The Nodulin 26 Intrinsic Protein Subfamily

Roberts, Daniel M.; Routray, Pratyush

doi:10.1007/978-3-319-49395-4_13

Cited by 21 publications

(31 citation statements)

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“…Experimental data on NIPs of different plant species suggest that they are either impermeable or only weakly permeable to water (Roberts and Routray, ). This is in agreement with our results, namely that only BnaC08.NIP3;1c, BnaC04.NIP4;1a and BnaC06.NIP5;1c showed a slightly increased water permeability.…”

Section: Discussionmentioning

confidence: 99%

Boron demanding tissues of Brassica napus express specific sets of functional Nodulin26‐like Intrinsic Proteins and BOR1 transporters

et al. 2019

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SummaryThe sophisticated uptake and translocation regulation of the essential element boron (B) in plants is ensured by two transmembrane transporter families: the Nodulin26‐like Intrinsic Protein (NIP) and BOR transporter family. Though the agriculturally important crop Brassica napus is highly sensitive to B deficiency, and NIPs and BORs have been suggested to be responsible for B efficiency in this species, functional information of these transporter subfamilies is extremely rare. Here, we molecularly characterized the NIP and BOR1 transporter family in the European winter‐type cv. Darmor‐PBY018. Our transport assays in the heterologous oocyte and yeast expression systems as well as in growth complementation assays in planta demonstrated B transport activity of NIP5, NIP6, NIP7 and BOR1 isoforms. Moreover, we provided functional and quantitative evidence that also members of the NIP2, NIP3 and NIP4 groups facilitate the transport of B. A detailed B‐ and tissue‐dependent B‐transporter expression map was generated by quantitative polymerase chain reaction. We showed that NIP5 isoforms are highly upregulated under B‐deficient conditions in roots, but also in shoot tissues. Moreover, we detected transcripts of several B‐permeable NIPs from various groups in floral tissues that contribute to the B distribution within the highly B deficiency‐sensitive flowers.

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Section: Discussionmentioning

confidence: 99%

Boron demanding tissues of Brassica napus express specific sets of functional Nodulin26‐like Intrinsic Proteins and BOR1 transporters

et al. 2019

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“…The nodulin 26-like intrinsic proteins (NIPs) constitute a plant-specific subfamily of the aquaporin superfamily that is named for the archetype of the family, nodulin 26, which was demonstrated originally in nitrogen-fixing soybean (Glycine max) root nodules (Fortin et al, 1987). NIPs appeared early in land plant evolution and have undergone substantial structural and functional diversification (Danielson and Johanson, 2010;Abascal et al, 2014;Roberts and Routray, 2017). As a result, while they possess the basic structural fold of the aquaporin superfamily, they have a broad array of biological and biochemical functions and transport an array of substrates besides water, including metalloid hydroxides (boric acid, arsenous acid, and others), glycerol, lactic acid, urea, and hydrogen peroxide (Ludewig and Dynowski, 2009;Pommerrenig et al, 2015;Roberts and Routray, 2017).…”

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“…NIPs appeared early in land plant evolution and have undergone substantial structural and functional diversification (Danielson and Johanson, 2010;Abascal et al, 2014;Roberts and Routray, 2017). As a result, while they possess the basic structural fold of the aquaporin superfamily, they have a broad array of biological and biochemical functions and transport an array of substrates besides water, including metalloid hydroxides (boric acid, arsenous acid, and others), glycerol, lactic acid, urea, and hydrogen peroxide (Ludewig and Dynowski, 2009;Pommerrenig et al, 2015;Roberts and Routray, 2017). In seed plants, structural modeling and phylogenetic analysis of NIPs show that they can be grouped into three pore families (NIP I, II, and III) based on the composition of the four amino acids forming the selectivity filter of the pore (ar/R region; Wallace and Roberts, 2004;Danielson and Johanson, 2010;Mitani-Ueno et al, 2011; for review, see Roberts and Routray, 2017).…”

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“…As a result, while they possess the basic structural fold of the aquaporin superfamily, they have a broad array of biological and biochemical functions and transport an array of substrates besides water, including metalloid hydroxides (boric acid, arsenous acid, and others), glycerol, lactic acid, urea, and hydrogen peroxide (Ludewig and Dynowski, 2009;Pommerrenig et al, 2015;Roberts and Routray, 2017). In seed plants, structural modeling and phylogenetic analysis of NIPs show that they can be grouped into three pore families (NIP I, II, and III) based on the composition of the four amino acids forming the selectivity filter of the pore (ar/R region; Wallace and Roberts, 2004;Danielson and Johanson, 2010;Mitani-Ueno et al, 2011; for review, see Roberts and Routray, 2017). Substantial genetic and Nodulin Intrinsic Protein 7;1 Is a Tapetal Boric Acid Channel Involved in Pollen Cell Wall Formation 1 [OPEN] biochemical evidence show that proteins of the NIP II subfamily serve as permeases of boric acid (Takano et al, 2006(Takano et al, , 2008Tanaka et al, 2008;Hanaoka et al, 2014;Pommerrenig et al, 2015;Bienert and Bienert, 2017;Yoshinari and Takano, 2017).…”

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Nodulin Intrinsic Protein 7;1 Is a Tapetal Boric Acid Channel Involved in Pollen Cell Wall Formation

et al. 2018

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Boron is an essential plant micronutrient that plays a structural role in the rhamnogalacturonan II component of the pectic cell wall. To prevent boron deficiency under limiting conditions, its uptake, distribution, and homeostasis are mediated by boric acid transporters and channel proteins. Among the membrane channels that facilitate boric acid uptake are the type II nodulin intrinsic protein (NIP) subfamily of aquaporin-like proteins. Arabidopsis (Arabidopsis thaliana) possesses three NIP II genes (NIP5;1, NIP6;1, and NIP7;1) that show distinct tissue expression profiles (predominantly expressed in roots, stem nodes, and developing flowers, respectively). Orthologs of each are represented in all dicots. Here, we show that purified and reconstituted NIP7;1 is a boric acid facilitator. By using native promoter-reporter fusions, we show that NIP7;1 is expressed predominantly in anthers of young flowers in a narrow developmental window, floral stages 9 and 10, with protein accumulation solely within tapetum cells, where it is localized to the plasma membrane. Under limiting boric acid conditions, loss-of-function T-DNA mutants (nip7;1-1 and nip7;1-2) show reduced fertility, including shorter siliques and an increase in aborted seeds, compared with the wild type. Under these conditions, nip7;1 mutant pollen grains show morphological defects, increased aggregation, defective exine cell wall formation, reduced germination frequency, and decreased viability. During stages 9 and 10, the tapetum is essential for supplying materials to the pollen microspore cell wall. We propose that NIP7;1 serves as a gated boric acid channel in developing anthers that aids in the uptake of this critical micronutrient by tapetal cells.

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“…The absence of NIPs in green algae [14], however, seems difficult to reconcile with a vertical transfer of NIP genes in the green lineage since its beginning, and a horizontal transfer after the terrestrialization of plants, which occurred ~700 million years later [40], is still imagined possible [41].…”

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Plant aquaporins: the origin of NIPs

Borstlap

2018

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Many of the aquaporin genes in Cyanobacteria belong to the AqpN-clade. This clade was also the cradle of plant NIPs (nodulin-26 like intrinsic proteins) whose members are transporters for glycerol and several hydroxylated metalloids. The superphylum of Archaeplastida acquired the primordial NIP-gene most likely from the cyanobacterium that, some 1500 million years ago, became the ancestor of all plastids.Nodulin-26 is the major protein in the peribacteroid membrane of soybean nodules. Its coding gene was identified in 1987 and appeared to be related to the gene of the major intrinsic protein of the bovine eye lens and that of the glycerol facilitator of Escherichia coli [1,2]. After the protein CHIP28 from erythrocytes joined the club [3] and was characterized as the first water channel or aquaporin protein [4], the family of 'Major Intrinsic Proteins (MIPs)' or 'Aquaporins' came into view. The protein family consists of two major clades: the clade of aquaporins sensu stricto, which function mainly as water channels, and that of the glycerol facilitators (GlpF clade or GIPs, GlpF-like intrinsic proteins). Representatives of both clades are widely distributed in all life forms [5][6][7][8][9].Plant aquaporins fall into four major subfamilies: plasma membrane intrinsic proteins (PIPs), tonoplast intrinsic proteins (TIPs), nodulin 26-like intrinsic proteins (NIPs), and small, basic intrinsic proteins (SIPs) [9,11]. Two minor groups are the XIPs (X intrinsic proteins), with members in fungi, slime molds and several dicot plant families, and the HIPs (hybrid intrinsic proteins), a small group only present in mosses and lycopods [9,12,13]. GIPs have been encountered in some green algae [14] and in the moss Physcomitrella patens [15] but not in vascular plants. The NIPs are specific for plants. The subfamily is widely represented in the plant kingdom. The number of NIPs range from five in Physcomitrella [12] and four in a tiny angiosperm, the duckweed Spirodela polyrhiza [16], up to 13 in soybean (Glycine max) [17] and 32 in the mesohexaploid oilseed rape (Brassica napus) [18]. The absence of NIPs in green algae is remarkable [14]. NIPs are primarily known as transporters for glycerol (C 3 H 5 (OH) 3 ) [19] but during plant evolution the proliferation and diversification of NIP genes has resulted in specific transporters for a range of substrates, hydroxylated metalloids in particular [20-22]. NIPs are known for the transport of boron (B(OH) 3 ), silicon (Si(OH) 4 ), arsenic (As(OH) 3 ), and antimony (Sb(OH) 3 ). In addition particular NIPs are transporters for lactic acid (COOH.CH(OH).CH 3 ) [23] and aluminium malate, ((Al 3+ ) 2 (COO¯.CH(OH).CH 2 .COO¯) 3 )[24]. Most telling, perhaps, is the number of 11 NIP-genes in the silicon-accumulating horsetail Equisetum arvensis, that are all assumed to code for transporters of silicic acid [25,26].

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The Nodulin 26 Intrinsic Protein Subfamily

Cited by 21 publications

References 163 publications

Boron demanding tissues of Brassica napus express specific sets of functional Nodulin26‐like Intrinsic Proteins and BOR1 transporters

Boron demanding tissues of Brassica napus express specific sets of functional Nodulin26‐like Intrinsic Proteins and BOR1 transporters

Nodulin Intrinsic Protein 7;1 Is a Tapetal Boric Acid Channel Involved in Pollen Cell Wall Formation

Plant aquaporins: the origin of NIPs

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