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Algal MIPs, high diversity and conserved motifs.

Anderberg HI, Danielson JÅ, Johanson U - BMC Evol. Biol. (2011)

Bottom Line: Our results suggest that at least two of the seven subfamilies found in land plants were present already in an algal ancestor.The total variation of MIPs and the number of different subfamilies in chlorophyte algae is likely to be even higher than that found in land plants.Our analyses indicate that genetic exchanges between several of the algal subfamilies have occurred.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Biochemistry, Center for Molecular Protein Science, Center for Chemistry and Chemical Engineering, Lund University, PO Box 124, S-221 00 Lund, Sweden.

ABSTRACT

Background: Major intrinsic proteins (MIPs) also named aquaporins form channels facilitating the passive transport of water and other small polar molecules across membranes. MIPs are particularly abundant and diverse in terrestrial plants but little is known about their evolutionary history. In an attempt to investigate the origin of the plant MIP subfamilies, genomes of chlorophyte algae, the sister group of charophyte algae and land plants, were searched for MIP encoding genes.

Results: A total of 22 MIPs were identified in the nine analysed genomes and phylogenetic analyses classified them into seven subfamilies. Two of these, Plasma membrane Intrinsic Proteins (PIPs) and GlpF-like Intrinsic Proteins (GIPs), are also present in land plants and divergence dating support a common origin of these algal and land plant MIPs, predating the evolution of terrestrial plants. The subfamilies unique to algae were named MIPA to MIPE to facilitate the use of a common nomenclature for plant MIPs reflecting phylogenetically stable groups. All of the investigated genomes contained at least one MIP gene but only a few species encoded MIPs belonging to more than one subfamily.

Conclusions: Our results suggest that at least two of the seven subfamilies found in land plants were present already in an algal ancestor. The total variation of MIPs and the number of different subfamilies in chlorophyte algae is likely to be even higher than that found in land plants. Our analyses indicate that genetic exchanges between several of the algal subfamilies have occurred. The PIP1 and PIP2 groups and the Ca2+ gating appear to be specific to land plants whereas the pH gating is a more ancient characteristic shared by all PIPs. Further studies are needed to discern the function of the algal specific subfamilies MIPA-E and to fully understand the evolutionary relationship of algal and terrestrial plant MIPs.

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Structural alignment of internal symmetry. All MIPs consist of 6 transmembrane helices and two half helices, HB and HE, that together form a seventh transmembrane domain, as illustrated by the cartoon representation of the AQP4 structure to the left (PDB ID: 3GD8). Internal sequence similarities and the two-fold quasi symmetry suggest that MIPs have evolved through an internal duplication. Highlighted in green are the structural elements H3 and HB, whereas corresponding parts in the second repeat are coloured in magenta. The close up to the right depicts a structural alignment of these elements showing asparagine and proline of the NPA motif at the beginning of HB and HE as sticks. The side chain of the conserved glutamine in H3 is directed towards the nitrogen of the NPA proline in HB. In almost all MIPs the corresponding interaction in the second half of the protein is provided by a backbone oxygen in H6. This is possible due to a conserved proline hindering an α-helical H-bond within H6. Interestingly, the proline in H6 is not conserved in MIPDs which in general have glutamine or glutamate at this position, suggesting that these MIPs are more symmetrical. This structure might in fact resemble the ancestral form created by the internal duplication.
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Figure 6: Structural alignment of internal symmetry. All MIPs consist of 6 transmembrane helices and two half helices, HB and HE, that together form a seventh transmembrane domain, as illustrated by the cartoon representation of the AQP4 structure to the left (PDB ID: 3GD8). Internal sequence similarities and the two-fold quasi symmetry suggest that MIPs have evolved through an internal duplication. Highlighted in green are the structural elements H3 and HB, whereas corresponding parts in the second repeat are coloured in magenta. The close up to the right depicts a structural alignment of these elements showing asparagine and proline of the NPA motif at the beginning of HB and HE as sticks. The side chain of the conserved glutamine in H3 is directed towards the nitrogen of the NPA proline in HB. In almost all MIPs the corresponding interaction in the second half of the protein is provided by a backbone oxygen in H6. This is possible due to a conserved proline hindering an α-helical H-bond within H6. Interestingly, the proline in H6 is not conserved in MIPDs which in general have glutamine or glutamate at this position, suggesting that these MIPs are more symmetrical. This structure might in fact resemble the ancestral form created by the internal duplication.

Mentions: As previously mentioned all MIPs have an internal symmetry believed to derive from a duplication of an ancestral gene encoding only half of the present MIP sequence. According to this evolutionary hypothesis the first and second half of the protein were initially identical but have later diverged. Beside the NPA motifs there are symmetrically conserved residues in all corresponding transmembrane helices in the first and second half of the MIPs [35]. However, during evolution functional constraints have also selected and conserved residues that create some asymmetries in the protein. The ar/R filter is one such asymmetric feature that is now present in all MIPs. Another less studied feature is found in helices HB-H3 of the first repeat and the corresponding helices HE-H6 of the second repeat (Figure 6). In H6 there is a conserved proline preventing the formation of a hydrogen bond in the α-helix and resulting in a backbone carbonyl oxygen pointing towards the nitrogen of the proline in the NPA box. At the corresponding position in H3 there is a conserved glutamine that appears to occupy the same position as the backbone carbonyl group in H6. These features are conserved in MIP structures, but interestingly some algal MIPs display a subfamily specific variation at these two sites. MIPCs, but not SIPs or AQP11/12, have serine or threonine in H3 and alanine in H6, suggesting a different interaction in this part of the protein. Another variation is found in GIPs that have a glutamate or an asparagine in H3, conservative replacements that might not change the interactions in these areas much. However, in MIPDs the glutamine in H3 is conserved but the proline in H6 is substituted to glutamine, glutamate and in one case to histidine. This suggests that MIPDs are more symmetrical than other MIPs and thus in this regard, possibly more similar to an ancestral MIP. The fixation of the asymmetry in all other MIPs indicates a functional advantage, however the effect of this substitution is not clear and has not to our knowledge been addressed experimentally.


Algal MIPs, high diversity and conserved motifs.

Anderberg HI, Danielson JÅ, Johanson U - BMC Evol. Biol. (2011)

Structural alignment of internal symmetry. All MIPs consist of 6 transmembrane helices and two half helices, HB and HE, that together form a seventh transmembrane domain, as illustrated by the cartoon representation of the AQP4 structure to the left (PDB ID: 3GD8). Internal sequence similarities and the two-fold quasi symmetry suggest that MIPs have evolved through an internal duplication. Highlighted in green are the structural elements H3 and HB, whereas corresponding parts in the second repeat are coloured in magenta. The close up to the right depicts a structural alignment of these elements showing asparagine and proline of the NPA motif at the beginning of HB and HE as sticks. The side chain of the conserved glutamine in H3 is directed towards the nitrogen of the NPA proline in HB. In almost all MIPs the corresponding interaction in the second half of the protein is provided by a backbone oxygen in H6. This is possible due to a conserved proline hindering an α-helical H-bond within H6. Interestingly, the proline in H6 is not conserved in MIPDs which in general have glutamine or glutamate at this position, suggesting that these MIPs are more symmetrical. This structure might in fact resemble the ancestral form created by the internal duplication.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3111385&req=5

Figure 6: Structural alignment of internal symmetry. All MIPs consist of 6 transmembrane helices and two half helices, HB and HE, that together form a seventh transmembrane domain, as illustrated by the cartoon representation of the AQP4 structure to the left (PDB ID: 3GD8). Internal sequence similarities and the two-fold quasi symmetry suggest that MIPs have evolved through an internal duplication. Highlighted in green are the structural elements H3 and HB, whereas corresponding parts in the second repeat are coloured in magenta. The close up to the right depicts a structural alignment of these elements showing asparagine and proline of the NPA motif at the beginning of HB and HE as sticks. The side chain of the conserved glutamine in H3 is directed towards the nitrogen of the NPA proline in HB. In almost all MIPs the corresponding interaction in the second half of the protein is provided by a backbone oxygen in H6. This is possible due to a conserved proline hindering an α-helical H-bond within H6. Interestingly, the proline in H6 is not conserved in MIPDs which in general have glutamine or glutamate at this position, suggesting that these MIPs are more symmetrical. This structure might in fact resemble the ancestral form created by the internal duplication.
Mentions: As previously mentioned all MIPs have an internal symmetry believed to derive from a duplication of an ancestral gene encoding only half of the present MIP sequence. According to this evolutionary hypothesis the first and second half of the protein were initially identical but have later diverged. Beside the NPA motifs there are symmetrically conserved residues in all corresponding transmembrane helices in the first and second half of the MIPs [35]. However, during evolution functional constraints have also selected and conserved residues that create some asymmetries in the protein. The ar/R filter is one such asymmetric feature that is now present in all MIPs. Another less studied feature is found in helices HB-H3 of the first repeat and the corresponding helices HE-H6 of the second repeat (Figure 6). In H6 there is a conserved proline preventing the formation of a hydrogen bond in the α-helix and resulting in a backbone carbonyl oxygen pointing towards the nitrogen of the proline in the NPA box. At the corresponding position in H3 there is a conserved glutamine that appears to occupy the same position as the backbone carbonyl group in H6. These features are conserved in MIP structures, but interestingly some algal MIPs display a subfamily specific variation at these two sites. MIPCs, but not SIPs or AQP11/12, have serine or threonine in H3 and alanine in H6, suggesting a different interaction in this part of the protein. Another variation is found in GIPs that have a glutamate or an asparagine in H3, conservative replacements that might not change the interactions in these areas much. However, in MIPDs the glutamine in H3 is conserved but the proline in H6 is substituted to glutamine, glutamate and in one case to histidine. This suggests that MIPDs are more symmetrical than other MIPs and thus in this regard, possibly more similar to an ancestral MIP. The fixation of the asymmetry in all other MIPs indicates a functional advantage, however the effect of this substitution is not clear and has not to our knowledge been addressed experimentally.

Bottom Line: Our results suggest that at least two of the seven subfamilies found in land plants were present already in an algal ancestor.The total variation of MIPs and the number of different subfamilies in chlorophyte algae is likely to be even higher than that found in land plants.Our analyses indicate that genetic exchanges between several of the algal subfamilies have occurred.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Biochemistry, Center for Molecular Protein Science, Center for Chemistry and Chemical Engineering, Lund University, PO Box 124, S-221 00 Lund, Sweden.

ABSTRACT

Background: Major intrinsic proteins (MIPs) also named aquaporins form channels facilitating the passive transport of water and other small polar molecules across membranes. MIPs are particularly abundant and diverse in terrestrial plants but little is known about their evolutionary history. In an attempt to investigate the origin of the plant MIP subfamilies, genomes of chlorophyte algae, the sister group of charophyte algae and land plants, were searched for MIP encoding genes.

Results: A total of 22 MIPs were identified in the nine analysed genomes and phylogenetic analyses classified them into seven subfamilies. Two of these, Plasma membrane Intrinsic Proteins (PIPs) and GlpF-like Intrinsic Proteins (GIPs), are also present in land plants and divergence dating support a common origin of these algal and land plant MIPs, predating the evolution of terrestrial plants. The subfamilies unique to algae were named MIPA to MIPE to facilitate the use of a common nomenclature for plant MIPs reflecting phylogenetically stable groups. All of the investigated genomes contained at least one MIP gene but only a few species encoded MIPs belonging to more than one subfamily.

Conclusions: Our results suggest that at least two of the seven subfamilies found in land plants were present already in an algal ancestor. The total variation of MIPs and the number of different subfamilies in chlorophyte algae is likely to be even higher than that found in land plants. Our analyses indicate that genetic exchanges between several of the algal subfamilies have occurred. The PIP1 and PIP2 groups and the Ca2+ gating appear to be specific to land plants whereas the pH gating is a more ancient characteristic shared by all PIPs. Further studies are needed to discern the function of the algal specific subfamilies MIPA-E and to fully understand the evolutionary relationship of algal and terrestrial plant MIPs.

Show MeSH
Related in: MedlinePlus