The Arabidopsis V-ATPase is localized to the TGN/EE via a seed plant specific motif

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Abstract

The V-ATPase is a versatile proton-pump found in a range of endomembrane compartments yet the mechanisms governing its differential targeting remain to be determined. In Arabidopsis, VHA-a1 targets the V-ATPase to the TGN/EE whereas VHA-a2 and VHA-a3 are localized to the tonoplast. We report here that the VHA-a1 targeting domain serves as both an ER-exit and as a TGN/EE-retention motif and is conserved among seed plants. In contrast, Marchantia encodes a single VHA-isoform that localizes to the TGN/EE and the tonoplast in Arabidopsis. Analysis of CRISPR/Cas9 generated null alleles revealed that VHA-a1 has an essential for male gametophyte development but acts redundantly with the tonoplast isoforms during vegetative growth. We propose that in the absence of VHA-a1, VHA-a3 is partially re-routed to the TGN/EE. Our findings contribute to understanding the evolutionary origin of V-ATPase targeting and provide a striking example that differential localization does not preclude functional redundancy.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files. Source data is provided for Figures 2,4B, 5B, 7B and C, 8C and D, 10A, Supplemental Figure 8B, Supplemental Figure 9 and Supplemental Figure 15A.

The following previously published data sets were used

1. Zhang J et al
(2019) The hornwort genome and early land plant evolution
Dryad Digital Repository,10.5061/dryad.msbcc2ftv.

https://doi.org/10.5061/dryad.msbcc2ftv

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Upendo Lupanga

Department of Cell Biology, Centre for Organismal Studies (COS), Heidelberg University, Heidelberg, Germany

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The authors declare that no competing interests exist.
Rachel Röhrich

Department of Cell Biology, Centre for Organismal Studies (COS), Heidelberg University, Heidelberg, Germany

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The authors declare that no competing interests exist.
Jana Askani

Department of Cell Biology, Centre for Organismal Studies (COS), Heidelberg University, Heidelberg, Germany

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"This ORCID iD identifies the author of this article:" 0000-0002-1390-7344
Stefan Hilmer

Electron Microscopy Core Facility, Heidelberg University, Heidelberg University, Heidelberg, Germany

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The authors declare that no competing interests exist.
Christiane Kiefer

Dep. Biodiversity and Plant Systematics, Centre fOrganismal Studies, Heidelberg University, Heidelberg University, Heidelberg, Germany

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The authors declare that no competing interests exist.
Melanie Krebs

Department of Cell Biology, Centre for Organismal Studies (COS), Heidelberg University, Heidelberg, Germany

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The authors declare that no competing interests exist.
Takehiko Kanazawa

Division of Cellular Dynamics, National Institute for Basic Biology, Okazaki, Japan

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The authors declare that no competing interests exist.
Takashi Ueda

Division of Cellular Dynamics, National Institute for Basic Biology, Okazaki, Japan

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The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-5190-892X
Karin Schumacher

Department of Cell Biology, Centre for Organismal Studies (COS), Heidelberg University, Heidelberg, Germany

For correspondence
karin.schumacher@cos.uni-heidelberg.de

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The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0001-6484-8105

Funding

DFG (SFB1101 TPA02)

Karin Schumacher

Grants-in-Aid for Scientific Research (19H05675,18H0247,18K14738)

Takehiko Kanazawa
Takashi Ueda

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Copyright

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.