Enhanced gravi- and phototropism in plant mdr mutants mislocalizing the auxin efflux protein PIN1

Abstract

Many aspects of plant growth and development are dependent on the flow of the hormone auxin down the plant from the growing shoot tip where it is synthesized1,2. The direction of auxin transport in stems is believed to result from the basal localization within cells of the PIN1 membrane protein, which controls the efflux of the auxin anion3. Mutations in two genes homologous to those encoding the P-glycoprotein ABC transporters that are especially abundant in multidrug-resistant tumour cells in animals4 were recently shown to block polar auxin transport in the hypocotyls of Arabidopsis seedlings5. Here we show that the mdr mutants display faster and greater gravitropism and enhanced phototropism instead of the impaired curvature development expected in mutants lacking polar auxin transport. We find that these phenotypes result from a disruption of the normal accumulation of PIN1 protein along the basal end of hypocotyl cells associated with basipetal auxin flow. Lateral auxin conductance becomes relatively larger as a result, enhancing the growth differentials responsible for tropic responses.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Figure 1: Localization of PIN1 in the hypocotyls of 5-day-old (4 days after germination) wild-type and mutant Arabidopsis seedlings.
Figure 2: Greater hypocotyl nutation and gravitropism in mdr seedlings.
Figure 3: Kinetics of hypocotyl gravitropism and phototropism.

References

  1. 1

    Muday, G. K. & DeLong, A. Polar auxin transport: controlling where and how much. Trends Plant Sci. 6, 535–542 (2001)

    CAS  Article  Google Scholar 

  2. 2

    Gil, P. et al. BIG: a calossin-like protein required for polar auxin transport in Arabidopsis. Genes Dev. 15, 1985–1997 (2001)

    CAS  Article  Google Scholar 

  3. 3

    Friml, J. & Palme, K. Polar auxin transport—old questions and new concepts? Plant Mol. Biol. 49, 273–284 (2002)

    CAS  Article  Google Scholar 

  4. 4

    Ambudkar, S. V. et al. Biochemical, cellular, and pharmacological aspects of the multidrug transporter. Annu. Rev. Pharmacol. Toxicol. 39, 361–398 (1999)

    CAS  Article  Google Scholar 

  5. 5

    Noh, B., Murphy, A. S. & Spalding, E. P. Multidrug resistance-like genes of Arabidopsis required for auxin transport and auxin-mediated development. Plant Cell 13, 2441–2454 (2001)

    CAS  Article  Google Scholar 

  6. 6

    Sánchez-Fernández, R., Davies, T. G. E., Coleman, J. O. D. & Rea, P. A. The Arabidopsis thaliana ABC protein superfamily, a complete inventory. J. Biol. Chem. 276, 30231–30244 (2001)

    Article  Google Scholar 

  7. 7

    Murphy, A. S., Hoogner, K. R., Peer, W. A. & Taiz, L. Identification, purification, and molecular cloning of N-1-naphthylphthalamic acid-binding plasma membrane-associated aminopeptidases from Arabidopsis. Plant Physiol. 128, 935–950 (2002)

    CAS  Article  Google Scholar 

  8. 8

    Sidler, M., Hassa, P., Hasan, S., Ringli, C. & Dudler, R. Involvement of an ABC transporter in a developmental pathway regulating hypocotyl cell elongation in the light. Plant Cell 10, 1623–1636 (1998)

    CAS  Article  Google Scholar 

  9. 9

    Geldner, N., Friml, J., Stierhof, Y.-D., Jürgens, G. & Palme, K. Auxin transport inhibitors block PIN1 cycling and vesicle trafficking. Nature 413, 425–428 (2001)

    ADS  CAS  Article  Google Scholar 

  10. 10

    Gälweiler, L. et al. Regulation of polar auxin transport by AtPIN1 in Arabidopsis vascular tissue. Science 282, 2226–2230 (1998)

    ADS  Article  Google Scholar 

  11. 11

    Muday, G. K. Auxins and tropisms. J. Plant Growth Regul. 20, 226–243 (2001)

    CAS  Article  Google Scholar 

  12. 12

    Friml, J., Wisniewska, J., Benkovà, E., Mendgen, K. & Palme, K. Lateral redistribution of auxin efflux regulator PIN3 mediates tropism in Arabidopsis. Nature 415, 806–809 (2002)

    ADS  Article  Google Scholar 

  13. 13

    Harper, J. D. I. et al. A simple and rapid technique for the immunofluorescence confocal microscopy of intact Arabidopsis root tips: Localization of a centrin-like protein to higher plant plasmodesmata. Cytobios 87, 71–78 (1996)

    CAS  PubMed  Google Scholar 

  14. 14

    Folta, K. M. & Spalding, E. P. Unexpected roles for cryptochrome 2 and phototropin revealed by high-resolution analysis of blue light-mediated hypocotyl growth inhibition. Plant J. 26, 471–478 (2001)

    CAS  Article  Google Scholar 

Download references

Acknowledgements

We thank K. Palme for the PIN1 antibody, M. Sussman and S. Bednarek for the AHA2 antibody, and J. Wagner for technical assistance.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Edgar P. Spalding.

Ethics declarations

Competing interests

The authors declare that they have no competing financial interests.

Supplementary information

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Noh, B., Bandyopadhyay, A., Peer, W. et al. Enhanced gravi- and phototropism in plant mdr mutants mislocalizing the auxin efflux protein PIN1. Nature 423, 999–1002 (2003). https://doi.org/10.1038/nature01716

Download citation

Further reading

Comments

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.

Search

Quick links

Sign up for the Nature Briefing newsletter for a daily update on COVID-19 science.
Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing