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Allene oxide synthase 1 contributes to limiting grain arsenic accumulation and seedling detoxification in rice
Arsenic (As) is a cancerogenic metalloid ubiquitously distributed in the environment, which can be easily accumulated in food crops like rice. Jasmonic acid (JA) and its derivatives play critical roles in plant growth and stress response. However, the role of endogenous JA in As accumulation and det...
Autores principales: | , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Springer Nature Singapore
2023
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10689621/ https://www.ncbi.nlm.nih.gov/pubmed/38032410 http://dx.doi.org/10.1007/s44154-023-00136-8 |
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author | Fan, Xin Tang, Haiyang Chen, Xuan Zeng, Fanrong Chen, Guang Chen, Zhong-Hua Qin, Yuan Deng, Fenglin |
author_facet | Fan, Xin Tang, Haiyang Chen, Xuan Zeng, Fanrong Chen, Guang Chen, Zhong-Hua Qin, Yuan Deng, Fenglin |
author_sort | Fan, Xin |
collection | PubMed |
description | Arsenic (As) is a cancerogenic metalloid ubiquitously distributed in the environment, which can be easily accumulated in food crops like rice. Jasmonic acid (JA) and its derivatives play critical roles in plant growth and stress response. However, the role of endogenous JA in As accumulation and detoxification is still poorly understood. In this study, we found that JA biosynthesis enzymes Allene Oxide Synthases, OsAOS1 and OsAOS2, regulate As accumulation and As tolerance in rice. Evolutionary bioinformatic analysis indicated that AOS1 and AOS2 have evolved from streptophyte algae (e.g. the basal lineage Klebsormidium flaccidum) – sister clade of land plants. Compared to other two AOSs, OsAOS1 and OsAOS2 were highly expressed in all examined rice tissues and their transcripts were highly induced by As in root and shoot. Loss-of-function of OsAOS1 (osaos1–1) showed elevated As concentration in grains, which was likely attributed to the increased As translocation from root to shoot when the plants were subjected to arsenate [As(V)] but not arsenite [As (III)]. However, the mutation of OsAOS2 (osaos2–1) showed no such effect. Moreover, osaos1–1 and osaos2–1 increased the sensitivity of rice plants to both As(V) and As(III). Disrupted expression of genes involved in As accumulation and detoxification, such as OsPT4, OsNIP3;2, and OsOASTL-A1, was observed in both osaos1–1 and osaos2–1 mutant lines. In addition, a As(V)-induced significant decrease in Reactive Oxygen Species (ROS) production was observed in the root of osaos1–1 but not in osaos2–1. Taken together, our results indicate OsAOS1 modulates both As allocation and detoxification, which could be partially attributed to the altered gene expression profiling and ROS homeostasis in rice while OsAOS2 is important for As tolerance. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1007/s44154-023-00136-8. |
format | Online Article Text |
id | pubmed-10689621 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2023 |
publisher | Springer Nature Singapore |
record_format | MEDLINE/PubMed |
spelling | pubmed-106896212023-12-02 Allene oxide synthase 1 contributes to limiting grain arsenic accumulation and seedling detoxification in rice Fan, Xin Tang, Haiyang Chen, Xuan Zeng, Fanrong Chen, Guang Chen, Zhong-Hua Qin, Yuan Deng, Fenglin Stress Biol Original Paper Arsenic (As) is a cancerogenic metalloid ubiquitously distributed in the environment, which can be easily accumulated in food crops like rice. Jasmonic acid (JA) and its derivatives play critical roles in plant growth and stress response. However, the role of endogenous JA in As accumulation and detoxification is still poorly understood. In this study, we found that JA biosynthesis enzymes Allene Oxide Synthases, OsAOS1 and OsAOS2, regulate As accumulation and As tolerance in rice. Evolutionary bioinformatic analysis indicated that AOS1 and AOS2 have evolved from streptophyte algae (e.g. the basal lineage Klebsormidium flaccidum) – sister clade of land plants. Compared to other two AOSs, OsAOS1 and OsAOS2 were highly expressed in all examined rice tissues and their transcripts were highly induced by As in root and shoot. Loss-of-function of OsAOS1 (osaos1–1) showed elevated As concentration in grains, which was likely attributed to the increased As translocation from root to shoot when the plants were subjected to arsenate [As(V)] but not arsenite [As (III)]. However, the mutation of OsAOS2 (osaos2–1) showed no such effect. Moreover, osaos1–1 and osaos2–1 increased the sensitivity of rice plants to both As(V) and As(III). Disrupted expression of genes involved in As accumulation and detoxification, such as OsPT4, OsNIP3;2, and OsOASTL-A1, was observed in both osaos1–1 and osaos2–1 mutant lines. In addition, a As(V)-induced significant decrease in Reactive Oxygen Species (ROS) production was observed in the root of osaos1–1 but not in osaos2–1. Taken together, our results indicate OsAOS1 modulates both As allocation and detoxification, which could be partially attributed to the altered gene expression profiling and ROS homeostasis in rice while OsAOS2 is important for As tolerance. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1007/s44154-023-00136-8. Springer Nature Singapore 2023-11-30 /pmc/articles/PMC10689621/ /pubmed/38032410 http://dx.doi.org/10.1007/s44154-023-00136-8 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This 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/) . |
spellingShingle | Original Paper Fan, Xin Tang, Haiyang Chen, Xuan Zeng, Fanrong Chen, Guang Chen, Zhong-Hua Qin, Yuan Deng, Fenglin Allene oxide synthase 1 contributes to limiting grain arsenic accumulation and seedling detoxification in rice |
title | Allene oxide synthase 1 contributes to limiting grain arsenic accumulation and seedling detoxification in rice |
title_full | Allene oxide synthase 1 contributes to limiting grain arsenic accumulation and seedling detoxification in rice |
title_fullStr | Allene oxide synthase 1 contributes to limiting grain arsenic accumulation and seedling detoxification in rice |
title_full_unstemmed | Allene oxide synthase 1 contributes to limiting grain arsenic accumulation and seedling detoxification in rice |
title_short | Allene oxide synthase 1 contributes to limiting grain arsenic accumulation and seedling detoxification in rice |
title_sort | allene oxide synthase 1 contributes to limiting grain arsenic accumulation and seedling detoxification in rice |
topic | Original Paper |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10689621/ https://www.ncbi.nlm.nih.gov/pubmed/38032410 http://dx.doi.org/10.1007/s44154-023-00136-8 |
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