Systematic Characterization of the <i>OSCA</i> Family Members in Soybean and Validation of Their Functions in Osmotic Stress
Since we discovered OSCA1, a hyperosmolarity-gated calcium-permeable channel that acted as an osmosensor in <i>Arabidopsis</i>, the <i>OSCA</i> family has been identified genome-wide in several crops, but only a few <i>OSCA</i> members’ functions have been experim...
| Main Authors: | , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
MDPI AG
2022-09-01
|
| Series: | International Journal of Molecular Sciences |
| Subjects: | |
| Online Access: | https://www.mdpi.com/1422-0067/23/18/10570 |
| _version_ | 1797487213332660224 |
|---|---|
| author | Congge Liu Hong Wang Yu Zhang Haijing Cheng Zhangli Hu Zhen-Ming Pei Qing Li |
| author_facet | Congge Liu Hong Wang Yu Zhang Haijing Cheng Zhangli Hu Zhen-Ming Pei Qing Li |
| author_sort | Congge Liu |
| collection | DOAJ |
| description | Since we discovered OSCA1, a hyperosmolarity-gated calcium-permeable channel that acted as an osmosensor in <i>Arabidopsis</i>, the <i>OSCA</i> family has been identified genome-wide in several crops, but only a few <i>OSCA</i> members’ functions have been experimentally demonstrated. Osmotic stress seriously restricts the yield and quality of soybean. Therefore, it is essential to decipher the molecular mechanism of how soybean responds to osmotic stress. Here, we first systematically studied and experimentally demonstrated the role of <i>OSCA</i> family members in the osmotic sensing of soybean. Phylogenetic relationships, gene structures, protein domains and structures analysis revealed that 20 <i>GmOSCA</i> members were divided into four clades, of which members in the same cluster may have more similar functions. In addition, <i>GmOSCA</i> members in clusters III and IV may be functionally redundant and diverged from those in clusters I and II. Based on the spatiotemporal expression patterns, <i>GmOSCA1.6</i>, <i>GmOSCA2.1</i>, <i>GmOSCA2.6</i>, and <i>GmOSCA4.1</i> were extremely low expressed or possible pseudogenes. The remaining 16 <i>GmOSCA</i> genes were heterologously overexpressed in an <i>Arabidopsis osca1</i> mutant, to explore their functions. Subcellular localization showed that most GmOSCA members could localize to the plasma membrane (PM). Among 16 <i>GmOSCA</i> genes, only overexpressing <i>GmOSCA1.1</i>, <i>GmOSCA1.2</i>, <i>GmOSCA1.3</i>, <i>GmOSCA1.4</i>, and <i>GmOSCA1.5</i> in cluster I could fully complement the reduced hyperosmolality-induced [Ca<sup>2+</sup>]<sub>i</sub> increase (OICI) in <i>osca1</i>. The expression profiles of <i>GmOSCA</i> genes against osmotic stress demonstrated that most <i>GmOSCA</i> genes, especially <i>GmOSCA1.1</i>, <i>GmOSCA1.2</i>, <i>GmOSCA1.3</i>, <i>GmOSCA1.4</i>, <i>GmOSCA1.5</i>, <i>GmOSCA3.1</i>, and <i>GmOSCA3.2</i>, strongly responded to osmotic stress. Moreover, overexpression of <i>GmOSCA1.1</i>, <i>GmOSCA1.2</i>, <i>GmOSCA1.3</i>, <i>GmOSCA1.4</i>, <i>GmOSCA1.5</i>, <i>GmOSCA3.1</i>, and <i>GmOSCA3.2</i> rescued the drought-hypersensitive phenotype of <i>osca1</i>. Our findings provide important clues for further studies of <i>GmOSCA</i>-mediated calcium signaling in the osmotic sensing of soybean and contribute to improving soybean drought tolerance through genetic engineering and molecular breeding. |
| first_indexed | 2024-03-09T23:45:23Z |
| format | Article |
| id | doaj.art-0080ab9d456742f39cc9c390b1015a17 |
| institution | Directory Open Access Journal |
| issn | 1661-6596 1422-0067 |
| language | English |
| last_indexed | 2024-03-09T23:45:23Z |
| publishDate | 2022-09-01 |
| publisher | MDPI AG |
| record_format | Article |
| series | International Journal of Molecular Sciences |
| spelling | doaj.art-0080ab9d456742f39cc9c390b1015a172023-11-23T16:44:01ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672022-09-0123181057010.3390/ijms231810570Systematic Characterization of the <i>OSCA</i> Family Members in Soybean and Validation of Their Functions in Osmotic StressCongge Liu0Hong Wang1Yu Zhang2Haijing Cheng3Zhangli Hu4Zhen-Ming Pei5Qing Li6Longping Branch, College of Biology, Hunan University, Changsha 410125, ChinaState Key Laboratory of Rice Biology, China National Rice Research Institute, Hangzhou 311401, ChinaCollege of Life Sciences and Oceanography, Shenzhen University, Shenzhen 518060, ChinaCollege of Life Sciences and Oceanography, Shenzhen University, Shenzhen 518060, ChinaCollege of Life Sciences and Oceanography, Shenzhen University, Shenzhen 518060, ChinaDepartment of Biology, Duke University, Durham, NC 27708, USACollege of Life Sciences and Oceanography, Shenzhen University, Shenzhen 518060, ChinaSince we discovered OSCA1, a hyperosmolarity-gated calcium-permeable channel that acted as an osmosensor in <i>Arabidopsis</i>, the <i>OSCA</i> family has been identified genome-wide in several crops, but only a few <i>OSCA</i> members’ functions have been experimentally demonstrated. Osmotic stress seriously restricts the yield and quality of soybean. Therefore, it is essential to decipher the molecular mechanism of how soybean responds to osmotic stress. Here, we first systematically studied and experimentally demonstrated the role of <i>OSCA</i> family members in the osmotic sensing of soybean. Phylogenetic relationships, gene structures, protein domains and structures analysis revealed that 20 <i>GmOSCA</i> members were divided into four clades, of which members in the same cluster may have more similar functions. In addition, <i>GmOSCA</i> members in clusters III and IV may be functionally redundant and diverged from those in clusters I and II. Based on the spatiotemporal expression patterns, <i>GmOSCA1.6</i>, <i>GmOSCA2.1</i>, <i>GmOSCA2.6</i>, and <i>GmOSCA4.1</i> were extremely low expressed or possible pseudogenes. The remaining 16 <i>GmOSCA</i> genes were heterologously overexpressed in an <i>Arabidopsis osca1</i> mutant, to explore their functions. Subcellular localization showed that most GmOSCA members could localize to the plasma membrane (PM). Among 16 <i>GmOSCA</i> genes, only overexpressing <i>GmOSCA1.1</i>, <i>GmOSCA1.2</i>, <i>GmOSCA1.3</i>, <i>GmOSCA1.4</i>, and <i>GmOSCA1.5</i> in cluster I could fully complement the reduced hyperosmolality-induced [Ca<sup>2+</sup>]<sub>i</sub> increase (OICI) in <i>osca1</i>. The expression profiles of <i>GmOSCA</i> genes against osmotic stress demonstrated that most <i>GmOSCA</i> genes, especially <i>GmOSCA1.1</i>, <i>GmOSCA1.2</i>, <i>GmOSCA1.3</i>, <i>GmOSCA1.4</i>, <i>GmOSCA1.5</i>, <i>GmOSCA3.1</i>, and <i>GmOSCA3.2</i>, strongly responded to osmotic stress. Moreover, overexpression of <i>GmOSCA1.1</i>, <i>GmOSCA1.2</i>, <i>GmOSCA1.3</i>, <i>GmOSCA1.4</i>, <i>GmOSCA1.5</i>, <i>GmOSCA3.1</i>, and <i>GmOSCA3.2</i> rescued the drought-hypersensitive phenotype of <i>osca1</i>. Our findings provide important clues for further studies of <i>GmOSCA</i>-mediated calcium signaling in the osmotic sensing of soybean and contribute to improving soybean drought tolerance through genetic engineering and molecular breeding.https://www.mdpi.com/1422-0067/23/18/10570osmotic stressosmosensorcalcium<i>OSCA</i>soybean |
| spellingShingle | Congge Liu Hong Wang Yu Zhang Haijing Cheng Zhangli Hu Zhen-Ming Pei Qing Li Systematic Characterization of the <i>OSCA</i> Family Members in Soybean and Validation of Their Functions in Osmotic Stress International Journal of Molecular Sciences osmotic stress osmosensor calcium <i>OSCA</i> soybean |
| title | Systematic Characterization of the <i>OSCA</i> Family Members in Soybean and Validation of Their Functions in Osmotic Stress |
| title_full | Systematic Characterization of the <i>OSCA</i> Family Members in Soybean and Validation of Their Functions in Osmotic Stress |
| title_fullStr | Systematic Characterization of the <i>OSCA</i> Family Members in Soybean and Validation of Their Functions in Osmotic Stress |
| title_full_unstemmed | Systematic Characterization of the <i>OSCA</i> Family Members in Soybean and Validation of Their Functions in Osmotic Stress |
| title_short | Systematic Characterization of the <i>OSCA</i> Family Members in Soybean and Validation of Their Functions in Osmotic Stress |
| title_sort | systematic characterization of the i osca i family members in soybean and validation of their functions in osmotic stress |
| topic | osmotic stress osmosensor calcium <i>OSCA</i> soybean |
| url | https://www.mdpi.com/1422-0067/23/18/10570 |
| work_keys_str_mv | AT conggeliu systematiccharacterizationoftheioscaifamilymembersinsoybeanandvalidationoftheirfunctionsinosmoticstress AT hongwang systematiccharacterizationoftheioscaifamilymembersinsoybeanandvalidationoftheirfunctionsinosmoticstress AT yuzhang systematiccharacterizationoftheioscaifamilymembersinsoybeanandvalidationoftheirfunctionsinosmoticstress AT haijingcheng systematiccharacterizationoftheioscaifamilymembersinsoybeanandvalidationoftheirfunctionsinosmoticstress AT zhanglihu systematiccharacterizationoftheioscaifamilymembersinsoybeanandvalidationoftheirfunctionsinosmoticstress AT zhenmingpei systematiccharacterizationoftheioscaifamilymembersinsoybeanandvalidationoftheirfunctionsinosmoticstress AT qingli systematiccharacterizationoftheioscaifamilymembersinsoybeanandvalidationoftheirfunctionsinosmoticstress |