Dynamic landscape of long noncoding RNAs during leaf aging in Arabidopsis

Jung Yeon Kim; Juhyeon Lee; Myeong Hoon Kang; Tran Thi My Trang; Jusung Lee; Heeho Lee; Hyobin Jeong; Pyung Ok Lim

doi:10.3389/fpls.2022.1068163

Dynamic landscape of long noncoding RNAs during leaf aging in Arabidopsis

Front Plant Sci. 2022 Dec 1:13:1068163. doi: 10.3389/fpls.2022.1068163. eCollection 2022.

Authors

Jung Yeon Kim¹, Juhyeon Lee¹, Myeong Hoon Kang¹, Tran Thi My Trang¹, Jusung Lee¹, Heeho Lee¹, Hyobin Jeong^{2

3}, Pyung Ok Lim¹

Affiliations

¹ Department of New Biology, Daegu Gyeongbuk Institute of Science and Technology (DGIST), Daegu, South Korea.
² Genome Biology Unit, European Molecular Biology Laboratory (EMBL), Meyerhofstraße 1, Heidelberg, Germany.
³ Department of Life Science, College of Natural Sciences, Hanyang University, Seoul, South Korea.

Abstract

Leaf senescence, the last stage of leaf development, is essential for whole-plant fitness as it marks the relocation of nutrients from senescing leaves to reproductive or other developing organs. Temporally coordinated physiological and functional changes along leaf aging are fine-tuned by a highly regulated genetic program involving multi-layered regulatory mechanisms. Long noncoding RNAs (lncRNAs) are newly emerging as hidden players in many biological processes; however, their contribution to leaf senescence has been largely unknown. Here, we performed comprehensive analyses of RNA-seq data representing all developmental stages of leaves to determine the genome-wide lncRNA landscape along leaf aging. A total of 771 lncRNAs, including 232 unannotated lncRNAs, were identified. Time-course analysis revealed 446 among 771 developmental age-related lncRNAs (AR-lncRNAs). Intriguingly, the expression of AR-lncRNAs was regulated more dynamically in senescing leaves than in growing leaves, revealing the relevant contribution of these lncRNAs to leaf senescence. Further analyses enabled us to infer the function of lncRNAs, based on their interacting miRNA or mRNA partners. We considered functionally diverse lncRNAs including antisense lncRNAs (which regulate overlapping protein-coding genes), competitive endogenous RNAs (ceRNAs; which regulate paired mRNAs using miRNAs as anchors), and mRNA-interacting lncRNAs (which affect the stability of mRNAs). Furthermore, we experimentally validated the senescence regulatory function of three novel AR-lncRNAs including one antisense lncRNA and two mRNA-interacting lncRNAs through molecular and phenotypic analyses. Our study provides a valuable resource of AR-lncRNAs and potential regulatory networks that link the function of coding mRNA and AR-lncRNAs. Together, our results reveal AR-lncRNAs as important elements in the leaf senescence process.

Keywords: Arabidopsis; RNA-RNA interaction; leaf senescence; long noncoding RNA; transcriptome (RNA-seq).