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

Abstract

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 Plutella xylostella, a devastating pest of cruciferous crops. In the current study, we performed a strand-specific RNA sequencing of Metarhizium anisopliae-infected (Px36hT, Px72hT) and uninfected (Px36hCK, Px72hCK) P. xylostella fat body tissues. Comprehensive bioinformatic analysis revealed a total of 5665 and 4941 lncRNAs at 36 and 72-hours 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 cis and trans manner. Functional annotation and pathway analysis of cis-acting lncRNAs revealed their role in several immune-related genes, including Toll, serpin, transferrin, βGRP 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 P. xylostella immune responses to M. anisopliae infection and shed light on understanding insect host–pathogen interactions.

Transcriptomic Analysis of Metarhizium anisopliae-Induced Immune-Related Long Non-Coding RNAs in Polymorphic Worker Castes of Solenopsis invicta

“…Recent studies have demonstrated that lncRNAs can regulate gene expression by acting in cis on neighboring loci [ 56 ]. Here, we investigated the cis -regulatory lncRNAs by screening the protein-coding genes as potential targets in the regions located 10 kb upstream/downstream of lncRNAs.…”

Genome-Wide Exploration of Long Non-Coding RNAs of Helicoverpa armigera in Response to Pyrethroid Insecticide Resistance

“…Notably, strand-specific RNA sequencing was used to investigate the roles of lncRNAs in the fatbody of P. xylostella during infection with Metarhizium anisopliae . Multiple lncRNAs have been identified as potential precursors of microRNAs, forming a complex involved in immune response and development [ 60 ]. In this study, we observed variations in the copy numbers of lncRNAs in the susceptible and resistant strains of H. armigera ( Figure 1 ).…”

“…lncRNAs are involved in various biological processes in insects, including wing development [ 67 ], insecticide resistance [ 55 ], and interactions with microRNAs. lncRNAs can also interact with microRNAs, acting as competing endogenous RNAs and modulating the expression of target genes [ 60 , 68 ]. A case study in Drosophila melanogaster (fruit fly) demonstrated a specific example in which a long non-coding RNA ( bsAS ) controlled wing development.…”

Systematic Characterization and Regulatory Role of lncRNAs in Asian Honey Bees Responding to Microsporidian Infestation

“…The action modes of lncRNAs are flexible and diverse [ 3 ]. One major regulatory manner of lncRNAs is the cis -acting effect, which has been verified in numerous animals, such as Plutella xylostella [ 27 ] and A. m. ligustica [ 9 ]. LncRNAs located upstream and downstream of the protein-encoding genes may generate partial overlap with promoters, enhancers, or inducible elements, thus exerting regulatory functions in the expression of neighboring protein-coding genes at the transcriptional or post-transcriptional level [ 2 , 3 ].…”