Cold Tolerance of <i>ScCBL6</i> Is Associated with Tonoplast Transporters and Photosynthesis in <i>Arabidopsis</i>

Plants that are adapted to harsh environments offer enormous opportunity to understand stress responses in ecological systems. <i>Stipa capillacea</i> is widely distributed in the frigid and arid region of the Tibetan Plateau, but its signal transduction system under cold stress has not...

Full description

Bibliographic Details
Main Authors: Yanli Zhou, Jingling Zhang, Changhong Zhao, Guangqiang Long, Chengli Zhou, Xudong Sun, Yunqiang Yang, Chengjun Zhang, Yongping Yang
Format: Article
Language:English
Published: MDPI AG 2022-11-01
Series:Current Issues in Molecular Biology
Subjects:
Online Access:https://www.mdpi.com/1467-3045/44/11/378
_version_ 1797468653806944256
author Yanli Zhou
Jingling Zhang
Changhong Zhao
Guangqiang Long
Chengli Zhou
Xudong Sun
Yunqiang Yang
Chengjun Zhang
Yongping Yang
author_facet Yanli Zhou
Jingling Zhang
Changhong Zhao
Guangqiang Long
Chengli Zhou
Xudong Sun
Yunqiang Yang
Chengjun Zhang
Yongping Yang
author_sort Yanli Zhou
collection DOAJ
description Plants that are adapted to harsh environments offer enormous opportunity to understand stress responses in ecological systems. <i>Stipa capillacea</i> is widely distributed in the frigid and arid region of the Tibetan Plateau, but its signal transduction system under cold stress has not been characterized. In this study, we isolated a cDNA encoding the signal transduction protein, ScCBL6, from <i>S</i>. <i>capillacea</i>, and evaluated its role in cold tolerance by ectopically expressing it in <i>Arabidopsis</i>. Full-length <i>ScCBL6</i> encode 227 amino acids, and are clustered with CBL6 in <i>Stipa purpurea</i> and <i>Oryza sativa</i> in a phylogenetic analysis. Compared with tolerance in wild-type (WT) plants, ScCBL6-overexpressing plants (<i>ScCBL6-OXP</i>) were more tolerant to cold stress but not to drought stress, as confirmed by their high photosynthetic capacity (Fv/Fm) and survival rate under cold stress. We further compared their cold-responsive transcriptome profiles by RNA sequencing. In total, 3931 genes were differentially expressed by the introduction of <i>ScCBL6</i>. These gene products were involved in multiple processes such as the immune system, lipid catabolism, and secondary metabolism. A KEGG pathway analysis revealed that they were mainly enriched in plant hormone signal transduction and biomacromolecule metabolism. Proteins encoded by differentially expressed genes were predicted to be localized in chloroplasts, mitochondria, and vacuoles, suggesting that ScCBL6 exerts a wide range of functions. Based on its tonoplast subcellular location combined with integrated transcriptome and physiological analyses of <i>ScCBL6-OXP</i>, we inferred that ScCBL6 improves plant cold stress tolerance in <i>Arabidopsis</i> via the regulation of photosynthesis, redox status, and tonoplast metabolite transporters.
first_indexed 2024-03-09T19:10:28Z
format Article
id doaj.art-87ee7bb0ed2f485aaa52ddb8ec074b65
institution Directory Open Access Journal
issn 1467-3037
1467-3045
language English
last_indexed 2024-03-09T19:10:28Z
publishDate 2022-11-01
publisher MDPI AG
record_format Article
series Current Issues in Molecular Biology
spelling doaj.art-87ee7bb0ed2f485aaa52ddb8ec074b652023-11-24T04:13:23ZengMDPI AGCurrent Issues in Molecular Biology1467-30371467-30452022-11-0144115579559210.3390/cimb44110378Cold Tolerance of <i>ScCBL6</i> Is Associated with Tonoplast Transporters and Photosynthesis in <i>Arabidopsis</i>Yanli Zhou0Jingling Zhang1Changhong Zhao2Guangqiang Long3Chengli Zhou4Xudong Sun5Yunqiang Yang6Chengjun Zhang7Yongping Yang8Germplasm Bank of Wild Species, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming 650201, ChinaCollege of Resource and Environment, Yunnan Agricultural University, Kunming 650201, ChinaCollege of Resource and Environment, Yunnan Agricultural University, Kunming 650201, ChinaCollege of Resource and Environment, Yunnan Agricultural University, Kunming 650201, ChinaSchool of Information Science and Engineering, Yunnan University, Kunming 650091, ChinaGermplasm Bank of Wild Species, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming 650201, ChinaGermplasm Bank of Wild Species, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming 650201, ChinaGermplasm Bank of Wild Species, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming 650201, ChinaGermplasm Bank of Wild Species, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming 650201, ChinaPlants that are adapted to harsh environments offer enormous opportunity to understand stress responses in ecological systems. <i>Stipa capillacea</i> is widely distributed in the frigid and arid region of the Tibetan Plateau, but its signal transduction system under cold stress has not been characterized. In this study, we isolated a cDNA encoding the signal transduction protein, ScCBL6, from <i>S</i>. <i>capillacea</i>, and evaluated its role in cold tolerance by ectopically expressing it in <i>Arabidopsis</i>. Full-length <i>ScCBL6</i> encode 227 amino acids, and are clustered with CBL6 in <i>Stipa purpurea</i> and <i>Oryza sativa</i> in a phylogenetic analysis. Compared with tolerance in wild-type (WT) plants, ScCBL6-overexpressing plants (<i>ScCBL6-OXP</i>) were more tolerant to cold stress but not to drought stress, as confirmed by their high photosynthetic capacity (Fv/Fm) and survival rate under cold stress. We further compared their cold-responsive transcriptome profiles by RNA sequencing. In total, 3931 genes were differentially expressed by the introduction of <i>ScCBL6</i>. These gene products were involved in multiple processes such as the immune system, lipid catabolism, and secondary metabolism. A KEGG pathway analysis revealed that they were mainly enriched in plant hormone signal transduction and biomacromolecule metabolism. Proteins encoded by differentially expressed genes were predicted to be localized in chloroplasts, mitochondria, and vacuoles, suggesting that ScCBL6 exerts a wide range of functions. Based on its tonoplast subcellular location combined with integrated transcriptome and physiological analyses of <i>ScCBL6-OXP</i>, we inferred that ScCBL6 improves plant cold stress tolerance in <i>Arabidopsis</i> via the regulation of photosynthesis, redox status, and tonoplast metabolite transporters.https://www.mdpi.com/1467-3045/44/11/378calcineurin B-like proteincold tolerance<i>Stipa capillacea</i>transcriptometonoplast
spellingShingle Yanli Zhou
Jingling Zhang
Changhong Zhao
Guangqiang Long
Chengli Zhou
Xudong Sun
Yunqiang Yang
Chengjun Zhang
Yongping Yang
Cold Tolerance of <i>ScCBL6</i> Is Associated with Tonoplast Transporters and Photosynthesis in <i>Arabidopsis</i>
Current Issues in Molecular Biology
calcineurin B-like protein
cold tolerance
<i>Stipa capillacea</i>
transcriptome
tonoplast
title Cold Tolerance of <i>ScCBL6</i> Is Associated with Tonoplast Transporters and Photosynthesis in <i>Arabidopsis</i>
title_full Cold Tolerance of <i>ScCBL6</i> Is Associated with Tonoplast Transporters and Photosynthesis in <i>Arabidopsis</i>
title_fullStr Cold Tolerance of <i>ScCBL6</i> Is Associated with Tonoplast Transporters and Photosynthesis in <i>Arabidopsis</i>
title_full_unstemmed Cold Tolerance of <i>ScCBL6</i> Is Associated with Tonoplast Transporters and Photosynthesis in <i>Arabidopsis</i>
title_short Cold Tolerance of <i>ScCBL6</i> Is Associated with Tonoplast Transporters and Photosynthesis in <i>Arabidopsis</i>
title_sort cold tolerance of i sccbl6 i is associated with tonoplast transporters and photosynthesis in i arabidopsis i
topic calcineurin B-like protein
cold tolerance
<i>Stipa capillacea</i>
transcriptome
tonoplast
url https://www.mdpi.com/1467-3045/44/11/378
work_keys_str_mv AT yanlizhou coldtoleranceofisccbl6iisassociatedwithtonoplasttransportersandphotosynthesisiniarabidopsisi
AT jinglingzhang coldtoleranceofisccbl6iisassociatedwithtonoplasttransportersandphotosynthesisiniarabidopsisi
AT changhongzhao coldtoleranceofisccbl6iisassociatedwithtonoplasttransportersandphotosynthesisiniarabidopsisi
AT guangqianglong coldtoleranceofisccbl6iisassociatedwithtonoplasttransportersandphotosynthesisiniarabidopsisi
AT chenglizhou coldtoleranceofisccbl6iisassociatedwithtonoplasttransportersandphotosynthesisiniarabidopsisi
AT xudongsun coldtoleranceofisccbl6iisassociatedwithtonoplasttransportersandphotosynthesisiniarabidopsisi
AT yunqiangyang coldtoleranceofisccbl6iisassociatedwithtonoplasttransportersandphotosynthesisiniarabidopsisi
AT chengjunzhang coldtoleranceofisccbl6iisassociatedwithtonoplasttransportersandphotosynthesisiniarabidopsisi
AT yongpingyang coldtoleranceofisccbl6iisassociatedwithtonoplasttransportersandphotosynthesisiniarabidopsisi