Salinity stress-induced phosphorylation of INDETERMINATE-DOMAIN 4 (IDD4) by MPK6 regulates plant growth adaptation in Arabidopsis

The INDETERMINATE DOMAIN (IDD) family belongs to a group of plant-specific transcription factors that coordinates plant growth/development and immunity. However, the function and mode of action of IDDs during abiotic stress, such as salt, are poorly understood. We used idd4 transgenic lines and scre...

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Main Authors: Anamika Rawat, Ronny Völz, Arsheed Sheikh, Kiruthiga G. Mariappan, Soon-Kap Kim, Naganand Rayapuram, Khairiah M. Alwutayd, Louai K. Alidrissi, Moussa Benhamed, Ikram Blilou, Heribert Hirt
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-10-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2023.1265687/full
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author Anamika Rawat
Ronny Völz
Arsheed Sheikh
Kiruthiga G. Mariappan
Soon-Kap Kim
Naganand Rayapuram
Khairiah M. Alwutayd
Louai K. Alidrissi
Moussa Benhamed
Ikram Blilou
Heribert Hirt
Heribert Hirt
author_facet Anamika Rawat
Ronny Völz
Arsheed Sheikh
Kiruthiga G. Mariappan
Soon-Kap Kim
Naganand Rayapuram
Khairiah M. Alwutayd
Louai K. Alidrissi
Moussa Benhamed
Ikram Blilou
Heribert Hirt
Heribert Hirt
author_sort Anamika Rawat
collection DOAJ
description The INDETERMINATE DOMAIN (IDD) family belongs to a group of plant-specific transcription factors that coordinates plant growth/development and immunity. However, the function and mode of action of IDDs during abiotic stress, such as salt, are poorly understood. We used idd4 transgenic lines and screened them under salt stress to find the involvement of IDD4 in salinity stress tolerance The genetic disruption of IDD4 increases salt-tolerance, characterized by sustained plant growth, improved Na+/K+ ratio, and decreased stomatal density/aperture. Yet, IDD4 overexpressing plants were hypersensitive to salt-stress with an increase in stomatal density and pore size. Transcriptomic and ChIP-seq analyses revealed that IDD4 directly controls an important set of genes involved in abiotic stress/salinity responses. Interestingly, using anti-IDD4-pS73 antibody we discovered that IDD4 is specifically phosphorylated at serine-73 by MPK6 in vivo under salinity stress. Analysis of plants expressing the phospho-dead and phospho-mimicking IDD4 versions proved that phosphorylation of IDD4 plays a crucial role in plant transcriptional reprogramming of salt-stress genes. Altogether, we show that salt stress adaption involves MPK6 phosphorylation of IDD4 thereby regulating IDD4 DNA-binding and expression of target genes.
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spelling doaj.art-3c801b78056b4a7dad2d2c3431418a682023-10-10T06:12:25ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2023-10-011410.3389/fpls.2023.12656871265687Salinity stress-induced phosphorylation of INDETERMINATE-DOMAIN 4 (IDD4) by MPK6 regulates plant growth adaptation in ArabidopsisAnamika Rawat0Ronny Völz1Arsheed Sheikh2Kiruthiga G. Mariappan3Soon-Kap Kim4Naganand Rayapuram5Khairiah M. Alwutayd6Louai K. Alidrissi7Moussa Benhamed8Ikram Blilou9Heribert Hirt10Heribert Hirt11Center for Desert Agriculture, Division of Biological and Environmental Sciences and Engineering, King Abdullah University of Science and Technology, Thuwal, Saudi ArabiaCenter for Desert Agriculture, Division of Biological and Environmental Sciences and Engineering, King Abdullah University of Science and Technology, Thuwal, Saudi ArabiaCenter for Desert Agriculture, Division of Biological and Environmental Sciences and Engineering, King Abdullah University of Science and Technology, Thuwal, Saudi ArabiaCenter for Desert Agriculture, Division of Biological and Environmental Sciences and Engineering, King Abdullah University of Science and Technology, Thuwal, Saudi ArabiaCenter for Desert Agriculture, Division of Biological and Environmental Sciences and Engineering, King Abdullah University of Science and Technology, Thuwal, Saudi ArabiaCenter for Desert Agriculture, Division of Biological and Environmental Sciences and Engineering, King Abdullah University of Science and Technology, Thuwal, Saudi ArabiaDepartment of Biology, College of Science, Princess Nourah bint Abdulrahman University, Riyadh, Saudi ArabiaCenter for Desert Agriculture, Division of Biological and Environmental Sciences and Engineering, King Abdullah University of Science and Technology, Thuwal, Saudi ArabiaInstitute of Plant Sciences Paris-Saclay IPS2, CNRS, INRA, Université Paris-Sud, Université Evry, Université Paris-Saclay, Orsay, FranceCenter for Desert Agriculture, Division of Biological and Environmental Sciences and Engineering, King Abdullah University of Science and Technology, Thuwal, Saudi ArabiaCenter for Desert Agriculture, Division of Biological and Environmental Sciences and Engineering, King Abdullah University of Science and Technology, Thuwal, Saudi ArabiaMax F. Perutz Laboratories, University of Vienna, Vienna, AustriaThe INDETERMINATE DOMAIN (IDD) family belongs to a group of plant-specific transcription factors that coordinates plant growth/development and immunity. However, the function and mode of action of IDDs during abiotic stress, such as salt, are poorly understood. We used idd4 transgenic lines and screened them under salt stress to find the involvement of IDD4 in salinity stress tolerance The genetic disruption of IDD4 increases salt-tolerance, characterized by sustained plant growth, improved Na+/K+ ratio, and decreased stomatal density/aperture. Yet, IDD4 overexpressing plants were hypersensitive to salt-stress with an increase in stomatal density and pore size. Transcriptomic and ChIP-seq analyses revealed that IDD4 directly controls an important set of genes involved in abiotic stress/salinity responses. Interestingly, using anti-IDD4-pS73 antibody we discovered that IDD4 is specifically phosphorylated at serine-73 by MPK6 in vivo under salinity stress. Analysis of plants expressing the phospho-dead and phospho-mimicking IDD4 versions proved that phosphorylation of IDD4 plays a crucial role in plant transcriptional reprogramming of salt-stress genes. Altogether, we show that salt stress adaption involves MPK6 phosphorylation of IDD4 thereby regulating IDD4 DNA-binding and expression of target genes.https://www.frontiersin.org/articles/10.3389/fpls.2023.1265687/fullIDD4MPK6salinity stress toleranceprotein phosphorylationtranscription factorstress signaling
spellingShingle Anamika Rawat
Ronny Völz
Arsheed Sheikh
Kiruthiga G. Mariappan
Soon-Kap Kim
Naganand Rayapuram
Khairiah M. Alwutayd
Louai K. Alidrissi
Moussa Benhamed
Ikram Blilou
Heribert Hirt
Heribert Hirt
Salinity stress-induced phosphorylation of INDETERMINATE-DOMAIN 4 (IDD4) by MPK6 regulates plant growth adaptation in Arabidopsis
Frontiers in Plant Science
IDD4
MPK6
salinity stress tolerance
protein phosphorylation
transcription factor
stress signaling
title Salinity stress-induced phosphorylation of INDETERMINATE-DOMAIN 4 (IDD4) by MPK6 regulates plant growth adaptation in Arabidopsis
title_full Salinity stress-induced phosphorylation of INDETERMINATE-DOMAIN 4 (IDD4) by MPK6 regulates plant growth adaptation in Arabidopsis
title_fullStr Salinity stress-induced phosphorylation of INDETERMINATE-DOMAIN 4 (IDD4) by MPK6 regulates plant growth adaptation in Arabidopsis
title_full_unstemmed Salinity stress-induced phosphorylation of INDETERMINATE-DOMAIN 4 (IDD4) by MPK6 regulates plant growth adaptation in Arabidopsis
title_short Salinity stress-induced phosphorylation of INDETERMINATE-DOMAIN 4 (IDD4) by MPK6 regulates plant growth adaptation in Arabidopsis
title_sort salinity stress induced phosphorylation of indeterminate domain 4 idd4 by mpk6 regulates plant growth adaptation in arabidopsis
topic IDD4
MPK6
salinity stress tolerance
protein phosphorylation
transcription factor
stress signaling
url https://www.frontiersin.org/articles/10.3389/fpls.2023.1265687/full
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