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MCU proteins dominate in vivo mitochondrial Ca2+ uptake in Arabidopsis roots

Ruberti, Cristina ; Feitosa-Araujo, Elias ; Xu, Zhaolong ; Wagner, Stephan ; Grenzi, Matteo ; Darwish, Essam LU ; Lichtenauer, Sophie ; Fuchs, Philippe ; Parmagnani, Ambra Selene and Balcerowicz, Daria , et al. (2022) In Plant Cell 34(11). p.4428-4452
Abstract

Ca2 + signaling is central to plant development and acclimation. While Ca2 + -responsive proteins have been investigated intensely in plants, only a few Ca2 + -permeable channels have been identified, and our understanding of how intracellular Ca2 + fluxes is facilitated remains limited. Arabidopsis thaliana homologs of the mammalian channel-forming mitochondrial calcium uniporter (MCU) protein showed Ca2 + transport activity in vitro. Yet, the evolutionary complexity of MCU proteins, as well as reports about alternative systems and unperturbed mitochondrial Ca2 + uptake in knockout lines of MCU genes, leave critical questions about the in vivo functions of the MCU... (More)

Ca2 + signaling is central to plant development and acclimation. While Ca2 + -responsive proteins have been investigated intensely in plants, only a few Ca2 + -permeable channels have been identified, and our understanding of how intracellular Ca2 + fluxes is facilitated remains limited. Arabidopsis thaliana homologs of the mammalian channel-forming mitochondrial calcium uniporter (MCU) protein showed Ca2 + transport activity in vitro. Yet, the evolutionary complexity of MCU proteins, as well as reports about alternative systems and unperturbed mitochondrial Ca2 + uptake in knockout lines of MCU genes, leave critical questions about the in vivo functions of the MCU protein family in plants unanswered. Here, we demonstrate that MCU proteins mediate mitochondrial Ca2 + transport in planta and that this mechanism is the major route for fast Ca2 + uptake. Guided by the subcellular localization, expression, and conservation of MCU proteins, we generated an mcu triple knockout line. Using Ca2 + imaging in living root tips and the stimulation of Ca2 + transients of different amplitudes, we demonstrated that mitochondrial Ca2 + uptake became limiting in the triple mutant. The drastic cell physiological phenotype of impaired subcellular Ca2 + transport coincided with deregulated jasmonic acid-related signaling and thigmomorphogenesis. Our findings establish MCUs as a major mitochondrial Ca2 + entry route in planta and link mitochondrial Ca2 + transport with phytohormone signaling.

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type
Contribution to journal
publication status
published
subject
in
Plant Cell
volume
34
issue
11
pages
25 pages
publisher
American Society of Plant Biologists
external identifiers
  • scopus:85140896180
ISSN
1040-4651
DOI
10.1093/plcell/koac242
language
English
LU publication?
yes
additional info
Publisher Copyright: © The Author(s) 2022.
id
9a025727-b52e-477d-af91-72ec12809206
date added to LUP
2024-10-16 09:36:18
date last changed
2025-04-04 14:12:11
@article{9a025727-b52e-477d-af91-72ec12809206,
  abstract     = {{<p>Ca<sup>2 +</sup> signaling is central to plant development and acclimation. While Ca<sup>2 +</sup> -responsive proteins have been investigated intensely in plants, only a few Ca<sup>2 +</sup> -permeable channels have been identified, and our understanding of how intracellular Ca<sup>2 +</sup> fluxes is facilitated remains limited. Arabidopsis thaliana homologs of the mammalian channel-forming mitochondrial calcium uniporter (MCU) protein showed Ca<sup>2 +</sup> transport activity in vitro. Yet, the evolutionary complexity of MCU proteins, as well as reports about alternative systems and unperturbed mitochondrial Ca<sup>2 +</sup> uptake in knockout lines of MCU genes, leave critical questions about the in vivo functions of the MCU protein family in plants unanswered. Here, we demonstrate that MCU proteins mediate mitochondrial Ca<sup>2 +</sup> transport in planta and that this mechanism is the major route for fast Ca<sup>2 +</sup> uptake. Guided by the subcellular localization, expression, and conservation of MCU proteins, we generated an mcu triple knockout line. Using Ca<sup>2 +</sup> imaging in living root tips and the stimulation of Ca<sup>2 +</sup> transients of different amplitudes, we demonstrated that mitochondrial Ca<sup>2 +</sup> uptake became limiting in the triple mutant. The drastic cell physiological phenotype of impaired subcellular Ca<sup>2 +</sup> transport coincided with deregulated jasmonic acid-related signaling and thigmomorphogenesis. Our findings establish MCUs as a major mitochondrial Ca<sup>2 +</sup> entry route in planta and link mitochondrial Ca<sup>2 +</sup> transport with phytohormone signaling.</p>}},
  author       = {{Ruberti, Cristina and Feitosa-Araujo, Elias and Xu, Zhaolong and Wagner, Stephan and Grenzi, Matteo and Darwish, Essam and Lichtenauer, Sophie and Fuchs, Philippe and Parmagnani, Ambra Selene and Balcerowicz, Daria and Schoenaers, Sébastjen and de la Torre, Carolina and Mekkaoui, Khansa and Nunes-Nesi, Adriano and Wirtz, Markus and Vissenberg, Kris and Van Aken, Olivier and Hause, Bettina and Costa, Alex and Schwarzländer, Markus}},
  issn         = {{1040-4651}},
  language     = {{eng}},
  number       = {{11}},
  pages        = {{4428--4452}},
  publisher    = {{American Society of Plant Biologists}},
  series       = {{Plant Cell}},
  title        = {{MCU proteins dominate in vivo mitochondrial Ca<sup>2+</sup> uptake in Arabidopsis roots}},
  url          = {{http://dx.doi.org/10.1093/plcell/koac242}},
  doi          = {{10.1093/plcell/koac242}},
  volume       = {{34}},
  year         = {{2022}},
}