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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...

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Autores principales: Fan, Xin, Tang, Haiyang, Chen, Xuan, Zeng, Fanrong, Chen, Guang, Chen, Zhong-Hua, Qin, Yuan, Deng, Fenglin
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Springer Nature Singapore 2023
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.
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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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