SpringerLink
Log in

Expressions of three cotton genes encoding the PIP proteins are regulated in root development and in response to stresses

  • Biotic and Abiotic Stress
  • Published:
Plant Cell Reports Aims and scope Submit manuscript

Abstract

Cotton (Gossypium hirsutum), the most important textile crop worldwide, often encounters water stress such as drought or waterlog during its growth season (Summer). To investigate molecular mechanism of water regulation in cotton plants, three cDNAs encoding the plasma membrane intrinsic protein (PIP) were isolated from cotton root cDNA library, and designated GhPIP1;1, GhPIP2;1 and GhPIP2;2, respectively. All of the three PIP proteins displayed water channel activity in Xenopus laevis oocytes. GhPIP2;1 and GhPIP2;2 proteins, however, showed much higher water transport activity than that of the GhPIP1;1 protein. Northern blot analysis revealed that all of the three genes were preferentially expressed in young roots. Further analysis by Real-time quantitative RT-PCR revealed that the transcripts of all the three genes were accumulated at high levels in 3-day-old young roots, but dramatically declined to much lower levels in 6–14 days old roots during seedling development, suggesting that expressions of the isolated GhPIP genes are developmentally regulated in roots. Additionally, expressions of the three genes were remarkably up-regulated or down-regulated under different stresses such as NaCl, cold, PEG (polyethylene glycol) treatments. Collectively, the results suggest that these genes may be involved in root development and in response to stresses.

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (Brazil)

Instant access to the full article PDF.

Institutional subscriptions

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

Similar content being viewed by others

References

  • Aharon R, Shahak Y, Wininger S, Bendov R, Kapulnik Y, Galili G (2003) Overexpression of a plasma membrane aquaporin in transgenic tobacco improves plant vigor under favorable growth conditions but not under drought or salt stress. Plant Cell 15:439–447. doi:10.1105/tpc.009225

    Article  PubMed  CAS  Google Scholar 

  • 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. doi:10.1007/s11103-005-0352-1

    Article  PubMed  CAS  Google Scholar 

  • Bienert GP, Moller AL, Kristiansen KA, Schulz A, Moller IM, Schjoerring JK, Jahn TP (2007) Specific aquaporins facilitate the diffusion of hydrogen peroxide across membranes. J Biol Chem 282:1183–1192. doi:10.1074/jbc.M603761200

    Article  PubMed  CAS  Google Scholar 

  • Bots M, Feron R, Uehlein N, Weterings K, Kaldenhoff R, Mariani T (2005) PIP1 and PIP2 aquaporins are differentially expressed during tobacco anther and stigma development. J Exp Bot 56:113–121. doi:10.1093/jxb/eri009

    PubMed  CAS  Google Scholar 

  • Chaumont F, Barrieu F, Jung R, Chrispeels MJ (2000) Plasma membrane intrinsic proteins from maize cluster in two sequence subgroups with differential aquaporin activity. Plant Physiol 122:1025–1034

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Chaumont F, Moshelion M, Daniels MJ (2005) Regulation of plant aquaporin activity. Bio Cell 97:749–764

    Article  CAS  Google Scholar 

  • Ciavatta VT, Morillon R, Pullman GS, Chrispeels MJ, Cairney J (2001) An aquaglyceroporin is abundantly expressed early in the development of the suspensor and the embryo proper of loblolly pine. Plant Physiol 127:1556–1567

    Article  PubMed  CAS  Google Scholar 

  • Dordas C, Chrispeels MJ, Brown PH (2000) Permeability and channel-mediated transport of boric acid across membrane vesicles isolated from squash roots. Plant Physiol 124:1349–1362

    Article  PubMed  CAS  Google Scholar 

  • Fetter K, Van Wilder V, Moshelion M, Chaumont F (2004) Interactions between plasma membrane aquaporins modulate their water channel activity. Plant Cell 16:215–228. doi:10.1105/tpc.017194

    Article  PubMed  CAS  Google Scholar 

  • Gerbeau P, Guclu J, Ripoche P, Maurel C (1999) Aquaporin Nt-TIPa can account for the high permeability of tobacco cell vacuolar membrane to small neutral solutes. Plant J 18:577–587. doi:10.1046/j.1365-313x.1999.00481.x

    Article  PubMed  CAS  Google Scholar 

  • Guenther JF, Roberts DM (2000) Water-selective and multifunctional aquaporins from Lotus japonicus nodules. Planta 210:741–748. doi:10.1007/s004250050675

    Article  PubMed  CAS  Google Scholar 

  • Hachez C, Moshelion M, Zelazny E, Cavez D, Chaumont F (2006) Localization and quantification of plasma membrane aquaporin expression in maize primary root: a clue to understanding their role as cellular plumbers. Plant Mol Biol 62:305–323. doi:10.1007/s11103-006-9022-1

    Article  PubMed  CAS  Google Scholar 

  • Henzler T, Steudle E (2000) Transport and metabolic degradation of hydrogen peroxide in Chara corallina: model calculations and measurements with the pressure probe suggest transport of H2O2 across water channels. J Exp Bot 51:2053–2066

    Article  PubMed  CAS  Google Scholar 

  • Ishikawa F, Suga S, Uemura T, Sato MH, Maeshima M (2005) Novel type aquaporin SIPs are mainly localized to the ER membrane and show cell-specific expression in Arabidopsis thaliana. FEBS Lett 579:5814–5820. doi:10.1016/j.febslet.2005.09.076

    PubMed  CAS  Google Scholar 

  • Jahn TP, Moller AL, Zeuthen T, Holm LM, Klaerke DA, Mohsin B, Kuhlbrandt W, Schjoerring JK (2004) Aquaporin homologues in plants and mammals transport ammonia. FEBS Lett 574:31–36. doi:10.1016/j.febslet.2004.08.004

    Article  PubMed  CAS  Google Scholar 

  • Jang JY, Kim DG, Kim YO, Kim JS, Kang H (2004) An expression analysis of a gene family encoding plasma membrane aquaporins in response to abiotic stresses in Arabidopsis thaliana. Plant Mol Biol 54:713–725. doi:10.1023/B:PLAN.0000040900.61345.a6

    Article  PubMed  CAS  Google Scholar 

  • Javot H, Maurel C (2002) The role of aquaporins in root water uptake. Ann Bot 90:301–303. doi:10.1093/aob/mcf199

    Article  PubMed  CAS  Google Scholar 

  • Javot H, Lauvergeat V, Santoni V, Martin-Laurent F, Guclu J, Vinh J, Heyes J, Franck KI, Schaffner AR, Bouchez D, Maurel C (2003) Role of a single aquaporin isoform in root water uptake. Plant Cell 15:509–522. doi:10.1105/tpc.008888

    Article  PubMed  CAS  Google Scholar 

  • Johansson I, Karlsson M, Shukla VK, Chrispeels MJ, Larsson C, Kjellbom P (1998) Water transport activity of the plasma membrane aquaporin PM28A is regulated by phosphorylation. Plant cell 10:451–459

    Article  PubMed  CAS  Google Scholar 

  • Johansson I, Karlsson M, Johanson U, Larsson C, Kjellbom P (2000) The role of aquaporins in cellular and whole plant water balance. Biochim Biophys Acta 1465:324–342. doi:10.1016/S0005-2736(00)00147-4

    Article  PubMed  CAS  Google Scholar 

  • Johanson U, Gustavsson S (2002) A new subfamily of major intrinsic proteins in plants. Mol Biol Evol 19:456–461

    PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Li DD, Huang GQ, Tan X, Wang J, Wang XL, Xu WL, Wu YJ, Wang H, Li XB (2006) Cloning of GhAQP1 gene and its specific expression during ovule development in cotton. Plant Physiol Mol Bio 32:543–550 in Chinese

    CAS  Google Scholar 

  • Li XB, Cai L, Cheng NH, Liu JW (2002) Molecular characterization of the cotton GhTUB1 gene that is preferentially expressed in fiber. Plant Physiol 130:666–674

    Article  PubMed  CAS  Google Scholar 

  • Li XB, Fan XP, Wang XL, Cai L, Yang WC (2005) The cotton ACTIN1 gene is functionally expressed in fibers and participates in fiber elongation. Plant Cell 17:859–875. doi:10.1105/tpc.104.029629

    Article  PubMed  CAS  Google Scholar 

  • Liu DQ, Tu LL, Wang L, Li YJ, Zhu LF, Zhang XL (2008) Characterization and expression of plasma and tonoplast membrane aquaporins in elongating cotton fibers. Plant Cell Rep (in press). doi:10.1007/s00299-008-0545-6

  • Marin-Olivier M, Chevalier T, Fobis-Loisy I, Dumas C, Gaude T (2000) Aquaporin PIP genes are not expressed in the stigma papillae in Brassica oleracea. Plant J 24:231–240. doi:10.1046/j.1365-313x.2000.00874.x

    Article  PubMed  CAS  Google Scholar 

  • Maurel C (2007) Plant aquaporins: novel functions and regulation properties. FEBS Lett 581:2227–2236. doi:10.1016/j.febslet.2007.03.021

    Article  PubMed  CAS  Google Scholar 

  • Mizutani M, Watanabe S, Nakagawa T, Maeshima M (2006) Aquaporin NIP2;1 is mainly localized to the ER membrane and shows root-specific accumulation in Arabidopsis thaliana. Plant Cell Physiol 47:1420–1426

    Article  PubMed  CAS  Google Scholar 

  • Moshelion M, Becker D, Biela A, Uehlein N, Hedrich R, Otto B, Levi H, Moran N, Kaldenhoff R (2002) Plasma membrane aquaporins in the motor cells of Samanea saman: diurnal and circadian regulation. Plant Cell 14:727–739. doi:10.1105/tpc.010351

    Article  PubMed  CAS  Google Scholar 

  • Murata K, Mitsuoka K, Hirai T, Walz T, Agre P, Heymann JB, Engel A, Fujiyoshi Y (2000) Structural determinants of water permeation through aquaporin-1. Nature 407:599–605. doi:10.1038/35036519

    Article  PubMed  CAS  Google Scholar 

  • Niemietz CM, Tyerman SD (2000) Channel-mediated permeation of ammonia gas through the peribacteroid membrane of soybean nodules. FEBS Lett 465:110–114. doi:10.1016/s0014-5793(99)01729-9

    Article  PubMed  CAS  Google Scholar 

  • Schäffner AR (1998) Aquaporin function, structure, and expression: are there more surprises to surface in water relations? Planta 204:131–139. doi:10.1007/s004250050239

    Article  PubMed  Google Scholar 

  • Siefritz F, Tyree MT, Lovisolo C, Schubert A, Kaldenhoff R (2002) PIP1 plasma membrane aquaporins in tobacco: from cellular effects to function in plants. Plant Cell 14:869–876. doi:10.1105/tpc.000901

    Article  PubMed  CAS  Google Scholar 

  • Sui H, Han BG, Lee JK, Walian P, Jap BK (2001) Structural basis of water-specific transport through the AQP1 water channel. Nature 414:872–878. doi:10.1038/414872a

    Article  PubMed  CAS  Google Scholar 

  • Takano J, Wada M, Ludewig U, Schaaf G, von Wiren N, Fujiwaraa T (2006) The Arabidopsis major intrinsic protein NIP5;1 is essential for efficient boron uptake and plant development under boron limitation. Plant Cell 18:1498–1509. doi:10.1105/tpc.106.041640

    Article  PubMed  Google Scholar 

  • Temmei Y, Uchida S, Hoshino D, Kanzawa N, Kuwahara M, Sasaki S, Tsuchiya T (2005) Water channel activities of Mimosa pudica plasma membrane intrinsic proteins are regulated by direct interaction and phosphorylation. FEBS Lett 579:4417–4422. doi:10.1016/j.febslet.2005.06.082

    Article  PubMed  CAS  Google Scholar 

  • Tyerman SD, Niemietz CM, Bramley H (2002) Plant aquaporins: multifunctional water and solute channels with expanding roles. Plant Cell Environ 25:173–194. doi:10.1046/j.0016-8025.2001.00791.x

    Article  PubMed  CAS  Google Scholar 

  • Wallace IS, Choi WG, Roberts DM (2006) The structure, function and regulation of the nodulin 26-like intrinsic protein family of plant aquaglyceroporins. Biochim Biophys Acta 1758:1165–1175. doi:10.1016/j.bbamem.2006.03.024

    Article  PubMed  CAS  Google Scholar 

  • Weig AR, Jakob C (2000) Functional identification of the glycerol permease activity of Arabidopsis thaliana NLM1 and NLM2 proteins by heterologous expression in Saccharomyces cerevisiae. FEBS Lett 481:293–298. doi:10.1016/S0014-5793(00)02027-5

    Article  PubMed  CAS  Google Scholar 

  • Zelazny E, Borst JW, Muylaert M, Batoko H, Hemminga MA, Chaumont F (2007) FRET imaging in living maize cells reveals that plasma membrane aquaporins interact to regulate their subcellular localization. PNAS 104:12359–12364. doi:10.1073/pnas.0701180104

    Article  PubMed  CAS  Google Scholar 

  • Zhang RB, Verkman AS (1991) Water and urea permeability properties of Xenopus oocytes: expression of mRNA from toad urinary bladder. Am J Physiol 260:C26–C34

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by National Natural Sciences Foundation of China (grant No. 30871317), and Natural Sciences Foundation of Hubei Province, China (grant No. 2006ABA181).

Author information

Authors and Affiliations

  1. Hubei Key Laboratory of Genetic Regulation and Integrative Biology, College of Life Sciences, HuaZhong Normal University, 430079, Wuhan, China

    Deng-Di Li, Ya-Jie Wu, **ang-Mei Ruan, Bing Li, Li Zhu, Hong Wang & Xue-Bao Li

Authors
  1. Deng-Di Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ya-Jie Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. **ang-Mei Ruan
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Bing Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Li Zhu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Hong Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Xue-Bao Li
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Xue-Bao Li.

Additional information

Communicated by W.-H. Wu.

D.-D. Li and Y.-J. Wu have contributed equally to this work.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Li, DD., Wu, YJ., Ruan, XM. et al. Expressions of three cotton genes encoding the PIP proteins are regulated in root development and in response to stresses. Plant Cell Rep 28, 291–300 (2009). https://doi.org/10.1007/s00299-008-0626-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00299-008-0626-6

Keywords

Search

Navigation