Alternative Splicing Regulation of Glycine-Rich Proteins via Target of Rapamycin-Reactive Oxygen Species Pathway in Arabidopsis Seedlings Upon Glucose Stress

• Published in: Frontiers in plant science Vol. 13; p. 830140
• Main Authors: Du, Chang, Bai, Hai-Yan, Chen, Jing-Jing, Wang, Jia-Hui, Wang, Zhi-Feng, Zhang, Zhong-Hui
• Format: Journal Article
• Language: English
• Published: Switzerland Frontiers Media S.A 15-04-2022
• Subjects: alternative splicing; glucose stress; glycine-rich proteins/GRPs; Plant Science; ROS; RS31; TOR pathway; alternative splicing; Arabidopsis; glycine-rich proteins/GRPs; ROS; TOR pathway; RS31; glucose stress
• ISSN: 1664-462X; 1664-462X
• DOI: 10.3389/fpls.2022.830140

Glucose can serve as both the source of energy and regulatory signaling molecule in plant. Due to the environmental and metabolic change, sugar levels could affect various developmental processes. High glucose environment is hardly conductive to the plant growth but cause development arrest. Increasing evidence indicate that alternative splicing (AS) plays a pivotal role in sugar signaling. However, the regulatory mechanism upon glucose stress remains unclear. The full-length transcriptomes were obtained from the samples of Arabidopsis seedlings with 3% glucose and mock treatment, using Oxford Nanopore sequencing technologies. Further analysis indicated that many genes involved in photosynthesis were significantly repressed and many genes involved in glycolysis, mitochondrial function, and the response to oxidative stress were activated. In total, 1,220 significantly differential alternative splicing (DAS) events related to 619 genes were identified, among which 75.74% belong to intron retention (IR). Notably, more than 20% of DAS events come from a large set of glycine-rich protein (
) family genes, such as
, whose AS types mostly belong to IR. Besides the known productive
transcript isoforms, we identified a lot of splicing variants with diverse introns spliced in messenger RNA (mRNA) region coding the glycine-rich (GR) domain. The AS pattern of
s changed and particularly, the productive
s increased upon glucose stress. These ASs of
pre-mRNAs triggered by glucose stress could be abolished by AZD-8055, which is an ATP competitive inhibitor for the target of rapamycin (TOR) kinase but could be mimicked by H
O
. Additionally, AS pattern change of
(
)
TOR pathway, which was previously described in response to light and sucrose signaling, was also induced in a similar manner by both glucose stress and reactive oxygen species (ROS). Here we conclude that (i) glucose stress suppresses photosynthesis and activates the glycolysis-mitochondria energy relay and ROS scavenging system; (ii) glucose stress triggers transcriptome-wide AS pattern changes including a large set of splicing factors, such as
s and
; (iii) high sugars regulate AS pattern change of both
s and
TOR-ROS pathway. The results from this study will deepen our understanding of the AS regulation mechanism in sugar signaling.