Whole-transcriptome profiling and identification of cold tolerance-related ceRNA networks in japonica rice varieties

IntroductionLow-temperature stress negatively impacts rice yield, posing a significant risk to food security. While previous studies have explored the physiological and linear gene expression alterations in rice under low-temperature conditions, the changes in competing endogenous RNA (ceRNA) networ...

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Main Authors: Hao Wang, Yan Jia, Xu Bai, Jin Wang, Ge Liu, Haixing Wang, Yulong Wu, Junying Xin, Huimiao Ma, Zhenyu Liu, Detang Zou, Hongwei Zhao
Format: Article
Language:English
Published: Frontiers Media S.A. 2024-03-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2024.1260591/full
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author Hao Wang
Yan Jia
Xu Bai
Jin Wang
Ge Liu
Haixing Wang
Yulong Wu
Junying Xin
Huimiao Ma
Zhenyu Liu
Detang Zou
Hongwei Zhao
author_facet Hao Wang
Yan Jia
Xu Bai
Jin Wang
Ge Liu
Haixing Wang
Yulong Wu
Junying Xin
Huimiao Ma
Zhenyu Liu
Detang Zou
Hongwei Zhao
author_sort Hao Wang
collection DOAJ
description IntroductionLow-temperature stress negatively impacts rice yield, posing a significant risk to food security. While previous studies have explored the physiological and linear gene expression alterations in rice under low-temperature conditions, the changes in competing endogenous RNA (ceRNA) networks remain largely unexamined.MethodsWe conducted RNA sequencing on two japonica rice varieties with differing cold-tolerance capabilities to establish ceRNA networks. This enabled us to investigate the transcriptional regulatory network and molecular mechanisms that rice employs in response to low-temperature stress.ResultsWe identified 364 differentially expressed circular RNAs (circRNAs), 224 differentially expressed microRNAs (miRNAs), and 12,183 differentially expressed messenger RNAs (mRNAs). WRKY family was the most prominent transcription factor family involved in cold tolerance. Based on the expression patterns and targeted relationships of these differentially expressed RNAs, we discerned five potential ceRNA networks related to low-temperature stress in rice: osa-miR166j-5p from the miR166 family was associated with cold tolerance; osa-miR528-3p and osa-miR156j-3p were linked to stress response; and osa-miR156j-3p was involved in the antioxidant system. In addition, Os03g0152000 in the antioxidant system, as well as Os12g0491800 and Os05g0381400, correlated with the corresponding stress response and circRNAs in the network. A gene sequence difference analysis and phenotypic validation of Os11g0685700 (OsWRKY61) within the WRKY family suggested its potential role in regulating cold tolerance in rice.Discussion and conclusionWe identified Os11g0685700 (OsWRKY61) as a promising candidate gene for enhancing cold tolerance in japonica rice. The candidate miRNAs, mRNAs, and circRNAs uncovered in this study are valuable targets for researchers and breeders. Our findings will facilitate the development of cold-tolerant rice varieties from multiple angles and provide critical directions for future research into the functions of cold-tolerance-related miRNAs, mRNAs, and circRNAs in rice.
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spelling doaj.art-084df191d2fe4ba4b20861816e000f6a2024-03-19T04:47:08ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2024-03-011510.3389/fpls.2024.12605911260591Whole-transcriptome profiling and identification of cold tolerance-related ceRNA networks in japonica rice varietiesHao Wang0Yan Jia1Xu Bai2Jin Wang3Ge Liu4Haixing Wang5Yulong Wu6Junying Xin7Huimiao Ma8Zhenyu Liu9Detang Zou10Hongwei Zhao11Key Laboratory of Germplasm Enhancement, Physiology and Ecology of Food Crops in Cold Region, Ministry of Education, Northeast Agricultural University, Harbin, ChinaKey Laboratory of Germplasm Enhancement, Physiology and Ecology of Food Crops in Cold Region, Ministry of Education, Northeast Agricultural University, Harbin, ChinaKey Laboratory of Germplasm Enhancement, Physiology and Ecology of Food Crops in Cold Region, Ministry of Education, Northeast Agricultural University, Harbin, ChinaBei Da Huang Kenfeng Seed Limited Company, Research and Breeding Center, Harbin, ChinaKey Laboratory of Germplasm Enhancement, Physiology and Ecology of Food Crops in Cold Region, Ministry of Education, Northeast Agricultural University, Harbin, ChinaKey Laboratory of Germplasm Enhancement, Physiology and Ecology of Food Crops in Cold Region, Ministry of Education, Northeast Agricultural University, Harbin, ChinaKey Laboratory of Germplasm Enhancement, Physiology and Ecology of Food Crops in Cold Region, Ministry of Education, Northeast Agricultural University, Harbin, ChinaKey Laboratory of Germplasm Enhancement, Physiology and Ecology of Food Crops in Cold Region, Ministry of Education, Northeast Agricultural University, Harbin, ChinaKey Laboratory of Germplasm Enhancement, Physiology and Ecology of Food Crops in Cold Region, Ministry of Education, Northeast Agricultural University, Harbin, ChinaKey Laboratory of Germplasm Enhancement, Physiology and Ecology of Food Crops in Cold Region, Ministry of Education, Northeast Agricultural University, Harbin, ChinaKey Laboratory of Germplasm Enhancement, Physiology and Ecology of Food Crops in Cold Region, Ministry of Education, Northeast Agricultural University, Harbin, ChinaKey Laboratory of Germplasm Enhancement, Physiology and Ecology of Food Crops in Cold Region, Ministry of Education, Northeast Agricultural University, Harbin, ChinaIntroductionLow-temperature stress negatively impacts rice yield, posing a significant risk to food security. While previous studies have explored the physiological and linear gene expression alterations in rice under low-temperature conditions, the changes in competing endogenous RNA (ceRNA) networks remain largely unexamined.MethodsWe conducted RNA sequencing on two japonica rice varieties with differing cold-tolerance capabilities to establish ceRNA networks. This enabled us to investigate the transcriptional regulatory network and molecular mechanisms that rice employs in response to low-temperature stress.ResultsWe identified 364 differentially expressed circular RNAs (circRNAs), 224 differentially expressed microRNAs (miRNAs), and 12,183 differentially expressed messenger RNAs (mRNAs). WRKY family was the most prominent transcription factor family involved in cold tolerance. Based on the expression patterns and targeted relationships of these differentially expressed RNAs, we discerned five potential ceRNA networks related to low-temperature stress in rice: osa-miR166j-5p from the miR166 family was associated with cold tolerance; osa-miR528-3p and osa-miR156j-3p were linked to stress response; and osa-miR156j-3p was involved in the antioxidant system. In addition, Os03g0152000 in the antioxidant system, as well as Os12g0491800 and Os05g0381400, correlated with the corresponding stress response and circRNAs in the network. A gene sequence difference analysis and phenotypic validation of Os11g0685700 (OsWRKY61) within the WRKY family suggested its potential role in regulating cold tolerance in rice.Discussion and conclusionWe identified Os11g0685700 (OsWRKY61) as a promising candidate gene for enhancing cold tolerance in japonica rice. The candidate miRNAs, mRNAs, and circRNAs uncovered in this study are valuable targets for researchers and breeders. Our findings will facilitate the development of cold-tolerant rice varieties from multiple angles and provide critical directions for future research into the functions of cold-tolerance-related miRNAs, mRNAs, and circRNAs in rice.https://www.frontiersin.org/articles/10.3389/fpls.2024.1260591/fullricelow-temperaturecompeting endogenous RNAmRNAmiRNA
spellingShingle Hao Wang
Yan Jia
Xu Bai
Jin Wang
Ge Liu
Haixing Wang
Yulong Wu
Junying Xin
Huimiao Ma
Zhenyu Liu
Detang Zou
Hongwei Zhao
Whole-transcriptome profiling and identification of cold tolerance-related ceRNA networks in japonica rice varieties
Frontiers in Plant Science
rice
low-temperature
competing endogenous RNA
mRNA
miRNA
title Whole-transcriptome profiling and identification of cold tolerance-related ceRNA networks in japonica rice varieties
title_full Whole-transcriptome profiling and identification of cold tolerance-related ceRNA networks in japonica rice varieties
title_fullStr Whole-transcriptome profiling and identification of cold tolerance-related ceRNA networks in japonica rice varieties
title_full_unstemmed Whole-transcriptome profiling and identification of cold tolerance-related ceRNA networks in japonica rice varieties
title_short Whole-transcriptome profiling and identification of cold tolerance-related ceRNA networks in japonica rice varieties
title_sort whole transcriptome profiling and identification of cold tolerance related cerna networks in japonica rice varieties
topic rice
low-temperature
competing endogenous RNA
mRNA
miRNA
url https://www.frontiersin.org/articles/10.3389/fpls.2024.1260591/full
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