A large-scale circular RNA profiling reveals universal molecular mechanisms responsive to drought stress in maize and Arabidopsis

Plant J. 2019 May;98(4):697-713. doi: 10.1111/tpj.14267. Epub 2019 Mar 5.

Abstract

Drought is a major abiotic stress that threatens global food security. Circular RNAs (circRNAs) are endogenous RNAs. How these molecules influence plant stress responses remains elusive. Here, a large-scale circRNA profiling identified 2174 and 1354 high-confidence circRNAs in maize and Arabidopsis, respectively, and most were differentially expressed in response to drought. A substantial number of drought-associated circRNA-hosting genes were involved in conserved or species-specific pathways in drought responses. Comparative analysis revealed that circRNA biogenesis was more complex in maize than in Arabidopsis. In most cases, maize circRNAs were negatively correlated with sRNA accumulation. In 368 maize inbred lines, the circRNA-hosting genes were enriched for single nucleotide polymorphisms (SNPs) associated with circRNA expression and drought tolerance, implying either important roles of circRNAs in maize drought responses or their potential use as biomarkers for breeding drought-tolerant maize. Additionally, the expression levels of circRNAs derived from drought-responsible genes encoding calcium-dependent protein kinase and cytokinin oxidase/dehydrogenase were significantly associated with drought tolerance of maize seedlings. Specifically, Arabidopsis plants overexpressing circGORK (Guard cell outward-rectifying K+ -channel) were hypersensitive to abscisic acid, but insensitive to drought, suggesting a positive role of circGORK in drought tolerance. We report the transcriptomic profiling and transgenic studies of circRNAs in plant drought responses, and provide evidence highlighting the universal molecular mechanisms involved in plant drought tolerance.

Keywords: Arabidopsis (Arabidopsis thaliana); association analysis; circular RNAs; drought stress; maize (Zea mays); transcriptome.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acclimatization / genetics
  • Acclimatization / physiology
  • Arabidopsis / genetics
  • Arabidopsis / metabolism*
  • Breeding
  • Droughts
  • Gene Expression Profiling
  • Gene Expression Regulation, Plant
  • Malondialdehyde / metabolism
  • Oxidoreductases / metabolism
  • Plant Proteins / genetics
  • Plant Proteins / metabolism
  • Plants, Genetically Modified / genetics
  • Proline / metabolism
  • RNA, Circular / genetics
  • RNA, Circular / metabolism*
  • RNA, Plant / genetics
  • RNA, Plant / metabolism*
  • Seedlings
  • Sequence Analysis, RNA
  • Stress, Physiological / genetics
  • Stress, Physiological / physiology*
  • Zea mays / genetics
  • Zea mays / metabolism*

Substances

  • Plant Proteins
  • RNA, Circular
  • RNA, Plant
  • Malondialdehyde
  • Proline
  • Oxidoreductases
  • cytokinin oxidase