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Comparative Study
. 2007 Apr 19;7:27.
doi: 10.1186/1472-6807-7-27.

Homology Modeling of Major Intrinsic Proteins in Rice, Maize and Arabidopsis: Comparative Analysis of Transmembrane Helix Association and Aromatic/Arginine Selectivity Filters

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Free PMC article
Comparative Study

Homology Modeling of Major Intrinsic Proteins in Rice, Maize and Arabidopsis: Comparative Analysis of Transmembrane Helix Association and Aromatic/Arginine Selectivity Filters

Anjali Bansal et al. BMC Struct Biol. .
Free PMC article

Abstract

Background: The major intrinsic proteins (MIPs) facilitate the transport of water and neutral solutes across the lipid bilayers. Plant MIPs are believed to be important in cell division and expansion and in water transport properties in response to environmental conditions. More than 30 MIP sequences have been identified in Arabidopsis thaliana, maize and rice. Plasma membrane intrinsic proteins (PIPs), tonoplast intrinsic proteins (TIPs), Nod26-like intrinsic protein (NIPs) and small and basic intrinsic proteins (SIPs) are subfamilies of plant MIPs. Despite sequence diversity, all the experimentally determined structures belonging to the MIP superfamily have the same "hour-glass" fold.

Results: We have structurally characterized 39 rice and 31 maize MIPs and compared them with that of Arabidopsis. Homology models of 105 MIPs from all three plant species were built. Structure-based sequence alignments were generated and the residues in the helix-helix interfaces were analyzed. Small residues (Gly/Ala/Ser/Thr) are found to be highly conserved as a group in the helix-helix interface of MIP structures. Individual families sometimes prefer one or another of the residues from this group. The narrow aromatic/arginine (ar/R) selectivity filter in MIPs has been shown to provide an important constriction for solute permeability. Ar/R regions were analyzed and compared between the three plant species. Seventeen TIP, NIP and SIP members from rice and maize have ar/R signatures that are not found in Arabidopsis. A subgroup of rice and maize NIPs has small residues in three of the four positions in the ar/R tetrad, resulting in a wider constriction. These MIP members could transport larger solute molecules.

Conclusion: Small residues are group-conserved in the helix-helix interface of MIP structures and they seem to be important for close helix-helix interactions. Such conservation might help to preserve the hour-glass fold in MIP structures. Analysis and comparison of ar/R selectivity filters suggest that rice and maize MIPs could transport more diverse solutes than Arabidopsis MIPs. Thus the MIP members show conservation in helix-helix interfaces and diversity in aromatic/arginine selectivity filters. The former is related to structural stability and the later can be linked to functional diversity.

Figures

Figure 1
Figure 1
Superposition of aquaporin crystal structures. The transmembrane regions of six aquaporin crystal structures (bovine AQP1, E. coli AqpZ, sheep AQP0, spinach plasma membrane aquaporin SoPIP2;1, archaeal aquaporin AqpM from Methanothermobacter marburgensis and E. coli GlpF) are superposed. The corresponding PDB IDs are 1J4N, 1RC2 (B chain), 2B6O, 1Z98 (A chain), 2F2B and 1FX8 respectively. For clarity, Cα traces of only the six transmembrane helices and the loops B and E are shown: TM1 – blue, TM2 – green, loop B – pink, TM3 – orange, TM4 – red, loop E – purple, TM5 – cyan and TM6 – green. The residues forming the Ar/R selectivity filter from SoPIP2;1 are shown in white and the asparagines from the conserved NPA motif of loops B and E are shown in yellow. The aquaporin structures from bacteria, archaea, plant and mammals show a conserved "hour-glass" fold and the helices form a right-handed bundle structure.
Figure 2
Figure 2
Ar/R selectivity filters of SoPIP2;1 and GlpF. Ar/R selectivity filter of water-specific SoPIP2;1 (green) and glycerol specific GlpF (blue). Transmembrane regions of both structures were first superposed and only the residues forming the ar/R tetrad from the superposed structures are shown in ball-and-stick model. Residue names in one letter code are given for SoPIP2;1 in green and for GlpF in blue. The transmembrane segments and the loop regions to which these residues belong are indicated. The projection shown for each filter is viewed perpendicular to the membrane plane from the extracellular side.
Figure 3
Figure 3
Additional rice MIPs in the phyologenetic tree of all rice MIPs. Phylogenetic analysis of all 39 rice MIP sequences is shown. This tree was created using the Neighbor-Joining method and the multiple sequence alignment for this purpose was generated by the T-Coffee program [81]. As observed in Arabidopsis and maize, rice MIPs also can be classified into four subfamilies. OsPIPs, OsTIPs, OsNIPs and OsSIPs respectively indicate plasma membrane intrinsic proteins, tonoplast intrinsic proteins, Nod26-like intrinsic proteins and small basic intrinsic proteins from rice. Thirty three out of thirty nine sequences have been identified by Sakurai et al. [43]. The additional six sequences identified in this study are shown within gray boxes.
Figure 4
Figure 4
Small and polar residues at the helix-helix interfaces of SoPIP2;1. Small and polar residues occurring in helix-helix interfaces of spinach plant aquaporin SoPIP2;1 are displayed. The helix pairs TM1–TM3 (left), TM2–TM5 (middle) and TM4–TM6 (right) are shown. The backbone is drawn in ribbon representation and the interfacial residues are depicted as space-filling models. Residue numbers of interfacial residues correspond to the PDB structure 1Z98.
Figure 5
Figure 5
Ar/R selectivity filters of OsTIP4;2 and OsNIP2;1. Ar/R selectivity filter of water-specific OsTIP4;2 (red; left) and OsNIP2;1 (pink; right) homology models. Transmembrane regions of both the models were first superposed individually on glycerol transporter GlpF (blue) and only the residues forming the ar/R tetrad from the superposed structures are shown in ball-and-stick model. Residue names in one letter code are given for OsTIP4;2 in red, for OsNIP2;1 in pink and for GlpF in blue. The transmembrane segments and the loop regions to which these residues belong are indicated. The projection shown for each filter is viewed perpendicular to the membrane plane from the extracellular side.
Figure 6
Figure 6
Comparison of pore radius profiles. Pore diameter profiles of water-specific SoPIP2;1 (PDB ID: 1Z98), glycerol-specific GlpF (PDB ID: 1FX8), OsTIP4;2 and OsNIP2;1 calculated using HOLE [63]. The black arrow indicates the approximate location of ar/R constriction region. The position Z = 0 Å corresponds to the location of NPA region.
Figure 7
Figure 7
Comparison of X-ray and model structures of SoPIP2;1. Homology model generated for SoPIP2;1 is superposed on the experimentally determined structure of SoPIP2;1. Left: Only the transmembrane helical regions and the loops B and E are shown. Right: Residues forming the Ar/R selectivity filters of modeled and the X-ray structures are shown after superposition in ball-and-stick representation. The transmembrane segments and the loop regions to which these residues belong are indicated. There is an excellent agreement between the modeled and the X-ray structures in the transmembrane region.

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