ATP sensing in living plant cells reveals tissue gradients and stress dynamics of energy physiology

Author:

De Col Valentina12ORCID,Fuchs Philippe1ORCID,Nietzel Thomas1ORCID,Elsässer Marlene1,Voon Chia Pao3ORCID,Candeo Alessia4ORCID,Seeliger Ingo1,Fricker Mark D5ORCID,Grefen Christopher6ORCID,Møller Ian Max7,Bassi Andrea4ORCID,Lim Boon Leong38ORCID,Zancani Marco2ORCID,Meyer Andreas J19ORCID,Costa Alex10ORCID,Wagner Stephan1ORCID,Schwarzländer Markus19ORCID

Affiliation:

1. Institute of Crop Science and Resource Conservation, University of Bonn, Bonn, Germany

2. Department of Agricultural, Food, Environmental and Animal Sciences, University of Udine, Udine, Italy

3. School of Biological Sciences, University of Hong Kong, Hong Kong, China

4. Dipartimento di Fisica, Politecnico di Milano, Milano, Italy

5. Department of Plant Sciences, University of Oxford, Oxford, United Kingdom

6. Centre for Plant Molecular Biology, Developmental Genetics, University of Tübingen, Tübingen, Germany

7. Department of Molecular Biology and Genetics, Aarhus University, Aarhus, Denmark

8. State Key Laboratory of Agrobiotechnology, Chinese University of Hong Kong, Hong Kong, China

9. Bioeconomy Science Center, Forschungszentrum Jülich, Jülich, Germany

10. Dipartimento di Bioscienze, Università degli Studi di Milano, Milano, Italy

Abstract

Growth and development of plants is ultimately driven by light energy captured through photosynthesis. ATP acts as universal cellular energy cofactor fuelling all life processes, including gene expression, metabolism, and transport. Despite a mechanistic understanding of ATP biochemistry, ATP dynamics in the living plant have been largely elusive. Here, we establish MgATP2- measurement in living plants using the fluorescent protein biosensor ATeam1.03-nD/nA. We generate Arabidopsis sensor lines and investigate the sensor in vitro under conditions appropriate for the plant cytosol. We establish an assay for ATP fluxes in isolated mitochondria, and demonstrate that the sensor responds rapidly and reliably to MgATP2- changes in planta. A MgATP2- map of the Arabidopsis seedling highlights different MgATP2- concentrations between tissues and within individual cell types, such as root hairs. Progression of hypoxia reveals substantial plasticity of ATP homeostasis in seedlings, demonstrating that ATP dynamics can be monitored in the living plant.

Funder

Deutsche Forschungsgemeinschaft

Bioeconomy Science Center, NRW

Ministero dell'Istruzione, dell'Università e della Ricerca

Piano di Sviluppo di Ateneo

Deutscher Akademischer Austauschdienst

European Social Fund

European Commission

Human Frontier Science Program

Leverhulme Trust

Independent Research Fund Denmark - Natural Sciences

Innovation and Technology Commission

Publisher

eLife Sciences Publications, Ltd

Subject

General Immunology and Microbiology,General Biochemistry, Genetics and Molecular Biology,General Medicine,General Neuroscience

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