Cargando…

The sucrose non-fermenting 1-related kinase 2 gene SAPK9 improves drought tolerance and grain yield in rice by modulating cellular osmotic potential, stomatal closure and stress-responsive gene expression

BACKGROUND: Family members of sucrose non-fermenting 1-related kinase 2 (SnRK2), being plant-specific serine/threonine protein kinases, constitute the central core of abscisic acid (ABA)-dependent and ABA-independent signaling pathways, and are key regulators of abiotic stress adaptation in plants....

Descripción completa

Detalles Bibliográficos
Autores principales: Dey, Avishek, Samanta, Milan Kumar, Gayen, Srimonta, Maiti, Mrinal K.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4944446/
https://www.ncbi.nlm.nih.gov/pubmed/27411911
http://dx.doi.org/10.1186/s12870-016-0845-x
_version_ 1782442766756741120
author Dey, Avishek
Samanta, Milan Kumar
Gayen, Srimonta
Maiti, Mrinal K.
author_facet Dey, Avishek
Samanta, Milan Kumar
Gayen, Srimonta
Maiti, Mrinal K.
author_sort Dey, Avishek
collection PubMed
description BACKGROUND: Family members of sucrose non-fermenting 1-related kinase 2 (SnRK2), being plant-specific serine/threonine protein kinases, constitute the central core of abscisic acid (ABA)-dependent and ABA-independent signaling pathways, and are key regulators of abiotic stress adaptation in plants. We report here the functional characterization of SAPK9 gene, one of the 10 SnRK2s of rice, through developing gain-of-function and loss-of-function phenotypes by transgenesis. RESULTS: The gene expression profiling revealed that the abundance of single gene-derived SAPK9 transcript was significantly higher in drought-tolerant rice genotypes than the drought-sensitive ones, and its expression was comparatively greater in reproductive stage than the vegetative stage. The highest expression of SAPK9 gene in drought-tolerant Oryza rufipogon prompted us to clone and characterise the CDS of this allele in details. The SAPK9 transcript expression was found to be highest in leaf and upregulated during drought stress and ABA treatment. In silico homology modelling of SAPK9 with Arabidopsis OST1 protein showed the bilobal kinase fold structure of SAPK9, which upon bacterial expression was able to phosphorylate itself, histone III and OsbZIP23 as substrates in vitro. Transgenic overexpression (OE) of SAPK9 CDS from O. rufipogon in a drought-sensitive indica rice genotype exhibited significantly improved drought tolerance in comparison to transgenic silencing (RNAi) lines and non-transgenic (NT) plants. In contrast to RNAi and NT plants, the enhanced drought tolerance of OE lines was concurrently supported by the upgraded physiological indices with respect to water retention capacity, soluble sugar and proline content, stomatal closure, membrane stability, and cellular detoxification. Upregulated transcript expressions of six ABA-dependent stress-responsive genes and increased sensitivity to exogenous ABA of OE lines indicate that the SAPK9 is a positive regulator of ABA-mediated stress signaling pathways in rice. The yield-related traits of OE lines were augmented significantly, which resulted from the highest percentage of fertile pollens in OE lines when compared with RNAi and NT plants. CONCLUSION: The present study establishes the functional role of SAPK9 as transactivating kinase and potential transcriptional activator in drought stress adaptation of rice plant. The SAPK9 gene has potential usefulness in transgenic breeding for improving drought tolerance and grain yield in crop plants. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12870-016-0845-x) contains supplementary material, which is available to authorized users.
format Online
Article
Text
id pubmed-4944446
institution National Center for Biotechnology Information
language English
publishDate 2016
publisher BioMed Central
record_format MEDLINE/PubMed
spelling pubmed-49444462016-07-15 The sucrose non-fermenting 1-related kinase 2 gene SAPK9 improves drought tolerance and grain yield in rice by modulating cellular osmotic potential, stomatal closure and stress-responsive gene expression Dey, Avishek Samanta, Milan Kumar Gayen, Srimonta Maiti, Mrinal K. BMC Plant Biol Research Article BACKGROUND: Family members of sucrose non-fermenting 1-related kinase 2 (SnRK2), being plant-specific serine/threonine protein kinases, constitute the central core of abscisic acid (ABA)-dependent and ABA-independent signaling pathways, and are key regulators of abiotic stress adaptation in plants. We report here the functional characterization of SAPK9 gene, one of the 10 SnRK2s of rice, through developing gain-of-function and loss-of-function phenotypes by transgenesis. RESULTS: The gene expression profiling revealed that the abundance of single gene-derived SAPK9 transcript was significantly higher in drought-tolerant rice genotypes than the drought-sensitive ones, and its expression was comparatively greater in reproductive stage than the vegetative stage. The highest expression of SAPK9 gene in drought-tolerant Oryza rufipogon prompted us to clone and characterise the CDS of this allele in details. The SAPK9 transcript expression was found to be highest in leaf and upregulated during drought stress and ABA treatment. In silico homology modelling of SAPK9 with Arabidopsis OST1 protein showed the bilobal kinase fold structure of SAPK9, which upon bacterial expression was able to phosphorylate itself, histone III and OsbZIP23 as substrates in vitro. Transgenic overexpression (OE) of SAPK9 CDS from O. rufipogon in a drought-sensitive indica rice genotype exhibited significantly improved drought tolerance in comparison to transgenic silencing (RNAi) lines and non-transgenic (NT) plants. In contrast to RNAi and NT plants, the enhanced drought tolerance of OE lines was concurrently supported by the upgraded physiological indices with respect to water retention capacity, soluble sugar and proline content, stomatal closure, membrane stability, and cellular detoxification. Upregulated transcript expressions of six ABA-dependent stress-responsive genes and increased sensitivity to exogenous ABA of OE lines indicate that the SAPK9 is a positive regulator of ABA-mediated stress signaling pathways in rice. The yield-related traits of OE lines were augmented significantly, which resulted from the highest percentage of fertile pollens in OE lines when compared with RNAi and NT plants. CONCLUSION: The present study establishes the functional role of SAPK9 as transactivating kinase and potential transcriptional activator in drought stress adaptation of rice plant. The SAPK9 gene has potential usefulness in transgenic breeding for improving drought tolerance and grain yield in crop plants. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12870-016-0845-x) contains supplementary material, which is available to authorized users. BioMed Central 2016-07-13 /pmc/articles/PMC4944446/ /pubmed/27411911 http://dx.doi.org/10.1186/s12870-016-0845-x Text en © The Author(s). 2016 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Dey, Avishek
Samanta, Milan Kumar
Gayen, Srimonta
Maiti, Mrinal K.
The sucrose non-fermenting 1-related kinase 2 gene SAPK9 improves drought tolerance and grain yield in rice by modulating cellular osmotic potential, stomatal closure and stress-responsive gene expression
title The sucrose non-fermenting 1-related kinase 2 gene SAPK9 improves drought tolerance and grain yield in rice by modulating cellular osmotic potential, stomatal closure and stress-responsive gene expression
title_full The sucrose non-fermenting 1-related kinase 2 gene SAPK9 improves drought tolerance and grain yield in rice by modulating cellular osmotic potential, stomatal closure and stress-responsive gene expression
title_fullStr The sucrose non-fermenting 1-related kinase 2 gene SAPK9 improves drought tolerance and grain yield in rice by modulating cellular osmotic potential, stomatal closure and stress-responsive gene expression
title_full_unstemmed The sucrose non-fermenting 1-related kinase 2 gene SAPK9 improves drought tolerance and grain yield in rice by modulating cellular osmotic potential, stomatal closure and stress-responsive gene expression
title_short The sucrose non-fermenting 1-related kinase 2 gene SAPK9 improves drought tolerance and grain yield in rice by modulating cellular osmotic potential, stomatal closure and stress-responsive gene expression
title_sort sucrose non-fermenting 1-related kinase 2 gene sapk9 improves drought tolerance and grain yield in rice by modulating cellular osmotic potential, stomatal closure and stress-responsive gene expression
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4944446/
https://www.ncbi.nlm.nih.gov/pubmed/27411911
http://dx.doi.org/10.1186/s12870-016-0845-x
work_keys_str_mv AT deyavishek thesucrosenonfermenting1relatedkinase2genesapk9improvesdroughttoleranceandgrainyieldinricebymodulatingcellularosmoticpotentialstomatalclosureandstressresponsivegeneexpression
AT samantamilankumar thesucrosenonfermenting1relatedkinase2genesapk9improvesdroughttoleranceandgrainyieldinricebymodulatingcellularosmoticpotentialstomatalclosureandstressresponsivegeneexpression
AT gayensrimonta thesucrosenonfermenting1relatedkinase2genesapk9improvesdroughttoleranceandgrainyieldinricebymodulatingcellularosmoticpotentialstomatalclosureandstressresponsivegeneexpression
AT maitimrinalk thesucrosenonfermenting1relatedkinase2genesapk9improvesdroughttoleranceandgrainyieldinricebymodulatingcellularosmoticpotentialstomatalclosureandstressresponsivegeneexpression
AT deyavishek sucrosenonfermenting1relatedkinase2genesapk9improvesdroughttoleranceandgrainyieldinricebymodulatingcellularosmoticpotentialstomatalclosureandstressresponsivegeneexpression
AT samantamilankumar sucrosenonfermenting1relatedkinase2genesapk9improvesdroughttoleranceandgrainyieldinricebymodulatingcellularosmoticpotentialstomatalclosureandstressresponsivegeneexpression
AT gayensrimonta sucrosenonfermenting1relatedkinase2genesapk9improvesdroughttoleranceandgrainyieldinricebymodulatingcellularosmoticpotentialstomatalclosureandstressresponsivegeneexpression
AT maitimrinalk sucrosenonfermenting1relatedkinase2genesapk9improvesdroughttoleranceandgrainyieldinricebymodulatingcellularosmoticpotentialstomatalclosureandstressresponsivegeneexpression