GOLLUM [FeFe]-hydrogenase-like proteins are essential for plant development in normoxic conditions and modulate energy metabolism

Samuel Mondy; Aurore Lenglet; Viviane Cosson; Sandra Pelletier; Stéphanie Pateyron; Françoise Gilard; Marije Scholte; Lysiane Brocard; Jean Malo Couzigou; Guillaume Tcherkez; Michel Péan; Pascal Ratet

doi:10.1111/pce.12128

GOLLUM [FeFe]-hydrogenase-like proteins are essential for plant development in normoxic conditions and modulate energy metabolism

Samuel Mondy, Aurore Lenglet, Viviane Cosson, Sandra Pelletier, Stéphanie Pateyron, Françoise Gilard, Marije Scholte, Lysiane Brocard, Jean Malo Couzigou, Guillaume Tcherkez, Michel Péan, Pascal Ratet^*

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

12 Citations (Scopus)

Abstract

[FeFe]-hydrogenase-like genes encode [Fe₄S₄]-containing proteins that are ubiquitous in eukaryotic cells. In humans, iron-only hydrogenase-like protein 1 (IOP1) represses hypoxia inducible factor-1α subunit (HIF1-α) at normal atmospheric partial O₂ pressure (normoxia, 21kPa O₂). In yeasts, the nar1 mutant cannot grow at 21kPa O_2, but can develop at a lower O₂ pressure (2kPa O₂). We show here that plant [FeFe]-hydrogenase-like GOLLUM genes are essential for plant development and cell cycle progression. The mutant phenotypes of these plants are seen in normoxic conditions, but not under conditions of mild hypoxia (5kPa O₂). Transcriptomic and metabolomic experiments showed that the mutation enhances the expression of some hypoxia-induced genes under normal atmospheric O₂ conditions and changes the cellular content of metabolites related to energy metabolism. In conclusion, [FeFe]-hydrogenase-like proteins play a central role in eukaryotes including the adaptation of plants to the ambient O₂ partial pressure.

Original language	English
Pages (from-to)	54-69
Number of pages	16
Journal	Plant, Cell and Environment
Volume	37
Issue number	1
DOIs	https://doi.org/10.1111/pce.12128
Publication status	Published - Jan 2014
Externally published	Yes

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Mondy, S., Lenglet, A., Cosson, V., Pelletier, S., Pateyron, S., Gilard, F., Scholte, M., Brocard, L., Couzigou, J. M., Tcherkez, G., Péan, M., & Ratet, P. (2014). GOLLUM [FeFe]-hydrogenase-like proteins are essential for plant development in normoxic conditions and modulate energy metabolism. Plant, Cell and Environment, 37(1), 54-69. https://doi.org/10.1111/pce.12128

@article{bd696967ba34433e8029bc36f2a284dc,

title = "GOLLUM [FeFe]-hydrogenase-like proteins are essential for plant development in normoxic conditions and modulate energy metabolism",

abstract = "[FeFe]-hydrogenase-like genes encode [Fe4S4]-containing proteins that are ubiquitous in eukaryotic cells. In humans, iron-only hydrogenase-like protein 1 (IOP1) represses hypoxia inducible factor-1α subunit (HIF1-α) at normal atmospheric partial O2 pressure (normoxia, 21kPa O2). In yeasts, the nar1 mutant cannot grow at 21kPa O2, but can develop at a lower O2 pressure (2kPa O2). We show here that plant [FeFe]-hydrogenase-like GOLLUM genes are essential for plant development and cell cycle progression. The mutant phenotypes of these plants are seen in normoxic conditions, but not under conditions of mild hypoxia (5kPa O2). Transcriptomic and metabolomic experiments showed that the mutation enhances the expression of some hypoxia-induced genes under normal atmospheric O2 conditions and changes the cellular content of metabolites related to energy metabolism. In conclusion, [FeFe]-hydrogenase-like proteins play a central role in eukaryotes including the adaptation of plants to the ambient O2 partial pressure.",

keywords = "Arabidopsis, HIF-1α, IOP, Medicago, NAR1, Oxygen, Warburg effect",

author = "Samuel Mondy and Aurore Lenglet and Viviane Cosson and Sandra Pelletier and St{\'e}phanie Pateyron and Fran{\c c}oise Gilard and Marije Scholte and Lysiane Brocard and Couzigou, {Jean Malo} and Guillaume Tcherkez and Michel P{\'e}an and Pascal Ratet",

year = "2014",

month = jan,

doi = "10.1111/pce.12128",

language = "English",

volume = "37",

pages = "54--69",

journal = "Plant, Cell and Environment",

issn = "0140-7791",

publisher = "Wiley-Blackwell Publishing Ltd",

number = "1",

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Mondy, S, Lenglet, A, Cosson, V, Pelletier, S, Pateyron, S, Gilard, F, Scholte, M, Brocard, L, Couzigou, JM, Tcherkez, G, Péan, M & Ratet, P 2014, 'GOLLUM [FeFe]-hydrogenase-like proteins are essential for plant development in normoxic conditions and modulate energy metabolism', Plant, Cell and Environment, vol. 37, no. 1, pp. 54-69. https://doi.org/10.1111/pce.12128

TY - JOUR

T1 - GOLLUM [FeFe]-hydrogenase-like proteins are essential for plant development in normoxic conditions and modulate energy metabolism

AU - Mondy, Samuel

AU - Lenglet, Aurore

AU - Cosson, Viviane

AU - Pelletier, Sandra

AU - Pateyron, Stéphanie

AU - Gilard, Françoise

AU - Scholte, Marije

AU - Brocard, Lysiane

AU - Couzigou, Jean Malo

AU - Tcherkez, Guillaume

AU - Péan, Michel

AU - Ratet, Pascal

PY - 2014/1

Y1 - 2014/1

N2 - [FeFe]-hydrogenase-like genes encode [Fe4S4]-containing proteins that are ubiquitous in eukaryotic cells. In humans, iron-only hydrogenase-like protein 1 (IOP1) represses hypoxia inducible factor-1α subunit (HIF1-α) at normal atmospheric partial O2 pressure (normoxia, 21kPa O2). In yeasts, the nar1 mutant cannot grow at 21kPa O2, but can develop at a lower O2 pressure (2kPa O2). We show here that plant [FeFe]-hydrogenase-like GOLLUM genes are essential for plant development and cell cycle progression. The mutant phenotypes of these plants are seen in normoxic conditions, but not under conditions of mild hypoxia (5kPa O2). Transcriptomic and metabolomic experiments showed that the mutation enhances the expression of some hypoxia-induced genes under normal atmospheric O2 conditions and changes the cellular content of metabolites related to energy metabolism. In conclusion, [FeFe]-hydrogenase-like proteins play a central role in eukaryotes including the adaptation of plants to the ambient O2 partial pressure.

AB - [FeFe]-hydrogenase-like genes encode [Fe4S4]-containing proteins that are ubiquitous in eukaryotic cells. In humans, iron-only hydrogenase-like protein 1 (IOP1) represses hypoxia inducible factor-1α subunit (HIF1-α) at normal atmospheric partial O2 pressure (normoxia, 21kPa O2). In yeasts, the nar1 mutant cannot grow at 21kPa O2, but can develop at a lower O2 pressure (2kPa O2). We show here that plant [FeFe]-hydrogenase-like GOLLUM genes are essential for plant development and cell cycle progression. The mutant phenotypes of these plants are seen in normoxic conditions, but not under conditions of mild hypoxia (5kPa O2). Transcriptomic and metabolomic experiments showed that the mutation enhances the expression of some hypoxia-induced genes under normal atmospheric O2 conditions and changes the cellular content of metabolites related to energy metabolism. In conclusion, [FeFe]-hydrogenase-like proteins play a central role in eukaryotes including the adaptation of plants to the ambient O2 partial pressure.

KW - Arabidopsis

KW - HIF-1α

KW - IOP

KW - Medicago

KW - NAR1

KW - Oxygen

KW - Warburg effect

UR - http://www.scopus.com/inward/record.url?scp=84896905240&partnerID=8YFLogxK

U2 - 10.1111/pce.12128

DO - 10.1111/pce.12128

M3 - Article

SN - 0140-7791

VL - 37

SP - 54

EP - 69

JO - Plant, Cell and Environment

JF - Plant, Cell and Environment

IS - 1

ER -

GOLLUM [FeFe]-hydrogenase-like proteins are essential for plant development in normoxic conditions and modulate energy metabolism

Abstract

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