Drought-induced circular RNAs in maize roots: separating signal from noise

Jie Xu; Qi Wang; Xin Tang; Xiaoju Feng; Xiaoyue Zhang; Tianhong Liu; Fengkai Wu; Qingjun Wang; Xuanjun Feng; Qi Tang; Damon Lisch; Yanli Lu

doi:10.1093/plphys/kiae229

Drought-induced circular RNAs in maize roots: separating signal from noise

Plant Physiol. 2024 Apr 26:kiae229. doi: 10.1093/plphys/kiae229. Online ahead of print.

Authors

Jie Xu^{1

2

3

4}, Qi Wang^{1

2

3}, Xin Tang^{1

2

3}, Xiaoju Feng^{1

2

3}, Xiaoyue Zhang^{1

2

3}, Tianhong Liu^{1

2

3}, Fengkai Wu^{1

2

3}, Qingjun Wang^{1

2

3}, Xuanjun Feng^{1

2

3}, Qi Tang^{1

2

3}, Damon Lisch⁵, Yanli Lu^{1

2

3}

Affiliations

¹ State Key Laboratory of Crop Gene Exploration and Utilization in Southwest China, Sichuan Agricultural University.
² Maize Research Institute, Sichuan Agricultural University, Wenjiang 611130, Sichuan, China.
³ Key Laboratory of Biology and Genetic Improvement of Maize in Southwest Region, Ministry of Agriculture, China.
⁴ Key Laboratory of Agricultural Bioinformatics，Ministry of Education，Sichuan Agricultural University, Wenjiang 611130, Sichuan, China.
⁵ Department of Botany and Plant Pathology, Purdue University, West Lafayette, Indiana 47907, USA.

PMID: 38669308
DOI: 10.1093/plphys/kiae229

Abstract

Circular RNAs (CircRNAs) play an important role in diverse biological processes; however, their origin and functions, especially in plants, remain largely unclear. Here, we used two maize (Zea mays) inbred lines, as well as 14 of their derivative RILs with different drought sensitivity, to systematically characterize 8,790 circRNAs in maize roots under well-watered (WW) and water-stress (WS) conditions. We found that a diverse set of circRNAs expressed at significantly higher levels under WS. Enhanced expression of circRNAs was associated with longer flanking introns and an enrichment of long interspersed nuclear element (LINE) retrotransposable elements. The epigenetic marks found at the back-splicing junctions of circRNA-producing genes were markedly different from canonical splicing, characterized by increased levels of H3K36me3/H3K4me1, as well as decreased levels of H3K9Ac/H3K27Ac. We found that genes expressing circRNAs are subject to relaxed selection. The significant enrichment of trait-associated sites along their genic regions suggested that genes giving rise to circRNAs were associated with plant survival rate under drought stress, implying that circRNAs play roles in plant drought responses. Furthermore, we found that overexpression of circMED16, one of the drought-responsive circRNAs, enhances drought tolerance in Arabidopsis (Arabidopsis thaliana). Our results provide a framework for understanding the intricate interplay of epigenetic modifications and how they contribute to the fine-tuning of circRNA expression under drought stress.

Keywords: Circular RNA; Drought stress; Histone modifications; Maize; Transposons.

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