ERFVII-controlled hypoxia responses are in part facilitated by MEDIATOR SUBUNIT 25 in Arabidopsis thaliana

Jos H M Schippers; Kira von Bongartz; Lisa Laritzki; Stephanie Frohn; Stephanie Frings; Tilo Renziehausen; Frauke Augstein; Katharina Winkels; Katrien Sprangers; Rashmi Sasidharan; Didier Vertommen; Frank Van Breusegem; Sjon Hartman; Gerrit T S Beemster; Amna Mhamdi; Joost T van Dongen; Romy R Schmidt-Schippers

doi:10.1111/tpj.17018

ERFVII-controlled hypoxia responses are in part facilitated by MEDIATOR SUBUNIT 25 in Arabidopsis thaliana

Jos H M Schippers^*, Kira von Bongartz, Lisa Laritzki, Stephanie Frohn, Stephanie Frings, Tilo Renziehausen, Frauke Augstein, Katharina Winkels, Katrien Sprangers, Rashmi Sasidharan, Didier Vertommen, Frank Van Breusegem, Sjon Hartman, Gerrit T S Beemster, Amna Mhamdi, Joost T van Dongen, Romy R Schmidt-Schippers^*

^*Corresponding author for this work

Research output: Contribution to journal › Article › Academic › peer-review

Abstract

Flooding impairs plant growth through oxygen deprivation, which activates plant survival and acclimation responses. Transcriptional responses to low oxygen are generally associated with the activation of group VII ETHYLENE-RESPONSE FACTOR (ERFVII) transcription factors. However, the exact mechanisms and molecular components by which ERFVII factors initiate gene expression are not fully elucidated. Here, we show that the ERFVII factors RELATED TO APETALA 2.2 (RAP2.2) and RAP2.12 cooperate with the Mediator complex subunit AtMED25 to coordinate gene expression under hypoxia in Arabidopsis thaliana. Respective med25 knock-out mutants display reduced low-oxygen stress tolerance. AtMED25 physically associates with a distinct set of hypoxia core genes and its loss partially impairs transcription under hypoxia due to decreased RNA polymerase II recruitment. Association of AtMED25 with target genes requires the presence of ERFVII transcription factors. Next to ERFVII protein stabilisation, also the composition of the Mediator complex including AtMED25 is potentially affected by hypoxia stress as shown by protein-complex pulldown assays. The dynamic response of the Mediator complex to hypoxia is furthermore supported by the fact that two subunits, AtMED8 and AtMED16, are not involved in the establishment of hypoxia tolerance, whilst both act in coordination with AtMED25 under other environmental conditions. We furthermore show that AtMED25 function under hypoxia is independent of ethylene signalling. Finally, functional conservation at the molecular level was found for the MED25-ERFVII module between A. thaliana and the monocot species Oryza sativa, pointing to a potentially universal role of MED25 in coordinating ERFVII-dependent transcript responses to hypoxia in plants.

Original language	English
Pages (from-to)	748-768
Number of pages	21
Journal	Plant Journal
Volume	120
Issue number	2
Early online date	11 Sept 2024
DOIs	https://doi.org/10.1111/tpj.17018
Publication status	Published - Oct 2024

Bibliographical note

Publisher Copyright:
© 2024 The Author(s). The Plant Journal published by Society for Experimental Biology and John Wiley & Sons Ltd.

Funding

We thank Alina Beling, Alina Rosinski, Brigitta Ehrt and Christian Hammerschmid for their technical support. Seeds of were kindly provided by Yunhai Li (Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing, China), whilst seeds were a gift from Michael Holdsworth (School of Biosciences, University of Nottingham, UK). We thank Li\u2010Jia Qu (School of Life Sciences, Peking University, Beijing, Peking) for providing seeds and , , , , , , and coding sequences in pENTR. We further thank Francesco Licausi (University of Oxford, UK) for giving , and promoters in pGWL7,0 and Beatrice Giuntoli (Dipartimento di Biologia, Universit\u00E0 di Pisa, Italy) for providing split\u2010YFP empty vectors. We acknowledge the kind providing of , and coding sequences in pENTR by Margret Sauter (Christian Albrechts University, Kiel, Germany). We are further grateful to Pamela C. Ronald (Department Plant Pathology and the Genome Center, University of California, Davis, USA) for providing coding sequence in pENTR. We very much regret that Rens Voesenek (University of Utrecht, The Netherlands) passed away during the course of this study; we acknowledge his valuable intellectual input and dedicate this manuscript to him. We will keep him in our fondest memory. Part of this work was funded by the Excellence Initiative of the German federal and state governments (StUpPD_332\u201018) and the Deutsche Forschungsgemeinschaft (DFG) grant number SCHM3345/2\u20101 provided to RRS\u2010S. This work was also partially supported by the Research Foundation Flanders (FWO) (The Excellence of Science [EOS] Research project 30829584), and NUCLEOX grant number G007723N to FVB and DV. Open Access funding enabled and organized by Projekt DEAL. med25\u20102 erfvii med16 AtMED8 AtMED16 AtMED19 AtMED21 AtMED28 AtMED32 AtMED34 AtMED36 PDC1 SAD6 HRA1 HRE1 HRE2 RAP2.3 SUB1A

Funders	Funder number
Excellence Initiative of the German federal and state governments	StUpPD_332‐18
Deutsche Forschungsgemeinschaft	SCHM3345/2‐1
Fonds Wetenschappelijk Onderzoek	G007723N, 30829584

Keywords

ERFVII factors
Mediator complex
flooding
hypoxia
transcription

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10.1111/tpj.17018Licence: CC BY-NC-ND

The Plant Journal - 2024 - Schippers - ERFVII‐controlled hypoxia responses are in part facilitated by MEDIATOR SUBUNIT 25Final published version, 9.17 MBLicence: CC BY-NC-ND

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Schippers, J. H. M., von Bongartz, K., Laritzki, L., Frohn, S., Frings, S., Renziehausen, T., Augstein, F., Winkels, K., Sprangers, K., Sasidharan, R., Vertommen, D., Van Breusegem, F., Hartman, S., Beemster, G. T. S., Mhamdi, A., van Dongen, J. T., & Schmidt-Schippers, R. R. (2024). ERFVII-controlled hypoxia responses are in part facilitated by MEDIATOR SUBUNIT 25 in Arabidopsis thaliana. Plant Journal, 120(2), 748-768. https://doi.org/10.1111/tpj.17018

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title = "ERFVII-controlled hypoxia responses are in part facilitated by MEDIATOR SUBUNIT 25 in Arabidopsis thaliana",

abstract = "Flooding impairs plant growth through oxygen deprivation, which activates plant survival and acclimation responses. Transcriptional responses to low oxygen are generally associated with the activation of group VII ETHYLENE-RESPONSE FACTOR (ERFVII) transcription factors. However, the exact mechanisms and molecular components by which ERFVII factors initiate gene expression are not fully elucidated. Here, we show that the ERFVII factors RELATED TO APETALA 2.2 (RAP2.2) and RAP2.12 cooperate with the Mediator complex subunit AtMED25 to coordinate gene expression under hypoxia in Arabidopsis thaliana. Respective med25 knock-out mutants display reduced low-oxygen stress tolerance. AtMED25 physically associates with a distinct set of hypoxia core genes and its loss partially impairs transcription under hypoxia due to decreased RNA polymerase II recruitment. Association of AtMED25 with target genes requires the presence of ERFVII transcription factors. Next to ERFVII protein stabilisation, also the composition of the Mediator complex including AtMED25 is potentially affected by hypoxia stress as shown by protein-complex pulldown assays. The dynamic response of the Mediator complex to hypoxia is furthermore supported by the fact that two subunits, AtMED8 and AtMED16, are not involved in the establishment of hypoxia tolerance, whilst both act in coordination with AtMED25 under other environmental conditions. We furthermore show that AtMED25 function under hypoxia is independent of ethylene signalling. Finally, functional conservation at the molecular level was found for the MED25-ERFVII module between A. thaliana and the monocot species Oryza sativa, pointing to a potentially universal role of MED25 in coordinating ERFVII-dependent transcript responses to hypoxia in plants.",

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note = "Publisher Copyright: {\textcopyright} 2024 The Author(s). The Plant Journal published by Society for Experimental Biology and John Wiley & Sons Ltd.",

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doi = "10.1111/tpj.17018",

language = "English",

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Schippers, JHM, von Bongartz, K, Laritzki, L, Frohn, S, Frings, S, Renziehausen, T, Augstein, F, Winkels, K, Sprangers, K, Sasidharan, R, Vertommen, D, Van Breusegem, F, Hartman, S, Beemster, GTS, Mhamdi, A, van Dongen, JT & Schmidt-Schippers, RR 2024, 'ERFVII-controlled hypoxia responses are in part facilitated by MEDIATOR SUBUNIT 25 in Arabidopsis thaliana', Plant Journal, vol. 120, no. 2, pp. 748-768. https://doi.org/10.1111/tpj.17018

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T1 - ERFVII-controlled hypoxia responses are in part facilitated by MEDIATOR SUBUNIT 25 in Arabidopsis thaliana

AU - Schippers, Jos H M

AU - von Bongartz, Kira

AU - Laritzki, Lisa

AU - Frohn, Stephanie

AU - Frings, Stephanie

AU - Renziehausen, Tilo

AU - Augstein, Frauke

AU - Winkels, Katharina

AU - Sprangers, Katrien

AU - Sasidharan, Rashmi

AU - Vertommen, Didier

AU - Van Breusegem, Frank

AU - Hartman, Sjon

AU - Beemster, Gerrit T S

AU - Mhamdi, Amna

AU - van Dongen, Joost T

AU - Schmidt-Schippers, Romy R

PY - 2024/10

Y1 - 2024/10

N2 - Flooding impairs plant growth through oxygen deprivation, which activates plant survival and acclimation responses. Transcriptional responses to low oxygen are generally associated with the activation of group VII ETHYLENE-RESPONSE FACTOR (ERFVII) transcription factors. However, the exact mechanisms and molecular components by which ERFVII factors initiate gene expression are not fully elucidated. Here, we show that the ERFVII factors RELATED TO APETALA 2.2 (RAP2.2) and RAP2.12 cooperate with the Mediator complex subunit AtMED25 to coordinate gene expression under hypoxia in Arabidopsis thaliana. Respective med25 knock-out mutants display reduced low-oxygen stress tolerance. AtMED25 physically associates with a distinct set of hypoxia core genes and its loss partially impairs transcription under hypoxia due to decreased RNA polymerase II recruitment. Association of AtMED25 with target genes requires the presence of ERFVII transcription factors. Next to ERFVII protein stabilisation, also the composition of the Mediator complex including AtMED25 is potentially affected by hypoxia stress as shown by protein-complex pulldown assays. The dynamic response of the Mediator complex to hypoxia is furthermore supported by the fact that two subunits, AtMED8 and AtMED16, are not involved in the establishment of hypoxia tolerance, whilst both act in coordination with AtMED25 under other environmental conditions. We furthermore show that AtMED25 function under hypoxia is independent of ethylene signalling. Finally, functional conservation at the molecular level was found for the MED25-ERFVII module between A. thaliana and the monocot species Oryza sativa, pointing to a potentially universal role of MED25 in coordinating ERFVII-dependent transcript responses to hypoxia in plants.

AB - Flooding impairs plant growth through oxygen deprivation, which activates plant survival and acclimation responses. Transcriptional responses to low oxygen are generally associated with the activation of group VII ETHYLENE-RESPONSE FACTOR (ERFVII) transcription factors. However, the exact mechanisms and molecular components by which ERFVII factors initiate gene expression are not fully elucidated. Here, we show that the ERFVII factors RELATED TO APETALA 2.2 (RAP2.2) and RAP2.12 cooperate with the Mediator complex subunit AtMED25 to coordinate gene expression under hypoxia in Arabidopsis thaliana. Respective med25 knock-out mutants display reduced low-oxygen stress tolerance. AtMED25 physically associates with a distinct set of hypoxia core genes and its loss partially impairs transcription under hypoxia due to decreased RNA polymerase II recruitment. Association of AtMED25 with target genes requires the presence of ERFVII transcription factors. Next to ERFVII protein stabilisation, also the composition of the Mediator complex including AtMED25 is potentially affected by hypoxia stress as shown by protein-complex pulldown assays. The dynamic response of the Mediator complex to hypoxia is furthermore supported by the fact that two subunits, AtMED8 and AtMED16, are not involved in the establishment of hypoxia tolerance, whilst both act in coordination with AtMED25 under other environmental conditions. We furthermore show that AtMED25 function under hypoxia is independent of ethylene signalling. Finally, functional conservation at the molecular level was found for the MED25-ERFVII module between A. thaliana and the monocot species Oryza sativa, pointing to a potentially universal role of MED25 in coordinating ERFVII-dependent transcript responses to hypoxia in plants.

KW - ERFVII factors

KW - Mediator complex

KW - flooding

KW - hypoxia

KW - transcription

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DO - 10.1111/tpj.17018

M3 - Article

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SN - 0960-7412

VL - 120

SP - 748

EP - 768

JO - Plant Journal

JF - Plant Journal

IS - 2

ER -

ERFVII-controlled hypoxia responses are in part facilitated by MEDIATOR SUBUNIT 25 in Arabidopsis thaliana

Abstract

Bibliographical note

Funding

Keywords

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