A guanosine tetraphosphate (ppGpp) mediated brake on photosynthesis is required for acclimation to nitrogen limitation in Arabidopsis
- Aix-Marseille University, CEA, CNRS, BIAM, France
- University of Carthage, Tunisia
- Université Paris-Saclay, UMR1318, INRAE, France
- Université Paris-Saclay, CNRS, INRAE, France
- University of Tunis El Manar, Tunisia
Abstract
Guanosine pentaphosphate and tetraphosphate (together referred to as ppGpp) are hyperphosphorylated nucleotides found in bacteria and the chloroplasts of plants and algae. In plants and algae artificial ppGpp accumulation can inhibit chloroplast gene expression, and influence photosynthesis, nutrient remobilisation, growth, and immunity. However, it is so far unknown whether ppGpp is required for abiotic stress acclimation in plants. Here, we demonstrate that ppGpp biosynthesis is necessary for acclimation to nitrogen starvation in Arabidopsis. We show that ppGpp is required for remodeling the photosynthetic electron transport chain to downregulate photosynthetic activity and for protection against oxidative stress. Furthermore, we demonstrate that ppGpp is required for coupling chloroplastic and nuclear gene expression during nitrogen starvation. Altogether, our work indicates that ppGpp is a pivotal regulator of chloroplast activity for stress acclimation in plants.
Data availability
All data presented in this study are included in the manuscript and supporting files Source Data files have been provided for Figures 1-5 (+ supplements).Sequencing data have been deposited at the European Nucleotide Archive under accession number PRJEB46181.
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Effects of ppGpp on gene expression during nitrogen deprivation in Arabidopsis.European Nucleotide Archive, PRJEB46181.
Article and author information
Author details
Funding
Agence Nationale de la Recherche (ANR-17-CE13-0005)
- Benjamin Field
Agence Nationale de la Recherche (ANR-17-EUR-0007)
- Sylvie Citerne
- Jose Caius
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Shinji Masuda, Tokyo Institute of Technology, Japan
Version history
- Preprint posted: September 20, 2021 (view preprint)
- Received: October 28, 2021
- Accepted: February 14, 2022
- Accepted Manuscript published: February 14, 2022 (version 1)
- Version of Record published: March 1, 2022 (version 2)
Copyright
© 2022, Romand et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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A guanosine tetraphosphate (ppGpp) mediated brake on photosynthesis is required for acclimation to nitrogen limitation in Arabidopsis
eLife 11:e75041.
https://doi.org/10.7554/eLife.75041
Further reading
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Transmembrane signaling by plant receptor kinases (RKs) has long been thought to involve reciprocal trans-phosphorylation of their intracellular kinase domains. The fact that many of these are pseudokinase domains, however, suggests that additional mechanisms must govern RK signaling activation. Non-catalytic signaling mechanisms of protein kinase domains have been described in metazoans, but information is scarce for plants. Recently, a non-catalytic function was reported for the leucine-rich repeat (LRR)-RK subfamily XIIa member EFR (elongation factor Tu receptor) and phosphorylation-dependent conformational changes were proposed to regulate signaling of RKs with non-RD kinase domains. Here, using EFR as a model, we describe a non-catalytic activation mechanism for LRR-RKs with non-RD kinase domains. EFR is an active kinase, but a kinase-dead variant retains the ability to enhance catalytic activity of its co-receptor kinase BAK1/SERK3 (brassinosteroid insensitive 1-associated kinase 1/somatic embryogenesis receptor kinase 3). Applying hydrogen-deuterium exchange mass spectrometry (HDX-MS) analysis and designing homology-based intragenic suppressor mutations, we provide evidence that the EFR kinase domain must adopt its active conformation in order to activate BAK1 allosterically, likely by supporting αC-helix positioning in BAK1. Our results suggest a conformational toggle model for signaling, in which BAK1 first phosphorylates EFR in the activation loop to stabilize its active conformation, allowing EFR in turn to allosterically activate BAK1.
