The membrane-localized protein kinase MAP4K4/TOT3 regulates thermomorphogenesis

Lam Dai Vu; Xiangyu Xu; Tingting Zhu; Lixia Pan; Martijn van Zanten; Dorrit de Jong; Yaowei Wang; Tim Vanremoortele; Anna M. Locke; Brigitte van de Cotte; Nancy De Winne; Elisabeth Stes; Eugenia Russinova; Geert De Jaeger; Daniël Van Damme; Cristobal Uauy; Kris Gevaert; Ive De Smet

doi:10.1038/s41467-021-23112-0

The membrane-localized protein kinase MAP4K4/TOT3 regulates thermomorphogenesis

Lam Dai Vu, Xiangyu Xu, Tingting Zhu, Lixia Pan, Martijn van Zanten, Dorrit de Jong, Yaowei Wang, Tim Vanremoortele, Anna M. Locke, Brigitte van de Cotte, Nancy De Winne, Elisabeth Stes, Eugenia Russinova, Geert De Jaeger, Daniël Van Damme, Cristobal Uauy, Kris Gevaert, Ive De Smet^*

^*Corresponding author for this work

Molecular Plant Physiology

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

Abstract

Plants respond to mild warm temperature conditions by increased elongation growth of organs to enhance cooling capacity, in a process called thermomorphogenesis. To this date, the regulation of thermomorphogenesis has been exclusively shown to intersect with light signalling pathways. To identify regulators of thermomorphogenesis that are conserved in flowering plants, we map changes in protein phosphorylation in both dicots and monocots exposed to warm temperature. We identify MITOGEN-ACTIVATED PROTEIN KINASE KINASE KINASE KINASE4 (MAP4K4)/TARGET OF TEMPERATURE3 (TOT3) as a regulator of thermomorphogenesis that impinges on brassinosteroid signalling in Arabidopsis thaliana. In addition, we show that TOT3 plays a role in thermal response in wheat, a monocot crop. Altogether, the conserved thermal regulation by TOT3 expands our knowledge of thermomorphogenesis beyond the well-studied pathways and can contribute to ensuring food security under a changing climate.

Original language	English
Article number	2842
Pages (from-to)	1-14
Journal	Nature Communications
Volume	12
Issue number	1
DOIs	https://doi.org/10.1038/s41467-021-23112-0
Publication status	Published - 14 May 2021

Bibliographical note

Funding Information:
We thank Barbara Wrzesinska for technical help and Bert De Rybel for providing critical comments on the manuscript. We thank the following colleagues for providing materials: Pablo D. Cerdán (phyb-9), Salomé Prat (pif4-101) and Yanhai Yin (anti-BES1 antibody). We also express our gratitude to Thomas Jacobs for advice on generating CRISPR mutants for TOI4 and TOI5 and Martha Ramirez for soybean growth. The EMS-mutagenized population of bread wheat cv. Cadenza was developed by Andy Phillips at Rothamsted. We acknowledge the Germplasm Resources Unit (GRU) at JIC for providing wheat seeds. L.D.V was a recipient of the VIB International PhD Scholarship in Life Sciences. X.X., T.Z and Y.W. are supported by grants from the Chinese Scholarship Council. A.L. was supported by a grant from the North Carolina Soybean Producers Association.

Publisher Copyright:
© 2021, The Author(s).

Funding

We thank Barbara Wrzesinska for technical help and Bert De Rybel for providing critical comments on the manuscript. We thank the following colleagues for providing materials: Pablo D. Cerdán (phyb-9), Salomé Prat (pif4-101) and Yanhai Yin (anti-BES1 antibody). We also express our gratitude to Thomas Jacobs for advice on generating CRISPR mutants for TOI4 and TOI5 and Martha Ramirez for soybean growth. The EMS-mutagenized population of bread wheat cv. Cadenza was developed by Andy Phillips at Rothamsted. We acknowledge the Germplasm Resources Unit (GRU) at JIC for providing wheat seeds. L.D.V was a recipient of the VIB International PhD Scholarship in Life Sciences. X.X., T.Z and Y.W. are supported by grants from the Chinese Scholarship Council. A.L. was supported by a grant from the North Carolina Soybean Producers Association.

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s41467-021-23112-0Final published version, 2.65 MBLicence: CC BY

Cite this

Vu, L. D., Xu, X., Zhu, T., Pan, L., van Zanten, M., de Jong, D., Wang, Y., Vanremoortele, T., Locke, A. M., van de Cotte, B., De Winne, N., Stes, E., Russinova, E., De Jaeger, G., Van Damme, D., Uauy, C., Gevaert, K., & De Smet, I. (2021). The membrane-localized protein kinase MAP4K4/TOT3 regulates thermomorphogenesis. Nature Communications, 12(1), 1-14. Article 2842. https://doi.org/10.1038/s41467-021-23112-0

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title = "The membrane-localized protein kinase MAP4K4/TOT3 regulates thermomorphogenesis",

abstract = "Plants respond to mild warm temperature conditions by increased elongation growth of organs to enhance cooling capacity, in a process called thermomorphogenesis. To this date, the regulation of thermomorphogenesis has been exclusively shown to intersect with light signalling pathways. To identify regulators of thermomorphogenesis that are conserved in flowering plants, we map changes in protein phosphorylation in both dicots and monocots exposed to warm temperature. We identify MITOGEN-ACTIVATED PROTEIN KINASE KINASE KINASE KINASE4 (MAP4K4)/TARGET OF TEMPERATURE3 (TOT3) as a regulator of thermomorphogenesis that impinges on brassinosteroid signalling in Arabidopsis thaliana. In addition, we show that TOT3 plays a role in thermal response in wheat, a monocot crop. Altogether, the conserved thermal regulation by TOT3 expands our knowledge of thermomorphogenesis beyond the well-studied pathways and can contribute to ensuring food security under a changing climate.",

author = "Vu, {Lam Dai} and Xiangyu Xu and Tingting Zhu and Lixia Pan and {van Zanten}, Martijn and {de Jong}, Dorrit and Yaowei Wang and Tim Vanremoortele and Locke, {Anna M.} and {van de Cotte}, Brigitte and {De Winne}, Nancy and Elisabeth Stes and Eugenia Russinova and {De Jaeger}, Geert and {Van Damme}, Dani{\"e}l and Cristobal Uauy and Kris Gevaert and {De Smet}, Ive",

note = "Funding Information: We thank Barbara Wrzesinska for technical help and Bert De Rybel for providing critical comments on the manuscript. We thank the following colleagues for providing materials: Pablo D. Cerd{\'a}n (phyb-9), Salom{\'e} Prat (pif4-101) and Yanhai Yin (anti-BES1 antibody). We also express our gratitude to Thomas Jacobs for advice on generating CRISPR mutants for TOI4 and TOI5 and Martha Ramirez for soybean growth. The EMS-mutagenized population of bread wheat cv. Cadenza was developed by Andy Phillips at Rothamsted. We acknowledge the Germplasm Resources Unit (GRU) at JIC for providing wheat seeds. L.D.V was a recipient of the VIB International PhD Scholarship in Life Sciences. X.X., T.Z and Y.W. are supported by grants from the Chinese Scholarship Council. A.L. was supported by a grant from the North Carolina Soybean Producers Association. Publisher Copyright: {\textcopyright} 2021, The Author(s).",

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Vu, LD, Xu, X, Zhu, T, Pan, L, van Zanten, M, de Jong, D, Wang, Y, Vanremoortele, T, Locke, AM, van de Cotte, B, De Winne, N, Stes, E, Russinova, E, De Jaeger, G, Van Damme, D, Uauy, C, Gevaert, K & De Smet, I 2021, 'The membrane-localized protein kinase MAP4K4/TOT3 regulates thermomorphogenesis', Nature Communications, vol. 12, no. 1, 2842, pp. 1-14. https://doi.org/10.1038/s41467-021-23112-0

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T1 - The membrane-localized protein kinase MAP4K4/TOT3 regulates thermomorphogenesis

AU - Vu, Lam Dai

AU - Xu, Xiangyu

AU - Zhu, Tingting

AU - Pan, Lixia

AU - van Zanten, Martijn

AU - de Jong, Dorrit

AU - Wang, Yaowei

AU - Vanremoortele, Tim

AU - Locke, Anna M.

AU - van de Cotte, Brigitte

AU - De Winne, Nancy

AU - Stes, Elisabeth

AU - Russinova, Eugenia

AU - De Jaeger, Geert

AU - Van Damme, Daniël

AU - Uauy, Cristobal

AU - Gevaert, Kris

AU - De Smet, Ive

N1 - Funding Information: We thank Barbara Wrzesinska for technical help and Bert De Rybel for providing critical comments on the manuscript. We thank the following colleagues for providing materials: Pablo D. Cerdán (phyb-9), Salomé Prat (pif4-101) and Yanhai Yin (anti-BES1 antibody). We also express our gratitude to Thomas Jacobs for advice on generating CRISPR mutants for TOI4 and TOI5 and Martha Ramirez for soybean growth. The EMS-mutagenized population of bread wheat cv. Cadenza was developed by Andy Phillips at Rothamsted. We acknowledge the Germplasm Resources Unit (GRU) at JIC for providing wheat seeds. L.D.V was a recipient of the VIB International PhD Scholarship in Life Sciences. X.X., T.Z and Y.W. are supported by grants from the Chinese Scholarship Council. A.L. was supported by a grant from the North Carolina Soybean Producers Association. Publisher Copyright: © 2021, The Author(s).

PY - 2021/5/14

Y1 - 2021/5/14

N2 - Plants respond to mild warm temperature conditions by increased elongation growth of organs to enhance cooling capacity, in a process called thermomorphogenesis. To this date, the regulation of thermomorphogenesis has been exclusively shown to intersect with light signalling pathways. To identify regulators of thermomorphogenesis that are conserved in flowering plants, we map changes in protein phosphorylation in both dicots and monocots exposed to warm temperature. We identify MITOGEN-ACTIVATED PROTEIN KINASE KINASE KINASE KINASE4 (MAP4K4)/TARGET OF TEMPERATURE3 (TOT3) as a regulator of thermomorphogenesis that impinges on brassinosteroid signalling in Arabidopsis thaliana. In addition, we show that TOT3 plays a role in thermal response in wheat, a monocot crop. Altogether, the conserved thermal regulation by TOT3 expands our knowledge of thermomorphogenesis beyond the well-studied pathways and can contribute to ensuring food security under a changing climate.

AB - Plants respond to mild warm temperature conditions by increased elongation growth of organs to enhance cooling capacity, in a process called thermomorphogenesis. To this date, the regulation of thermomorphogenesis has been exclusively shown to intersect with light signalling pathways. To identify regulators of thermomorphogenesis that are conserved in flowering plants, we map changes in protein phosphorylation in both dicots and monocots exposed to warm temperature. We identify MITOGEN-ACTIVATED PROTEIN KINASE KINASE KINASE KINASE4 (MAP4K4)/TARGET OF TEMPERATURE3 (TOT3) as a regulator of thermomorphogenesis that impinges on brassinosteroid signalling in Arabidopsis thaliana. In addition, we show that TOT3 plays a role in thermal response in wheat, a monocot crop. Altogether, the conserved thermal regulation by TOT3 expands our knowledge of thermomorphogenesis beyond the well-studied pathways and can contribute to ensuring food security under a changing climate.

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The membrane-localized protein kinase MAP4K4/TOT3 regulates thermomorphogenesis

Abstract

Bibliographical note

Funding

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