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Functional evolution of nodulin 26-like intrinsic proteins: from bacterial arsenic detoxification to plant nutrient transport.

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Pommerrenig, Benjamin Diehn, Till A Bernhardt, Nadine Bienert, Manuela D Mitani-Ueno, Namiki Chaumont, François [UCL] Bienert, Gerd P

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.

Document type Article de périodique (Journal article) – Article de recherche
Access type Accès libre
Publication date 2019
Language Anglais
Journal information "New Phytologist (Online)" - Vol. 225, no. 3, p. 1383-1396 (2020)
Peer reviewed yes
Publisher Wiley-Blackwell Publishing Ltd. (Oxford)
e-issn 1469-8137
Publication status Publié
Affiliation UCL - SST/LIBST - Louvain Institute of Biomolecular Science and Technology
Keywords aquaporin ; arsenic ; boron ; evolution ; metalloid ; nodulin 26-like intrinsic proteins ; nutrient transport
Links
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Bibliographic reference Pommerrenig, Benjamin ; Diehn, Till A ; Bernhardt, Nadine ; Bienert, Manuela D ; Mitani-Ueno, Namiki ; et. al. Functional evolution of nodulin 26-like intrinsic proteins: from bacterial arsenic detoxification to plant nutrient transport.. In: New Phytologist (Online), Vol. 225, no. 3, p. 1383-1396 (2020)
Permanent URL http://hdl.handle.net/2078.1/221771