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

Abstract

BackgroundSeveral 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.ResultsWe 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.ConclusionsOur 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.

Genomic and Transcriptomic Analysis Identified Novel Putative Cassava lncRNAs Involved in Cold and Drought Stress

“…The WRKY family transcription factors have been widely studied in various plants under cold stress [72][73][74]. Some TFs in the WRKY family have been reported as hubs in plant co-expression networks under abiotic stress, including cold stress [75]. In this work, a novel putative lncRNA (ncP456) was predicted to directly bind complementarily with Manes.09G112700, annotated as WRKY DNA-binding protein 33 ( Figure S22).…”

Genomics of Evolutionary Novelty in Hybrids and Polyploids

“…Moreover, as noted above, TEs are the main target of epigenetic silencing, and therefore, the insertion of a TE within or close to a gene may bring the silencing machinery to this gene altering its expression ( Zhang H. et al, 2018 ). In addition to bringing new promoters and promoter elements, TEs can also be the source of small RNAs that regulate gene expression ( McCue and Slotkin, 2012 ), and in particular that of defense-related genes ( Poretti et al, 2020 ), and it has been recently shown that they can also contribute long non-coding RNAs that regulate plant stress responses ( Lv et al, 2019 ). TEs are therefore an important force that facilitates plant, and also animal ( Rech et al, 2019 ) and yeast ( Esnault et al, 2019 ), adaptation to stress.…”

The Emerging Role of Long Non-Coding RNAs in Plant Defense Against Fungal Stress

“…The second is that lncRNAs tend to be expressed at lower levels than protein-coding genes, but with precise spatio-temporal patterns [55,56]. Thirdly, some lncRNAs contain parts of an exon, while a proportion of lncRNAs are derived from transposable elements (TEs) or contain remnants of TEs [57,58]. Here, we focus on the advance and regulatory function in plants responding to fungi underlying these properties and recent research on lncRNAs.…”

“…However, 1077 DE-lncRNA were predicted in maize during abiotic stress, like heat, cold, salt, and drought. Studies inferring co-expression networks revealed that 39 lncRNAs are major hubs in the co-expression networks, and 18 lncRNAs were considered to be derived from long-terminal-repeat transposable elements (TEs) [57]. A ceRNA network was constructed with the identified DElncRNAs, DEmiRNAs, and DEmRNAs in the roots of Ziyang Xiangcheng (Citrus junos) under Cu toxicity [97].…”