Trehalose-6-phosphate signaling regulates lateral root formation in Arabidopsis thaliana.


Journal

Proceedings of the National Academy of Sciences of the United States of America
ISSN: 1091-6490
Titre abrégé: Proc Natl Acad Sci U S A
Pays: United States
ID NLM: 7505876

Informations de publication

Date de publication:
03 10 2023
Historique:
pmc-release: 25 03 2024
medline: 27 9 2023
pubmed: 25 9 2023
entrez: 25 9 2023
Statut: ppublish

Résumé

Plant roots explore the soil for water and nutrients, thereby determining plant fitness and agricultural yield, as well as determining ground substructure, water levels, and global carbon sequestration. The colonization of the soil requires investment of carbon and energy, but how sugar and energy signaling are integrated with root branching is unknown. Here, we show through combined genetic and chemical modulation of signaling pathways that the sugar small-molecule signal, trehalose-6-phosphate (T6P) regulates root branching through master kinases SNF1-related kinase-1 (SnRK1) and Target of Rapamycin (TOR) and with the involvement of the plant hormone auxin. Increase of T6P levels both via genetic targeting in lateral root (LR) founder cells and through light-activated release of the presignaling T6P-precursor reveals that T6P increases root branching through coordinated inhibition of SnRK1 and activation of TOR. Auxin, the master regulator of LR formation, impacts this T6P function by transcriptionally down-regulating the T6P-degrader trehalose phosphate phosphatase B in LR cells. Our results reveal a regulatory energy-balance network for LR formation that links the 'sugar signal' T6P to both SnRK1 and TOR downstream of auxin.

Identifiants

pubmed: 37748053
doi: 10.1073/pnas.2302996120
pmc: PMC10556606
doi:

Substances chimiques

trehalose-6-phosphate 4484-88-2
Trehalose B8WCK70T7I
Sugar Phosphates 0
Indoleacetic Acids 0
SnRK1 protein, Arabidopsis EC 2.7.11.1
Protein Serine-Threonine Kinases EC 2.7.11.1
Arabidopsis Proteins 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

e2302996120

Subventions

Organisme : Biotechnology and Biological Sciences Research Council
ID : BB/P016855/1
Pays : United Kingdom

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Auteurs

Stefania Morales-Herrera (S)

Department of Plant Biotechnology and Bioinformatics Ghent University, Ghent B-9052, Belgium.
Vlaams Instituut voor Biotechnologie Center for Plant Systems Biology, Ghent B-9052, Belgium.
Laboratory of Molecular Cell Biology, Katholieke Universiteit Leuven, Leuven B3001, Belgium.
Vlaams Instituut voor Biotechnologie-Katholieke Universiteit Leuven Center for Microbiology, Leuven B3001, Belgium.

Joris Jourquin (J)

Department of Plant Biotechnology and Bioinformatics Ghent University, Ghent B-9052, Belgium.
Vlaams Instituut voor Biotechnologie Center for Plant Systems Biology, Ghent B-9052, Belgium.

Frederic Coppé (F)

Department of Plant Biotechnology and Bioinformatics Ghent University, Ghent B-9052, Belgium.
Vlaams Instituut voor Biotechnologie Center for Plant Systems Biology, Ghent B-9052, Belgium.

Lorena Lopez-Galvis (L)

Department of Plant Biotechnology and Bioinformatics Ghent University, Ghent B-9052, Belgium.
Vlaams Instituut voor Biotechnologie Center for Plant Systems Biology, Ghent B-9052, Belgium.
Laboratory of Molecular Cell Biology, Katholieke Universiteit Leuven, Leuven B3001, Belgium.
Vlaams Instituut voor Biotechnologie-Katholieke Universiteit Leuven Center for Microbiology, Leuven B3001, Belgium.

Tom De Smet (T)

Department of Organic and Macromolecular Chemistry, Laboratory for Organic and Bio-Organic Synthesis, Ghent University, Ghent B-9000, Belgium.

Alaeddine Safi (A)

Department of Plant Biotechnology and Bioinformatics Ghent University, Ghent B-9052, Belgium.
Vlaams Instituut voor Biotechnologie Center for Plant Systems Biology, Ghent B-9052, Belgium.

Maria Njo (M)

Department of Plant Biotechnology and Bioinformatics Ghent University, Ghent B-9052, Belgium.
Vlaams Instituut voor Biotechnologie Center for Plant Systems Biology, Ghent B-9052, Belgium.

Cara A Griffiths (CA)

Department of Sustainable Soils and Crops, Rothamsted Research, Harpenden AL5 2JQ, United Kingdom.

John D Sidda (JD)

Department of Chemistry, Chemistry Research Laboratory, University of Oxford, Oxford OX1 3TA, United Kingdom.

James S O Mccullagh (JSO)

Department of Chemistry, Chemistry Research Laboratory, University of Oxford, Oxford OX1 3TA, United Kingdom.

Xiaochao Xue (X)

Department of Chemistry, Chemistry Research Laboratory, University of Oxford, Oxford OX1 3TA, United Kingdom.

Benjamin G Davis (BG)

Department of Chemistry, Chemistry Research Laboratory, University of Oxford, Oxford OX1 3TA, United Kingdom.
Next Generation Chemistry, The Rosalind Franklin Institute, Didcot OX1 3TA, United Kingdom.
Department of Pharmacology, University of Oxford, Oxford OX1 3TA, United Kingdom.

Johan Van der Eycken (J)

Department of Organic and Macromolecular Chemistry, Laboratory for Organic and Bio-Organic Synthesis, Ghent University, Ghent B-9000, Belgium.

Matthew J Paul (MJ)

Department of Sustainable Soils and Crops, Rothamsted Research, Harpenden AL5 2JQ, United Kingdom.

Patrick Van Dijck (P)

Laboratory of Molecular Cell Biology, Katholieke Universiteit Leuven, Leuven B3001, Belgium.
Vlaams Instituut voor Biotechnologie-Katholieke Universiteit Leuven Center for Microbiology, Leuven B3001, Belgium.
Katholieke Universiteit Leuven Plant Institute, Katholieke Universiteit Leuven, Leuven B3001, Belgium.

Tom Beeckman (T)

Department of Plant Biotechnology and Bioinformatics Ghent University, Ghent B-9052, Belgium.
Vlaams Instituut voor Biotechnologie Center for Plant Systems Biology, Ghent B-9052, Belgium.

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Classifications MeSH