Origin of plant glycerol transporters by horizontal gene transfer and functional recruitment.
Gene-family evolution mostly relies on gene duplication coupled with functional diversification of gene products. However, other evolutionary mechanisms may also be important in generating protein diversity. The ubiquitous membrane intrinsic protein (MIP) gene family is an excellent model system to search for such alternative evolutionary mechanisms. MIPs are proteins that transport water, glycerol, and small solutes across cell membranes in all living organisms. We reconstructed the molecular phylogeny of MIPs based on amino acid sequence data by using neighbor-joining, maximum-likelihood, and Bayesian methods of phylogenetic inference. The recovered trees show an early and distinct separation of water and glycerol transporters, i.e., aquaporins (AQPs), and aquaglyceroporins. The latter are absent from plants. As expected, gene duplication and functional diversification account for most of the diversity of animal and plant members of the family. However, in contrast to this model, we find that the sister group of plant glycerol transporters are bacterial AQPs. This relationship suggests first that plant glycerol transporters may resulted from a single event of horizontal gene transfer from bacteria, which we have estimated to have occurred approximately 1,200 million years ago, at the origin of plants, and second that bacterial AQPs were likely recruited to transport glycerol in plants because of their absence of aquaglyceroporins. This striking example of adaptive evolution at the molecular level was demonstrated further by finding convergent or parallel replacements at particular amino acid positions related to water- and glycerol-transporting specificity.
Zardoya
Rafael
R
Departamento de Biodiversidad y Biologia Evolutiva, Museo Nacional de Ciencias Naturales, José Gutierrez Abascal 2, 28006 Madrid, Spain. rafaz@mncn.csic.es
Ding
Xiaodong
X
Kitagawa
Yoshichika
Y
Chrispeels
Maarten J
MJ
D000595:Amino Acid Sequence; D002352:Carrier Proteins / Q000235:genetics*; D016384:Consensus Sequence; D017124:Conserved Sequence; D019143:Evolution, Molecular; D018014:Gene Transfer Techniques; D005990:Glycerol / Q000378:metabolism*; D008969:Molecular Sequence Data; D010802:Phylogeny; D010944:Plants / Q000145:classification / Q000235:genetics / Q000378:metabolism*; D016415:Sequence Alignment; D017386:Sequence Homology, Amino Acid
D002352:Carrier Proteins; D005990:Glycerol