Plants growing in high densities experience a reduced red (R) to far-red (FR) light ratio and shade-intolerant species respond with accelerated elongation growth to reach the top of the canopy: the shade avoidance syndrome (SAS). FR-enriched light inactivates phytochrome photoreceptors, which results in subsequent action of several plant hormones regulating growth. SAS is adaptive for shade-intolerant plants, but is suppressed in shade-tolerant plant species. Inspired by a previously published transcriptome analysis, we use two species of the genus Geranium here to study the involvement of auxin, brassinosteroids (BRs), and gibberellins (GAs) in supplemental FR-induced elongation growth. G. pyrenaicum, a shade-avoiding species, strongly induces auxin and gibberellin levels, but not BR, in elongating petioles. We show that, in this species, FR light perception, hormone synthesis, and growth are local and restricted to the petiole, and not the leaf lamina. Using chemical hormone inhibitors, we confirm the essential role of auxin and GAs in supplemental FR-induced elongation growth. Shade-tolerant G. robertianum does not display the change in hormone levels upon FR light enrichment, resulting in the lack of a shade avoidance response.

Laboratory of Growth Regulators Centre of the Region Haná for Biotechnological and Agricultural Research Institute of Experimental Botany ASCR Faculty of Science Palacký University Olomouc Czechia

Plant Development and Signal Transduction Program Center for Research in Agricultural Genomics Barcelona Spain

Plant Ecophysiology Institute of Environmental Biology Utrecht University Utrecht The Netherlands

Present address Centre for Plant Integrative Biology School of Biosciences University of Nottingham Sutton Bonington UK

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Ballaré, C. L. , & Pierik, R. (2017). The shade‐avoidance syndrome: Multiple signals and ecological consequences. Plant, Cell and Environment, 40, 2530–2543. 10.1111/pce.12914 PubMed DOI

Bernardo‐García, S. , de Lucas, M. , Martínez, C. , Espinosa‐Ruiz, A. , Davière, J. M. , & Prat, S. (2014). BR‐dependent phosphorylation modulates PIF4 transcriptional activity and shapes diurnal hypocotyl growth. Genes & Development, 28, 1681–1694. 10.1101/gad.243675.114 PubMed DOI PMC

Bou‐Torrent, J. , Galstyan, A. , Gallemí, M. , Cifuentes‐Esquivel, N. , Molina‐Contreras, M. J. , Salla‐Martret, M. , … Martínez‐García, J. F. (2014). Plant proximity perception dynamically modulates hormone levels and sensitivity in Arabidopsis. Journal of Experimental Botany, 65, 2937–2947. 10.1093/jxb/eru083 PubMed DOI PMC

Casal, J. J. (2013). Photoreceptor signaling networks in plant responses to shade. Annual Review of Plant Biology, 64, 403–427. 10.1146/annurev-arplant-050312-120221 PubMed DOI

Cifuentes‐Esquivel, N. , Bou‐Torrent, J. , Galstyan, A. , Gallemí, M. , Sessa, G. , Salla Martret, M. , … Martínez‐García, J. F. (2013). The bHLH proteins BEE and BIM positively modulate the shade avoidance syndrome in Arabidopsis seedlings. The Plant Journal, 75, 989–1002. 10.1111/tpj.12264 PubMed DOI

de Lucas, M. , Davière, J.‐M. , Rodríguez‐Falcón, M. , Pontin, M. , Iglesias‐Pedraz, J. M. , Lorrain, S. , … Prat, S. (2008). A molecular framework for light and gibberellin control of cell elongation. Nature, 451, 480–484. 10.1038/nature06520 PubMed DOI

de Wit, M. , Costa Galvão, V. , & Fankhauser, C. (2016). Light‐mediated hormonal regulation of plant growth and development. Annual Review of Plant Biology, 67, 513–537. 10.1146/annurev-arplant-043015-112252 PubMed DOI

de Wit, M. , Keuskamp, D. H. , Bongers, F. J. , Hornitschek, P. , Gommers, C. M. M. , Reinen, E. , … Pierik, R. (2016). Integration of phytochrome and cryptochrome signals determines plant growth during competition for light. Current Biology, 26, 3320–3326. 10.1016/j.cub.2016.10.031 PubMed DOI

de Wit, M. , Ljung, K. , & Fankhauser, C. (2015). Contrasting growth responses in lamina and petiole during neighbor detection depend on differential auxin responsiveness rather than different auxin levels. New Phytologist, 208, 198–209. PubMed

de Wit, M. , Lorrain, S. , & Fankhauser, C. (2013). Auxin‐mediated plant architectural changes in response to shade and high temperature. Physiologia Plantarum, 105, 13–24. 10.1111/ppl.12099 PubMed DOI

de Wit, M. , Spoel, S. H. , Sanchez‐Perez, G. F. , Gommers, C. M. M. , Pieterse, C. M. J. , Voesenek, L. A. C. J. , & Pierik, R. (2013). Perception of low red:Far‐red ratio compromises both salicylic acid‐ and jasmonic acid‐dependent pathogen defences in Arabidopsis. The Plant Journal, 75, 90–103. 10.1111/tpj.12203 PubMed DOI

Djakovic‐Petrovic, T. , de Wit, M. , Voesenek, L. A. C. J. , & Pierik, R. (2007). DELLA protein function in growth responses to canopy signals. The Plant Journal, 51, 117–126. 10.1111/j.1365-313X.2007.03122.x PubMed DOI

Feng, S. , Martinez, C. , Gusmaroli, G. , Wang, Y. , Zhou, J. , Wang, F. , … Deng, X. W. (2008). Coordinated regulation of arabidopsis thaliana development by light and gibberellins. Nature, 451, 475–479. 10.1038/nature06448 PubMed DOI PMC

García‐Martinez, J. L. , & Gil, J. (2001). Light regulation of gibberellin biosynthesis and mode of action. Journal of Plant Growth Regulation, 20, 354–368. 10.1007/s003440010033 PubMed DOI

Gommers, C. M. M. , Keuskamp, D. H. , Buti, S. , van Veen, H. , Koevoets, I. T. , Reinen, E. , … Pierik, R. (2017). Molecular profiles of contrasting shade response strategies in wild plants: Differential control of immunity and shoot elongation. Plant Cell, 29, 331–344. 10.1105/tpc.16.00790 PubMed DOI PMC

Gommers, C. M. M. , Visser, E. J. W. , St Onge, K. R. , Voesenek, L. A. C. J. , & Pierik, R. (2013). Shade tolerance: When growing tall is not an option. Trends in Plant Science, 18, 65–71. 10.1016/j.tplants.2012.09.008 PubMed DOI

Goyal, A. , Karayekov, E. , Galvão, V. C. , Ren, H. , Casal, J. J. , & Fankhauser, C. (2016). Shade promotes phototropism through phytochrome B‐controlled auxin production. Current Biology, 26(24), 1–8. 10.1016/j.cub.2016.10.001 PubMed DOI

Hayashi, K.‐i. , Tan, X. , Zheng, N. , Hatate, T. , Kimura, Y. , Kepinski, S. , & Nozaki, H. (2008). Small‐molecule agonists and antagonists of F‐box protein‐substrate interactions in auxin perception and signaling. Proceedings of the National Academy of Sciences, 105, 5632–5637. 10.1073/pnas.0711146105 PubMed DOI PMC

Hisamatsu, T. , King, R. W. , Helliwell, C. A. , & Koshioka, M. (2005). The involvement of gibberellin 20‐oxidase genes in phytochrome‐regulated petiole elongation of Arabidopsis. Plant Physiology, 138, 1106–1116. 10.1104/pp.104.059055 PubMed DOI PMC

Hornitschek, P. , Kohnen, M. V. , Lorrain, S. , Rougemont, J. , Ljung, K. , López‐Vidriero, I. , … Fankhauser, C. (2012). Phytochrome interacting factors 4 and 5 control seedling growth in changing light conditions by directly controlling auxin signaling. The Plant Journal, 71, 699–711. 10.1111/j.1365-313X.2012.05033.x PubMed DOI

Hornitschek, P. , Lorrain, S. , Zoete, V. , Michielin, O. , & Fankhauser, C. (2009). Inhibition of the shade avoidance response by formation of non‐DNA binding bHLH heterodimers. EMBO Journal, 28, 3893–3902. 10.1038/emboj.2009.306 PubMed DOI PMC

Joo, S. H. , Kim, T. W. , Son, S. H. , Lee, W. S. , Yokota, T. , & Kim, S. K. (2012). Biosynthesis of a cholesterol‐derived brassinosteroid, 28‐norcastasterone, in Arabidopsis thaliana. Journal of Experimental Botany, 63, 1823–1833. 10.1093/jxb/err354 PubMed DOI PMC

Keuskamp, D. H. , Pollmann, S. , Voesenek, L. A. C. J. , Peeters, A. J. M. , & Pierik, R. (2010). Auxin transport through PIN‐FORMED 3 (PIN3) controls shade avoidance and fitness during competition. Proceedings of the National Academy of Sciences, 107, 22740–22744. 10.1073/pnas.1013457108/-/DCSupplemental.www.pnas.org/cgi/doi/10.1073/pnas.1013457108. PubMed DOI PMC

Keuskamp, D. H. , Sasidharan, R. , Vos, I. , Peeters, A. J. M. , Voesenek, L. A. C. J. , & Pierik, R. (2011). Blue‐light‐mediated shade avoidance requires combined auxin and brassinosteroid action in Arabidopsis seedlings. The Plant Journal, 67, 208–217. 10.1111/j.1365-313X.2011.04597.x PubMed DOI

Kohnen, M. V. , Schmid‐Siegert, E. , Trevisan, M. , Petrolati, L. A. , Sénéchal, F. , Müller‐Moulé, P. , … Fankhauser, C. (2016). Neighbor detection induces organ‐specific transcriptomes, revealing patterns underlying hypocotyl‐specific growth. Plant Cell, 28, 2889–2904. 10.1105/tpc.16.00463 PubMed DOI PMC

Kozuka, T. , Kobayashi, J. , Horiguchi, G. , Demura, T. , Sakakibara, H. , Tsukaya, H. , & Nagatani, A. (2010). Involvement of auxin and brassinosteroid in the regulation of petiole elongation under the shade. Plant Physiology, 153, 1608–1618. 10.1104/pp.110.156802 PubMed DOI PMC

Kurepin, L. V. , Joo, S. H. , Kim, S. K. , Pharis, R. P. , & Back, T. G. (2012). Interaction of brassinosteroids with light quality and plant hormones in regulating shoot growth of young sunflower and arabidopsis seedlings. Journal of Plant Growth Regulation, 31, 156–164. 10.1007/s00344-011-9227-7 DOI

Li, W. , Katin‐Grazzini, L. , Krishnan, S. , Thammina, C. , El‐Tanbouly, R. , Yer, H. , … Li, Y. (2016). A novel two‐step method for screening shade tolerant mutant plants via dwarfism. Frontiers in Plant Science, 7, 1–12. 10.3389/fpls.2016.01495 PubMed DOI PMC

Michaud, O. , Fiorucci, A.‐S. , Xenarios, I. , & Fankhauser, C. (2017). Local auxin production underlies a spatially restricted neighbor‐detection response in Arabidopsis. Proceedings of the National Academy of Sciences, 114, 7444–7449. 10.1073/pnas.1702276114 PubMed DOI PMC

Murase, K. , Hirano, Y. , Sun, T. , & Hakoshima, T. (2008). Gibberellin‐induced DELLA recognition by the gibberellin receptor GID1. Nature, 456, 459–463. 10.1038/nature07519 PubMed DOI

Nishimura, T. , Hayashi, K. , Suzuki, H. , Gyohda, A. , Takaoka, C. , Sakaguchi, Y. , … Koshiba, T. (2013). Yucasin is a potent inhibitor of YUCCA, a key enzyme in auxin biosynthesis. The Plant Journal, 77, 352–366. 10.1111/tpj.12399 PubMed DOI

Nozue, K. , Tat, A. V. , Kumar Devisetty, U. , Robinson, M. , Mumbach, M. R. , Ichihashi, Y. , … Maloof, J. N. (2015). Shade avoidance components and pathways in adult plants revealed by phenotypic profiling. PLoS Genetics, 11, e1004953 10.1371/journal.pgen.1004953 PubMed DOI PMC

Oh, E. , Zhu, J.‐Y. , Bai, M.‐Y. , Arenhart, R. A. , Sun, Y. , & Wang, Z.‐Y. (2014). Cell elongation is regulated through a central circuit of interacting transcription factors in the Arabidopsis hypocotyl. Elife, 3, 1–19. 10.7554/eLife.03031 PubMed DOI PMC

Oh, E. , Zhu, J.‐Y. , & Wang, Z.‐Y. (2012). Interaction between BZR1 and PIF4 integrates brassinosteroid and environmental responses. Nature Cell Biology, 14, 802–809. 10.1038/ncb2545 PubMed DOI PMC

Pantazopoulou, C. K. , Bongers, F. J. , Küpers, J. J. , Reinen, E. , Das, D. , Evers, J. B. , … Pierik, R. (2017). Neighbor detection at the leaf tip adaptively regulates upward leaf movement through spatial auxin dynamics. Proceedings of the National Academy of Sciences, 114, 7450–7455. 10.1073/pnas.1702275114 PubMed DOI PMC

Pěnčík, A. , Rolčík, J. , Novák, O. , Magnus, V. , Barták, P. , Buchtík, R. , … Strnad, M. (2009). Isolation of novel indole‐3‐acetic acid conjugates by immunoaffinity extraction. Talanta, 80, 651–655. 10.1016/j.talanta.2009.07.043 PubMed DOI

Reed, J. W. , Foster, K. R. , Morgan, P. W. , & Chory, J. (1996). Phytochrome B affects responsiveness to giberellins in Arabidopsis. Plant Physiology, 112, 337–342. PubMed PMC

Rittenberg, D. , & Foster, G. L. (1940). A new procedure for quantitative analysis by isotope dilution, with application to the determination of amino acids and fatty acids. Journal of Biological Chemistry, 133, 737–744.

Roig‐Villanova, I. , Bou‐Torrent, J. , Galstyan, A. , Carretero‐Paulet, L. , Portolés, S. , Rodríguez‐Concepción, M. , & Martínez‐García, J. F. (2007). Interaction of shade avoidance and auxin responses: A role for two novel atypical bHLH proteins. EMBO Journal, 26, 4756–4767. 10.1038/sj.emboj.7601890 PubMed DOI PMC

Shahnejat‐Bushehri, S. , Tarkowska, D. , Sakuraba, Y. , & Balazadeh, S. (2016). Arabidopsis NAC transcription factor JUB1 regulates GA/BR metabolism and signalling. Nature Plants, 2, 16013 10.1038/nplants.2016.13 PubMed DOI

Symons, G. M. , Schultz, L. , Kerckhoffs, L. H. J. , Davies, N. W. , Gregory, D. , & Reid, J. B. (2002). Uncoupling brassinosteroid levels and de‐etiolation in pea. Physiologia Plantarum, 115, 311–319. https://doi.org/ppl1150219 [pii] PubMed

Tao, Y. , Ferrer, J.‐L. , Ljung, K. , Pojer, F. , Hong, F. , Long, J. A. , … Chory, J. (2008). Rapid synthesis of auxin via a new tryptophan‐dependent pathway is required for shade avoidance in plants. Cell, 133, 164–176. 10.1016/j.cell.2008.01.049 PubMed DOI PMC

Tarkowská, D. , Novák, O. , Oklestkova, J. , & Strnad, M. (2016). The determination of 22 natural brassinosteroids in a minute sample of plant tissue by UHPLC–ESI–MS/MS. Analytical and Bioanalytical Chemistry, 408, 6799–6812. 10.1007/s00216-016-9807-2 PubMed DOI

Urbanová, T. , Tarkowská, D. , Novák, O. , Hedden, P. , & Strnad, M. (2013). Analysis of gibberellins as free acids by ultra performance liquid chromatography‐tandem mass spectrometry. Talanta, 112, 85–94. 10.1016/j.talanta.2013.03.068 PubMed DOI

Young, M. D. , Wakefield, M. J. , Smyth, G. K. , & Oshlack, A. (2010). Gene ontology analysis for RNA‐seq: Accounting for selection bias. Genome Biology, 11, R14 10.1186/gb-2010-11-2-r14 PubMed DOI PMC