Maize transposable elements contribute to long non-coding RNAs that are regulatory hubs for abiotic stress response

BMC Genomics. 2019 Nov 15;20(1):864. doi: 10.1186/s12864-019-6245-5.

Abstract

Background: Several studies have mined short-read RNA sequencing datasets to identify long non-coding RNAs (lncRNAs), and others have focused on the function of individual lncRNAs in abiotic stress response. However, our understanding of the complement, function and origin of lncRNAs - and especially transposon derived lncRNAs (TE-lncRNAs) - in response to abiotic stress is still in its infancy.

Results: We utilized a dataset of 127 RNA sequencing samples that included total RNA datasets and PacBio fl-cDNA data to discover lncRNAs in maize. Overall, we identified 23,309 candidate lncRNAs from polyA+ and total RNA samples, with a strong discovery bias within total RNA. The majority (65%) of the 23,309 lncRNAs had sequence similarity to transposable elements (TEs). Most had similarity to long-terminal-repeat retrotransposons from the Copia and Gypsy superfamilies, reflecting a high proportion of these elements in the genome. However, DNA transposons were enriched for lncRNAs relative to their genomic representation by ~ 2-fold. By assessing the fraction of lncRNAs that respond to abiotic stresses like heat, cold, salt and drought, we identified 1077 differentially expressed lncRNA transcripts, including 509 TE-lncRNAs. In general, the expression of these lncRNAs was significantly correlated with their nearest gene. By inferring co-expression networks across our large dataset, we found that 39 lncRNAs are as major hubs in co-expression networks that respond to abiotic stress, and 18 appear to be derived from TEs.

Conclusions: Our results show that lncRNAs are enriched in total RNA samples, that most (65%) are derived from TEs, that at least 1077 are differentially expressed during abiotic stress, and that 39 are hubs in co-expression networks, including a small number that are evolutionary conserved. These results suggest that lncRNAs, including TE-lncRNAs, may play key regulatory roles in moderating abiotic responses.

Keywords: Abiotic stress; Co-expression network; Long non-coding RNA; Transposable elements.

MeSH terms

  • Adaptation, Physiological / genetics
  • Cold Temperature
  • DNA Transposable Elements*
  • Droughts
  • Gene Expression Regulation, Plant*
  • Gene Regulatory Networks
  • Genome, Plant*
  • Hot Temperature
  • RNA, Long Noncoding / classification
  • RNA, Long Noncoding / genetics*
  • RNA, Long Noncoding / metabolism
  • RNA, Plant / classification
  • RNA, Plant / genetics*
  • RNA, Plant / metabolism
  • Salinity
  • Sequence Analysis, RNA
  • Stress, Physiological / genetics*
  • Zea mays / genetics*
  • Zea mays / metabolism

Substances

  • DNA Transposable Elements
  • RNA, Long Noncoding
  • RNA, Plant