Asgard Arf GTPases can act as membrane-associating molecular switches with the potential to function in organelle biogenesis

Jing Zhu, Ruize Xie, Qiaoying Ren, Jiaming Zhou, Chen Chen, Meng-Xi Xie, You Zhou, Yan Zhang, Ningjing Liu, Jinchao Wang, Zhengwei Zhang, Xipeng Liu, Wupeng Yan (), Qingqiu Gong (), Liang Dong (), Jinwei Zhu (), Fengping Wang () and Zhiping Xie ()
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Jing Zhu: Shanghai Jiao Tong University
Ruize Xie: Shanghai Jiao Tong University
Qiaoying Ren: Shanghai Jiao Tong University
Jiaming Zhou: Shanghai Jiao Tong University
Chen Chen: Shanghai Jiao Tong University
Meng-Xi Xie: Shanghai Jiao Tong University
You Zhou: Shanghai Jiao Tong University
Yan Zhang: Shanghai Jiao Tong University
Ningjing Liu: Shanghai Jiao Tong University
Jinchao Wang: Shanghai Jiao Tong University
Zhengwei Zhang: Shanghai Jiao Tong University
Xipeng Liu: Shanghai Jiao Tong University
Wupeng Yan: Shanghai Jiao Tong University
Qingqiu Gong: Shanghai Jiao Tong University
Liang Dong: Shanghai Jiao Tong University
Jinwei Zhu: Shanghai Jiao Tong University
Fengping Wang: Shanghai Jiao Tong University
Zhiping Xie: Shanghai Jiao Tong University

Nature Communications, 2025, vol. 16, issue 1, 1-14

Abstract: Abstract Inward membrane budding, i.e., the bending of membrane towards the cytosol, is essential for forming and maintaining eukaryotic organelles. In eukaryotes, Arf GTPases initiate this inward budding. Our research shows that Asgard archaea genomes encode putative Arf proteins (AArfs). AArfs possess structural elements characteristic of their eukaryotic counterparts. When expressed in yeast and mammalian cells, some AArfs displayed GTP-dependent membrane targeting. In vitro, AArf associated with both eukaryotic and archaeal membranes. In yeast, AArfs interacted with and were regulated by key organelle biogenesis players. Expressing an AArf led to a massive proliferation of endomembrane organelles including the endoplasmic reticulum and Golgi. This AArf interacted with Sec23, a COPII vesicle coat component, in a GTP-dependent manner. These findings suggest certain AArfs are membrane-associating molecular switches with the functional potential to initiate organelle biogenesis, and the evolution of a functional coat could be the next critical step towards establishing eukaryotic cell architecture.

Date: 2025
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DOI: 10.1038/s41467-025-57902-7

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