Phenotypic and transcriptomic analysis reveals early stress responses in transgenic rice expressing Arabidopsis DREB1a

Abstract Overexpression of Arabidopsis dehydration response element binding 1a (DREB1a) is a well‐known approach for developing salinity, cold and/or drought stress tolerance. However, understanding of the genetic mechanisms associated with DREB1a expression in rice is generally limited. In this stu...

Full description

Bibliographic Details
Main Authors: Yasmin Vasques Berchembrock, Bhuvan Pathak, Chandan Maurya, Flávia Barbosa Silva Botelho, Vibha Srivastava
Format: Article
Language:English
Published: Wiley 2022-10-01
Series:Plant Direct
Subjects:
Online Access:https://doi.org/10.1002/pld3.456
_version_ 1811329514482958336
author Yasmin Vasques Berchembrock
Bhuvan Pathak
Chandan Maurya
Flávia Barbosa Silva Botelho
Vibha Srivastava
author_facet Yasmin Vasques Berchembrock
Bhuvan Pathak
Chandan Maurya
Flávia Barbosa Silva Botelho
Vibha Srivastava
author_sort Yasmin Vasques Berchembrock
collection DOAJ
description Abstract Overexpression of Arabidopsis dehydration response element binding 1a (DREB1a) is a well‐known approach for developing salinity, cold and/or drought stress tolerance. However, understanding of the genetic mechanisms associated with DREB1a expression in rice is generally limited. In this study, DREB1a‐associated early responses were investigated in a transgenic rice line harboring cold‐inducible DREB1a at a gene stacked locus. Although the function of other genes in the stacked locus was not relevant to stress tolerance, this study demonstrates DREB1a can be co‐localized with other genes for multigenic trait enhancement. As expected, the transgenic lines displayed improved tolerance to salinity stress and water withholding as compared with non‐transgenic controls. RNA sequencing and transcriptome analysis showed upregulation of complex transcriptional networks and metabolic reprogramming as DREB1a expression led to the upregulation of multiple transcription factor gene families, suppression of photosynthesis, and induction of secondary metabolism. In addition to the detection of previously described mechanisms such as production of protective molecules, potentially novel pathways were also revealed. These include jasmonate, auxin, and ethylene signaling, induction of JAZ and WRKY regulons, trehalose synthesis, and polyamine catabolism. These genes regulate various stress responses and ensure timely attenuation of the stress signal. Furthermore, genes associated with heat stress response were downregulated in DREB1a expressing lines, suggesting antagonism between heat and dehydration stress response pathways. In summary, through a complex transcriptional network, multiple stress signaling pathways are induced by DREB1a that presumably lead to early perception and prompt response toward stress tolerance as well as attenuation of the stress signal to prevent deleterious effects of the runoff response.
first_indexed 2024-04-13T15:46:30Z
format Article
id doaj.art-7228a0ba3ca245a39bf0bfb2de5fdd69
institution Directory Open Access Journal
issn 2475-4455
language English
last_indexed 2024-04-13T15:46:30Z
publishDate 2022-10-01
publisher Wiley
record_format Article
series Plant Direct
spelling doaj.art-7228a0ba3ca245a39bf0bfb2de5fdd692022-12-22T02:40:59ZengWileyPlant Direct2475-44552022-10-01610n/an/a10.1002/pld3.456Phenotypic and transcriptomic analysis reveals early stress responses in transgenic rice expressing Arabidopsis DREB1aYasmin Vasques Berchembrock0Bhuvan Pathak1Chandan Maurya2Flávia Barbosa Silva Botelho3Vibha Srivastava4Department of Crop, Soil, and Environmental Sciences University of Arkansas System Division of Agriculture Fayetteville Arkansas USADepartment of Crop, Soil, and Environmental Sciences University of Arkansas System Division of Agriculture Fayetteville Arkansas USADepartment of Crop, Soil, and Environmental Sciences University of Arkansas System Division of Agriculture Fayetteville Arkansas USADepartment of Agriculture Federal University of Lavras Lavras Minas Gerais BrazilDepartment of Crop, Soil, and Environmental Sciences University of Arkansas System Division of Agriculture Fayetteville Arkansas USAAbstract Overexpression of Arabidopsis dehydration response element binding 1a (DREB1a) is a well‐known approach for developing salinity, cold and/or drought stress tolerance. However, understanding of the genetic mechanisms associated with DREB1a expression in rice is generally limited. In this study, DREB1a‐associated early responses were investigated in a transgenic rice line harboring cold‐inducible DREB1a at a gene stacked locus. Although the function of other genes in the stacked locus was not relevant to stress tolerance, this study demonstrates DREB1a can be co‐localized with other genes for multigenic trait enhancement. As expected, the transgenic lines displayed improved tolerance to salinity stress and water withholding as compared with non‐transgenic controls. RNA sequencing and transcriptome analysis showed upregulation of complex transcriptional networks and metabolic reprogramming as DREB1a expression led to the upregulation of multiple transcription factor gene families, suppression of photosynthesis, and induction of secondary metabolism. In addition to the detection of previously described mechanisms such as production of protective molecules, potentially novel pathways were also revealed. These include jasmonate, auxin, and ethylene signaling, induction of JAZ and WRKY regulons, trehalose synthesis, and polyamine catabolism. These genes regulate various stress responses and ensure timely attenuation of the stress signal. Furthermore, genes associated with heat stress response were downregulated in DREB1a expressing lines, suggesting antagonism between heat and dehydration stress response pathways. In summary, through a complex transcriptional network, multiple stress signaling pathways are induced by DREB1a that presumably lead to early perception and prompt response toward stress tolerance as well as attenuation of the stress signal to prevent deleterious effects of the runoff response.https://doi.org/10.1002/pld3.456abiotic stressArabidopsis DREB1adrought stressOryza sativasalinity stressstress tolerance
spellingShingle Yasmin Vasques Berchembrock
Bhuvan Pathak
Chandan Maurya
Flávia Barbosa Silva Botelho
Vibha Srivastava
Phenotypic and transcriptomic analysis reveals early stress responses in transgenic rice expressing Arabidopsis DREB1a
Plant Direct
abiotic stress
Arabidopsis DREB1a
drought stress
Oryza sativa
salinity stress
stress tolerance
title Phenotypic and transcriptomic analysis reveals early stress responses in transgenic rice expressing Arabidopsis DREB1a
title_full Phenotypic and transcriptomic analysis reveals early stress responses in transgenic rice expressing Arabidopsis DREB1a
title_fullStr Phenotypic and transcriptomic analysis reveals early stress responses in transgenic rice expressing Arabidopsis DREB1a
title_full_unstemmed Phenotypic and transcriptomic analysis reveals early stress responses in transgenic rice expressing Arabidopsis DREB1a
title_short Phenotypic and transcriptomic analysis reveals early stress responses in transgenic rice expressing Arabidopsis DREB1a
title_sort phenotypic and transcriptomic analysis reveals early stress responses in transgenic rice expressing arabidopsis dreb1a
topic abiotic stress
Arabidopsis DREB1a
drought stress
Oryza sativa
salinity stress
stress tolerance
url https://doi.org/10.1002/pld3.456
work_keys_str_mv AT yasminvasquesberchembrock phenotypicandtranscriptomicanalysisrevealsearlystressresponsesintransgenicriceexpressingarabidopsisdreb1a
AT bhuvanpathak phenotypicandtranscriptomicanalysisrevealsearlystressresponsesintransgenicriceexpressingarabidopsisdreb1a
AT chandanmaurya phenotypicandtranscriptomicanalysisrevealsearlystressresponsesintransgenicriceexpressingarabidopsisdreb1a
AT flaviabarbosasilvabotelho phenotypicandtranscriptomicanalysisrevealsearlystressresponsesintransgenicriceexpressingarabidopsisdreb1a
AT vibhasrivastava phenotypicandtranscriptomicanalysisrevealsearlystressresponsesintransgenicriceexpressingarabidopsisdreb1a