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

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.

RNA Methylome Reveals the m6A-Mediated Regulation of Flavor Metabolites in Tea Leaves under Solar-Withering

“…Therefore, the mechanism underlying the regulatory effect of m 6 A modification on mRNAs under solar-withering stage needs in-depth dissection. A recent study unveiled that abiotic stress leads to the relocation of m 6 A enrichment on mRNA transcripts [9]. Data from this study showed that m 6 A peaks in CsDXS and other three DMP-associated genes were all distributed within 3′UTR and around stop codon under solar-withering, indicating that solar-withering only affects m 6 A levels of these DMP-associated genes but did not redistribute m 6 A marks on these genes.…”

“…Evidence is accumulating that m 6 A deposition affect the mRNA levels under different developmental stages or environmental stresses [9,13,32,35]. To evaluate the overall correlation between m 6 A modification and gene expression levels under solar-withering, a total of 1137 DMP-associated genes with altered expression levels between samples were selected (Figure S5).…”

“…Reportedly, m 6 A-mediated regulatory mechanism has been shown to affect the normal growth of root and shoot in Arabidopsis thaliana [6,7]. Furthermore, an increasing number of studies suggest that m 6 A modification is also involved in the regulating response to diverse environmental stresses, including drought [8], cold [9], and ultraviolet (UV) radiation stresses [10]. More recently, a few studies have started on the precise functions of m 6 A regulatory mechanism or m 6 A regulatory genes in plant kingdom [11][12][13][14].…”

m6A‐mediated regulation of crop development and stress responses

“…Accordingly, the m 6 A-mediated stress responses have been extensively studied in ª 2022 The Authors. Plant Biotechnology Journal published by Society for Experimental Biology and The Association of Applied Biologists and John Wiley & Sons Ltd., 20, 1447-1455 various crops, including tobacco (Nicotiana tabacum) (Li et al, 2018), rice (Cheng et al, 2021;Shi et al, 2019b;Tian et al, 2021;Zhang et al, 2021a), wheat (Sun et al, 2020;Zhang et al, 2021b), sweet sorghum (Zheng et al, 2021), tomato (Yang et al, 2021), apple (Guo et al, 2021;Mao et al, 2021), and pakchoi (Liu et al, 2020).…”

“…In Arabidopsis, thousands of transcripts contain m 6 A modifications, which distribute preferentially around the stop codon or in the 3′ untranslated region (UTR) (Luo et al ., 2014 ; Wan et al ., 2015 ). This distribution preference is conserved among several important crops, including rice ( Oryza sativa ) (Cheng et al ., 2021 ; Zhang et al ., 2019a ), maize ( Zea mays ) (Miao et al ., 2020 ), wheat ( Triticum aestivum ) (Zhang et al ., 2021b ), tomato ( Solanum lycopersicum ) (Hu et al ., 2021b ; Yang et al ., 2021 ; Zhou et al ., 2019 ), and sweet sorghum ( Sorghum bicolor ) (Zheng et al ., 2021 ) (Figure 1 ). A recent study that compared the m 6 A methylomes for 13 representative plant species spanning over half a billion years of evolution confirmed the conserved distribution of m 6 A modifications in the stop codon and 3′ UTR regions (Miao et al ., 2022 ).…”