MicroRNA162 regulates stomatal conductance in response to low night temperature stress via abscisic acid signaling pathway in tomato
MicroRNAs (miRNAs) mediate the degradation of target mRNA and inhibit mRNA translation to regulate gene expression at the transcriptional and post-transcriptional levels in response to environmental stress in plants. We characterized the post-transcriptional mechanism by deep sequencing small RNA (s...
Main Authors: | , , , , , , , |
---|---|
Format: | Article |
Language: | English |
Published: |
Frontiers Media S.A.
2023-03-01
|
Series: | Frontiers in Plant Science |
Subjects: | |
Online Access: | https://www.frontiersin.org/articles/10.3389/fpls.2023.1045112/full |
_version_ | 1811161696308297728 |
---|---|
author | Yangyang Li Yangyang Li Yangyang Li Yang Liu Yang Liu Zhenhua Gao Zhenhua Gao Zhenhua Gao Feng Wang Feng Wang Feng Wang Tao Xu Tao Xu Tao Xu Mingfang Qi Mingfang Qi Mingfang Qi Yufeng Liu Yufeng Liu Yufeng Liu Tianlai Li Tianlai Li Tianlai Li |
author_facet | Yangyang Li Yangyang Li Yangyang Li Yang Liu Yang Liu Zhenhua Gao Zhenhua Gao Zhenhua Gao Feng Wang Feng Wang Feng Wang Tao Xu Tao Xu Tao Xu Mingfang Qi Mingfang Qi Mingfang Qi Yufeng Liu Yufeng Liu Yufeng Liu Tianlai Li Tianlai Li Tianlai Li |
author_sort | Yangyang Li |
collection | DOAJ |
description | MicroRNAs (miRNAs) mediate the degradation of target mRNA and inhibit mRNA translation to regulate gene expression at the transcriptional and post-transcriptional levels in response to environmental stress in plants. We characterized the post-transcriptional mechanism by deep sequencing small RNA (sRNA) to examine how miRNAs were involved in low night temperature (LNT) stress in tomato and whether the molecular mechanism depended on the abscisic acid (ABA) signaling pathway. We annotated conserved miRNAs and novel miRNAs with four sRNA libraries composed of wild-type (WT) tomato plants and ABA-deficient mutant (sit) plants under normal growth and LNT stress conditions. Reverse genetics analysis suggested that miR162 participated in LNT resistance and the ABA-dependent signaling pathway in tomato. miR162-overexpressing (pRI-miR162) and miR162-silenced (pRNAi-miR162) transgenic tomato plants were generated to evaluate miR162 functions in response to LNT stress. miR162 deficiency exhibited high photosynthetic capacity and regulated stomatal opening, suggesting negative regulation of miR162 in the ABA-dependent signaling pathway in response to LNT stress. As feedback regulation, miR162 positively regulated ABA to maintain homeostasis of tomato under diverse abiotic stresses. The mRNA of DICER-LIKE1 (DCL1) was targeted by miR162, and miR162 inhibited DCL1 cleavage in LNT response, including the regulation of miRNA160/164/171a and their targets. The DCL1-deficient mutants (dcl1) with CRISPR/Cas9 prevented stomatal opening to influence photosynthesis in the ABA signaling pathway under LNT stress. Finally, we established the regulatory mechanism of ABA-miR162-DCL1, which systematically mediated cold tolerance in tomato. This study suggests that post-transcriptional modulators acted as systemic signal responders via the stress hormone signaling pathway, and the model at the post-transcriptional level presents a new direction for research in plant abiotic stress resistance. |
first_indexed | 2024-04-10T06:18:33Z |
format | Article |
id | doaj.art-75a47787117e4ed8b76552a6e3abd20d |
institution | Directory Open Access Journal |
issn | 1664-462X |
language | English |
last_indexed | 2024-04-10T06:18:33Z |
publishDate | 2023-03-01 |
publisher | Frontiers Media S.A. |
record_format | Article |
series | Frontiers in Plant Science |
spelling | doaj.art-75a47787117e4ed8b76552a6e3abd20d2023-03-02T05:20:54ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2023-03-011410.3389/fpls.2023.10451121045112MicroRNA162 regulates stomatal conductance in response to low night temperature stress via abscisic acid signaling pathway in tomatoYangyang Li0Yangyang Li1Yangyang Li2Yang Liu3Yang Liu4Zhenhua Gao5Zhenhua Gao6Zhenhua Gao7Feng Wang8Feng Wang9Feng Wang10Tao Xu11Tao Xu12Tao Xu13Mingfang Qi14Mingfang Qi15Mingfang Qi16Yufeng Liu17Yufeng Liu18Yufeng Liu19Tianlai Li20Tianlai Li21Tianlai Li22Department of Horticulture, Shenyang Agricultural University, Shenyang, ChinaKey Laboratory of Protected Horticulture of Education Ministry and Liaoning Province, Shenyang, ChinaCollaborative Innovation Center of Protected Vegetable Surrounds Bohai Gulf Region, Shenyang, ChinaDepartment of Horticulture, Shenyang Agricultural University, Shenyang, ChinaTongliao Agricultural Technology Extension Center, Tongliao, ChinaDepartment of Horticulture, Shenyang Agricultural University, Shenyang, ChinaKey Laboratory of Protected Horticulture of Education Ministry and Liaoning Province, Shenyang, ChinaCollaborative Innovation Center of Protected Vegetable Surrounds Bohai Gulf Region, Shenyang, ChinaDepartment of Horticulture, Shenyang Agricultural University, Shenyang, ChinaKey Laboratory of Protected Horticulture of Education Ministry and Liaoning Province, Shenyang, ChinaCollaborative Innovation Center of Protected Vegetable Surrounds Bohai Gulf Region, Shenyang, ChinaDepartment of Horticulture, Shenyang Agricultural University, Shenyang, ChinaKey Laboratory of Protected Horticulture of Education Ministry and Liaoning Province, Shenyang, ChinaCollaborative Innovation Center of Protected Vegetable Surrounds Bohai Gulf Region, Shenyang, ChinaDepartment of Horticulture, Shenyang Agricultural University, Shenyang, ChinaKey Laboratory of Protected Horticulture of Education Ministry and Liaoning Province, Shenyang, ChinaCollaborative Innovation Center of Protected Vegetable Surrounds Bohai Gulf Region, Shenyang, ChinaDepartment of Horticulture, Shenyang Agricultural University, Shenyang, ChinaKey Laboratory of Protected Horticulture of Education Ministry and Liaoning Province, Shenyang, ChinaCollaborative Innovation Center of Protected Vegetable Surrounds Bohai Gulf Region, Shenyang, ChinaDepartment of Horticulture, Shenyang Agricultural University, Shenyang, ChinaKey Laboratory of Protected Horticulture of Education Ministry and Liaoning Province, Shenyang, ChinaCollaborative Innovation Center of Protected Vegetable Surrounds Bohai Gulf Region, Shenyang, ChinaMicroRNAs (miRNAs) mediate the degradation of target mRNA and inhibit mRNA translation to regulate gene expression at the transcriptional and post-transcriptional levels in response to environmental stress in plants. We characterized the post-transcriptional mechanism by deep sequencing small RNA (sRNA) to examine how miRNAs were involved in low night temperature (LNT) stress in tomato and whether the molecular mechanism depended on the abscisic acid (ABA) signaling pathway. We annotated conserved miRNAs and novel miRNAs with four sRNA libraries composed of wild-type (WT) tomato plants and ABA-deficient mutant (sit) plants under normal growth and LNT stress conditions. Reverse genetics analysis suggested that miR162 participated in LNT resistance and the ABA-dependent signaling pathway in tomato. miR162-overexpressing (pRI-miR162) and miR162-silenced (pRNAi-miR162) transgenic tomato plants were generated to evaluate miR162 functions in response to LNT stress. miR162 deficiency exhibited high photosynthetic capacity and regulated stomatal opening, suggesting negative regulation of miR162 in the ABA-dependent signaling pathway in response to LNT stress. As feedback regulation, miR162 positively regulated ABA to maintain homeostasis of tomato under diverse abiotic stresses. The mRNA of DICER-LIKE1 (DCL1) was targeted by miR162, and miR162 inhibited DCL1 cleavage in LNT response, including the regulation of miRNA160/164/171a and their targets. The DCL1-deficient mutants (dcl1) with CRISPR/Cas9 prevented stomatal opening to influence photosynthesis in the ABA signaling pathway under LNT stress. Finally, we established the regulatory mechanism of ABA-miR162-DCL1, which systematically mediated cold tolerance in tomato. This study suggests that post-transcriptional modulators acted as systemic signal responders via the stress hormone signaling pathway, and the model at the post-transcriptional level presents a new direction for research in plant abiotic stress resistance.https://www.frontiersin.org/articles/10.3389/fpls.2023.1045112/fullmicroRNAsABAstomataresistancecold stresstomato |
spellingShingle | Yangyang Li Yangyang Li Yangyang Li Yang Liu Yang Liu Zhenhua Gao Zhenhua Gao Zhenhua Gao Feng Wang Feng Wang Feng Wang Tao Xu Tao Xu Tao Xu Mingfang Qi Mingfang Qi Mingfang Qi Yufeng Liu Yufeng Liu Yufeng Liu Tianlai Li Tianlai Li Tianlai Li MicroRNA162 regulates stomatal conductance in response to low night temperature stress via abscisic acid signaling pathway in tomato Frontiers in Plant Science microRNAs ABA stomata resistance cold stress tomato |
title | MicroRNA162 regulates stomatal conductance in response to low night temperature stress via abscisic acid signaling pathway in tomato |
title_full | MicroRNA162 regulates stomatal conductance in response to low night temperature stress via abscisic acid signaling pathway in tomato |
title_fullStr | MicroRNA162 regulates stomatal conductance in response to low night temperature stress via abscisic acid signaling pathway in tomato |
title_full_unstemmed | MicroRNA162 regulates stomatal conductance in response to low night temperature stress via abscisic acid signaling pathway in tomato |
title_short | MicroRNA162 regulates stomatal conductance in response to low night temperature stress via abscisic acid signaling pathway in tomato |
title_sort | microrna162 regulates stomatal conductance in response to low night temperature stress via abscisic acid signaling pathway in tomato |
topic | microRNAs ABA stomata resistance cold stress tomato |
url | https://www.frontiersin.org/articles/10.3389/fpls.2023.1045112/full |
work_keys_str_mv | AT yangyangli microrna162regulatesstomatalconductanceinresponsetolownighttemperaturestressviaabscisicacidsignalingpathwayintomato AT yangyangli microrna162regulatesstomatalconductanceinresponsetolownighttemperaturestressviaabscisicacidsignalingpathwayintomato AT yangyangli microrna162regulatesstomatalconductanceinresponsetolownighttemperaturestressviaabscisicacidsignalingpathwayintomato AT yangliu microrna162regulatesstomatalconductanceinresponsetolownighttemperaturestressviaabscisicacidsignalingpathwayintomato AT yangliu microrna162regulatesstomatalconductanceinresponsetolownighttemperaturestressviaabscisicacidsignalingpathwayintomato AT zhenhuagao microrna162regulatesstomatalconductanceinresponsetolownighttemperaturestressviaabscisicacidsignalingpathwayintomato AT zhenhuagao microrna162regulatesstomatalconductanceinresponsetolownighttemperaturestressviaabscisicacidsignalingpathwayintomato AT zhenhuagao microrna162regulatesstomatalconductanceinresponsetolownighttemperaturestressviaabscisicacidsignalingpathwayintomato AT fengwang microrna162regulatesstomatalconductanceinresponsetolownighttemperaturestressviaabscisicacidsignalingpathwayintomato AT fengwang microrna162regulatesstomatalconductanceinresponsetolownighttemperaturestressviaabscisicacidsignalingpathwayintomato AT fengwang microrna162regulatesstomatalconductanceinresponsetolownighttemperaturestressviaabscisicacidsignalingpathwayintomato AT taoxu microrna162regulatesstomatalconductanceinresponsetolownighttemperaturestressviaabscisicacidsignalingpathwayintomato AT taoxu microrna162regulatesstomatalconductanceinresponsetolownighttemperaturestressviaabscisicacidsignalingpathwayintomato AT taoxu microrna162regulatesstomatalconductanceinresponsetolownighttemperaturestressviaabscisicacidsignalingpathwayintomato AT mingfangqi microrna162regulatesstomatalconductanceinresponsetolownighttemperaturestressviaabscisicacidsignalingpathwayintomato AT mingfangqi microrna162regulatesstomatalconductanceinresponsetolownighttemperaturestressviaabscisicacidsignalingpathwayintomato AT mingfangqi microrna162regulatesstomatalconductanceinresponsetolownighttemperaturestressviaabscisicacidsignalingpathwayintomato AT yufengliu microrna162regulatesstomatalconductanceinresponsetolownighttemperaturestressviaabscisicacidsignalingpathwayintomato AT yufengliu microrna162regulatesstomatalconductanceinresponsetolownighttemperaturestressviaabscisicacidsignalingpathwayintomato AT yufengliu microrna162regulatesstomatalconductanceinresponsetolownighttemperaturestressviaabscisicacidsignalingpathwayintomato AT tianlaili microrna162regulatesstomatalconductanceinresponsetolownighttemperaturestressviaabscisicacidsignalingpathwayintomato AT tianlaili microrna162regulatesstomatalconductanceinresponsetolownighttemperaturestressviaabscisicacidsignalingpathwayintomato AT tianlaili microrna162regulatesstomatalconductanceinresponsetolownighttemperaturestressviaabscisicacidsignalingpathwayintomato |