Skip to main content

Thank you for visiting nature.com. 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.

  • Article
  • Published:

Local auxin metabolism regulates environment-induced hypocotyl elongation

Nature Plants volume 2, Article number: 16025 (2016) Cite this article

Subjects

Abstract

A hallmark of plants is their adaptability of size and form in response to widely fluctuating environments. The metabolism and redistribution of the phytohormone auxin play pivotal roles in establishing active auxin gradients and resulting cellular differentiation. In Arabidopsis thaliana, cotyledons and leaves synthesize indole-3-acetic acid (IAA) from tryptophan through indole-3-pyruvic acid (3-IPA) in response to vegetational shade. This newly synthesized auxin moves to the hypocotyl where it induces elongation of hypocotyl cells. Here we show that loss of function of VAS2 (IAA-amido synthetase Gretchen Hagen 3 (GH3).17) leads to increases in free IAA at the expense of IAA-Glu (IAA-glutamate) in the hypocotyl epidermis. This active IAA elicits shade- and high temperature-induced hypocotyl elongation largely independently of 3-IPA-mediated IAA biosynthesis in cotyledons. Our results reveal an unexpected capacity of local auxin metabolism to modulate the homeostasis and spatial distribution of free auxin in specialized organs such as hypocotyls in response to shade and high temperature.

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

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

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

Figure 1: Identification of the VAS2 gene.
Figure 2: vas2 mutant accumulates more free IAA and IAA biosynthetic precursors, but less of amino acid conjugate IAA-Glu.
Figure 3: Shade-induced hypocotyl elongation of vas2, but not vas1, is largely independent of auxin transport from cotyledons to hypocotyls.
Figure 4: vas2 mutation has no effect on the responses of the cotyledon's angle and size of the sav3 mutant on treatment with a combination of NPA and shade.
Figure 5: DR5::GUS intensity and distribution indicate that vas2 mutant accumulates more free IAA, which is distributed to the epidermis of hypocotyl under shade regardless of NPA treatment.
Figure 6: VAS2 regulates high temperature-induced hypocotyl elongation.

Similar content being viewed by others

References

  1. Franklin, K. A. Shade avoidance. New Phytol. 179, 930–944 (2008).

    Article  CAS  Google Scholar 

  2. Casal, J. J. Shade avoidance. Arabidopsis Book 10, e0157 (2012).

    Article  Google Scholar 

  3. Li, L. et al. Linking photoreceptor excitation to changes in plant architecture. Genes Dev. 26, 785–790 (2012).

    Article  CAS  Google Scholar 

  4. Tao, Y. et al. Rapid synthesis of auxin via a new tryptophan-dependent pathway is required for shade avoidance in plants. Cell 133, 164–176 (2008).

    Article  CAS  Google Scholar 

  5. de Wit, M., Lorrain, S. & Fankhauser, C. Auxin-mediated plant architectural changes in response to shade and high temperature. Physiol. Plant 151, 13–24 (2014).

    Article  CAS  Google Scholar 

  6. Stepanova, A. N. et al. TAA1-mediated auxin biosynthesis is essential for hormone crosstalk and plant development. Cell 133, 177–191 (2008).

    Article  CAS  Google Scholar 

  7. Sun, J., Qi, L., Li, Y., Chu, J. & Li, C. PIF4-mediated activation of YUCCA8 expression integrates temperature into the auxin pathway in regulating Arabidopsis hypocotyl growth. PLoS Genet. 8, e1002594 (2012).

    Article  CAS  Google Scholar 

  8. Keuskamp, D. H., Pollmann, S., Voesenek, L. A., Peeters, A. J. & Pierik, R. Auxin transport through PIN-FORMED 3 (PIN3) controls shade avoidance and fitness during competition. Proc. Natl Acad. Sci. USA 107, 22740–22744 (2010).

    Article  CAS  Google Scholar 

  9. Franklin, K. A. et al. Phytochrome-interacting factor 4 (PIF4) regulates auxin biosynthesis at high temperature. Proc. Natl Acad. Sci. USA 108, 20231–20235 (2011).

    Article  CAS  Google Scholar 

  10. Yamada, M., Greenham, K., Prigge, M. J., Jensen, P. J. & Estelle, M. The TRANSPORT INHIBITOR RESPONSE2 gene is required for auxin synthesis and diverse aspects of plant development. Plant Physiol. 151, 168–179 (2009).

    Article  CAS  Google Scholar 

  11. Procko, C., Crenshaw, C. M., Ljung, K., Noel, J. P. & Chory, J. Cotyledon-generated auxin is required for shade-induced hypocotyl growth in Brassica rapa. Plant Physiol. 165, 1285–1301 (2014).

    Article  CAS  Google Scholar 

  12. Petrasek, J. & Friml, J. Auxin transport routes in plant development. Development 136, 2675–2688 (2009).

    Article  CAS  Google Scholar 

  13. Zheng, Z. et al. Coordination of auxin and ethylene biosynthesis by the aminotransferase VAS1. Nature Chem. Biol. 9, 244–246 (2013).

    Article  CAS  Google Scholar 

  14. Hagen, G., Kleinschmidt, A. & Guilfoyle, T. Auxin-regulated gene expression in intact soybean hypocotyl and excised hypocotyl sections. Planta 162, 147–153 (1984).

    Article  CAS  Google Scholar 

  15. Staswick, P. E. et al. Characterization of an Arabidopsis enzyme family that conjugates amino acids to indole-3-acetic acid. Plant Cell 17, 616–627 (2005).

    Article  CAS  Google Scholar 

  16. Westfall, C. S., Herrmann, J., Chen, Q., Wang, S. & Jez, J. M. Modulating plant hormones by enzyme action: the GH3 family of acyl acid amido synthetases. Plant Signal. Behav. 5, 1607–1612 (2010).

    Article  CAS  Google Scholar 

  17. Ludwig-Muller, J. Auxin conjugates: their role for plant development and in the evolution of land plants. J. Exp. Bot. 62, 1757–1773 (2011).

    Article  Google Scholar 

  18. Korasick, D. A., Enders, T. A. & Strader, L. C. Auxin biosynthesis and storage forms. J. Exp. Bot. 64, 2541–2555 (2013).

    Article  CAS  Google Scholar 

  19. Morant, M. et al. Metabolomic, transcriptional, hormonal, and signaling cross-talk in superroot2. Mol. Plant 3, 192–211 (2010).

    Article  CAS  Google Scholar 

  20. Paponov, I. A. et al. Comprehensive transcriptome analysis of auxin responses in Arabidopsis. Mol. Plant 1, 321–337 (2008).

    Article  CAS  Google Scholar 

  21. Terol, J., Domingo, C. & Talon, M. The GH3 family in plants: genome wide analysis in rice and evolutionary history based on EST analysis. Gene 371, 279–290 (2006).

    Article  CAS  Google Scholar 

  22. Novak, O. et al. Tissue-specific profiling of the Arabidopsis thaliana auxin metabolome. Plant J. 72, 523–536 (2012).

    Article  CAS  Google Scholar 

  23. Ljung, K. Auxin metabolism and homeostasis during plant development. Development 140, 943–950 (2013).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  25. Rampey, R. A. et al. A family of auxin-conjugate hydrolases that contributes to free indole-3-acetic acid levels during Arabidopsis germination. Plant Physiol. 135, 978–988 (2004).

    Article  CAS  Google Scholar 

  26. LeClere, S., Tellez, R., Rampey, R. A., Matsuda, S. P. & Bartel, B. Characterization of a family of IAA-amino acid conjugate hydrolases from Arabidopsis. J. Biol. Chem. 277, 20446–20452 (2002).

    Article  CAS  Google Scholar 

  27. Sauer, M., Robert, S. & Kleine-Vehn, J . Auxin: simply complicated. J. Exp. Bot. 64, 2565–2577 (2013).

    Article  CAS  Google Scholar 

  28. Kim, J. Y. et al. Identification of an ABCB/P-glycoprotein-specific inhibitor of auxin transport by chemical genomics. J. Biol. Chem. 285, 23309–23317 (2010).

    Article  CAS  Google Scholar 

  29. Pencik, A. et al. Regulation of auxin homeostasis and gradients in Arabidopsis roots through the formation of the indole-3-acetic acid catabolite 2-oxindole-3-acetic acid. Plant Cell 25, 3858–3870 (2013).

    Article  CAS  Google Scholar 

  30. Khan, S. & Stone, J. M. Arabidopsis thaliana GH3.9 influences primary root growth. Planta 226, 21–34 (2007).

    Article  CAS  Google Scholar 

  31. Westfall, C. S. et al. Structural basis for prereceptor modulation of plant hormones by GH3 proteins. Science 336, 1708–1711 (2012).

    Article  CAS  Google Scholar 

  32. Yuan, H. et al. Genome-wide analysis of the GH3 family in apple (Malus × domestica). BMC Genomics 14, 297 (2013).

    Article  CAS  Google Scholar 

  33. Fu, J., Yu, H., Li, X., Xiao, J. & Wang, S. Rice GH3 gene family: regulators of growth and development. Plant Signal. Behav. 6, 570–574 (2011).

    Article  CAS  Google Scholar 

  34. Khan, S. & Stone, J. M. Arabidopsis thaliana GH3.9 in auxin and jasmonate cross talk. Plant Signal. Behav. 2, 483–485 (2007).

    Article  Google Scholar 

  35. Mittag, J., Gabrielyan, A. & Ludwig-Muller, J. Knockout of GH3 genes in the moss Physcomitrella patens leads to increased IAA levels at elevated temperature and in darkness. Plant Physiol. Biochem. 97, 339–349 (2015).

    Article  CAS  Google Scholar 

  36. Jagadeeswaran, G. et al. Arabidopsis GH3-LIKE DEFENSE GENE 1 is required for accumulation of salicylic acid, activation of defense responses and resistance to Pseudomonas syringae. Plant J. 51, 234–246 (2007).

    Article  CAS  Google Scholar 

  37. Takase, T., Nakazawa, M., Ishikawa, A., Manabe, K. & Matsui, M. DFL2, a new member of the Arabidopsis GH3 gene family, is involved in red light-specific hypocotyl elongation. Plant Cell Physiol. 44, 1071–1080 (2003).

    Article  CAS  Google Scholar 

  38. Nakazawa, M. et al. DFL1, an auxin-responsive GH3 gene homologue, negatively regulates shoot cell elongation and lateral root formation, and positively regulates the light response of hypocotyl length. Plant J. 25, 213–221 (2001).

    Article  CAS  Google Scholar 

  39. Santner, A., Calderon-Villalobos, L. I. & Estelle, M. Plant hormones are versatile chemical regulators of plant growth. Nature Chem. Biol. 5, 301–307 (2009).

    Article  CAS  Google Scholar 

  40. Nemhauser, J. L., Hong, F. & Chory, J. Different plant hormones regulate similar processes through largely nonoverlapping transcriptional responses. Cell 126, 467–475 (2006).

    Article  CAS  Google Scholar 

  41. Zhao, Y. Auxin biosynthesis. Arabidopsis Book 12, e0173 (2014).

    Article  Google Scholar 

  42. van Berkel, K., de Boer, R. J., Scheres, B. & ten Tusscher, K. Polar auxin transport: models and mechanisms. Development 140, 2253–2268 (2013).

    Article  CAS  Google Scholar 

  43. Blilou, I. et al. The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots. Nature 433, 39–44 (2005).

    Article  CAS  Google Scholar 

  44. Grieneisen, V. A., Xu, J., Maree, A. F., Hogeweg, P. & Scheres, B. Auxin transport is sufficient to generate a maximum and gradient guiding root growth. Nature 449, 1008–1013 (2007).

    Article  CAS  Google Scholar 

  45. Pinon, V., Prasad, K., Grigg, S. P., Sanchez-Perez, G. F. & Scheres, B. Local auxin biosynthesis regulation by PLETHORA transcription factors controls phyllotaxis in Arabidopsis. Proc. Natl Acad. Sci. USA 110, 1107–1112 (2013).

    Article  CAS  Google Scholar 

  46. Mravec, J. et al. Subcellular homeostasis of phytohormone auxin is mediated by the ER-localized PIN5 transporter. Nature 459, 1136–1140 (2009).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  48. Morgan, D. C., O'Brien, T. & Smith, H. Rapid photomodulation of stem extension in light-grown Sinapis alba L.: studies on kinetics, site of perception and photoreceptor. Planta 150, 95–101 (1980).

    Article  CAS  Google Scholar 

  49. Preuten, T., Hohm, T., Bergmann, S. & Fankhauser, C. Defining the site of light perception and initiation of phototropism in Arabidopsis. Curr. Biol. 23, 1934–1938 (2013).

    Article  CAS  Google Scholar 

  50. Yamamoto, Y. et al. Quality control of PSII: behavior of PSII in the highly crowded grana thylakoids under excessive light. Plant Cell Physiol. 55, 1206–1215 (2014).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank M. Geisler for the generous gift of BUM, and the Arabidopsis Biological Resource Center for mutant seeds. These studies were supported by US National Institutes of Health (NIH) grant 5R01GM52413 to J.C., the Swedish Governmental Agency for Innovation Systems (VINNOVA) and the Swedish Research Council (VR) to K.L. and O.N., the Ministry of Education, Youth and Sports of the Czech Republic (the National Program for Sustainability I No. LO1204) to O.N., the National Science Foundation under award nos EEC-0813570 and MCB-0645794 to J.P.N. and the Howard Hughes Medical Institute (Z.Z., J.P.N., J.C.).

Author information

Authors and Affiliations

  1. Howard Hughes Medical Institute and Plant Biology Laboratory, The Salk Institute for Biological Studies, La Jolla, 92037, California, USA

    Zuyu Zheng & Joanne Chory

  2. The Jack H. Skirball Center for Chemical Biology and Proteomics, The Salk Institute for Biological Studies, La Jolla, 92037, California, USA

    Yongxia Guo

  3. Department of Forest Genetics and Plant Physiology, Umeå Plant Science Centre, Swedish University of Agricultural Sciences, SE-901 83 Umeå, Sweden

    Ondřej Novák & Karin Ljung

  4. Laboratory of Growth Regulators, Faculty of Science, Palacký University and Institute of Experimental Botany ASCR, Šlechtielů 11, 783 71 Olomouc, Czech Republic

    Ondřej Novák

  5. Plant Biology Laboratory, The Salk Institute for Biological Studies, La Jolla, 92037, California, USA

    William Chen

  6. Howard Hughes Medical Institute and The Jack H. Skirball Center for Chemical Biology and Proteomics, The Salk Institute for Biological Studies, La Jolla, California 92037, USA, Czech Republic

    Joseph P. Noel

Authors
  1. Zuyu Zheng
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yongxia Guo
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ondřej Novák
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. William Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Karin Ljung
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Joseph P. Noel
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Joanne Chory
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Z.Y.Z. designed the experiments with the input from J.P.N. and J.C., Z.Y.Z., Y.X.G., O.N., W.C. and K.L. performed the experiments. Z.Y.Z., J.P.N. and J.C. wrote the manuscript. All authors discussed the results and commented on the experimental design.

Corresponding authors

Correspondence to Joseph P. Noel or Joanne Chory.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zheng, Z., Guo, Y., Novák, O. et al. Local auxin metabolism regulates environment-induced hypocotyl elongation. Nature Plants 2, 16025 (2016). https://doi.org/10.1038/nplants.2016.25

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1038/nplants.2016.25

This article is cited by

Search

Advanced search

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