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...
Main Authors: | , , , , , , , , , , |
---|---|
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 |
_version_ | 1797662921028796416 |
---|---|
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. |
first_indexed | 2024-03-11T19:07:05Z |
format | Article |
id | doaj.art-3c801b78056b4a7dad2d2c3431418a68 |
institution | Directory Open Access Journal |
issn | 1664-462X |
language | English |
last_indexed | 2024-03-11T19:07:05Z |
publishDate | 2023-10-01 |
publisher | Frontiers Media S.A. |
record_format | Article |
series | Frontiers in Plant Science |
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 |
work_keys_str_mv | AT anamikarawat salinitystressinducedphosphorylationofindeterminatedomain4idd4bympk6regulatesplantgrowthadaptationinarabidopsis AT ronnyvolz salinitystressinducedphosphorylationofindeterminatedomain4idd4bympk6regulatesplantgrowthadaptationinarabidopsis AT arsheedsheikh salinitystressinducedphosphorylationofindeterminatedomain4idd4bympk6regulatesplantgrowthadaptationinarabidopsis AT kiruthigagmariappan salinitystressinducedphosphorylationofindeterminatedomain4idd4bympk6regulatesplantgrowthadaptationinarabidopsis AT soonkapkim salinitystressinducedphosphorylationofindeterminatedomain4idd4bympk6regulatesplantgrowthadaptationinarabidopsis AT naganandrayapuram salinitystressinducedphosphorylationofindeterminatedomain4idd4bympk6regulatesplantgrowthadaptationinarabidopsis AT khairiahmalwutayd salinitystressinducedphosphorylationofindeterminatedomain4idd4bympk6regulatesplantgrowthadaptationinarabidopsis AT louaikalidrissi salinitystressinducedphosphorylationofindeterminatedomain4idd4bympk6regulatesplantgrowthadaptationinarabidopsis AT moussabenhamed salinitystressinducedphosphorylationofindeterminatedomain4idd4bympk6regulatesplantgrowthadaptationinarabidopsis AT ikramblilou salinitystressinducedphosphorylationofindeterminatedomain4idd4bympk6regulatesplantgrowthadaptationinarabidopsis AT heriberthirt salinitystressinducedphosphorylationofindeterminatedomain4idd4bympk6regulatesplantgrowthadaptationinarabidopsis AT heriberthirt salinitystressinducedphosphorylationofindeterminatedomain4idd4bympk6regulatesplantgrowthadaptationinarabidopsis |