PFK), lactate dehydrogenase (LDH), succinate dehydrogenase (SDH) and isocitrate dehydrogenase (IDH) in glycolysis and tricarboxylic acid (TCA) cycles were increased. Conclusions Our results clearly demonstrated that O. formosanus defended against SM1 by activating the antioxidant system, innate immunity and energy metabolism. This study would provide useful information for the development of biological controls of O. formosanus. |
| format | Article |
| id | doaj-art-c9fb8cc6eb5c4adc998a70b2d9955e8b |
| institution | DOAJ |
| issn | 1471-2164 |
| language | English |
| publishDate | 2024-11-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Genomics |
| spelling | doaj-art-c9fb8cc6eb5c4adc998a70b2d9955e8b2025-08-20T02:49:56ZengBMCBMC Genomics1471-21642024-11-0125111710.1186/s12864-024-10955-2A comprehensive analysis of the defense responses of Odontotermes formosanus (Shiraki) provides insights into the changes during Serratia marcescens infectionZhiqiang Wang0Mingyu Wang1Yujingyun Zhou2Kai Feng3Fang Tang4Co-Innovation Center for Sustainable Forestry in Southern China, Nanjing Forestry UniversityCo-Innovation Center for Sustainable Forestry in Southern China, Nanjing Forestry UniversityCo-Innovation Center for Sustainable Forestry in Southern China, Nanjing Forestry UniversityCo-Innovation Center for Sustainable Forestry in Southern China, Nanjing Forestry UniversityCo-Innovation Center for Sustainable Forestry in Southern China, Nanjing Forestry UniversityAbstract Background Odontotermes formosanus (Shiraki) is a highly damaging agroforestry pest. Serratia marcescens is a broad-spectrum insecticidal pathogen and is highly lethal to O. formosanus. However, little is known about the mechanism between them. To improve the biological control of pests, a more in-depth analysis of the interactions between the pests and the pathogens is essential. Results We used RNA-seq, enzyme activity assays and real-time fluorescent quantitative PCR (qPCR) to explore the defense responses of O. formosanus against SM1. RNA-seq results showed that 1,160, 2,531 and 4,536 genes were differentially expressed at 3, 6 and 12 h after SM1 infection, and Kyoto Encyclopedia of Genes and Genomes (KEGG) results indicated that immune response and energy metabolism were involved in the defense of O. formosanus against SM1. Reactive oxygen species (ROS) levels and ROS synthesis genes were significantly elevated, and the antioxidant system were induced in O. formosanus after SM1 infection. In addition, the cellular immune genes were affected, and the Toll, immune deficiency (Imd), Janus kinase/signal transducer and activator of transcription (JAK/STAT), c-Jun N-terminal Kinase (JNK) and melanization pathways were activated. In vitro, Oftermicin, an antimicrobial peptide, had a significantly inhibitory effect on SM1. Furthermore, the expression levels and enzyme activities of phosphofructokinase (PFK), lactate dehydrogenase (LDH), succinate dehydrogenase (SDH) and isocitrate dehydrogenase (IDH) in glycolysis and tricarboxylic acid (TCA) cycles were increased. Conclusions Our results clearly demonstrated that O. formosanus defended against SM1 by activating the antioxidant system, innate immunity and energy metabolism. This study would provide useful information for the development of biological controls of O. formosanus.https://doi.org/10.1186/s12864-024-10955-2Odontotermes formosanus (Shiraki)Serratia marcescensTranscriptomeOxidative stressInnate immunityEnergy metabolism |
| spellingShingle | Zhiqiang Wang Mingyu Wang Yujingyun Zhou Kai Feng Fang Tang A comprehensive analysis of the defense responses of Odontotermes formosanus (Shiraki) provides insights into the changes during Serratia marcescens infection BMC Genomics Odontotermes formosanus (Shiraki) Serratia marcescens Transcriptome Oxidative stress Innate immunity Energy metabolism |
| title | A comprehensive analysis of the defense responses of Odontotermes formosanus (Shiraki) provides insights into the changes during Serratia marcescens infection |
| title_full | A comprehensive analysis of the defense responses of Odontotermes formosanus (Shiraki) provides insights into the changes during Serratia marcescens infection |
| title_fullStr | A comprehensive analysis of the defense responses of Odontotermes formosanus (Shiraki) provides insights into the changes during Serratia marcescens infection |
| title_full_unstemmed | A comprehensive analysis of the defense responses of Odontotermes formosanus (Shiraki) provides insights into the changes during Serratia marcescens infection |
| title_short | A comprehensive analysis of the defense responses of Odontotermes formosanus (Shiraki) provides insights into the changes during Serratia marcescens infection |
| title_sort | comprehensive analysis of the defense responses of odontotermes formosanus shiraki provides insights into the changes during serratia marcescens infection |
| topic | Odontotermes formosanus (Shiraki) Serratia marcescens Transcriptome Oxidative stress Innate immunity Energy metabolism |
| url | https://doi.org/10.1186/s12864-024-10955-2 |
| work_keys_str_mv | AT zhiqiangwang acomprehensiveanalysisofthedefenseresponsesofodontotermesformosanusshirakiprovidesinsightsintothechangesduringserratiamarcescensinfection AT mingyuwang acomprehensiveanalysisofthedefenseresponsesofodontotermesformosanusshirakiprovidesinsightsintothechangesduringserratiamarcescensinfection AT yujingyunzhou acomprehensiveanalysisofthedefenseresponsesofodontotermesformosanusshirakiprovidesinsightsintothechangesduringserratiamarcescensinfection AT kaifeng acomprehensiveanalysisofthedefenseresponsesofodontotermesformosanusshirakiprovidesinsightsintothechangesduringserratiamarcescensinfection AT fangtang acomprehensiveanalysisofthedefenseresponsesofodontotermesformosanusshirakiprovidesinsightsintothechangesduringserratiamarcescensinfection AT zhiqiangwang comprehensiveanalysisofthedefenseresponsesofodontotermesformosanusshirakiprovidesinsightsintothechangesduringserratiamarcescensinfection AT mingyuwang comprehensiveanalysisofthedefenseresponsesofodontotermesformosanusshirakiprovidesinsightsintothechangesduringserratiamarcescensinfection AT yujingyunzhou comprehensiveanalysisofthedefenseresponsesofodontotermesformosanusshirakiprovidesinsightsintothechangesduringserratiamarcescensinfection AT kaifeng comprehensiveanalysisofthedefenseresponsesofodontotermesformosanusshirakiprovidesinsightsintothechangesduringserratiamarcescensinfection AT fangtang comprehensiveanalysisofthedefenseresponsesofodontotermesformosanusshirakiprovidesinsightsintothechangesduringserratiamarcescensinfection |