RNA N6-Methyladenosine Responds to Low-Temperature Stress in Tomato Anthers.

Dandan Yang,Yue Liu,Xiangyang Xu,Mengzhuo Li,Huachao Xu,Gang Lu,Muhammad Ali

doi:10.3389/fpls.2021.687826

Dandan Yang, Yue Liu + Show 5 more

Open Access

https://doi.org/10.3389/fpls.2021.687826

Copy DOI

Abstract

Cold stress is a serious threat to subtropical crop pollen development and induces yield decline. N6-methyladenosine (m6A) is the most frequent mRNA modification and plays multiple physiological functions in plant development. However, whether m6A regulates pollen development is unclear, and its putative role in cold stress response remains unknown. Here, we observed that moderate low-temperature (MLT) stress induced pollen abortion in tomato. This phenotype was caused by disruption of tapetum development and pollen exine formation, accompanied by reduced m6A levels in tomato anther. Analysis of m6A-seq data revealed 1,805 transcripts displayed reduced m6A levels and 978 transcripts showed elevated m6A levels in MLT-stressed anthers compared with those in anthers under normal temperature. These differentially m6A enriched transcripts under MLT stress were mainly related to lipid metabolism, adenosine triphosphatase (ATPase) activity, and ATP-binding pathways. An ATP-binding transcript, SlABCG31, had significantly upregulated m6A modification levels, which was inversely correlated to the dramatically downregulated expression level. These changes correlated with higher abscisic acid (ABA) levels in anthers and disrupted pollen wall formation under low-temperature stress. Our findings characterized m6A as a novel layer of complexity in gene expression regulation and established a molecular link between m6A methylation and tomato anther development under low-temperature conditions.

Highlights

In flowering plants, male reproductive development is vulnerable to abiotic stress (Al Mamun et al, 2010; De Storme and Geelen, 2014; Sharma and Nayyar, 2016; Kiran et al, 2019)
We found that m6A methylation was prevalent in tomato anther mRNA but that the levels declined upon moderate low-temperature (MLT) stress
To further investigate the timing of tapetal cell degeneration in pollen development, we performed transferase-mediated dUTP nick-end labeling (TUNEL) assays on different stage anthers from plants grown under NT or MLTR conditions

Summary

Introduction

Male reproductive development is vulnerable to abiotic stress (Al Mamun et al, 2010; De Storme and Geelen, 2014; Sharma and Nayyar, 2016; Kiran et al, 2019). The male gametogenesis of plants depends on a series of complicated processes that lead to the development of premeiotic pollen mother cells into mature pollen grains. Increasing evidence indicates that male sterility induced by low- or high-temperature stresses is linked to tapetal dysfunction. Oliver et al (2007) reported that in rice, male gametogenesis occurring under low-temperature stress, increased abscisic acid (ABA) levels and suppressed the expression of the tapetum-specific cell wall invertase (CWIN), OsINV4, and monosaccharide transporter genes, OSMST8 and OSMST7. These expression changes interfere with tapetum PCD and lead to pollen abortion (Oliver et al, 2007)

Methods

Results

Conclusion