Analysis of Long Non-Coding RNA-Mediated Regulatory Networks of <i>Plutella xylostella</i> in Response to <i>Metarhizium anisopliae</i> Infection

Long non-coding RNAs (lncRNAs) represent a diverse class of RNAs that are structurally similar to messenger RNAs (mRNAs) but do not encode proteins. Growing evidence suggests that in response to biotic and abiotic stresses, the lncRNAs play crucial regulatory roles in plants and animals. However, th...

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Main Authors: Junaid Zafar, Junlin Huang, Xiaoxia Xu, Fengliang Jin
Format: Article
Language:English
Published: MDPI AG 2022-10-01
Series:Insects
Subjects:
Online Access:https://www.mdpi.com/2075-4450/13/10/916
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author Junaid Zafar
Junlin Huang
Xiaoxia Xu
Fengliang Jin
author_facet Junaid Zafar
Junlin Huang
Xiaoxia Xu
Fengliang Jin
author_sort Junaid Zafar
collection DOAJ
description Long non-coding RNAs (lncRNAs) represent a diverse class of RNAs that are structurally similar to messenger RNAs (mRNAs) but do not encode proteins. Growing evidence suggests that in response to biotic and abiotic stresses, the lncRNAs play crucial regulatory roles in plants and animals. However, the potential role of lncRNAs during fungal infection has yet to be characterized in <i>Plutella xylostella</i>, a devastating pest of cruciferous crops. In the current study, we performed a strand-specific RNA sequencing of <i>Metarhizium anisopliae</i>-infected (Px36hT, Px72hT) and uninfected (Px36hCK, Px72hCK) <i>P. xylostella</i> fat body tissues. Comprehensive bioinformatic analysis revealed a total of 5665 and 4941 lncRNAs at 36 and 72-h post-infection (hpi), including 563 (Px36hT), 532 (Px72hT) known and 5102 (Px36hT), 4409 (Px72hT) novel lncRNA transcripts. These lncRNAs shared structural similarities with their counterparts in other species, including shorter exon and intron length, fewer exon numbers, and a lower expression profile than mRNAs. LncRNAs regulate the expression of neighboring protein-coding genes by acting in a <i>cis</i> and <i>trans</i> manner. Functional annotation and pathway analysis of <i>cis</i>-acting lncRNAs revealed their role in several immune-related genes, including <i>Toll</i>, <i>serpin</i>, <i>transferrin</i>, <i>βGRP</i> etc. Furthermore, we identified multiple lncRNAs acting as microRNA (miRNA) precursors. These miRNAs can potentially regulate the expression of mRNAs involved in immunity and development, suggesting a crucial lncRNA–miRNA-mRNA complex. Our findings will provide a genetic resource for future functional studies of lncRNAs involved in <i>P. xylostella</i> immune responses to <i>M. anisopliae</i> infection and shed light on understanding insect host–pathogen interactions.
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spelling doaj.art-ebf5413172284bffaebd4a9c7f91bf1b2023-12-03T14:47:53ZengMDPI AGInsects2075-44502022-10-01131091610.3390/insects13100916Analysis of Long Non-Coding RNA-Mediated Regulatory Networks of <i>Plutella xylostella</i> in Response to <i>Metarhizium anisopliae</i> InfectionJunaid Zafar0Junlin Huang1Xiaoxia Xu2Fengliang Jin3Key Laboratory of Bio-Pesticide Innovation and Application of Guangdong Province, College of Plant Protection, South China Agricultural University, Guangzhou 510642, ChinaKey Laboratory of Bio-Pesticide Innovation and Application of Guangdong Province, College of Plant Protection, South China Agricultural University, Guangzhou 510642, ChinaKey Laboratory of Bio-Pesticide Innovation and Application of Guangdong Province, College of Plant Protection, South China Agricultural University, Guangzhou 510642, ChinaKey Laboratory of Bio-Pesticide Innovation and Application of Guangdong Province, College of Plant Protection, South China Agricultural University, Guangzhou 510642, ChinaLong non-coding RNAs (lncRNAs) represent a diverse class of RNAs that are structurally similar to messenger RNAs (mRNAs) but do not encode proteins. Growing evidence suggests that in response to biotic and abiotic stresses, the lncRNAs play crucial regulatory roles in plants and animals. However, the potential role of lncRNAs during fungal infection has yet to be characterized in <i>Plutella xylostella</i>, a devastating pest of cruciferous crops. In the current study, we performed a strand-specific RNA sequencing of <i>Metarhizium anisopliae</i>-infected (Px36hT, Px72hT) and uninfected (Px36hCK, Px72hCK) <i>P. xylostella</i> fat body tissues. Comprehensive bioinformatic analysis revealed a total of 5665 and 4941 lncRNAs at 36 and 72-h post-infection (hpi), including 563 (Px36hT), 532 (Px72hT) known and 5102 (Px36hT), 4409 (Px72hT) novel lncRNA transcripts. These lncRNAs shared structural similarities with their counterparts in other species, including shorter exon and intron length, fewer exon numbers, and a lower expression profile than mRNAs. LncRNAs regulate the expression of neighboring protein-coding genes by acting in a <i>cis</i> and <i>trans</i> manner. Functional annotation and pathway analysis of <i>cis</i>-acting lncRNAs revealed their role in several immune-related genes, including <i>Toll</i>, <i>serpin</i>, <i>transferrin</i>, <i>βGRP</i> etc. Furthermore, we identified multiple lncRNAs acting as microRNA (miRNA) precursors. These miRNAs can potentially regulate the expression of mRNAs involved in immunity and development, suggesting a crucial lncRNA–miRNA-mRNA complex. Our findings will provide a genetic resource for future functional studies of lncRNAs involved in <i>P. xylostella</i> immune responses to <i>M. anisopliae</i> infection and shed light on understanding insect host–pathogen interactions.https://www.mdpi.com/2075-4450/13/10/916lncRNAinsect immunityhost–pathogenlepidopterabio-controlentomopathogenic fungus
spellingShingle Junaid Zafar
Junlin Huang
Xiaoxia Xu
Fengliang Jin
Analysis of Long Non-Coding RNA-Mediated Regulatory Networks of <i>Plutella xylostella</i> in Response to <i>Metarhizium anisopliae</i> Infection
Insects
lncRNA
insect immunity
host–pathogen
lepidoptera
bio-control
entomopathogenic fungus
title Analysis of Long Non-Coding RNA-Mediated Regulatory Networks of <i>Plutella xylostella</i> in Response to <i>Metarhizium anisopliae</i> Infection
title_full Analysis of Long Non-Coding RNA-Mediated Regulatory Networks of <i>Plutella xylostella</i> in Response to <i>Metarhizium anisopliae</i> Infection
title_fullStr Analysis of Long Non-Coding RNA-Mediated Regulatory Networks of <i>Plutella xylostella</i> in Response to <i>Metarhizium anisopliae</i> Infection
title_full_unstemmed Analysis of Long Non-Coding RNA-Mediated Regulatory Networks of <i>Plutella xylostella</i> in Response to <i>Metarhizium anisopliae</i> Infection
title_short Analysis of Long Non-Coding RNA-Mediated Regulatory Networks of <i>Plutella xylostella</i> in Response to <i>Metarhizium anisopliae</i> Infection
title_sort analysis of long non coding rna mediated regulatory networks of i plutella xylostella i in response to i metarhizium anisopliae i infection
topic lncRNA
insect immunity
host–pathogen
lepidoptera
bio-control
entomopathogenic fungus
url https://www.mdpi.com/2075-4450/13/10/916
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