Transcriptomic Analysis of <i>Metarhizium anisopliae</i>-Induced Immune-Related Long Non-Coding RNAs in Polymorphic Worker Castes of <i>Solenopsis invicta</i>
Long non-coding RNAs (lncRNAs) represent a class of RNA molecules that do not encode proteins. Generally studied for their regulatory potential in model insects, relatively little is known about their immunoregulatory functions in different castes of eusocial insects, including <i>Solenopsis i...
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| Format: | Article |
| Language: | English |
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MDPI AG
2023-09-01
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| Series: | International Journal of Molecular Sciences |
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| Online Access: | https://www.mdpi.com/1422-0067/24/18/13983 |
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| author | Junaid Zafar Hongxin Wu Yating Xu Liangjie Lin Zehong Kang Jie Zhang Ruonan Zhang Yongyue Lu Fengliang Jin Xiaoxia Xu |
| author_facet | Junaid Zafar Hongxin Wu Yating Xu Liangjie Lin Zehong Kang Jie Zhang Ruonan Zhang Yongyue Lu Fengliang Jin Xiaoxia Xu |
| author_sort | Junaid Zafar |
| collection | DOAJ |
| description | Long non-coding RNAs (lncRNAs) represent a class of RNA molecules that do not encode proteins. Generally studied for their regulatory potential in model insects, relatively little is known about their immunoregulatory functions in different castes of eusocial insects, including <i>Solenopsis invicta</i>, a notoriously invasive insect pest. In the current study, we used <i>Metarhizium anisopliae</i>, an entomopathogenic fungus, to infect the polymorphic worker castes (Major and Minor Workers) and subjected them to RNA sequencing at different intervals (6, 24, and 48 h post-infection (hpi)). Comprehensive bioinformatic analysis identified 5719 (1869 known and 3850 novel) lncRNAs in all libraries. Genomic characteristics analysis showed that <i>S. invicta</i> lncRNAs exhibited structural similarities with lncRNAs from other eusocial insects, including lower exon numbers, shorter intron and exon lengths, and a lower expression profile. A comparison of lncRNAs in major and minor worker ants revealed that several lncRNAs were exclusively expressed in one worker caste and remained absent in the other. LncRNAs such as <i>MSTRG.12029.1</i>, <i>XR_005575440.1</i> (6 h), <i>MSTRG.16728.1</i>, <i>XR_005575440.1</i> (24 h), <i>MSTRG.20263.41</i>, and <i>MSTRG.11994.5</i> (48 h) were only present in major worker ants, while lncRNAs such as <i>MSTRG.8896.1</i>, <i>XR_005574239.1</i> (6 h), <i>MSTRG.20289.8</i>, <i>XR_005575051.1</i> (24 h), <i>MSTRG.20289.8</i>, and <i>MSTRG.6682.1</i> (48 h) were only detected in minor workers. Additionally, we performed real-time quantitative PCR and experimentally validated these findings. Functional annotation of <i>cis</i>-acting lncRNAs in major worker ants showed that lncRNAs targeted genes such as <i>serine protease</i>, <i>trypsin</i>, <i>melanization protease-1</i>, <i>spaetzle-3</i>, etc. In contrast, apoptosis and autophagy-related genes were identified as targets of lncRNAs in minor ants. Lastly, we identified several lncRNAs as precursors of microRNAs (miRNAs), such as miR-8, miR-14, miR-210, miR-6038, etc., indicating a regulatory relationship between lncRNAs, miRNAs, and mRNAs in antifungal immunity. These findings will serve as a genetic resource for lncRNAs in polymorphic eusocial ants and provide a theoretical basis for exploring the function of lncRNAs from a unique and novel perspective. |
| first_indexed | 2024-03-10T22:40:37Z |
| format | Article |
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| institution | Directory Open Access Journal |
| issn | 1661-6596 1422-0067 |
| language | English |
| last_indexed | 2024-03-10T22:40:37Z |
| publishDate | 2023-09-01 |
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| series | International Journal of Molecular Sciences |
| spelling | doaj.art-c680bc33db324458b566f10cb80d2ebf2023-11-19T11:06:05ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672023-09-0124181398310.3390/ijms241813983Transcriptomic Analysis of <i>Metarhizium anisopliae</i>-Induced Immune-Related Long Non-Coding RNAs in Polymorphic Worker Castes of <i>Solenopsis invicta</i>Junaid Zafar0Hongxin Wu1Yating Xu2Liangjie Lin3Zehong Kang4Jie Zhang5Ruonan Zhang6Yongyue Lu7Fengliang Jin8Xiaoxia Xu9National Key Laboratory of Green Pesticide, “Belt and Road” Technology Industry and Innovation Institute for Green and Biological Control of Agricultural Pests, College of Plant Protection, South China Agricultural University, Guangzhou 510642, ChinaNational Key Laboratory of Green Pesticide, “Belt and Road” Technology Industry and Innovation Institute for Green and Biological Control of Agricultural Pests, College of Plant Protection, South China Agricultural University, Guangzhou 510642, ChinaNational Key Laboratory of Green Pesticide, “Belt and Road” Technology Industry and Innovation Institute for Green and Biological Control of Agricultural Pests, College of Plant Protection, South China Agricultural University, Guangzhou 510642, ChinaNational Key Laboratory of Green Pesticide, “Belt and Road” Technology Industry and Innovation Institute for Green and Biological Control of Agricultural Pests, College of Plant Protection, South China Agricultural University, Guangzhou 510642, ChinaNational Key Laboratory of Green Pesticide, “Belt and Road” Technology Industry and Innovation Institute for Green and Biological Control of Agricultural Pests, College of Plant Protection, South China Agricultural University, Guangzhou 510642, ChinaNational Key Laboratory of Green Pesticide, “Belt and Road” Technology Industry and Innovation Institute for Green and Biological Control of Agricultural Pests, College of Plant Protection, South China Agricultural University, Guangzhou 510642, ChinaNational Key Laboratory of Green Pesticide, “Belt and Road” Technology Industry and Innovation Institute for Green and Biological Control of Agricultural Pests, College of Plant Protection, South China Agricultural University, Guangzhou 510642, ChinaNational Key Laboratory of Green Pesticide, “Belt and Road” Technology Industry and Innovation Institute for Green and Biological Control of Agricultural Pests, College of Plant Protection, South China Agricultural University, Guangzhou 510642, ChinaNational Key Laboratory of Green Pesticide, “Belt and Road” Technology Industry and Innovation Institute for Green and Biological Control of Agricultural Pests, College of Plant Protection, South China Agricultural University, Guangzhou 510642, ChinaNational Key Laboratory of Green Pesticide, “Belt and Road” Technology Industry and Innovation Institute for Green and Biological Control of Agricultural Pests, College of Plant Protection, South China Agricultural University, Guangzhou 510642, ChinaLong non-coding RNAs (lncRNAs) represent a class of RNA molecules that do not encode proteins. Generally studied for their regulatory potential in model insects, relatively little is known about their immunoregulatory functions in different castes of eusocial insects, including <i>Solenopsis invicta</i>, a notoriously invasive insect pest. In the current study, we used <i>Metarhizium anisopliae</i>, an entomopathogenic fungus, to infect the polymorphic worker castes (Major and Minor Workers) and subjected them to RNA sequencing at different intervals (6, 24, and 48 h post-infection (hpi)). Comprehensive bioinformatic analysis identified 5719 (1869 known and 3850 novel) lncRNAs in all libraries. Genomic characteristics analysis showed that <i>S. invicta</i> lncRNAs exhibited structural similarities with lncRNAs from other eusocial insects, including lower exon numbers, shorter intron and exon lengths, and a lower expression profile. A comparison of lncRNAs in major and minor worker ants revealed that several lncRNAs were exclusively expressed in one worker caste and remained absent in the other. LncRNAs such as <i>MSTRG.12029.1</i>, <i>XR_005575440.1</i> (6 h), <i>MSTRG.16728.1</i>, <i>XR_005575440.1</i> (24 h), <i>MSTRG.20263.41</i>, and <i>MSTRG.11994.5</i> (48 h) were only present in major worker ants, while lncRNAs such as <i>MSTRG.8896.1</i>, <i>XR_005574239.1</i> (6 h), <i>MSTRG.20289.8</i>, <i>XR_005575051.1</i> (24 h), <i>MSTRG.20289.8</i>, and <i>MSTRG.6682.1</i> (48 h) were only detected in minor workers. Additionally, we performed real-time quantitative PCR and experimentally validated these findings. Functional annotation of <i>cis</i>-acting lncRNAs in major worker ants showed that lncRNAs targeted genes such as <i>serine protease</i>, <i>trypsin</i>, <i>melanization protease-1</i>, <i>spaetzle-3</i>, etc. In contrast, apoptosis and autophagy-related genes were identified as targets of lncRNAs in minor ants. Lastly, we identified several lncRNAs as precursors of microRNAs (miRNAs), such as miR-8, miR-14, miR-210, miR-6038, etc., indicating a regulatory relationship between lncRNAs, miRNAs, and mRNAs in antifungal immunity. These findings will serve as a genetic resource for lncRNAs in polymorphic eusocial ants and provide a theoretical basis for exploring the function of lncRNAs from a unique and novel perspective.https://www.mdpi.com/1422-0067/24/18/13983lncRNAfire ants<i>Metarhizium anisopliae</i>biocontrolhost-pathogen interactionentomopathogenic fungus |
| spellingShingle | Junaid Zafar Hongxin Wu Yating Xu Liangjie Lin Zehong Kang Jie Zhang Ruonan Zhang Yongyue Lu Fengliang Jin Xiaoxia Xu Transcriptomic Analysis of <i>Metarhizium anisopliae</i>-Induced Immune-Related Long Non-Coding RNAs in Polymorphic Worker Castes of <i>Solenopsis invicta</i> International Journal of Molecular Sciences lncRNA fire ants <i>Metarhizium anisopliae</i> biocontrol host-pathogen interaction entomopathogenic fungus |
| title | Transcriptomic Analysis of <i>Metarhizium anisopliae</i>-Induced Immune-Related Long Non-Coding RNAs in Polymorphic Worker Castes of <i>Solenopsis invicta</i> |
| title_full | Transcriptomic Analysis of <i>Metarhizium anisopliae</i>-Induced Immune-Related Long Non-Coding RNAs in Polymorphic Worker Castes of <i>Solenopsis invicta</i> |
| title_fullStr | Transcriptomic Analysis of <i>Metarhizium anisopliae</i>-Induced Immune-Related Long Non-Coding RNAs in Polymorphic Worker Castes of <i>Solenopsis invicta</i> |
| title_full_unstemmed | Transcriptomic Analysis of <i>Metarhizium anisopliae</i>-Induced Immune-Related Long Non-Coding RNAs in Polymorphic Worker Castes of <i>Solenopsis invicta</i> |
| title_short | Transcriptomic Analysis of <i>Metarhizium anisopliae</i>-Induced Immune-Related Long Non-Coding RNAs in Polymorphic Worker Castes of <i>Solenopsis invicta</i> |
| title_sort | transcriptomic analysis of i metarhizium anisopliae i induced immune related long non coding rnas in polymorphic worker castes of i solenopsis invicta i |
| topic | lncRNA fire ants <i>Metarhizium anisopliae</i> biocontrol host-pathogen interaction entomopathogenic fungus |
| url | https://www.mdpi.com/1422-0067/24/18/13983 |
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