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Golgi anti-apoptotic proteins are evolutionarily conserved ion channels that regulate cell death in plants

View ORCID ProfileMaija Sierla, View ORCID ProfileDavid L. Prole, View ORCID ProfileNuno Saraiva, Guia Carrara, Natalia Dinischiotu, View ORCID ProfileAleksia Vaattovaara, View ORCID ProfileMichael Wrzaczek, View ORCID ProfileColin W. Taylor, View ORCID ProfileGeoffrey L. Smith, Bart Feys
doi: https://doi.org/10.1101/859678
Maija Sierla
1Department of Life Sciences, Division of Biology, Imperial College London, South Kensington Campus, London SW7 2AZ, United Kingdom
2Organismal and Evolutionary Biology Research Programme, Faculty of Biological and Environmental Sciences, and Viikki Plant Science Centre, University of Helsinki, FI-00014 Helsinki, Finland
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  • For correspondence: maija.sierla@helsinki.fi
David L. Prole
3Department of Pharmacology, University of Cambridge, Tennis Court Road, Cambridge, CB2 1PD, UK
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Nuno Saraiva
4Department of Pathology, University of Cambridge, Cambridge, Tennis Court Road, CB2 1QP, UK
5CBIOS, Universidade Lusófona Research Centre for Biosciences & Health Technologies, Campo Grande 376, Lisbon 1749-024, Portugal
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Guia Carrara
4Department of Pathology, University of Cambridge, Cambridge, Tennis Court Road, CB2 1QP, UK
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Natalia Dinischiotu
1Department of Life Sciences, Division of Biology, Imperial College London, South Kensington Campus, London SW7 2AZ, United Kingdom
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Aleksia Vaattovaara
2Organismal and Evolutionary Biology Research Programme, Faculty of Biological and Environmental Sciences, and Viikki Plant Science Centre, University of Helsinki, FI-00014 Helsinki, Finland
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Michael Wrzaczek
2Organismal and Evolutionary Biology Research Programme, Faculty of Biological and Environmental Sciences, and Viikki Plant Science Centre, University of Helsinki, FI-00014 Helsinki, Finland
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Colin W. Taylor
3Department of Pharmacology, University of Cambridge, Tennis Court Road, Cambridge, CB2 1PD, UK
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Geoffrey L. Smith
4Department of Pathology, University of Cambridge, Cambridge, Tennis Court Road, CB2 1QP, UK
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Bart Feys
1Department of Life Sciences, Division of Biology, Imperial College London, South Kensington Campus, London SW7 2AZ, United Kingdom
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ABSTRACT

Programmed cell death regulates developmental and stress responses in eukaryotes. Golgi anti-apoptotic proteins (GAAPs) are evolutionarily conserved cell death regulators. Human and viral GAAPs inhibit apoptosis and modulate intracellular Ca2+ fluxes, and viral GAAPs form cation-selective channels. Although most mammalian cell death regulators are not conserved at the sequence level in plants, the GAAP gene family shows expansion, with five paralogues (AtGAAP1-5) in the Arabidopsis genome. We pursued molecular and physiological characterization of AtGAAPs making use of the advanced knowledge of their human and viral counterparts. Structural modeling of AtGAAPs predicted the presence of a channel-like pore, and electrophysiological recordings from purified AtGAAP3 reconstituted into lipid bilayers confirmed that plant GAAPs can function as ion channels. AtGAAP1 and AtGAAP4 localized exclusively to the Golgi within the plant cell, while AtGAAP2, AtGAAP3 and AtGAAP5 also showed tonoplastic localization. Gene expression analysis revealed differential spatial expression and abundance of transcript for AtGAAP paralogues in Arabidopsis tissues. We demonstrate that AtGAAP1-5 inhibit Bax-induced cell death in yeast. However, overexpression of AtGAAP1 induces cell death in Nicotiana benthamiana leaves and lesion mimic phenotype in Arabidopsis. We propose that AtGAAPs function as Golgi-localized ion channels that regulate cell death by affecting ionic homeostasis within the cell.

Highlight Arabidopsis Golgi anti-apoptotic proteins (GAAPs) share functional conservation with their human and viral counterparts in cell death regulation and ion channel activity

Abbreviations AtGAAP, Arabidopsis thaliana GAAP; BI-1, Bax inhibitor-1; CFP, cyan fluorescent protein; CMLV, camelpox virus; ER, Endoplasmic reticulum; GAAP, Golgi anti-apoptotic protein; GFP, green fluorescent protein; hGAAP, human GAAP; LFG, Lifeguard; LMM, lesion mimic mutant; PCD, programmed cell death; TMBIM, transmembrane Bax inhibitor-1 motif-containing; TMDs, transmembrane domains; vGAAP, viral GAAP; YFP, yellow fluorescent protein

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Posted November 29, 2019.
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Golgi anti-apoptotic proteins are evolutionarily conserved ion channels that regulate cell death in plants
Maija Sierla, David L. Prole, Nuno Saraiva, Guia Carrara, Natalia Dinischiotu, Aleksia Vaattovaara, Michael Wrzaczek, Colin W. Taylor, Geoffrey L. Smith, Bart Feys
bioRxiv 859678; doi: https://doi.org/10.1101/859678
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Golgi anti-apoptotic proteins are evolutionarily conserved ion channels that regulate cell death in plants
Maija Sierla, David L. Prole, Nuno Saraiva, Guia Carrara, Natalia Dinischiotu, Aleksia Vaattovaara, Michael Wrzaczek, Colin W. Taylor, Geoffrey L. Smith, Bart Feys
bioRxiv 859678; doi: https://doi.org/10.1101/859678

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