OsOSCA1.1 Mediates Hyperosmolality and Salt Stress Sensing in <i>Oryza sativa</i>

OSCA (<i>reduced hyperosmolality-induced [Ca<sup>2+</sup>]<sub>i</sub> increase</i>) is a family of mechanosensitive calcium-permeable channels that play a role in osmosensing and stomatal immunity in plants. <i>Oryza sativa</i> has 11 <i>OsOSCA&...

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Main Authors: Yang Han, Yinxing Wang, Yuanjun Zhai, Zhaohong Wen, Jin Liu, Chao Xi, Heping Zhao, Yingdian Wang, Shengcheng Han
Format: Article
Language:English
Published: MDPI AG 2022-04-01
Series:Biology
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Online Access:https://www.mdpi.com/2079-7737/11/5/678
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author Yang Han
Yinxing Wang
Yuanjun Zhai
Zhaohong Wen
Jin Liu
Chao Xi
Heping Zhao
Yingdian Wang
Shengcheng Han
author_facet Yang Han
Yinxing Wang
Yuanjun Zhai
Zhaohong Wen
Jin Liu
Chao Xi
Heping Zhao
Yingdian Wang
Shengcheng Han
author_sort Yang Han
collection DOAJ
description OSCA (<i>reduced hyperosmolality-induced [Ca<sup>2+</sup>]<sub>i</sub> increase</i>) is a family of mechanosensitive calcium-permeable channels that play a role in osmosensing and stomatal immunity in plants. <i>Oryza sativa</i> has 11 <i>OsOSCA</i> genes; some of these were shown to complement hyperosmolality-induced [Ca<sup>2+</sup>]<sub>cyt</sub> increases (OICI<sub>cyt</sub>), salt stress-induced [Ca<sup>2+</sup>]<sub>cyt</sub> increases (SICI<sub>cyt</sub>), and the associated growth phenotype in the <i>Arabidopsis thaliana</i> mutant <i>osca1</i>. However, their biological functions in rice remain unclear. In this paper, we found that OsOSCA1.1 mediates OICI<sub>cyt</sub> and SICI<sub>cyt</sub> in rice roots, which are critical for stomatal closure, plant survival, and gene expression in shoots, in response to hyperosmolality and the salt stress treatment of roots. Compared with wild-type (Zhonghua11, ZH11) plants, OICI<sub>cyt</sub> and SICI<sub>cyt</sub> were abolished in the roots of 10-day-old <i>ososca1.1</i> seedlings, in response to treatment with 250 mM of sorbitol and 100 mM of NaCl, respectively. Moreover, hyperosmolality- and salt stress-induced stomatal closure were also disrupted in a 30-day-old <i>ososca1.1</i> mutant, resulting in lower stomatal resistance and survival rates than that in ZH11. However, overexpression of <i>OsOSCA1.1</i> in <i>ososca1.1</i> complemented stomatal movement and survival, in response to hyperosmolality and salt stress. The transcriptomic analysis further revealed the following three types of OsOSCA1.1-regulated genes in the shoots: 2416 sorbitol-responsive, 2349 NaCl-responsive and 1844 common osmotic stress-responsive genes after treated with 250 mM of sorbitol and 125 mM NaCl of in 30-day-old rice roots for 24 h. The Gene Ontology enrichment analysis showed that these OsOSCA1.1-regulated genes were relatively enriched in transcription regulation, hormone response, and phosphorylation terms of the biological processes category, which is consistent with the <i>Cis</i>-regulatory elements ABRE, ARE, MYB and MYC binding motifs that were overrepresented in 2000-bp promoter regions of these OsOSCA1.1-regulated genes. These results indicate that OsOSCA-mediated calcium signaling specifically regulates gene expression, in response to drought and salt stress in rice.
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spelling doaj.art-aab74ee1e8424da99a1ebe2c3a5e6e6f2023-11-23T10:06:53ZengMDPI AGBiology2079-77372022-04-0111567810.3390/biology11050678OsOSCA1.1 Mediates Hyperosmolality and Salt Stress Sensing in <i>Oryza sativa</i>Yang Han0Yinxing Wang1Yuanjun Zhai2Zhaohong Wen3Jin Liu4Chao Xi5Heping Zhao6Yingdian Wang7Shengcheng Han8Beijing Key Laboratory of Gene Resources and Molecular Development, College of Life Sciences, Beijing Normal University, Beijing 100875, ChinaBeijing Key Laboratory of Gene Resources and Molecular Development, College of Life Sciences, Beijing Normal University, Beijing 100875, ChinaBeijing Key Laboratory of Gene Resources and Molecular Development, College of Life Sciences, Beijing Normal University, Beijing 100875, ChinaBeijing Key Laboratory of Gene Resources and Molecular Development, College of Life Sciences, Beijing Normal University, Beijing 100875, ChinaBeijing Key Laboratory of Gene Resources and Molecular Development, College of Life Sciences, Beijing Normal University, Beijing 100875, ChinaBeijing Key Laboratory of Gene Resources and Molecular Development, College of Life Sciences, Beijing Normal University, Beijing 100875, ChinaBeijing Key Laboratory of Gene Resources and Molecular Development, College of Life Sciences, Beijing Normal University, Beijing 100875, ChinaBeijing Key Laboratory of Gene Resources and Molecular Development, College of Life Sciences, Beijing Normal University, Beijing 100875, ChinaBeijing Key Laboratory of Gene Resources and Molecular Development, College of Life Sciences, Beijing Normal University, Beijing 100875, ChinaOSCA (<i>reduced hyperosmolality-induced [Ca<sup>2+</sup>]<sub>i</sub> increase</i>) is a family of mechanosensitive calcium-permeable channels that play a role in osmosensing and stomatal immunity in plants. <i>Oryza sativa</i> has 11 <i>OsOSCA</i> genes; some of these were shown to complement hyperosmolality-induced [Ca<sup>2+</sup>]<sub>cyt</sub> increases (OICI<sub>cyt</sub>), salt stress-induced [Ca<sup>2+</sup>]<sub>cyt</sub> increases (SICI<sub>cyt</sub>), and the associated growth phenotype in the <i>Arabidopsis thaliana</i> mutant <i>osca1</i>. However, their biological functions in rice remain unclear. In this paper, we found that OsOSCA1.1 mediates OICI<sub>cyt</sub> and SICI<sub>cyt</sub> in rice roots, which are critical for stomatal closure, plant survival, and gene expression in shoots, in response to hyperosmolality and the salt stress treatment of roots. Compared with wild-type (Zhonghua11, ZH11) plants, OICI<sub>cyt</sub> and SICI<sub>cyt</sub> were abolished in the roots of 10-day-old <i>ososca1.1</i> seedlings, in response to treatment with 250 mM of sorbitol and 100 mM of NaCl, respectively. Moreover, hyperosmolality- and salt stress-induced stomatal closure were also disrupted in a 30-day-old <i>ososca1.1</i> mutant, resulting in lower stomatal resistance and survival rates than that in ZH11. However, overexpression of <i>OsOSCA1.1</i> in <i>ososca1.1</i> complemented stomatal movement and survival, in response to hyperosmolality and salt stress. The transcriptomic analysis further revealed the following three types of OsOSCA1.1-regulated genes in the shoots: 2416 sorbitol-responsive, 2349 NaCl-responsive and 1844 common osmotic stress-responsive genes after treated with 250 mM of sorbitol and 125 mM NaCl of in 30-day-old rice roots for 24 h. The Gene Ontology enrichment analysis showed that these OsOSCA1.1-regulated genes were relatively enriched in transcription regulation, hormone response, and phosphorylation terms of the biological processes category, which is consistent with the <i>Cis</i>-regulatory elements ABRE, ARE, MYB and MYC binding motifs that were overrepresented in 2000-bp promoter regions of these OsOSCA1.1-regulated genes. These results indicate that OsOSCA-mediated calcium signaling specifically regulates gene expression, in response to drought and salt stress in rice.https://www.mdpi.com/2079-7737/11/5/678OsOSCAhyperosmolality-induced calcium increasessalt stress-induced calcium increasesOsOSCA1.1-regulated gene expressionrice
spellingShingle Yang Han
Yinxing Wang
Yuanjun Zhai
Zhaohong Wen
Jin Liu
Chao Xi
Heping Zhao
Yingdian Wang
Shengcheng Han
OsOSCA1.1 Mediates Hyperosmolality and Salt Stress Sensing in <i>Oryza sativa</i>
Biology
OsOSCA
hyperosmolality-induced calcium increases
salt stress-induced calcium increases
OsOSCA1.1-regulated gene expression
rice
title OsOSCA1.1 Mediates Hyperosmolality and Salt Stress Sensing in <i>Oryza sativa</i>
title_full OsOSCA1.1 Mediates Hyperosmolality and Salt Stress Sensing in <i>Oryza sativa</i>
title_fullStr OsOSCA1.1 Mediates Hyperosmolality and Salt Stress Sensing in <i>Oryza sativa</i>
title_full_unstemmed OsOSCA1.1 Mediates Hyperosmolality and Salt Stress Sensing in <i>Oryza sativa</i>
title_short OsOSCA1.1 Mediates Hyperosmolality and Salt Stress Sensing in <i>Oryza sativa</i>
title_sort ososca1 1 mediates hyperosmolality and salt stress sensing in i oryza sativa i
topic OsOSCA
hyperosmolality-induced calcium increases
salt stress-induced calcium increases
OsOSCA1.1-regulated gene expression
rice
url https://www.mdpi.com/2079-7737/11/5/678
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