Directional transport of the phytohormone auxin is a versatile, plant-specific mechanism regulating many aspects of plant development. The recently identified plant hormones, strigolactones (SLs), are implicated in many plant traits; among others, they modify the phenotypic output of PIN-FORMED (PIN) auxin transporters for fine-tuning of growth and developmental responses. Here, we show in pea and Arabidopsis that SLs target processes dependent on the canalization of auxin flow, which involves auxin feedback on PIN subcellular distribution. D14 receptor- and MAX2 F-box-mediated SL signaling inhibits the formation of auxin-conducting channels after wounding or from artificial auxin sources, during vasculature de novo formation and regeneration. At the cellular level, SLs interfere with auxin effects on PIN polar targeting, constitutive PIN trafficking as well as clathrin-mediated endocytosis. Our results identify a non-transcriptional mechanism of SL action, uncoupling auxin feedback on PIN polarity and trafficking, thereby regulating vascular tissue formation and regeneration.

ARC Centre of Excellence in Plant Energy Biology School of Agriculture Food and Wine Waite Research Precinct The University of Adelaide Glen Osmond SA 5064 Australia

Central European Institute of Technology Mendel University in Brno Zemedelska 1 61300 Brno Czech Republic

Central Laboratories and Research Support Centre of the Region Haná for Biotechnological and Agricultural Research Palacký University Šlechtitelů 27 78371 Olomouc Czech Republic

Department of Applied Genetics and Cell Biology University of Natural Resources and Life Sciences Vienna Muthgasse 18 1190 Wien Austria

Department of Plant Biology Mendel University in Brno Zemedelska 1 61300 Brno Czech Republic

Institute of Science and Technology Klosterneuburg 3400 Austria

Mendel Centre for Plant Genomics and Proteomics Central European Institute of Technology 62500 Brno Czech Republic

State Key Laboratory of Plant Physiology and Biochemistry College of Biological Sciences China Agricultural University Beijing 100193 China

University of Silesia in Katowice Faculty of Natural Sciences Institute of Biology Biotechnology and Environmental Protection Jagiellońska 28 40 032 Katowice Poland

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Adamowski M, Friml J. PIN-dependent auxin transport: action, regulation, and evolution. Plant Cell. 2015;27:20–32. PubMed PMC

Sachs T. The control of the patterned differentiation of vascular tissues. Adv. Bot. Res. 1981;9:151–162.

Bennett T, et al. Connective auxin transport in the shoot facilitates communication between shoot apices. PLoS Biol. 2016;14:e1002446. PubMed PMC

Sauer M, et al. Canalization of auxin flow by Aux/IAA-ARF-dependent feedback regulation of PIN polarity. Genes Dev. 2006;20:2902–2911. PubMed PMC

Balla J, Kalousek P, Reinohl V, Friml J, Prochazka S. Competitive canalization of PIN-dependent auxin flow from axillary buds controls pea bud outgrowth. Plant J. 2011;65:571–577. PubMed

Scarpella E, Marcos D, Friml J, Berleth T. Control of leaf vascular patterning by polar auxin transport. Genes Dev. 2006;20:1015–1027. PubMed PMC

Rolland-Lagan AG, Prusinkiewicz P. Reviewing models of auxin canalization in the context of leaf vein pattern formation in Arabidopsis. Plant J. 2005;44:854–865. PubMed

Sawchuk MG, Scarpella E. Polarity, continuity, and alignment in plant vascular strands. J. Integr. Plant Biol. 2013;55:824–834. PubMed

Robert HS, et al. Local auxin sources orient the apical-basal axis in Arabidopsis embryos. Curr. Biol. 2013;23:2506–2512. PubMed

Robert HS, et al. Maternal auxin supply contributes to early embryo patterning in Arabidopsis. Nat. Plants. 2018;4:548–553. PubMed PMC

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

Heisler MG, et al. Patterns of auxin transport and gene expression during primordium development revealed by live imaging of the Arabidopsis inflorescence meristem. Curr. Biol. 2005;15:1899–1911. PubMed

Rakusová H, et al. Termination of shoot gravitropic responses by auxin feedback on PIN3 polarity. Curr. Biol. 2016;26:3026–3032. PubMed

Wabnik K, et al. Emergence of tissue polarization from synergy of intracellular and extracellular auxin signaling. Mol. Syst. Biol. 2010;6:447. PubMed PMC

Paciorek T, et al. Auxin inhibits endocytosis and promotes its own efflux from cells. Nature. 2005;435:1251–1256. PubMed

Robert S, et al. ABP1 mediates auxin inhibition of clathrin-dependent endocytosis in. Arabidopsis. Cell. 2010;143:111–121. PubMed PMC

Baster P, et al. SCFTIR1/AFB-auxin signalling regulates PIN vacuolar trafficking and auxin fluxes during root gravitropism. EMBO J. 2013;32:260–274. PubMed PMC

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

Dhonukshe P, et al. Clathrin-mediated constitutive endocytosis of PIN auxin efflux carriers in Arabidopsis. Curr. Biol. 2007;17:520–527. PubMed

Wang X, et al. The roles of endomembrane trafficking in plant abiotic stress responses. J. Integr. Plant Biol. 2019;62:55–69. PubMed

Kleine-Vehn J, et al. ARF GEF-dependent transcytosis and polar delivery of PIN auxin carriers in Arabidopsis. Curr. Biol. 2008;18:526–531. PubMed

Kleine-Vehn J, et al. Cellular and molecular requirements for polar PIN targeting and transcytosis in plants. Mol. Plant. 2008;1:1056–1066. PubMed

Marhavý P, et al. Cytokinin controls polarity of PIN1-dependent auxin transport during lateral root organogenesis. Curr. Biol. 2014;24:1031–1037. PubMed

Du J, et al. Somatic embryogenesis receptor kinases control root development mainly via brassinosteroid-independent actions in Arabidopsis thaliana. J. Integr. Plant Biol. 2012;54:388–399. PubMed

Retzer K, et al. Brassinosteroid signaling delimits root gravitropism via sorting of the Arabidopsis PIN2 auxin transporter. Nat. Commun. 2019;10:5516. PubMed PMC

Löfke C, et al. Asymmetric gibberellin signaling regulates vacuolar trafficking of PIN auxin transporters during root gravitropism. Proc. Natl Acad. Sci. USA. 2013;110:3627–3632. PubMed PMC

Du Y, et al. Salicylic acid interferes with clathrin-mediated endocytic protein trafficking. Proc. Natl Acad. Sci. USA. 2013;110:7946–7951. PubMed PMC

Li Y, et al. Root growth adaptation is mediated by PYLs ABA receptor-PP2A protein phosphatase complex. Adv. Sci. (Weinh.) 2019;7:1901455. PubMed PMC

Crawford S, et al. Strigolactones enhance competition between shoot branches by dampening auxin transport. Development. 2010;137:2905–2913. PubMed

Waldie T, McCulloch H, Leyser O. Strigolactones and the control of plant development: lessons from shoot branching. Plant J. 2014;79:607–622. PubMed

Chen J, et al. Non-dormant Axillary Bud 1 regulates axillary bud outgrowth in sorghum. J. Integr. Plant Biol. 2018;60:938–955. PubMed

Sang D, et al. Strigolactones regulate rice tiller angle by attenuating shoot gravitropism through inhibiting auxin biosynthesis. Proc. Natl Acad. Sci. USA. 2014;111:11199–11204. PubMed PMC

Agusti J, et al. Strigolactone signaling is required for auxin-dependent stimulation of secondary growth in plants. Proc. Natl Acad. Sci. USA. 2011;108:20242–20247. PubMed PMC

Rasmussen A, et al. Strigolactones suppress adventitious rooting in Arabidopsis and pea. Plant Physiol. 2012;158:1976–1987. PubMed PMC

Koltai H. Cellular events of strigolactone signalling and their crosstalk with auxin in roots. J. Exp. Bot. 2015;66:4855–4861. PubMed

Kapulnik Y, Koltai H. Fine-tuning by strigolactones of root response to low phosphate. J. Integr. Plant Biol. 2016;58:203–212. PubMed

Shinohara N, Taylor C, Leyser O. Strigolactone can promote or inhibit shoot branching by triggering rapid depletion of the auxin efflux protein PIN1 from the plasma membrane. PLoS Biol. 2013;11:e1001474. PubMed PMC

Gomez-Roldan V, et al. Strigolactone inhibition of shoot branching. Nature. 2008;455:189–194. PubMed

Brewer PB, Dun EA, Gui R, Mason MG, Beveridge CA. Strigolactone Inhibition of Branching Independent of Polar Auxin Transport. Plant Physiol. 2015;168:1820–1829. PubMed PMC

Balla J, et al. Auxin flow-mediated competition between axillary buds to restore apical dominance. Sci. Rep. 2016;6:35955. PubMed PMC

Mazur E, Benková E, Friml J. Vascular cambium regeneration and vessel formation in wounded inflorescence stems of Arabidopsis. Sci. Rep. 2016;6:33754. PubMed PMC

Toh S, Holbrook-Smith D, Stokes ME, Tsuchiya Y, McCourt P. Detection of parasitic plant suicide germination compounds using a high-throughput Arabidopsis HTL/KAI2 strigolactone perception system. Chem. Biol. 2014;21:988–998. PubMed

Dong J, Huang H. Auxin polar transport flanking incipient primordium initiates leaf adaxial-abaxial polarity patterning. J. Integr. Plant Biol. 2018;60:455–464. PubMed

Kang H-G, Fang Y, Singh KB. A glucocorticoid-inducible transcription system causes severe growth defects in Arabidopsis and induces defense-related genes. Plant J. 1999;20:127–133. PubMed

Prát T, et al. WRKY23 is a component of the transcriptional network mediating auxin feedback on PIN polarity. PLoS Genet. 2018;14:e1007177. PubMed PMC

Sancho-Andrés G, et al. Sorting motifs involved in the trafficking and localization of the PIN1 auxin efflux carrier. Plant Physiol. 2016;171:1965–1982. PubMed PMC

Naramoto S, et al. ADP-ribosylation factor machinery mediates endocytosis in plant cells. Proc. Natl Acad. Sci. USA. 2010;107:21890–21895. PubMed PMC

Kitakura S, et al. Clathrin mediates endocytosis and polar distribution of PIN auxin transporters in Arabidopsis. Plant Cell. 2011;23:1920–1931. PubMed PMC

Kleine-Vehn J, et al. Recycling, clustering, and endocytosis jointly maintain PIN auxin carrier polarity at the plasma membrane. Mol. Syst. Biol. 2011;7:540. PubMed PMC

Tanaka H, et al. Cell polarity and patterning by PIN trafficking through early endosomal compartments in Arabidopsis thaliana. PLoS Genet. 2013;9:e1003540. PubMed PMC

Tsuchiya Y, et al. A small-molecule screen identifies new functions for the plant hormone strigolactone. Nat. Chem. Biol. 2010;6:741–749. PubMed

Scaffidi A, et al. Strigolactone hormones and their stereoisomers signal through two related receptor proteins to induce different physiological responses in Arabidopsis. Plant Physiol. 2014;165:1221–1232. PubMed PMC

Hu Z, et al. Strigolactone and cytokinin act antagonistically in regulating rice mesocotyl elongation in darkness. Plant Cell Physiol. 2014;55:30–41. PubMed

Bennett T, et al. Strigolactone regulates shoot development through a core signalling pathway. Biol. Open. 2016;5:1806–1820. PubMed PMC

Hu Q, et al. DWARF14, a receptor covalently linked with the active form of strigolactones, undergoes strigolactone-dependent degradation in rice. Front Plant Sci. 2017;8:1935. PubMed PMC

Jelínková A, et al. Probing plant membranes with FM dyes: tracking, dragging or blocking? Plant J. 2010;61:883–892. PubMed

Konopka CA, Backues SK, Bednarek SY. Dynamics of Arabidopsis dynamin-related protein 1C and a clathrin light chain at the plasma membrane. Plant Cell. 2008;20:1363–1380. PubMed PMC

Leitner J, et al. Lysine63-linked ubiquitylation of PIN2 auxin carrier protein governs hormonally controlled adaptation of Arabidopsis root growth. Proc. Natl Acad. Sci. USA. 2012;109:8322–8327. PubMed PMC

Mazur E, et al. Clathrin-mediated trafficking and PIN trafficking are required for auxin canalization and vascular tissue formation in Arabidopsis. Plant Sci. 2020;293:110414. PubMed

Ljung K, Bhalerao RP, Sandberg G. Sites and homeostatic control of auxin biosynthesis in Arabidopsis during vegetative growth. Plant J. 2001;28:465–474. PubMed

Soundappan I, et al. SMAX1-LIKE/D53 family members enable distinct MAX2-dependent responses to strigolactones and karrikins in Arabidopsis. Plant Cell. 2015;27:3143–3159. PubMed PMC

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

Stirnberg P, van De Sande K, Leyser HM. MAX1 and MAX2 control shoot lateral branching in. Arabidopsis. Dev. 2002;129:1131–1141. PubMed

Umehara M, et al. Inhibition of shoot branching by new terpenoid plant hormones. Nature. 2008;455:195–200. PubMed

Sorefan K, et al. MAX4 and RMS1 are orthologous dioxygenase-like genes that regulate shoot branching in Arabidopsis and pea. Genes Dev. 2003;17:1469–1474. PubMed PMC

Waters MT, et al. Specialisation within the DWARF14 protein family confers distinct responses to karrikins and strigolactones in. Arabidopsis. Dev. 2012;139:1285–1295. PubMed

Aoyama T, Chua NH. A glucocorticoid-mediated transcriptional induction system in transgenic plants. Plant J. 1997;11:605–612. PubMed

Mazur E, Kulik I, Hajný J, Friml J. Auxin canalization and vascular tissue formation by TIR1/AFB-mediated auxin signaling in Arabidopsis. N. Phytol. 2020;226:1375–1383. PubMed PMC

Friml J, Benková E, Mayer U, Palme K, Muster G. Automated whole mount localisation techniques for plant seedlings. Plant J. 2003;34:115–124. PubMed

Abas L, et al. Intracellular trafficking and proteolysis of the Arabidopsis auxin-efflux facilitator PIN2 are involved in root gravitropism. Nat. Cell Biol. 2006;8:249–256. PubMed

GR24, A Synthetic Strigolactone Analog, and Light Affect the Organization of Cortical Microtubules in Arabidopsis Hypocotyl Cells