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 are facilitated remains limited. Arabidopsis thaliana homologues 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 jasmonate-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.

MCU proteins dominate in vivo mitochondrial Ca2+ uptake in Arabidopsis roots / C. Ruberti, E. Feitosa-Araujo, Z. Xu, S. Wagner, M. Grenzi, E. Darwish, S. Lichtenauer, P. Fuchs, A.S. Parmagnani, D. Balcerowicz, S. Schoenaers, C. de la Torre, K. Mekkaoui, A. Nunes-Nesi, M. Wirtz, K. Vissenberg, O. Van Aken, B. Hause, A. Costa, M. Schwarzländer. - In: PLANT CELL. - ISSN 1040-4651. - 34:11(2022 Nov), pp. 4428-4452. [10.1093/plcell/koac242]

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

C. Ruberti
Primo
;
M. Grenzi;A.S. Parmagnani;A. Costa
Penultimo
;
2022

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 are facilitated remains limited. Arabidopsis thaliana homologues 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 jasmonate-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.
Settore BIO/04 - Fisiologia Vegetale
   Piano di Sostegno alla Ricerca 2015-2017 - Linea 2 "Dotazione annuale per attività istituzionali" (anno 2019)
   UNIVERSITA' DEGLI STUDI DI MILANO
nov-2022
8-ago-2022
https://academic.oup.com/plcell/advance-article/doi/10.1093/plcell/koac242/6656361
Article (author)
File in questo prodotto:
File Dimensione Formato  
koac242.pdf

accesso aperto

Tipologia: Publisher's version/PDF
Dimensione 3.55 MB
Formato Adobe PDF
3.55 MB Adobe PDF Visualizza/Apri
Pubblicazioni consigliate

I documenti in IRIS sono protetti da copyright e tutti i diritti sono riservati, salvo diversa indicazione.

Utilizza questo identificativo per citare o creare un link a questo documento: https://hdl.handle.net/2434/936527
Citazioni
  • ???jsp.display-item.citation.pmc??? 3
  • Scopus 15
  • ???jsp.display-item.citation.isi??? 14
social impact