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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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Overview of identified MIP subfamilies in green plants. A schematic tree showing the evolutionary relationship between green plant lineages is combined with a table summarizing the distribution of plant MIP subfamilies. MIPA-E constitutes novel subfamilies identified in this study. The PIP and the GIP subfamilies appear to have evolved before the split of the chlorophyte and the streptophyte lineages. For all plants except S. lycopersicum and P. incise the number of MIPs is derived from annotations of whole genomes [9,55,56]. a) The occurrence of MIPs in S. lycopersicum is based on an extensive analysis of ESTs [57].
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Figure 7: Overview of identified MIP subfamilies in green plants. A schematic tree showing the evolutionary relationship between green plant lineages is combined with a table summarizing the distribution of plant MIP subfamilies. MIPA-E constitutes novel subfamilies identified in this study. The PIP and the GIP subfamilies appear to have evolved before the split of the chlorophyte and the streptophyte lineages. For all plants except S. lycopersicum and P. incise the number of MIPs is derived from annotations of whole genomes [9,55,56]. a) The occurrence of MIPs in S. lycopersicum is based on an extensive analysis of ESTs [57].

Mentions: The distribution of all the MIP subfamilies in different phylogenetic groups of plants is summarized in Figure 7. Compared to terrestrial plants, chlorophyte algal species in general have fewer subfamilies. Based on this limited dataset trebouxiophyceae have the highest number of subfamilies (3-4), followed by mamiellophyceae (1-2) whereas chlorophyceae only have a single subfamily. Still the diversity of MIPs in chlorophytes at large appears to be higher than that of land plants, resulting in a large number of subfamilies with an interspersed species distribution. A similarly complex picture was seen in a study of the ammonium transporters (AMT) presenting several chlorophyte specific subfamilies [36]. The reason for the variation is not clear but it is possible that a more careful comparison of lifestyle or habitat will reveal a logical pattern that can provide clues to the MIPs physiological function. Interestingly, trebouxiophyceae algae are not only found as free living organisms in aquatic habitats but also as symbionts in protozoa and lichen, and as a part of aeroterrestrial biofilms [37]. More specifically, some Coccomyxa species are free living terrestrial algae [38], whereas Chlorella NC64A is an endosymbiont of the ciliate Paramecium bursaria [39]. We speculate that the large number of MIP subfamilies found in members of trebouxiophyceae is part of an adaptation to these particular lifestyles. For an endosymbiont it is easy to envision that a facilitated exchange of solutes with the host would be beneficial, whereas the solute concentrations possible in terrestrial environments might favour a passive mode of uptake in free living non-aquatic plants.


Algal MIPs, high diversity and conserved motifs.

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

Overview of identified MIP subfamilies in green plants. A schematic tree showing the evolutionary relationship between green plant lineages is combined with a table summarizing the distribution of plant MIP subfamilies. MIPA-E constitutes novel subfamilies identified in this study. The PIP and the GIP subfamilies appear to have evolved before the split of the chlorophyte and the streptophyte lineages. For all plants except S. lycopersicum and P. incise the number of MIPs is derived from annotations of whole genomes [9,55,56]. a) The occurrence of MIPs in S. lycopersicum is based on an extensive analysis of ESTs [57].
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 7: Overview of identified MIP subfamilies in green plants. A schematic tree showing the evolutionary relationship between green plant lineages is combined with a table summarizing the distribution of plant MIP subfamilies. MIPA-E constitutes novel subfamilies identified in this study. The PIP and the GIP subfamilies appear to have evolved before the split of the chlorophyte and the streptophyte lineages. For all plants except S. lycopersicum and P. incise the number of MIPs is derived from annotations of whole genomes [9,55,56]. a) The occurrence of MIPs in S. lycopersicum is based on an extensive analysis of ESTs [57].
Mentions: The distribution of all the MIP subfamilies in different phylogenetic groups of plants is summarized in Figure 7. Compared to terrestrial plants, chlorophyte algal species in general have fewer subfamilies. Based on this limited dataset trebouxiophyceae have the highest number of subfamilies (3-4), followed by mamiellophyceae (1-2) whereas chlorophyceae only have a single subfamily. Still the diversity of MIPs in chlorophytes at large appears to be higher than that of land plants, resulting in a large number of subfamilies with an interspersed species distribution. A similarly complex picture was seen in a study of the ammonium transporters (AMT) presenting several chlorophyte specific subfamilies [36]. The reason for the variation is not clear but it is possible that a more careful comparison of lifestyle or habitat will reveal a logical pattern that can provide clues to the MIPs physiological function. Interestingly, trebouxiophyceae algae are not only found as free living organisms in aquatic habitats but also as symbionts in protozoa and lichen, and as a part of aeroterrestrial biofilms [37]. More specifically, some Coccomyxa species are free living terrestrial algae [38], whereas Chlorella NC64A is an endosymbiont of the ciliate Paramecium bursaria [39]. We speculate that the large number of MIP subfamilies found in members of trebouxiophyceae is part of an adaptation to these particular lifestyles. For an endosymbiont it is easy to envision that a facilitated exchange of solutes with the host would be beneficial, whereas the solute concentrations possible in terrestrial environments might favour a passive mode of uptake in free living non-aquatic plants.

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