Functional evolution of Nodulin26-like Intrinsic Proteins: From bacterial arsenic detoxification to plant nutrient transport.
Functional evolution of Nodulin26-like Intrinsic Proteins: From bacterial arsenic detoxification to plant nutrient transport.
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DOI：
10.1111/nph.16217
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发表时间：
2019-11
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通讯作者：
Benjamin Pommerrenig;T. A. Diehn;Nadine Bernhardt;M. Bienert;Namiki Mitani-Ueno;Jacqueline Fuge;Annett Bieber;Christoph Spitzer;A. Bräutigam;J. Ma;F. Chaumont;G. Bienert
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作者：
Benjamin Pommerrenig;T. A. Diehn;Nadine Bernhardt;M. Bienert;Namiki Mitani-Ueno;Jacqueline Fuge;Annett Bieber;Christoph Spitzer;A. Bräutigam;J. Ma;F. Chaumont;G. Bienert
结瘤素26样内在蛋白（nodulin26-like-intrinsic-protein，NIPs）在种子植物中对硅、硼等营养物质的转运中起着重要作用，但这种转运功能的进化起源以及对有毒砷的共渗透性仍然是个谜。水平基因转移的细菌AqpN-aquaporin组尚未特征化的是植物NIP进化的起点。我们结合了密集的序列，系统发育和遗传背景分析和突变的方法与卵母细胞和植物中的各种运输试验，以解决细菌和藻类和陆生植物NIP的跨有机体和功能进化，并揭示其分子运输特异性特征。我们发现aqpN基因主要存在于原核生物的抗砷操纵子中。我们提供的遗传和功能证据表明，这些蛋白质有助于砷解毒机制。我们在藻类、苔类、苔藓、金鱼藻和蕨类植物中鉴定了具有祖先细菌AqpN选择性过滤器组合物的NIPs，并证明了这些原型植物NIPs及其原核祖细胞几乎不透水和硅，但转运砷和硼。通过突变方法，我们证明了在进化过程中，祖先NIP选择性转移到允许亚功能化。总之，我们的数据提供的证据表明，进化转化为必需的种子植物营养转运细菌砷外排通道。
Nodulin26-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 uncharacterized 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 trans-organismal 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 subfunctionalizations. Together, our data provided evidence that evolution converted bacterial arsenic efflux channels into essential seed plant nutrient transporters.