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Transcriptomic, proteomic, and physiological comparative analyses of flooding mitigation of the damage induced by low-temperature stress in direct seeded early indica rice at the seedling stage

BACKGROUND: Low temperature (LT) often occurs at the seedling stage in the early rice-growing season, especially for direct seeded early-season indica rice, and using flooding irrigation can mitigate LT damage in rice seedlings. The molecular mechanism by which flooding mitigates the damage induced...

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Autores principales: Wang, Wenxia, Du, Jie, Chen, Liming, Zeng, Yongjun, Tan, Xueming, Shi, Qinghua, Pan, Xiaohua, Wu, Ziming, Zeng, Yanhua
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7952222/
https://www.ncbi.nlm.nih.gov/pubmed/33706696
http://dx.doi.org/10.1186/s12864-021-07458-9
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author Wang, Wenxia
Du, Jie
Chen, Liming
Zeng, Yongjun
Tan, Xueming
Shi, Qinghua
Pan, Xiaohua
Wu, Ziming
Zeng, Yanhua
author_facet Wang, Wenxia
Du, Jie
Chen, Liming
Zeng, Yongjun
Tan, Xueming
Shi, Qinghua
Pan, Xiaohua
Wu, Ziming
Zeng, Yanhua
author_sort Wang, Wenxia
collection PubMed
description BACKGROUND: Low temperature (LT) often occurs at the seedling stage in the early rice-growing season, especially for direct seeded early-season indica rice, and using flooding irrigation can mitigate LT damage in rice seedlings. The molecular mechanism by which flooding mitigates the damage induced by LT stress has not been fully elucidated. Thus, LT stress at 8 °C, LT accompanied by flooding (LTF) and CK (control) treatments were established for 3 days to determine the transcriptomic, proteomic and physiological response in direct seeded rice seedlings at the seedling stage. RESULTS: LT damaged chloroplasts, and thylakoid lamellae, and increased osmiophilic bodies and starch grains compared to CK, but LTF alleviated the damage to chloroplast structure caused by LT. The physiological characteristics of treated plants showed that compared with LT, LTF significantly increased the contents of rubisco, chlorophyll, PEPCK, ATP and GA(3) but significantly decreased soluble protein, MDA and ABA contents. 4D-label-free quantitative proteomic profiling showed that photosynthesis-responsive proteins, such as phytochrome, as well as chlorophyll and the tricarboxylic acid cycle were significantly downregulated in LT/CK and LTF/CK comparison groups. However, compared with LT, phytochrome, chlorophyllide oxygenase activity and the glucan branching enzyme in LTF were significantly upregulated in rice leaves. Transcriptomic and proteomic studies identified 72,818 transcripts and 5639 proteins, and 4983 genes that were identified at both the transcriptome and proteome levels. Differentially expressed genes (DEGs) and differentially expressed proteins (DEPs) were significantly enriched in glycine, serine and threonine metabolism, biosynthesis of secondary metabolites, glycolysis/gluconeogenesis and metabolic pathways. CONCLUSION: Through transcriptomic, proteomic and physiological analyses, we determined that a variety of metabolic pathway changes were induced by LT and LTF. GO and KEGG enrichment analyses demonstrated that DEGs and DEPs were associated with photosynthesis pathways, antioxidant enzymes and energy metabolism pathway-related proteins. Our study provided new insights for efforts to reduce the damage to direct seeded rice caused by low-temperature stress and provided a breeding target for low temperature flooding-resistant cultivars. Further analysis of translational regulation and metabolites may help to elucidate the molecular mechanisms by which flooding mitigates low-temperature stress in direct seeded early indica rice at the seedling stage. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-021-07458-9.
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spelling pubmed-79522222021-03-12 Transcriptomic, proteomic, and physiological comparative analyses of flooding mitigation of the damage induced by low-temperature stress in direct seeded early indica rice at the seedling stage Wang, Wenxia Du, Jie Chen, Liming Zeng, Yongjun Tan, Xueming Shi, Qinghua Pan, Xiaohua Wu, Ziming Zeng, Yanhua BMC Genomics Research Article BACKGROUND: Low temperature (LT) often occurs at the seedling stage in the early rice-growing season, especially for direct seeded early-season indica rice, and using flooding irrigation can mitigate LT damage in rice seedlings. The molecular mechanism by which flooding mitigates the damage induced by LT stress has not been fully elucidated. Thus, LT stress at 8 °C, LT accompanied by flooding (LTF) and CK (control) treatments were established for 3 days to determine the transcriptomic, proteomic and physiological response in direct seeded rice seedlings at the seedling stage. RESULTS: LT damaged chloroplasts, and thylakoid lamellae, and increased osmiophilic bodies and starch grains compared to CK, but LTF alleviated the damage to chloroplast structure caused by LT. The physiological characteristics of treated plants showed that compared with LT, LTF significantly increased the contents of rubisco, chlorophyll, PEPCK, ATP and GA(3) but significantly decreased soluble protein, MDA and ABA contents. 4D-label-free quantitative proteomic profiling showed that photosynthesis-responsive proteins, such as phytochrome, as well as chlorophyll and the tricarboxylic acid cycle were significantly downregulated in LT/CK and LTF/CK comparison groups. However, compared with LT, phytochrome, chlorophyllide oxygenase activity and the glucan branching enzyme in LTF were significantly upregulated in rice leaves. Transcriptomic and proteomic studies identified 72,818 transcripts and 5639 proteins, and 4983 genes that were identified at both the transcriptome and proteome levels. Differentially expressed genes (DEGs) and differentially expressed proteins (DEPs) were significantly enriched in glycine, serine and threonine metabolism, biosynthesis of secondary metabolites, glycolysis/gluconeogenesis and metabolic pathways. CONCLUSION: Through transcriptomic, proteomic and physiological analyses, we determined that a variety of metabolic pathway changes were induced by LT and LTF. GO and KEGG enrichment analyses demonstrated that DEGs and DEPs were associated with photosynthesis pathways, antioxidant enzymes and energy metabolism pathway-related proteins. Our study provided new insights for efforts to reduce the damage to direct seeded rice caused by low-temperature stress and provided a breeding target for low temperature flooding-resistant cultivars. Further analysis of translational regulation and metabolites may help to elucidate the molecular mechanisms by which flooding mitigates low-temperature stress in direct seeded early indica rice at the seedling stage. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-021-07458-9. BioMed Central 2021-03-12 /pmc/articles/PMC7952222/ /pubmed/33706696 http://dx.doi.org/10.1186/s12864-021-07458-9 Text en © The Author(s) 2021 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/. The Creative Commons Public Domain Dedication waiver (http://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 Article
Wang, Wenxia
Du, Jie
Chen, Liming
Zeng, Yongjun
Tan, Xueming
Shi, Qinghua
Pan, Xiaohua
Wu, Ziming
Zeng, Yanhua
Transcriptomic, proteomic, and physiological comparative analyses of flooding mitigation of the damage induced by low-temperature stress in direct seeded early indica rice at the seedling stage
title Transcriptomic, proteomic, and physiological comparative analyses of flooding mitigation of the damage induced by low-temperature stress in direct seeded early indica rice at the seedling stage
title_full Transcriptomic, proteomic, and physiological comparative analyses of flooding mitigation of the damage induced by low-temperature stress in direct seeded early indica rice at the seedling stage
title_fullStr Transcriptomic, proteomic, and physiological comparative analyses of flooding mitigation of the damage induced by low-temperature stress in direct seeded early indica rice at the seedling stage
title_full_unstemmed Transcriptomic, proteomic, and physiological comparative analyses of flooding mitigation of the damage induced by low-temperature stress in direct seeded early indica rice at the seedling stage
title_short Transcriptomic, proteomic, and physiological comparative analyses of flooding mitigation of the damage induced by low-temperature stress in direct seeded early indica rice at the seedling stage
title_sort transcriptomic, proteomic, and physiological comparative analyses of flooding mitigation of the damage induced by low-temperature stress in direct seeded early indica rice at the seedling stage
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7952222/
https://www.ncbi.nlm.nih.gov/pubmed/33706696
http://dx.doi.org/10.1186/s12864-021-07458-9
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