Skip to main content
Log in

Genome-wide comparative analysis of tonoplast intrinsic protein (TIP) genes in plants

  • Review
  • Published:
Functional & Integrative Genomics Aims and scope Submit manuscript

Abstract

Tonoplast intrinsic proteins (TIPs) play a vital role in water transport across membranes. In the present study, we performed a comparative analysis of TIP genes in ten plant species including both monocots and dicots. A total of 100 TIP aquaporin genes were identified, and their relationships among the plant species were analyzed. Phylogenetic analysis was performed to evaluate the relationship of these genes within the plant species. Based on the phylogenetic analysis results, TIPs were classified into five distinct arbitrary groups (group I to group V), which represented TIP2, TIP5, TIP4, TIP1, and TIP3, respectively. Group I represented the largest arbitrary group, followed by group IV, in the phylogenetic tree. The result clearly indicates that TIP2 and TIP1 are abundant aquaporins and highly related among the species. In the present review, a comparative study of gene structure analysis between dicots and monocots has been performed to analyze their structural variation. Most of the predicted motifs are conserved among the species, signifying an evolutionary relationship. The gene expression analysis indicated that the expression of TIP genes varies during different developmental stages and also during stressed conditions. The results indicated a great degree of evolutionary relationship and variation in the expression levels of TIPs in plants.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

Abbreviations

APQ:

Aquaporin

TIPs:

Tonoplast intrinsic proteins

CDS:

Coding DNA sequence

NPA:

Asparagine-Proline-Alanine

References

  • Alexandersson E, Fraysse L, Sjovall-Larsen S, Gustavsson S, Fellert M, Karlsson M, Johanson U, Kjellbom P (2005) Whole gene family expression and drought stress regulation of aquaporins. Plant Mol Biol 59:469–484

    Article  CAS  PubMed  Google Scholar 

  • Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Bailey TL, Elkan C (1994) Fitting a mixture model by expectation maximization to discover motifs in biopolymers. Proceedings of the second international conference on 132 intelligent systems for molecular biology. AAAI Press, Menlo Park, pp 28–36

    Google Scholar 

  • Beebo A et al (2009) Life with and without AtTIP1;1, an Arabidopsis aquaporin preferentially localized in the apposing tonoplasts of adjacent vacuoles. Plant Mol Biol 70:193–209. doi:10.1007/s11103-009-9465-2

    Article  CAS  PubMed  Google Scholar 

  • Boursiac Y, Chen S, Luu DT, Sorieul M, van den Dries N, Maurel C (2005) Early effects of salinity on water transport in Arabidopsis roots. Molecular and cellular features of aquaporin expression. Plant Physiol 139:790–805

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Chaumont F, Barrieu F, Wojcik E, Chrispeels MJ, Jung R (2001) Aquaporins constitute a large and highly divergent protein family in maize. Plant Physiol 125:1206–1215

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Conesa A, Gotz S, Garcia-Gomez JM, Terol J, Talon M, Robles M (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21(18):3674–3676

    Article  CAS  PubMed  Google Scholar 

  • Danielson JAH, Johanson U (2008) Unexpected complexity of the aquaporin gene family in the moss Physcomitrella patens. BMC Plant Biol 8:45

    Article  PubMed Central  PubMed  Google Scholar 

  • Danielson JAH, Johanson U (2010) Phylogeny of major intrinsic proteins. Adv Exp Med Biol 679:19–31

    Article  CAS  PubMed  Google Scholar 

  • Forrest KL, Bhave M (2008) The PIP and TIP aquaporins in wheat form a large and diverse family with unique gene structures and functionally important features. Funct Integr Genom 8:115–133

    Article  CAS  Google Scholar 

  • Gattolin S, Sorieul M, Hunter PR, Khonsari RH, Frigerio L (2009) In vivo imaging of the tonoplast intrinsic protein family in Arabidopsis roots. BMC Plant Biol 9(1):133. doi:10.1186/1471-2229-9-133

    Article  PubMed Central  PubMed  Google Scholar 

  • Gattolin S, Sorieul M, Frigerio L (2011) Mapping of tonoplast intrinsic proteins in maturing and germinating Arabidopsis seeds reveals dual localization of embryonic TIPs to the tonoplast and plasma membrane. Mol Plant 4(1):180–189. doi:10.1093/mp/ssq051

    Article  CAS  PubMed  Google Scholar 

  • Gomes D, Agasse A, Thiébaud P, Delrot S, Delrot S, Chaumont F (2009) Aquaporins are multifunctional water and solute transporters highly divergent in living organisms. Biochim Biophys Acta 1788:1213–1228

    Article  CAS  PubMed  Google Scholar 

  • Goodstein DM et al (2012) Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res 40(D1):D1178–D1186. doi:10.1093/nar/gkr944

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Gustavsson S, Lebrun AS, Norden K, Chaumont F, Johanson U (2005) A novel plant major intrinsic protein in Physcomitrella patens most similar to bacterial glycerol channels. Plant Physiol 139:287–295

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Higuchi T, Suga S, Tsuchiya T, Hisada H, Morishima S, Okada Y, Maeshima M (1998) Molecular cloning, water channel activity and tissue specific expression of two isoforms of radish vacuolar aquaporin. Plant Cell Physiol 39:905–913

    Article  CAS  PubMed  Google Scholar 

  • Hruz T, Laule O, Szabo G, Wessendorp F, Bleuler S, Oertle L, Zimmermann P (2008) Genevestigator v3: a reference expression database for the meta-analysis of transcriptomes. Adv Bioinforma 2008:420747. doi:10.1155/2008/420747

    Article  Google Scholar 

  • Jami SK, Clark GB, Ayele BT, Ashe P, Kirti PB (2012) Genome-wide comparative analysis of annexin superfamily in plants. PLoS ONE 7:e47801

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Johanson U, Karlsson M, Johansson I, Gustavsson S, Sjovall S, Fraysse L, Weig AR, Kjellbom P (2001) 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 126:1358–1369

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Johnson KD, Hofte H, Chrispeels MJ (1990) An intrinsic tonoplast protein of protein storage vacuoles in seeds is structurally related to a bacterial solute transporter (GIpF). Plant Cell 2:525–532

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kaldenhoff R, Fischer M (2006) Functional aquaporin diversity in plants. Biochim Biophys Acta 1758(8):1134–1141. doi:10.1016/j.bbamem.2006.03.012

    Article  CAS  PubMed  Google Scholar 

  • Kruse E, Uehlein N, Kaldenhoff R (2006) The aquaporins. Genome Biol 7(2):206. doi:10.1186/gb-2006-7-2-206

    Article  PubMed Central  PubMed  Google Scholar 

  • Lamesch P et al (2012) The Arabidopsis Information Resource (TAIR): improved gene annotation and new tools. Nucleic Acids Res 40:D1202–D1210. doi:10.1093/nar/gkr1090

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948

    Article  CAS  PubMed  Google Scholar 

  • Ludevid D, Hofte H, Himelblau E, Chrispeels MJ (1992) The expression pattern of the tonoplast intrinsic protein gamma-TIP in Arabidopsis thaliana is correlated with cell enlargement. Plant Physiol 100:1633–1639

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Maeshima M (2001) Tonoplast transporters: organization and function. Annu Rev Plant Physiol Plant Mol Biol 52:469–497. doi:10.1146/annurev.arplant.52.1.469

    Article  CAS  PubMed  Google Scholar 

  • Maurel C, Tacnet F, Guclu J, Guern J, Ripoche P (1997) Purified vesicles of tobacco cell vacuolar and plasma membranes exhibit dramatically different water permeability and water channel activity. Proc Natl Acad Sci U S A 94:7103–7108

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Maurel C, Verdoucq L, Luu DT, Santoni V (2008) Plant aquaporins: membrane channels with multiple integrated functions. Annu Rev Plant Biol 59:595–624

    Article  CAS  PubMed  Google Scholar 

  • Pao GM, Wu LF, Johnson KD, Hofte H, Chrispeels MJ, Sweet G, Sandal NN, Saier MH Jr (1991) Evolution of the MIP family of integral membrane transport proteins. Mol Microbiol 5:33–37

    Article  CAS  PubMed  Google Scholar 

  • Proost S, Van Bel M, Sterck L, Billiau K, Van Parys T, Van de Peer Y, Vandepoele K (2009) PLAZA: a comparative genomics resource to study gene and genome evolution in plants. Plant Cell 21:3718–3731

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Quigley F, Rosenberg JM, Shachar-Hill Y, Bohnert HJ (2002) From genome to function: the Arabidopsis aquaporins. Genome Biol 3(1):RESEARCH0001

    PubMed Central  PubMed  Google Scholar 

  • Rambaut A (2012) FigTree v1.4. Institute of Evolutionary Biology, University of Edinburgh, Edinburgh

    Google Scholar 

  • Roy SW, Penny D (2007) Patterns of intron loss and gains in plants: intron loss-dominated evolution and genome-wide comparison of O. sativa and A. thaliana. Mol Biol Evol 24(1):171–181

    Article  CAS  PubMed  Google Scholar 

  • Schultz J et al (1998) SMART, a simple modular architecture research tool: identification of signaling domains. Proc Natl Acad Sci U S A 95:5857–5864

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Silvestro D, Michalak I (2011) raxmlGUI: a graphical front-end for RAxML. Org Divers Evol 12(4):335–337. doi:10.1007/s13127-011-0056-0

    Article  Google Scholar 

  • Ye CY, Yang X, Xia X, Yin W (2013) Comparative analysis of cation/proton antiporter superfamily in plants. Gene 521:245–251

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Preetom Regon.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Regon, P., Panda, P., Kshetrimayum, E. et al. Genome-wide comparative analysis of tonoplast intrinsic protein (TIP) genes in plants. Funct Integr Genomics 14, 617–629 (2014). https://doi.org/10.1007/s10142-014-0389-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10142-014-0389-9

Keywords

Navigation