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Light triggers PILS-dependent reduction in nuclear auxin signalling for growth transition

Nature Plants volume 3, Article number: 17105 (2017) Cite this article

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An Author Correction to this article was published on 04 May 2021

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Abstract

The phytohormone auxin induces or represses growth depending on its concentration and the underlying tissue type. However, it remains unknown how auxin signalling is modulated to allow tissues transiting between repression and promotion of growth. Here, we used apical hook development as a model for growth transitions in plants. A PIN-FORMED (PIN)-dependent intercellular auxin transport module defines an auxin maximum that is causal for growth repression during the formation of the apical hook. Our data illustrate that growth transition for apical hook opening is largely independent of this PIN module, but requires the PIN-LIKES (PILS) putative auxin carriers at the endoplasmic reticulum. PILS proteins reduce nuclear auxin signalling in the apical hook, leading to the de-repression of growth and the onset of hook opening. We also show that the phytochrome (phy) B-reliant light-signalling pathway directly regulates PILS gene activity, thereby enabling light perception to repress nuclear auxin signalling and to control growth. We propose a novel mechanism, in which PILS proteins allow external signals to alter tissue sensitivity to auxin, defining differential growth rates.

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Figure 1: PILS expression during apical hook development.
Figure 2: PILS2 and PILS5 requirements for apical hook development.
Figure 3: Light-induced apical hook opening correlates with elevated PILS expression.
Figure 4: Light-induced apical hook opening is a PILS-dependent manner.
Figure 5: Phytochrome Interacting Factor 5 represses PILS expression.
Figure 6: phyB/PIF5 pathway regulates PILS-dependent growth transition during apical hook early opening.

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References

  1. Dharmasiri, N., Dharmasiri, S. & Estelle, M. The F-box protein TIR1 is an auxin receptor. Nature 435, 441–445 (2005).

    Article  CAS  Google Scholar 

  2. Kepinski, S. & Leyser, O. The Arabidopsis F-box protein TIR1 is an auxin receptor. Nature 435, 446–451 (2005).

    Article  CAS  Google Scholar 

  3. Rosquete, M. R., Barbez, E. & Kleine-Vehn, J. Cellular auxin homeostasis: gatekeeping is housekeeping. Mol. Plant 5, 772–786 (2012).

    Article  Google Scholar 

  4. Evans, M. L., Ishikawa, H. & Estelle, M. A. Responses of Arabidopsis roots to auxin studied with high temporal resolution: comparison of wild type and auxin-response mutants. Planta 194, 215–222 (1994).

    Article  CAS  Google Scholar 

  5. Abbas, M., Alabadí, D. & Blázquez, M. A. Differential growth at the apical hook: all roads lead to auxin. Front Plant Sci. 4, 441 (2013).

    Article  Google Scholar 

  6. Vandenbussche, F. et al. The auxin influx carriers AUX1 and LAX3 are involved in auxin-ethylene interactions during apical hook development in Arabidopsis thaliana seedlings. Development 137, 597–606 (2010).

    Article  CAS  Google Scholar 

  7. Žádníková, P. et al. Role of PIN-mediated auxin efflux in apical hook development of Arabidopsis thaliana. Development 137, 607–617 (2010).

    Article  Google Scholar 

  8. Žádníková, P. et al. A model of differential growth-guided apical hook formation in plants. Plant Cell 28, 2464–2477 (2016).

    Article  Google Scholar 

  9. Willige, B. C., Ogiso-Tanaka, E., Zourelidou, M. & Schwechheimer, C. WAG2 represses apical hook opening downstream from gibberellin and PHYTOCHROME INTERACTING FACTOR 5. Development 139, 4020–4028 (2012).

    Article  CAS  Google Scholar 

  10. Rubinstein, B. Auxin and red light in the control of hypocotyl hook opening in beans. Plant Physiol. 48, 187–192 (1971).

    Article  CAS  Google Scholar 

  11. Yu, Q. et al. Clathrin-mediated auxin efflux and maxima regulate hypocotyl hook formation and light-stimulated hook opening in Arabidopsis. Mol. Plant 9, 101–112 (2016).

    Article  CAS  Google Scholar 

  12. 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 

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

    Article  Google Scholar 

  14. Grieneisen, V. A., Xu, J., Marée, 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 

  15. 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 

  16. Won, C. et al. Conversion of tryptophan to indole-3-acetic acid by TRYPTOPHAN AMINOTRANSFERASES OF ARABIDOPSIS and YUCCAs in Arabidopsis. Proc. Natl Acad. Sci. USA 108, 18518–18523 (2011).

    Article  CAS  Google Scholar 

  17. Mashiguchi, K. et al. The main auxin biosynthesis pathway in Arabidopsis. Proc. Natl Acad. Sci. USA 108, 18512–18517 (2011).

    Article  CAS  Google Scholar 

  18. Boer, D. R. et al. Structural basis for DNA binding specificity by the auxin-dependent ARF transcription factors. Cell 156, 577–589 (2014).

    Article  CAS  Google Scholar 

  19. 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 

  20. Barbez, E. et al. Single-cell-based system to monitor carrier driven cellular auxin homeostasis. BMC Plant Biol. 13, 20 (2013).

    Article  CAS  Google Scholar 

  21. Reed, J. W. & Chory, J. Mutational analyses of light-controlled seedling development in Arabidopsis. Semin. Cell Biol. 5, 327–334 (1994).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  23. Duek, P. D. & Fankhauser, C. bHLH class transcription factors take centre stage in phytochrome signalling. Trends Plant Sci. 10, 51–54 (2005).

    Article  CAS  Google Scholar 

  24. Vieten, A. et al. Functional redundancy of PIN proteins is accompanied by auxin-dependent cross-regulation of PIN expression. Development 132, 4521–4531 (2005).

    Article  CAS  Google Scholar 

  25. de Wit, M. & Pierik, R. in Canopy Photosynthesis: From Basics to Applications (eds Hikosaka, K., Niinemets, Ü. & Anten, N. P. R. ) 171–186 (Springer, 2016).

    Book  Google Scholar 

  26. Hornitschek, P. et al. Phytochrome interacting factors 4 and 5 control seedling growth in changing light conditions by directly controlling auxin signaling. Plant J. 71, 699–711 (2012).

    Article  CAS  Google Scholar 

  27. 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 

  28. Hersch, M. et al. Light intensity modulates the regulatory network of the shade avoidance response in Arabidopsis. Proc. Natl Acad. Sci. USA 111, 6515–6520 (2014).

    Article  CAS  Google Scholar 

  29. Krishna Reddy, S. & Finlayson, S. A. Phytochrome B promotes branching in Arabidopsis by suppressing auxin signaling. Plant Physiol. 164, 1542–1550 (2014).

    Article  Google Scholar 

  30. Fendrych, M., Leung, J. & Friml, J. TIR1/AFB-Aux/IAA auxin perception mediates rapid cell wall acidification and growth of Arabidopsis hypocotyls. eLife 5, 297 (2016).

    Article  Google Scholar 

  31. Reed, J. W., Nagatani, A., Elich, T. D., Fagan, M. & Chory, J. Phytochrome A and phytochrome B have overlapping but distinct functions in Arabidopsis development. Plant Physiol. 104, 1139–1149 (1994).

    Article  CAS  Google Scholar 

  32. 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 

  33. Béziat, C., Kleine-Vehn, J. & Feraru, E. Histochemical staining of β-glucuronidase and its spatial quantification. Methods Mol. Biol. 1497, 73–80 (2017).

    Article  Google Scholar 

  34. Gendrel, A.-V., Lippman, Z., Yordan, C., Colot, V. & Martienssen, R. A. Dependence of heterochromatic histone H3 methylation patterns on the Arabidopsis gene DDM1. Science 297, 1871–1873 (2002).

    Article  CAS  Google Scholar 

  35. Kumar, S. V. et al. Transcription factor PIF4 controls the thermosensory activation of flowering. Nature 484, 242–245 (2012).

    Article  CAS  Google Scholar 

  36. Livak, K. J. & Schmittgen, T. D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(T)(-Delta Delta C) method. Methods 25, 402–408 (2001).

    Article  CAS  Google Scholar 

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Acknowledgements

We are grateful to P. Zadnikova and E. Benkova for introducing us to infrared-based time lapse imaging; D. Scheuring and F. Barbez for helping us establishing our infrared imaging station; C. Fankhauser, P. Wigge, J. Friml and A. Maizel for providing published material; E. Benkova, M. Geisler, U. Hammes and J.K.-V. group members for critical reading of the manuscript; J. Thacker for help with the manuscript; and the BOKU-VIBT Imaging Centre for access and expertise. This work was supported by the Vienna Research Group (VRG) programme of the Vienna Science and Technology Fund (WWTF), the Austrian Science Fund (FWF) (Projects: P26568-B16 and P26591-B16) and the European Research Council (ERC) (Starting Grant 639478-AuxinER) (to J.K.-V.) as well as the APART fellowship of the Austrian Academy of Sciences (ÖAW) (to D.L.).

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Authors and Affiliations

  1. Department of Applied Genetics and Cell Biology, University of Natural Resources and Life Sciences (BOKU), Muthgasse 18, 1190 Vienna, Austria

    Chloé Béziat, Elke Barbez, Mugurel I. Feraru, Doris Lucyshyn & Jürgen Kleine-Vehn

  2. Department of Plant Systems Biology, VIB and Department of Plant Biotechnology and Bioinformatics, Ghent University, Technologiepark 927, 9052 Gent, Belgium

    Chloé Béziat, Elke Barbez & Jürgen Kleine-Vehn

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  1. Chloé Béziat
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  2. Elke Barbez
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Contributions

C.B. carried out most of the experiments; J.K.-V. and C.B. interpreted the results and designed experiments. E.B. cloned most constructs and contributed to the statistical analysis. M.I.F. genotyped pils loss-of-function mutant and crosses. D.L. and C.B. performed ChIP and qPCR experiments, J.K.-V. and C.B. wrote the manuscript. All authors saw and commented on the manuscript.

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Correspondence to Jürgen Kleine-Vehn.

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The authors declare no competing financial interests.

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Supplementary Figures 1–12, Supplementary Table 1. (PDF 7526 kb)

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Béziat, C., Barbez, E., Feraru, M. et al. Light triggers PILS-dependent reduction in nuclear auxin signalling for growth transition. Nature Plants 3, 17105 (2017). https://doi.org/10.1038/nplants.2017.105

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