Skip to main content

Thank you for visiting You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

A novel putative auxin carrier family regulates intracellular auxin homeostasis in plants


The phytohormone auxin acts as a prominent signal, providing, by its local accumulation or depletion in selected cells, a spatial and temporal reference for changes in the developmental program1,2,3,4,5,6,7. The distribution of auxin depends on both auxin metabolism (biosynthesis, conjugation and degradation)8,9,10 and cellular auxin transport11,12,13,14,15. We identified in silico a novel putative auxin transport facilitator family, called PIN-LIKES (PILS). Here we illustrate that PILS proteins are required for auxin-dependent regulation of plant growth by determining the cellular sensitivity to auxin. PILS proteins regulate intracellular auxin accumulation at the endoplasmic reticulum and thus auxin availability for nuclear auxin signalling. PILS activity affects the level of endogenous auxin indole-3-acetic acid (IAA), presumably via intracellular accumulation and metabolism. Our findings reveal that the transport machinery to compartmentalize auxin within the cell is of an unexpected molecular complexity and demonstrate this compartmentalization to be functionally important for a number of developmental processes.

This is a preview of subscription content, access via your institution

Relevant articles

Open Access articles citing this article.

Access options

Rent or buy this article

Get just this article for as long as you need it


Prices may be subject to local taxes which are calculated during checkout

Figure 1: Novel PILS protein family.
Figure 2: Phenotypes of PILS loss- and gain-of function mutants.
Figure 3: PILS proteins affect auxin-dependent cellular growth.
Figure 4: PILS involvement in cellular auxin homeostasis.


  1. Benková, E. et al. Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell 115, 591–602 (2003)

    Article  Google Scholar 

  2. Friml, J. et al. Efflux-dependent auxin gradients establish the apical-basal axis of Arabidopsis. Nature 426, 147–153 (2003)

    Article  CAS  ADS  Google Scholar 

  3. Reinhardt, D. et al. Regulation of phyllotaxis by polar auxin transport. Nature 426, 255–260 (2003)

    Article  CAS  ADS  Google Scholar 

  4. Leyser, O. Dynamic integration of auxin transport and signalling. Curr. Biol. 16, R424–R433 (2006)

    Article  CAS  Google Scholar 

  5. Dubrovsky, J. G. et al. Auxin acts as a local morphogenetic trigger to specify lateral root founder cells. Proc. Natl Acad. Sci. USA 105, 8790–8794 (2008)

    Article  CAS  ADS  Google Scholar 

  6. Sorefan, K. et al. A regulated auxin minimum is required for seed dispersal in Arabidopsis. Nature 459, 583–586 (2009)

    Article  CAS  ADS  Google Scholar 

  7. Prasad, K. et al. Arabidopsis PLETHORA transcription factors control phyllotaxis. Curr. Biol. 21, 1123–1128 (2011)

    Article  CAS  Google Scholar 

  8. Woodward, A. W. & Bartel, B. Auxin: regulation, action, and interaction. Ann. Bot. 95, 707–735 (2005)

    Article  CAS  Google Scholar 

  9. Ikeda, Y. et al. Local auxin biosynthesis modulates gradient-directed planar polarity in Arabidopsis. Nature Cell Biol. 11, 731–738 (2009)

    Article  CAS  Google Scholar 

  10. Zhao, Y. Auxin biosynthesis and its role in plant development. Annu. Rev. Plant Biol. 61, 49–64 (2010)

    Article  CAS  Google Scholar 

  11. Bennett, M. J. et al. Arabidopsis AUX1 gene: a permease-like regulator of root gravitropism. Science 273, 948–950 (1996)

    Article  CAS  ADS  Google Scholar 

  12. Luschnig, C., Gaxiola, R. A., Grisafi, P. & Fink, G. R. EIR1, a root-specific protein involved in auxin transport, is required for gravitropism in Arabidopsis thaliana. Genes Dev. 12, 2175–2187 (1998)

    Article  CAS  Google Scholar 

  13. Geisler, M. et al. Cellular efflux of auxin catalyzed by the Arabidopsis MDR/PGP transporter AtPGP1. Plant J. 44, 179–194 (2005)

    Article  CAS  Google Scholar 

  14. Petrášek, J. et al. PIN proteins perform a rate-limiting function in cellular auxin efflux. Science 312, 914–918 (2006)

    Article  ADS  Google Scholar 

  15. Zažímalová, E., Murphy, A. S., Yang, H., Hoyerová, K. & Hošek, P. Auxin transporters–why so many? Cold Spring Harb. Perspect. Biol. 2, a001552 (2010)

    Article  Google Scholar 

  16. Mravec, J. et al. ER-localized PIN5 auxin transporter mediates subcellular homeostasis of phytohormone auxin. Nature 459, 1136–1140 (2009)

    Article  CAS  ADS  Google Scholar 

  17. Ulmasov, T., Murfett, J., Hagen, G. & Guilfoyle, T. J. Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements. Plant Cell 9, 1963–1971 (1997)

    Article  CAS  Google Scholar 

  18. Lee, S. H. & Cho, H. T. PINOID positively regulates auxin efflux in Arabidopsis root hair cells and tobacco cells. Plant Cell 18, 1604–1616 (2006)

    Article  CAS  Google Scholar 

  19. Nagata, T., Nemoto, Y. & Hasezawa, S. Tobacco BY-2 cell line as the “HeLa” cells in the cell biology of higher plants. Int. Rev. Cytol. 132, 1–30 (1992)

    Article  CAS  Google Scholar 

  20. Marin, E. et al. miR390, Arabidopsis TAS3 tasiRNAs, and their AUXIN RESPONSE FACTOR targets define an autoregulatory network quantitatively regulating lateral root growth. Plant Cell 22, 1104–1117 (2010)

    Article  CAS  Google Scholar 

  21. Langhans, M. et al. In vivo trafficking and localization of p24 proteins in plant cells. Traffic 9, 770–785 (2008)

    Article  CAS  Google Scholar 

  22. Sauer, M., Paciorek, T., Benkova, E. & Friml, J. Immunocytochemical techniques for whole-mount in situ protein localization in plants. Nature Protocols 1, 98–103 (2006)

    Article  CAS  Google Scholar 

  23. Delbarre, A., Muller, P., Imhoff, V. & Guern, J. Comparison of mechanisms controlling uptake and accumulation of 2,4-dichlorophenoxy acetic acid, naphthalene-1-acetic acid, and indole-3-acetic acid in suspension-cultured tobacco cells. Planta 198, 532–541 (1996)

    Article  CAS  Google Scholar 

  24. Bailly, A. et al. Modulation of P-glycoproteins by auxin transport inhibitors is mediated by interaction with immunophilins. J. Biol. Chem. 283, 21817–21826 (2008)

    Article  CAS  Google Scholar 

  25. Dobrev, P. I., Havlíček, L., Vágner, M., Malbeck, J. & Kamínek, M. Purification and determination of plant hormones auxin and abscisic acid using solid phase extraction and two-dimensional high performance liquid chromatography. J. Chromatogr. A 1075, 159–166 (2005)

    Article  CAS  Google Scholar 

  26. Dobrev, P. I. & Kamínek, M. Fast and efficient separation of cytokinins from auxin and abscisic acid and their purification using mixed-mode solid-phase extraction. J. Chromatogr. A 950, 21–29 (2002)

    Article  Google Scholar 

  27. Schultz, J., Milpetz, F., Bork, P. & Ponting, C. P. SMART, a simple modular architecture research tool: identification of signaling domains. Proc. Natl Acad. Sci. USA 95, 5857–5864 (1998)

    Article  CAS  ADS  Google Scholar 

  28. Letunic, I., Doerks, T. & Bork, P. SMART 6: recent updates and new developments. Nucleic Acids Res. 37, 229–232 (2009)

    Article  Google Scholar 

  29. Tusnády, G. E. & Simon, I. The HMMTOP transmembrane topology prediction server. Bioinformatics 17, 849–850 (2001)

    Article  Google Scholar 

  30. Spyropoulos, I. C., Liakopoulos, T. D., Bagos, P. G. & Hamodrakas, S. J. TMRPres2D: high quality visual representation of transmembrane protein models. Bioinformatics 20, 3258–3260 (2004)

    Article  CAS  Google Scholar 

  31. Proost, S. et al. PLAZA: a comparative genomics resource to study gene and genome evolution in plants. Plant Cell 21, 3718–3731 (2009)

    Article  CAS  Google Scholar 

  32. Pěnčík, A. et al. Isolation of novel indole-3-acetic acid conjugates by immunoaffinity extraction. Talanta 80, 651–655 (2009)

    Article  Google Scholar 

  33. Karimi, M., De Meyer, B. & Hilson, P. Modular cloning in plant cells. Trends Plant Sci. 10, 103–105 (2005)

    Article  CAS  Google Scholar 

  34. Karimi, M., Inze, D. & Depicker, A. GATEWAY vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci. 7, 193–195 (2002)

    Article  CAS  Google Scholar 

  35. Curtis, M. D. & Grossniklaus, U. A gateway cloning vector set for high-throughput functional analysis of genes in planta. Plant Physiol. 133, 462–469 (2003)

    Article  CAS  Google Scholar 

Download references


We are grateful to C. Braeckman for plant transformation; W. Ardiles for sequencing support; L. Charrier for technical assistance; A. Maizel, N. Geldner and P. Pimpl for providing material; J.K.-V. group members for critical reading of the manuscript and the BOKU-VIBT Imaging Center for access and expertise. This work was supported by the Vienna Science and Technology Fund (WWTF) (to J.K.-V.), the Agency for Innovation by Science and Technology (IWT) (predoctoral fellowship to E.B.), the Odysseus program of the Research Foundation-Flanders (to J.F.), the Swiss National Funds (to M.G.), the Ministry of Education, Youth and Sports of the Czech Republic (LC06034) (to E.Z.), Grant Agency of the Czech Republic project P305/11/2476 (to J.P.) and P305/11/0797 (to E.Z).

Author information

Authors and Affiliations



E.B. and J.K.V. conceived the project. E.B. carried out most of the experiments. M.K., P.I.B., E.Z. and J.P. performed auxin metabolite profile and auxin accumulation in BY-2. C.B. analysed auxin-dependent PILS expression and contributed to phenotype analysis. M.R.R. contributed to PILS cloning. J.R. and A.P. measured auxin content in Arabidopsis. B.W., J.Z. and M.G. performed auxin accumulation in yeast and protoplasts. Y.L. modified the oestradiol-inducible vector. E.B., M.K., J.R., E.Z., J.P., M.G., J.F. and J.K.V. discussed the experimental procedures. All authors analysed and discussed the data; E.B. and J.K.V. wrote the paper and all authors saw and commented on the manuscript.

Corresponding author

Correspondence to Jürgen Kleine-Vehn.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Information

This file contains Supplementary Figures 1-10 and Supplementary References. (PDF 3594 kb)

PowerPoint slides

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Barbez, E., Kubeš, M., Rolčík, J. et al. A novel putative auxin carrier family regulates intracellular auxin homeostasis in plants. Nature 485, 119–122 (2012).

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI:

This article is cited by


By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.


Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing