A precise spacing between the NPA domains of aquaporins is essential for silicon permeability in plants

A precise spacing between the NPA domains of aquaporins is essential for silicon permeability in plants
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DOI:
10.1111/tpj.12904
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发表时间:
2015-08-01
期刊:
影响因子:
7.2
通讯作者:
Belanger, Richard R.
Belanger, Richard R.
中科院分区:
生物学1区
文献类型:
--
作者:
Deshmukh, Rupesh Kailasrao;Vivancos, Julien;Belanger, Richard R.

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围绕硅(Si)在植物中的益处和必要性的争论因不同物种吸收这种元素的能力而加剧。这种特性似乎在携带特异性结节蛋白26样内在蛋白(NIPs)的物种中得到增强,NIPs是水通道蛋白的一个亚类。在这项工作中,我们的目的是表征植物水通道蛋白,以确定赋予硅渗透性的特征。通过对25个具有不同硅吸收能力的物种的985种水通道蛋白的比较分析,我们能够预测30种硅转运蛋白,并发现硅吸收仅限于具有GSGR选择性过滤器的NIP-III水通道蛋白的物种,并且天冬氨酸-脯氨酸-丙氨酸(NPA)结构域之间精确距离为108个氨基酸(AA)。后一个特征是特别重要的,因为它从来没有报道是必要的硅选择性。在非洲爪蟾卵母细胞表达系统中评估的功能表明,具有108 AA间距的NIPs具有Si渗透性,而在该距离上不同的蛋白质则没有。在随后的功能研究中,一个来自杨树的Si转运体突变为109-或107-AA的突变体无法导入,而一个从109- 108 AA突变的番茄NIP基因表现出罕见的功能获得。这些结果为将高等植物划分为硅富集体或硅排斥体提供了精确的分子基础。
The controversy surrounding silicon (Si) benefits and essentiality in plants is exacerbated by the differential ability of species to absorb this element. This property is seemingly enhanced in species carrying specific nodulin 26-like intrinsic proteins (NIPs), a subclass of aquaporins. In this work, our aim was to characterize plant aquaporins to define the features that confer Si permeability. Through comparative analysis of 985 aquaporins in 25 species with differing abilities to absorb Si, we were able to predict 30 Si transporters and discovered that Si absorption is exclusively confined to species that possess NIP-III aquaporins with a GSGR selectivity filter and a precise distance of 108 amino acids (AA) between the asparagine-proline-alanine (NPA) domains. The latter feature is of particular significance since it had never been reported to be essential for Si selectivity. Functionality assessed in the Xenopus oocyte expression system showed that NIPs with 108 AA spacing exhibited Si permeability, while proteins differing in that distance did not. In subsequent functional studies, a Si transporter from poplar mutated into variants with 109-or 107-AA spacing failed to import, and a tomato NIP gene mutated from 109 to 108 AA exhibited a rare gain of function. These results provide a precise molecular basis to classify higher plants into Si accumulators or excluders.