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

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 put...

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Main Authors: Dandan Yang, Huachao Xu, Yue Liu, Mengzhuo Li, Muhammad Ali, Xiangyang Xu, Gang Lu
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-06-01
Series:Frontiers in Plant Science
Subjects:
m6A
Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2021.687826/full
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spelling doaj-76446995bb1e46718b678692d71ca55c2021-06-04T08:16:54ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2021-06-011210.3389/fpls.2021.687826687826RNA N6-Methyladenosine Responds to Low-Temperature Stress in Tomato AnthersDandan Yang0Huachao Xu1Yue Liu2Mengzhuo Li3Muhammad Ali4Xiangyang Xu5Gang Lu6Gang Lu7Department of Horticulture, Zhejiang University, Hangzhou, ChinaDepartment of Horticulture, Zhejiang University, Hangzhou, ChinaDepartment of Horticulture, Zhejiang University, Hangzhou, ChinaDepartment of Horticulture, Zhejiang University, Hangzhou, ChinaDepartment of Horticulture, Zhejiang University, Hangzhou, ChinaCollege of Horticulture, Northeast Agricultural University, Harbin, ChinaDepartment of Horticulture, Zhejiang University, Hangzhou, ChinaKey Laboratory of Horticultural Plant Growth, Development and Quality Improvement, Ministry of Agricultural, Zhejiang University, Hangzhou, ChinaCold 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.https://www.frontiersin.org/articles/10.3389/fpls.2021.687826/fullabscisic acidm6Amoderate low temperaturepollen developmenttomato anther
collection DOAJ
language English
format Article
sources DOAJ
author Dandan Yang
Huachao Xu
Yue Liu
Mengzhuo Li
Muhammad Ali
Xiangyang Xu
Gang Lu
Gang Lu
spellingShingle Dandan Yang
Huachao Xu
Yue Liu
Mengzhuo Li
Muhammad Ali
Xiangyang Xu
Gang Lu
Gang Lu
RNA N6-Methyladenosine Responds to Low-Temperature Stress in Tomato Anthers
Frontiers in Plant Science
abscisic acid
m6A
moderate low temperature
pollen development
tomato anther
author_facet Dandan Yang
Huachao Xu
Yue Liu
Mengzhuo Li
Muhammad Ali
Xiangyang Xu
Gang Lu
Gang Lu
author_sort Dandan Yang
title RNA N6-Methyladenosine Responds to Low-Temperature Stress in Tomato Anthers
title_short RNA N6-Methyladenosine Responds to Low-Temperature Stress in Tomato Anthers
title_full RNA N6-Methyladenosine Responds to Low-Temperature Stress in Tomato Anthers
title_fullStr RNA N6-Methyladenosine Responds to Low-Temperature Stress in Tomato Anthers
title_full_unstemmed RNA N6-Methyladenosine Responds to Low-Temperature Stress in Tomato Anthers
title_sort rna n6-methyladenosine responds to low-temperature stress in tomato anthers
publisher Frontiers Media S.A.
series Frontiers in Plant Science
issn 1664-462X
publishDate 2021-06-01
description 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.
topic abscisic acid
m6A
moderate low temperature
pollen development
tomato anther
url https://www.frontiersin.org/articles/10.3389/fpls.2021.687826/full
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