Whole-transcriptome characterization and functional analysis of lncRNA-miRNA-mRNA regulatory networks responsive to sugarcane mosaic virus in maize resistant and susceptible inbred lines

Int J Biol Macromol. 2024 Feb;257(Pt 2):128685. doi: 10.1016/j.ijbiomac.2023.128685. Epub 2023 Dec 12.

Abstract

Sugarcane mosaic virus (SCMV) is one of the most important pathogens causing maize dwarf mosaic disease, which seriously affects the yield and quality of maize. Currently, the molecular mechanism of non-coding RNAs (ncRNAs) responding to SCMV infection in maize is still uncovered. In this study, a total of 112 differentially expressed (DE)-long non-coding RNAs (lncRNAs), 24 DE-microRNAs (miRNAs), and 1822 DE-messenger RNAs (mRNAs), and 363 DE-lncRNAs, 230 DE-miRNAs, and 4376 DE-mRNAs were identified in maize resistant (Chang7-2) and susceptible (Mo17) inbred lines in response to SCMV infection through whole-transcriptome RNA sequencing, respectively. Moreover, 4874 mRNAs potentially targeted by 635 miRNAs were obtained by degradome sequencing. Subsequently, several crucial SCMV-responsive lncRNA-miRNA-mRNA networks were established, of which the expression levels of lncRNA10865-miR166j-3p-HDZ25/69 (class III homeodomain-leucine zipper 25/69) module, and lncRNA14234-miR394a-5p-SPL11 (squamosal promoter-binding protein-like 11) module were further verified. Additionally, silencing lncRNA10865 increased the accumulations of SCMV and miR166j-3p, while silencing lncRNA14234 decreased the accumulations of SCMV and SPL11 targeted by miR394a-5p. This study revealed the interactions of lncRNAs, miRNAs and mRNAs in maize resistant and susceptible materials, providing novel clues to reveal the mechanism of maize in resistance to SCMV from the perspective of competing endogenous RNA (ceRNA) regulatory networks.

Keywords: Competing endogenous RNA (ceRNA); Long non-coding RNA (lncRNA); Maize resistant and susceptible inbred lines; Messenger RNA (mRNA); MicroRNA (miRNA); Sugarcane mosaic virus (SCMV).

MeSH terms

  • Gene Expression Regulation, Plant
  • Gene Regulatory Networks
  • MicroRNAs* / genetics
  • Plant Diseases / genetics
  • Potyvirus*
  • RNA, Long Noncoding* / genetics
  • RNA, Messenger / genetics
  • Saccharum* / genetics
  • Transcriptome / genetics

Substances

  • MicroRNAs
  • RNA, Long Noncoding
  • RNA, Messenger

Supplementary concepts

  • Sugarcane mosaic virus