@article{64ac6317f8ce4ffb8fecd81287a0c35b,
title = "Functional evolution of nodulin 26-like intrinsic proteins: from bacterial arsenic detoxification to plant nutrient transport",
abstract = "Nodulin 26-like intrinsic proteins (NIPs) play essential roles in transporting the nutrients silicon and boron in seed plants, but the evolutionary origin of this transport function and the co-permeability to toxic arsenic remains enigmatic. Horizontal gene transfer of a yet uncharacterised bacterial AqpN-aquaporin group was the starting-point for plant NIP evolution. We combined intense sequence, phylogenetic and genetic context analyses and a mutational approach with various transport assays in oocytes and plants to resolve the transorganismal and functional evolution of bacterial and algal and terrestrial plant NIPs and to reveal their molecular transport specificity features. We discovered that aqpN genes are prevalently located in arsenic resistance operons of various prokaryotic phyla. We provided genetic and functional evidence that these proteins contribute to the arsenic detoxification machinery. We identified NIPs with the ancestral bacterial AqpN selectivity filter composition in algae, liverworts, moss, hornworts and ferns and demonstrated that these archetype plant NIPs and their prokaryotic progenitors are almost impermeable to water and silicon but transport arsenic and boron. With a mutational approach, we demonstrated that during evolution, ancestral NIP selectivity shifted to allow subfunctionalisations. Together, our data provided evidence that evolution converted bacterial arsenic efflux channels into essential seed plant nutrient transporters.",
keywords = "aquaporin, arsenic, boron, evolution, metalloid, nodulin 26-like intrinsic proteins, nutrient transport",
author = "Benjamin Pommerrenig and Diehn, {Till A.} and Nadine Bernhardt and Bienert, {Manuela D.} and Namiki Mitani-Ueno and Jacqueline Fuge and Annett Bieber and Christoph Spitzer and Andrea Br{\"a}utigam and Ma, {Jian Feng} and Fran{\c c}ois Chaumont and Bienert, {Gerd P.}",
note = "Funding Information: We thank Dr Tandron Moja and Dr Eggert (IPK‐Gatersleben, Germany) for ICP‐MS analyses, and Dr Takano (University of Hokkaido, Japan) for the provision of the plasmid pP46 containing the ). The authors declare no competing interest. This work was supported by the Deutsche Forschungsgemeinschaft (1668/1‐1 to GPB), Grant‐in‐Aid for Specially Promoted Research (16H06296 to JFM), Belgian National Fund for Scientific Research to FC, the Belgian French community (ARC16/21‐075 to FC) and the Bauchau Award to FC. AtNIP5;1 promoter. We are thankful to Dr Finn for providing processable MIP sequences which have been used for the phylogenetic analyses (Finn & Cerd{\`a}, Funding Information: We thank Dr Tandron Moja and Dr Eggert (IPK-Gatersleben, Germany) for ICP-MS analyses, and Dr Takano (University of Hokkaido, Japan) for the provision of the plasmid pP46 containing the AtNIP5;1 promoter. We are thankful to Dr Finn for providing processable MIP sequences which have been used for the phylogenetic analyses (Finn & Cerd?,). The authors declare no competing interest. This work was supported by the Deutsche Forschungsgemeinschaft (1668/1-1 to GPB), Grant-in-Aid for Specially Promoted Research (16H06296 to JFM), Belgian National Fund for Scientific Research to FC, the Belgian French community (ARC16/21-075 to FC) and the Bauchau Award to FC. Publisher Copyright: {\textcopyright} 2019 The Authors. New Phytologist {\textcopyright} 2019 New Phytologist Trust",
year = "2020",
month = feb,
day = "1",
doi = "10.1111/nph.16217",
language = "English",
volume = "225",
pages = "1383--1396",
journal = "New Phytologist",
issn = "0028-646X",
publisher = "Wiley-Blackwell",
number = "3",
}