Phylogeny of Major Intrinsic Proteins

Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 679)


Major intrinsic proteins (MIPs) form a large superfamily of proteins that can be divided into different subfamilies and groups according to phylogenetic analyses. Plants encode more MIPs than other organisms and seven subfamilies have been defined, whereof the Nodulin26-like major intrinsic proteins (NIPs) have been shown to permeate metalloids. In this chapter we review the phylogeny of MIPs in general and especially of the plant MIPs. We also identify bacterial NIP-like MIPs and discuss the evolutionary implications of this finding regarding the origin and ancestral transport specificity of the NIPs.


Horizontal Gene Transfer Intrinsic Protein Major Intrinsic Protein Peribacteroid Membrane Membrane Channel Protein 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 1.
    Gorin MB, Yancey SB, Cline J et al. The major intrinsic protein (MIP) of the bovine lens fiber membrane: Characterization and structure based on cDNA cloning. Cell 1984; 39:49–59.CrossRefPubMedGoogle Scholar
  2. 2.
    Fortin MG, Morrison NA, Verma DP. Nodulin-26, a peribacteroid membrane nodulin is expressed independently of the development of the peribacteroid compartment. Nucleic Acids Res 1987; 15:813–824.CrossRefPubMedGoogle Scholar
  3. 3.
    Shiels A, Kent NA, McHale M et al. Homology of MIP26 to NOD26. Nucleic Acids Res 1988; 16:9348.CrossRefPubMedGoogle Scholar
  4. 4.
    Sandal NN, Marcker KA. Soybean nodulin 26 is homologous to the major intrinsic protein of the bovine lens fiber membrane. Nucleic Acids Res 1988; 16:9347.CrossRefPubMedGoogle Scholar
  5. 5.
    Muramatsu S, Mizuno T. Nucleotide sequence of the region encompassing the GlpKF operon and its upstream region containing a bent DNA sequence of Escherichia coli. Nucleic Acids Res 1989; 17:4378.CrossRefPubMedGoogle Scholar
  6. 6.
    Baker ME, Saier MH Jr. A common ancestor for bovine lens fiber major intrinsic protein, soybean nodulin-26 protein and E. coli glycerol facilitator. Cell 1990; 60:185–186.CrossRefPubMedGoogle Scholar
  7. 7.
    Rao Y, Jan LY, Jan YN. Similarity of the product of the Drosophila neurogenic gene big brain to transmembrane channel proteins. Nature 1990; 345:163–167.CrossRefPubMedGoogle Scholar
  8. 8.
    Johnson KD, Hofte H, Chrispeels MJ. An intrinsic tonoplast protein of protein storage vacuoles in seeds is structurally related to a bacterial solute transporter (GIpF). Plant Cell 1990; 2:525–532.CrossRefPubMedGoogle Scholar
  9. 9.
    Yamamoto YT, Cheng CL, Conkling MA. Root-specific genes from tobacco and Arabidopsis homologous to an evolutionarily conserved gene family of membrane channel proteins. Nucleic Acids Res 1990; 18:7449.CrossRefPubMedGoogle Scholar
  10. 10.
    Pao GM, Wu LF, Johnson KD et al. Evolution of the MIP family of integral membrane transport proteins. Mol Microbiol 1991; 5:33–37.CrossRefPubMedGoogle Scholar
  11. 11.
    Preston GM, Agre P. Isolation of the cDNA for erythrocyte integral membrane protein of 28 kilodaltons: Member of an ancient channel family. Proc Natl Acad Sci USA 1991; 88:11110–11114.CrossRefPubMedGoogle Scholar
  12. 12.
    Reizer J, Reizer A, Saier MH Jr. The MIP family of integral membrane channel proteins: Sequence comparisons, evolutionary relationships, reconstructed pathway of evolution and proposed functional differentiation of the two repeated halves of the proteins. Crit Rev Biochem Mol Biol 1993; 28:235–257.CrossRefPubMedGoogle Scholar
  13. 13.
    Park JH, Saier MH Jr. Phylogenetic characterization of the MIP family of transmembrane channel proteins. J Membr Biol 1996; 153:171–180.CrossRefPubMedGoogle Scholar
  14. 14.
    Froger A, Tallur B, Thomas D et al. Prediction of functional residues in water channels and related proteins. Protein Sci 1998; 7:1458–1468.CrossRefPubMedGoogle Scholar
  15. 15.
    Heymann JB, Engel A. Aquaporins: Phylogeny, structure and physiology of water channels. News Physiol Sci 1999; 14:187–193.PubMedGoogle Scholar
  16. 16.
    Zardoya R, Villalba S. A phylogenetic framework for the aquaporin family in eukaryotes. J Mol Evol 2001; 52:391–404.PubMedGoogle Scholar
  17. 17.
    Zardoya R. Phylogeny and evolution of the major intrinsic protein family. Biol Cell 2005; 97:397–414.CrossRefPubMedGoogle Scholar
  18. 18.
    Zardoya R, Ding X, Kitagawa Y et al. Origin of plant glycerol transporters by horizontal gene transfer and functional recruitment. Proc Natl Acad Sci USA 2002; 99:14893–14896.CrossRefPubMedGoogle Scholar
  19. 19.
    Johanson U, Karlsson M, Johansson I et al. The complete set of genes encoding major intrinsic proteins in Arabidopsis provides a framework for a new nomenclature for major intrinsic proteins in plants. Plant Physiol 2001; 126:1358–1369.CrossRefPubMedGoogle Scholar
  20. 20.
    Danielson JÅ, Johanson U. Unexpected complexity of the aquaporin gene family in the moss Physcomitrella patens. BMC Plant Biol 2008; 8:45.CrossRefPubMedGoogle Scholar
  21. 21.
    Gustavsson S, Lebrun AS, Norden K et al. A novel plant major intrinsic protein in Physcomitrella patens most similar to bacterial glycerol channels. Plant Physiol 2005; 139:287–295.CrossRefPubMedGoogle Scholar
  22. 22.
    Höfte H, Hubbard L, Reizer J et al. Vegetative and seed-specific forms of tonoplast intrinsic protein in the vacuolar membrane of Arabidopsis thaliana. Plant Physiol 1992; 99:561–570.CrossRefPubMedGoogle Scholar
  23. 23.
    Kaldenhoff R, Kolling A, Richter G. A novel blue light-and abscisic acid-inducible gene of Arabidopsis thaliana encoding an intrinsic membrane protein. Plant Mol Biol 1993; 23:1187–1198.CrossRefPubMedGoogle Scholar
  24. 24.
    Kammerloher W, Fischer U, Piechottka GP et al. Water channels in the plant plasma membrane cloned by immunoselection from a mammalian expression system. Plant J 1994; 6:187–199.CrossRefPubMedGoogle Scholar
  25. 25.
    Yamaguchi-Shinozaki K, Koizumi M, Urao S et al. Molecular cloning and characterization of 9 cDNAs for genes that are responsive to desiccation in Arabidopsis thaliana: Sequence analysis of one cDNA clone that encodes a putative transmembrane channel protein. Plant Cell Physiol 1992; 33:217–224.Google Scholar
  26. 26.
    Weig A, Deswarte C, Chrispeels MJ. The major intrinsic protein family of Arabidopsis has 23 members that form three distinct groups with functional aquaporins in each group. Plant Physiol 1997; 114:1347–1357.CrossRefPubMedGoogle Scholar
  27. 27.
    Karlsson M, Johansson I, Bush M et al. An abundant TIP expressed in mature highly vacuolated cells. Plant J 2000; 21:83–90.CrossRefPubMedGoogle Scholar
  28. 28.
    Johansson I, Karlsson M, Johanson U et al. The role of aquaporins in cellular and whole plant water balance. Biochim Biophys Acta 2000; 1465:324–342.CrossRefPubMedGoogle Scholar
  29. 29.
    Chaumont F, Barrieu F, Wojcik E et al. Aquaporins constitute a large and highly divergent protein family in maize. Plant Physiol 2001; 125:1206–1215.CrossRefPubMedGoogle Scholar
  30. 30.
    Quigley F, Rosenberg JM, Shachar-Hill Y et al. From genome to function: The Arabidopsis aquaporins. Genome Biol 2001; 3:RESEARCH0001.Google Scholar
  31. 31.
    Johanson U, Gustavsson S. A new subfamily of major intrinsic proteins in plants. Mol Biol Evol 2002; 19:456–461.PubMedGoogle Scholar
  32. 32.
    Borstlap AC. Early diversification of plant aquaporins. Trends Plant Sci 2002; 7:529–530.CrossRefPubMedGoogle Scholar
  33. 33.
    Sakurai J, Ishikawa F, Yamaguchi T et al. Identification of 33 rice aquaporin genes and analysis of their expression and function. Plant Cell Physiol 2005; 46:1568–1577.CrossRefPubMedGoogle Scholar
  34. 34.
    Bansal A, Sankararamakrishnan R. Homology modeling of major intrinsic proteins in rice, maize and Arabidopsis: Comparative analysis of transmembrane helix association and aromatic/arginine selectivity filters. BMC Struct Biol 2007; 7:27.CrossRefPubMedGoogle Scholar
  35. 35.
    Forrest KL, Bhave M. The PIP and TIP aquaporins in wheat form a large and diverse family with unique gene structures and functionally important features. Funct Integr Genomics 2008; 8:115–133.CrossRefPubMedGoogle Scholar
  36. 36.
    Bienert GP, Thorsen M, Schüssler MD et al. A subgroup of plant aquaporins facilitate the bi-directional diffusion of As(OH)3 and Sb(OH)3 across membranes. BMC Biol 2008; 6:26.CrossRefPubMedGoogle Scholar
  37. 37.
    Wallace IS, Roberts DM. Homology modeling of representative subfamilies of Arabidopsis major intrinsic proteins. Classification based on the aromatic/arginine selectivity filter. Plant Physiol 2004; 135:1059–1068.CrossRefPubMedGoogle Scholar
  38. 38.
    Wallace IS, Wills DM, Guenther JF et al. Functional selectivity for glycerol of the nodulin 26 subfamily of plant membrane intrinsic proteins. FEBS Lett 2002; 523:109–112.CrossRefPubMedGoogle Scholar
  39. 39.
    Wallace IS, Roberts DM. Distinct transport selectivity of two structural subclasses of the nodulin-like intrinsic protein family of plant aquaglyceroporin channels. Biochemistry 2005; 44:16826–16834.CrossRefPubMedGoogle Scholar
  40. 40.
    Ma JF, Tamai K, Yamaji N et al. A silicon transporter in rice. Nature 2006; 440:688–691.CrossRefPubMedGoogle Scholar
  41. 41.
    Mitani N, Yamaji N, Ma JF. Identification of maize silicon influx transporters. Plant Cell Physiol 2009; 50:5–12.CrossRefPubMedGoogle Scholar
  42. 42.
    Chiba Y, Mitani N, Yamaji N et al. HvLsi1 is a silicon influx transporter in barley. Plant J 2009; 57:810–818.CrossRefPubMedGoogle Scholar
  43. 43.
    Wallace IS, Choi WG, Roberts DM. The structure, function and regulation of the nodulin 26-like intrinsic protein family of plant aquaglyceroporins. Biochim Biophys Acta 2006; 1758:1165–1175.CrossRefPubMedGoogle Scholar
  44. 44.
    Mitani N, Yamaji N, Ma JF. Characterization of substrate specificity of a rice silicon transporter, Lsi1. Pflugers Arch 2008; 456:679–686.CrossRefPubMedGoogle Scholar
  45. 45.
    Rouge P, Barre A. A molecular modeling approach defines a new group of nodulin 26-like aquaporins in plants. Biochem Biophys Res Commun 2008; 367:60–66.CrossRefPubMedGoogle Scholar
  46. 46.
    Ali W, Isayenkov SV, Zhao FJ et al. Arsenite transport in plants. Cell Mol Life Sci 2009; 66:2329–2339.CrossRefPubMedGoogle Scholar
  47. 47.
    Kamiya T, Tanaka M, Mitani N et al. NIP1;1, an aquaporin homolog, determines the arsenite sensitivity of Arabidopsis thaliana. J Biol Chem 2009; 284:2114–2120.CrossRefPubMedGoogle Scholar
  48. 48.
    Takano J, Wada M, Ludewig U et al. The Arabidopsis major intrinsic protein NIP5;1 is essential for efficient boron uptake and plant development under boron limitation. Plant Cell 2006; 18:1498–1509.CrossRefPubMedGoogle Scholar
  49. 49.
    Isayenkov SV, Maathuis FJ. The Arabidopsis thaliana aquaglyceroporin AtNIP7;1 is a pathway for arsenite uptake. FEBS Lett 2008; 582:1625–1628.CrossRefPubMedGoogle Scholar
  50. 50.
    Ma JF, Yamaji N, Mitani N et al. Transporters of arsenite in rice and their role in arsenic accumulation in rice grain. Proc Natl Acad Sci USA 2008; 105:9931–9935.CrossRefPubMedGoogle Scholar
  51. 51.
    Tanaka M, Wallace IS, Takano J et al. NIP6;1 is a boric acid channel for preferential transport of boron to growing shoot tissues in Arabidopsis. Plant Cell 2008; 20:2860–2875.CrossRefPubMedGoogle Scholar
  52. 52.
    Bienert GP, Schüssler MD, Jahn TP. Metalloids: Essential, beneficial or toxic? Major intrinsic proteins sort it out. Trends Biochem Sci 2008; 33:20–26.CrossRefPubMedGoogle Scholar
  53. 53.
    Matsunaga T, Ishii T, Matsumoto S et al. Occurrence of the primary cell wall polysaccharide rhamnogalacturonan II in pteridophytes, lycophytes and bryophytes. Implications for the evolution of vascular plants. Plant Physiol 2004; 134:339–351.CrossRefPubMedGoogle Scholar
  54. 54.
    Liu Q, Wang H, Zhang Z et al. Divergence in function and expression of the NOD26-like intrinsic proteins in plants. BMC Genomics 2009; 10:313.CrossRefPubMedGoogle Scholar

Copyright information

© Landes Bioscience and Springer Science+Business Media 2010

Authors and Affiliations

  1. 1.Department of Biochemistry, Molecular Protein Science Centre, Centre for Chemistry and Chemical EngineeringLund UniversityLundSweden

Personalised recommendations