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An integrated analysis of the rice transcriptome and lipidome reveals lipid metabolism plays a central role in rice cold tolerance

BACKGROUND: Rice (Oryza sativa L.) is one of the most widely grown food crops, and its yield and quality are particularly important for a warm-saturated diet. Cold stress restricts rice growth, development, and yield; however, the specific mechanism of cold tolerance in rice remains unknown. RESULTS...

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Autores principales: Liu, Hualong, Xin, Wei, Wang, Yinglin, Zhang, Dezhuang, Wang, Jingguo, Zheng, Hongliang, Yang, Luomiao, Nie, Shoujun, Zou, Detang
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8889772/
https://www.ncbi.nlm.nih.gov/pubmed/35232394
http://dx.doi.org/10.1186/s12870-022-03468-1
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author Liu, Hualong
Xin, Wei
Wang, Yinglin
Zhang, Dezhuang
Wang, Jingguo
Zheng, Hongliang
Yang, Luomiao
Nie, Shoujun
Zou, Detang
author_facet Liu, Hualong
Xin, Wei
Wang, Yinglin
Zhang, Dezhuang
Wang, Jingguo
Zheng, Hongliang
Yang, Luomiao
Nie, Shoujun
Zou, Detang
author_sort Liu, Hualong
collection PubMed
description BACKGROUND: Rice (Oryza sativa L.) is one of the most widely grown food crops, and its yield and quality are particularly important for a warm-saturated diet. Cold stress restricts rice growth, development, and yield; however, the specific mechanism of cold tolerance in rice remains unknown. RESULTS: The analysis of leaf physiological and photosynthetic characteristics showed that the two rice varieties were significantly affected by cold stress, but the cold-tolerant variety KY131 had more stable physiological characteristics, maintaining relatively good photosynthetic capacity. To better explore the transcriptional regulation mechanism and biological basis of rice response to cold stress, a comprehensive analysis of the rice transcriptome and lipidome under low temperature and control temperature conditions was carried out. The transcriptomic analysis revealed that lipid metabolism, including membrane lipid and fatty acid metabolism, may be an important factor in rice cold tolerance, and 397 lipid metabolism related genes have been identified. Lipidomics data confirmed the importance of membrane lipid remodeling and fatty acid unsaturation for rice adaptation to cold stress. This indicates that the changes in the fluidity and integrity of the photosynthetic membrane under cold stress lead to the reduction of photosynthetic capacity, which could be relieved by increased levels of monogalactosyldiacylglycerol that mainly caused by markedly increased expression of levels of 1,2-diacylglycerol 3-beta-galactosyltransferase (MGD). The upregulation of phosphatidate phosphatase (PAP2) inhibited the excessive accumulation of phosphatidate (PA) to produce more phosphatidylcholine (PC), phosphatidylethanolamine (PE), and phosphatidylglycerol (PG), thereby preventing of membrane phase transition under cold stress. In addition, fatty acid β-oxidation is worth further study in rice cold tolerance. Finally, we constructed a metabolic model for the regulatory mechanism of cold tolerance in rice, in which the advanced lipid metabolism system plays a central role. CONCLUSIONS: Lipidome analysis showed that membrane lipid composition and unsaturation were significantly affected, especially phospholipids and galactolipids. Our study provides new information to further understand the response of rice to cold stress. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12870-022-03468-1.
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spelling pubmed-88897722022-03-09 An integrated analysis of the rice transcriptome and lipidome reveals lipid metabolism plays a central role in rice cold tolerance Liu, Hualong Xin, Wei Wang, Yinglin Zhang, Dezhuang Wang, Jingguo Zheng, Hongliang Yang, Luomiao Nie, Shoujun Zou, Detang BMC Plant Biol Research BACKGROUND: Rice (Oryza sativa L.) is one of the most widely grown food crops, and its yield and quality are particularly important for a warm-saturated diet. Cold stress restricts rice growth, development, and yield; however, the specific mechanism of cold tolerance in rice remains unknown. RESULTS: The analysis of leaf physiological and photosynthetic characteristics showed that the two rice varieties were significantly affected by cold stress, but the cold-tolerant variety KY131 had more stable physiological characteristics, maintaining relatively good photosynthetic capacity. To better explore the transcriptional regulation mechanism and biological basis of rice response to cold stress, a comprehensive analysis of the rice transcriptome and lipidome under low temperature and control temperature conditions was carried out. The transcriptomic analysis revealed that lipid metabolism, including membrane lipid and fatty acid metabolism, may be an important factor in rice cold tolerance, and 397 lipid metabolism related genes have been identified. Lipidomics data confirmed the importance of membrane lipid remodeling and fatty acid unsaturation for rice adaptation to cold stress. This indicates that the changes in the fluidity and integrity of the photosynthetic membrane under cold stress lead to the reduction of photosynthetic capacity, which could be relieved by increased levels of monogalactosyldiacylglycerol that mainly caused by markedly increased expression of levels of 1,2-diacylglycerol 3-beta-galactosyltransferase (MGD). The upregulation of phosphatidate phosphatase (PAP2) inhibited the excessive accumulation of phosphatidate (PA) to produce more phosphatidylcholine (PC), phosphatidylethanolamine (PE), and phosphatidylglycerol (PG), thereby preventing of membrane phase transition under cold stress. In addition, fatty acid β-oxidation is worth further study in rice cold tolerance. Finally, we constructed a metabolic model for the regulatory mechanism of cold tolerance in rice, in which the advanced lipid metabolism system plays a central role. CONCLUSIONS: Lipidome analysis showed that membrane lipid composition and unsaturation were significantly affected, especially phospholipids and galactolipids. Our study provides new information to further understand the response of rice to cold stress. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12870-022-03468-1. BioMed Central 2022-03-02 /pmc/articles/PMC8889772/ /pubmed/35232394 http://dx.doi.org/10.1186/s12870-022-03468-1 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Liu, Hualong
Xin, Wei
Wang, Yinglin
Zhang, Dezhuang
Wang, Jingguo
Zheng, Hongliang
Yang, Luomiao
Nie, Shoujun
Zou, Detang
An integrated analysis of the rice transcriptome and lipidome reveals lipid metabolism plays a central role in rice cold tolerance
title An integrated analysis of the rice transcriptome and lipidome reveals lipid metabolism plays a central role in rice cold tolerance
title_full An integrated analysis of the rice transcriptome and lipidome reveals lipid metabolism plays a central role in rice cold tolerance
title_fullStr An integrated analysis of the rice transcriptome and lipidome reveals lipid metabolism plays a central role in rice cold tolerance
title_full_unstemmed An integrated analysis of the rice transcriptome and lipidome reveals lipid metabolism plays a central role in rice cold tolerance
title_short An integrated analysis of the rice transcriptome and lipidome reveals lipid metabolism plays a central role in rice cold tolerance
title_sort integrated analysis of the rice transcriptome and lipidome reveals lipid metabolism plays a central role in rice cold tolerance
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8889772/
https://www.ncbi.nlm.nih.gov/pubmed/35232394
http://dx.doi.org/10.1186/s12870-022-03468-1
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