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Genome-wide analysis of plant nat-siRNAs reveals insights into their distribution, biogenesis and function

  • Author(s): Zhang, Xiaoming
  • Xia, Jing
  • Lii, Yifan E
  • Barrera-Figueroa, Blanca E
  • Zhou, Xuefeng
  • Gao, Shang
  • Lu, Lu
  • Niu, Dongdong
  • Chen, Zheng
  • Leung, Christy
  • Wong, Timothy
  • Zhang, Huiming
  • Guo, Jianhua
  • Li, Yi
  • Liu, Renyi
  • Liang, Wanqi
  • Zhu, Jian-Kang
  • Zhang, Weixiong
  • Jin, Hailing
  • et al.
Abstract

Abstract Background Many eukaryotic genomes encode cis-natural antisense transcripts (cis-NATs). Sense and antisense transcripts may form double-stranded RNAs that are processed by the RNA interference machinery into small interfering RNAs (siRNAs). A few so-called nat-siRNAs have been reported in plants, mammals, Drosophila, and yeasts. However, many questions remain regarding the features and biogenesis of nat-siRNAs. Results Through deep sequencing, we identified more than 17,000 unique siRNAs corresponding to cis-NATs from biotic and abiotic stress-challenged Arabidopsis thaliana and 56,000 from abiotic stress-treated rice. These siRNAs were enriched in the overlapping regions of NATs and exhibited either site-specific or distributed patterns, often with strand bias. Out of 1,439 and 767 cis-NAT pairs identified in Arabidopsis and rice, respectively, 84 and 119 could generate at least 10 siRNAs per million reads from the overlapping regions. Among them, 16 cis-NAT pairs from Arabidopsis and 34 from rice gave rise to nat-siRNAs exclusively in the overlap regions. Genetic analysis showed that the overlapping double-stranded RNAs could be processed by Dicer-like 1 (DCL1) and/or DCL3. The DCL3-dependent nat-siRNAs were also dependent on RNA-dependent RNA polymerase 2 (RDR2) and plant-specific RNA polymerase IV (PolIV), whereas only a fraction of DCL1-dependent nat-siRNAs was RDR- and PolIV-dependent. Furthermore, the levels of some nat-siRNAs were regulated by specific biotic or abiotic stress conditions in Arabidopsis and rice. Conclusions Our results suggest that nat-siRNAs display distinct distribution patterns and are generated by DCL1 and/or DCL3. Our analysis further supported the existence of nat-siRNAs in plants and advanced our understanding of their characteristics.

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