Strigolactones are plant hormones regulating cytoskeleton-mediated developmental events in roots, such as lateral root formation and elongation of root hairs and hypocotyls. The latter process was addressed herein by the exogenous application of a synthetic strigolactone, GR24, and an inhibitor of strigolactone biosynthesis, TIS108, on hypocotyls of wild-type Arabidopsis and a strigolactone signaling mutant max2-1 (more axillary growth 2-1). Owing to the interdependence between light and strigolactone signaling, the present work was extended to seedlings grown under a standard light/dark regime, or under continuous darkness. Given the essential role of the cortical microtubules in cell elongation, their organization and dynamics were characterized under the conditions of altered strigolactone signaling using fluorescence microscopy methods with different spatiotemporal capacities, such as confocal laser scanning microscopy (CLSM) and structured illumination microscopy (SIM). It was found that GR24-dependent inhibition of hypocotyl elongation correlated with changes in cortical microtubule organization and dynamics, observed in living wild-type and max2-1 seedlings stably expressing genetically encoded fluorescent molecular markers for microtubules. Quantitative assessment of microscopic datasets revealed that chemical and/or genetic manipulation of strigolactone signaling affected microtubule remodeling, especially under light conditions. The application of GR24 in dark conditions partially alleviated cytoskeletal rearrangement, suggesting a new mechanistic connection between cytoskeletal behavior and the light-dependence of strigolactone signaling.

Department of Cell Biology Centre of the Region Haná for Biotechnological and Agricultural Research Faculty of Science Palacký University Olomouc Olomouc Czechia

Department of Chemical Biology and Genetics Centre of the Region Haná for Biotechnological and Agricultural Research Faculty of Science Palacký University Olomouc Olomouc Czechia

Zobrazit více v PubMed

Abbas M., Alabadí D., Blázquez M. A. (2013). Differential growth at the apical hook: all roads lead to auxin. Front. Plant Sci. 4:441. 10.3389/fpls.2013.00441 PubMed DOI PMC

Agusti J., Herold S., Schwarz M., Sanchez P., Ljung K., Dun E. A., et al. (2011). Strigolactone signaling is required for auxin-dependent stimulation of secondary growth in plants. Proc. Natl. Acad. Sci. U.S.A. 108 20242–20247. 10.1073/pnas.1111902108 PubMed DOI PMC

Akiyama K., Matsuzaki K., Hayashi H. (2005). Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435 824–827. 10.1038/nature03608 PubMed DOI

Ambrose C., Wasteneys G. O. (2014). Microtubule initiation from the nuclear surface controls cortical microtubule growth polarity and orientation in Arabidopsis thaliana. Plant Cell Physiol. 55 1636–1645. 10.1093/pcp/pcu094 PubMed DOI PMC

Baral A., Aryal B., Jonsson K., Morris E., Demes E., Takatani S., et al. (2021). External mechanical cues reveal a katanin-independent mechanism behind auxin-mediated tissue bending in plants. Dev. Cell 56 67–80.e3. 10.1016/j.devcel.2020.12.008 PubMed DOI

Bennett T., Liang Y., Seale M., Ward S., Müller D., Leyser O. (2016). Strigolactone regulates shoot development through a core signalling pathway. Biol. Open 5 1806–1820. 10.1242/bio.021402 PubMed DOI PMC

Blume Y. B., Krasylenko Y. A., Yemets A. I. (2017). “The role of the plant cytoskeleton in phytohormone signaling under abiotic and biotic stresses,” in The Mechanism of Plant Hormone Signaling Under Stress, ed. Pandey G. K. (Hoboken, NJ: John Wiley and Sons, Inc; ), 127–185.

Booker J., Auldridge M., Wills S., McCarty D., Klee H., Leyser O. (2004). MAX3/CCD7 is a carotenoid cleavage dioxygenase required for the synthesis of a novel plant signaling molecule. Curr. Biol. 14 1232–1238. 10.1016/j.cub.2004.06.061 PubMed DOI

Boudaoud A., Burian A., Borowska-Wykrȩt D., Uyttewaal M., Wrzalik R., Kwiatkowska D., et al. (2014). FibrilTool, an ImageJ plug-in to quantify fibrillar structures in raw microscopy images. Nat. Protoc. 9 457–463. 10.1038/nprot.2014.024 PubMed DOI

Brewer P. B., Koltai H., Beveridge C. A. (2013). Diverse roles of strigolactones in plant development. Mol. Plant 6 18–28. 10.1093/mp/sss130 PubMed DOI

Burkart G. M., Dixit R. (2019). Microtubule bundling by MAP65-1 protects against severing by inhibiting the binding of katanin. Mol. Biol. Cell 30 1587–1597. 10.1091/mbc.E18-12-0776 PubMed DOI PMC

Chen X. U., Wu S., Liu Z., Friml J. (2016). Environmental and endogenous control of cortical microtubule orientation. Trends Cell Biol. 26 409–419. 10.1016/j.tcb.2016.02.003 PubMed DOI

Cook C. E., Whichard L. P., Turner B., Wall M. E., Egley G. H. (1966). Germination of witchweed (Striga lutea Lour.): isolation and properties of a potent stimulant. Science 154 1189–1190. 10.1126/science.154.3753.1189 PubMed DOI

De Cuyper C., Struk S., Braem L., Gevaert K., De Jaeger G., Goormachtig S. (2017). Strigolactones, karrikins and beyond. Plant Cell Environ. 40 1691–1703. 10.1111/pce.12996 PubMed DOI

de Saint Germain A., Ligerot Y., Dun E. A., Pillot J. P., Ross J. J., Beveridge C. A., et al. (2013). Strigolactones stimulate internode elongation independently of gibberellins. Plant Physiol. 163 1012–1025. 10.1104/pp.113.220541 PubMed DOI PMC

Delaux P. M., Xie X., Timme R. E., Puech-Pages V., Dunand C., Lecompte E., et al. (2012). Origin of strigolactones in the green lineage. New Phytol. 195 857–871. 10.1111/j.1469-8137.2012.04209.x PubMed DOI

Deng J., Wang X., Liu Z., Mao T. (2021). The microtubule-associated protein WDL4 modulates auxin distribution to promote apical hook opening in Arabidopsis. Plant Cell 17:koab080. 10.1093/plcell/koab080 PubMed DOI PMC

Domagalska M. A., Leyser O. (2011). Signal integration in the control of shoot branching. Nat. Rev. Mol. Cell Biol. 12 211–221. 10.1038/nrm3088 PubMed DOI

Elliott A., Shaw S. L. (2018). A cycloheximide-sensitive step in transverse microtubule array patterning. Plant Physiol. 178 684–698. 10.1104/pp.18.0067 PubMed DOI PMC

Fischer K., Schopfer P. (1997). Separation of photolabile-phytochrome and photostable-phytochrome actions on growth and microtubule orientation in maize coleoptiles (A physiological approach). Plant Physiol. 115 511–518. 10.1104/pp.115.2.511 PubMed DOI PMC

Foo E., Ferguson B. J., Reid J. B. (2014). The potential roles of strigolactones and brassinosteroids in the autoregulation of nodulation pathway. Ann. Bot. 113 1037–1045. 10.1093/aob/mcu030 PubMed DOI PMC

Foo E., Yoneyama K., Hugill C. J., Quittenden L. J., Reid J. B. (2013). Strigolactones and the regulation of pea symbioses in response to nitrate and phosphate deficiency. Mol. Plant 6 76–87. 10.1093/mp/sss115 PubMed DOI

Galen C., Rabenold J. J., Liscum E. (2007). Light-sensing in roots. Plant Signal. Behav. 2 106–108. 10.4161/psb.2.2.3638 PubMed DOI PMC

Gomez-Roldan V., Fermas S., Brewer P. B., Puech-Pagès V., Dun E. A., Pillot J.-P., et al. (2008). Strigolactone inhibition of shoot branching. Nature 455 189–194. 10.1038/nature07271 PubMed DOI

Ha C. V., Leyva-Gonzalez M. A., Osakabe Y., Tran U. T., Nishiyama R., Watanabe Y., et al. (2014). Positive regulatory role of strigolactone in plant responses to drought and salt stress. Proc. Natl. Acad. Sci. U.S.A. 111 851–856. 10.1073/pnas.1322135111 PubMed DOI PMC

Halat L., Gyte K., Wasteneys G. (2020). The microtubule-associated protein CLASP is translationally regulated in light-dependent root apical meristem growth. Plant Physiol. 184 2154–2167. 10.1104/pp.20.00474 PubMed DOI PMC

Halouzka R., Zeljković S.Ć, Klejdus B., Tarkowski P. (2020). Analytical methods in strigolactone research. Plant Methods 16:76. 10.1186/s13007-020-00616-2 PubMed DOI PMC

Hasan M. N., Choudhry H., Razvi S. S., Moselhy S. S., Kumosani T. A., Zamzami M. A., et al. (2018). Synthetic strigolactone analogues reveal anti-cancer activities on hepatocellular carcinoma cells. Bioorg. Med. Chem. Lett. 28 1077–1083. 10.1016/j.bmcl.2018.02.016 PubMed DOI

Hoffmann B., Proust H., Belcram K., Labrune C., Boyer F.-D., Rameau C., et al. (2014). strigolactones inhibit caulonema elongation and cell division in the moss Physcomitrella patens. PLoS One 9:e99206. 10.1371/journal.pone.0099206 PubMed DOI PMC

Higaki T., Kutsuna N., Sano T., Kondo N., Hasezawa S. (2010). Quantification and cluster analysis of actin cytoskeletal structures in plant cells: role of actin bundling in stomatal movement during diurnal cycles in Arabidopsis guard cells. Plant J. 61 156–165. 10.1111/j.1365-313X.2009.04032.x PubMed DOI

Ho-Plágaro T., Huertas R., Tamayo-Navarrete M. I., Blancaflor E., Gavara N., García-Garrido J. M. (2021). A novel putative microtubule-associated protein is involved in arbuscule development during arbuscular mycorrhiza formation. Plant Cell Physiol. 62 306–320. 10.1093/pcp/pcaa159 PubMed DOI PMC

Hu Q., Zhang S., Huang B. (2019). Strigolactones promote leaf elongation in tall fescue through upregulation of cell cycle genes and downregulation of auxin transport genes in tall fescue under different temperature regimes. Int. J. Mol. Sci. 20:1836. 10.3390/ijms20081836 PubMed DOI PMC

Hu Z., Yan H., Yang J., Yamaguchi S., Maekawa M., Takamure I., et al. (2010). Strigolactones negatively regulate mesocotyl elongation in rice during germination and growth in darkness. Plant Cell Physiol. 51 1136–1142. 10.1093/pcp/pcq075 PubMed DOI PMC

Ito S., Kitahata N., Umehara M., Hanada A., Kato A., Ueno K., et al. (2010). A new lead chemical for strigolactone biosynthesis inhibitors. Plant Cell Physiol. 51 1143–1150. 10.1093/pcp/pcq077 PubMed DOI PMC

Ito S., Umehara M., Hanada A., Kitahata N., Hayase H., Yamaguchi S., et al. (2011). Effects of triazole derivatives on strigolactone levels and growth retardation in rice. PLoS One 6:e21723. 10.1371/journal.pone.0021723 PubMed DOI PMC

Ito S., Umehara M., Hanada A., Yamaguchi S., Asami T. (2013). Effects of strigolactone-biosynthesis inhibitor TIS108 on Arabidopsis. Plant Signal. Behav. 5:e24193. 10.4161/psb.24193 PubMed DOI PMC

Ivakov A., Persson S. (2013). Plant cell shape: modulators and measurements. Front. Plant Sci. 4:439. 10.3389/fpls.2013.00439 PubMed DOI PMC

Jensen P. J., Hangarter R. P., Estelle M. (1998). Auxin transport is required for hypocotyl elongation in light-grown but not dark-grown Arabidopsis. Plant Physiol. 116 455–462. 10.1104/pp.116.2.455 PubMed DOI PMC

Jia K. P., Luo Q., He S. B., Lu X. D., Yang H. Q. (2014). Strigolactone-regulated hypocotyl elongation is dependent on cryptochrome and phytochrome signaling pathways in Arabidopsis. Mol. Plant 7 528–540. 10.1093/mp/sst093 PubMed DOI

Jiang L., Liu X., Xiong G., Liu H., Chen F., Wang L., et al. (2013). DWARF 53 acts as a repressor of strigolactone signalling in rice. Nature 504 401–405. 10.1038/nature12870 PubMed DOI PMC

Jiang L., Matthys C., Marquez-Garcia B., De Cuyper C., Smet L., De Keyser A., et al. (2016). Strigolactones spatially influence lateral root development through the cytokinin signaling network. J. Exp. Bot. 67 379–389. 10.1093/jxb/erv478 PubMed DOI PMC

Kapulnik Y., Delaux P. M., Resnick N., Mayzlish-Gati E., Wininger S., Bhattacharya C., et al. (2011). Strigolactones affect lateral root formation and root-hair elongation in Arabidopsis. Planta 233 209–216. 10.1007/s00425-010-1310-y PubMed DOI

Kartasalo K., Pölönen R. P., Ojala M., Rasku J., Lekkala J., Aalto-Setälä K., et al. (2015). CytoSpectre: a tool for spectral analysis of oriented structures on cellular and subcellular levels. BMC Bioinformatics 16:344. 10.1186/s12859-015-0782-y PubMed DOI PMC

Kawada K., Takahashi I., Arai M., Sasaki Y., Asami T., Yajima S., et al. (2019). Synthesis and biological evaluation of novel triazole derivatives as strigolactone biosynthesis inhibitors. J. Agric. Food Chem. 67 6143–6149. 10.1021/acs.jafc.9b01276 PubMed DOI

Kawada K., Uchida Y., Takahashi I., Nomura T., Sasaki Y., Asami T., et al. (2020). Triflumizole as a novel lead compound for strigolactone biosynthesis inhibitor. Molecules 25:5525. 10.3390/molecules25235525 PubMed DOI PMC

Khanna R., Li J., Tseng T. S., Schroeder J. I., Ehrhardt D. W., Briggs W. R. (2014). COP1 jointly modulates cytoskeletal processes and electrophysiological responses required for stomatal closure. Mol. Plant 7 1441–1454. 10.1093/mp/ssu065 PubMed DOI PMC

Kohlen W., Charnikhova T., Liu Q., Bours R., Domagalska M. A., Beguerie S., et al. (2011). Strigolactones are transported through the xylem and play a key role in shoot architectural response to phosphate deficiency in non-arbuscular mycorrhizal host Arabidopsis. Plant Physiol. 155 974–987. 10.1104/pp.110.164640 PubMed DOI PMC

Koltai H. (2014). Receptors, repressors, PINs: a playground for strigolactone signaling. Trends Plant Sci. 19 727–733. 10.1016/j.tplants.2014.06.008 PubMed DOI

Komis G., Apostolakos P., Galatis B. (2002). Hyperosmotic stress−induced actin filament reorganization in leaf cells of Chlorophyton comosum. J. Exp. Bot. 53 1699–1710. 10.1093/jxb/erf018 PubMed DOI

Komis G., Mistrik M., Šamajová O., Doskočilová A., Ovečka M., Illés P., et al. (2014). Dynamics and organization of cortical microtubules as revealed by superresolution structured illumination microscopy. Plant Physiol. 165 129–148. 10.1104/pp.114.238477 PubMed DOI PMC

Komis G., Mistrik M., Šamajová O., Ovečka M., Bartek J., Šamaj J. (2015). Superresolution live imaging of plant cells using structured illumination microscopy. Nat. Protoc. 10 1248–1263. 10.1038/nprot.2015.083 PubMed DOI

Koren D., Resnick N., Gati E. M., Belausov E., Weininger S., Kapulnik Y., et al. (2013). Strigolactone signaling in the endodermis is sufficient to restore root responses and involves SHORT HYPOCOTYL 2 (SHY2) activity. New Phytol. 198 866–874. 10.1111/nph.12189 PubMed DOI

Kumar M., Pandya-Kumar N., Dam A., Haor H., Mayzlish-Gati E., Belausov E., et al. (2015a). Arabidopsis response to low-phosphate conditions includes active changes in actin filaments and PIN2 polarization and is dependent on strigolactone signalling. J. Exp. Bot. 66 1499–1510. 10.1093/jxb/eru513 PubMed DOI PMC

Kumar M., Pandya-Kumar N., Kapulnik Y., Koltai H. (2015b). Strigolactone signaling in root development and phosphate starvation. Plant Signal. Behav. 10:e1045174. 10.1080/15592324.2015.1045174 PubMed DOI PMC

Landrein B., Hamant O. (2013). How mechanical stress controls microtubule behavior and morphogenesis in plants: history, experiments and revisited theories. Plant J. 75 324–338. 10.1111/tpj.12188 PubMed DOI

Li W., Nguyen K. H., Watanabe Y., Yamaguchi S., Tran L. S. (2016). OaMAX2 of Orobanche aegyptiaca and Arabidopsis AtMAX2 share conserved functions in both development and drought responses. Biochem. Biophys. Res. Commun. 478 521–526. 10.1016/j.bbrc.2016.07.065 PubMed DOI

Lian N., Liu X., Wang X., Zhou Y., Li H., Li J., et al. (2017). COP1 mediates dark-specific degradation of microtubule-associated protein WDL3 in regulating Arabidopsis hypocotyl elongation. Proc. Natl. Acad. Sci. U.S.A. 114 12321–12326. 10.1073/pnas.1708087114 PubMed DOI PMC

Lindeboom J. J., Nakamura M., Hibbel A., Shundyak K., Gutierrez R., Ketelaar T., et al. (2013). A mechanism for reorientation of cortical microtubule arrays driven by microtubule severing. Science 342:1245533. 10.1126/science.1245533 PubMed DOI

Liu H. (2015). Comparing Welch’s ANOVA, A Kruskal-Wallis Test and Traditional ANOVA in Case of Heterogeneity of Variance. Available online at: https://scholarscompass.vcu.edu/cgi/viewcontent.cgi?article=5026&context=etd (accessed May 2020).

Liu Q., Zhang Y., Matusova R., Charnikhova T., Amini M., Jamil M., et al. (2014). Striga hermonthica MAX2 restores branching but not the very low fluence response in the Arabidopsis thaliana max2 mutant. New Phytol. 202 531–541. 10.1111/nph.12692 PubMed DOI

Liu X., Qin T., Ma Q., Sun J., Liu Z., Yuan M., et al. (2013). Light-regulated hypocotyl elongation involves proteasome-dependent degradation of the microtubule regulatory protein WDL3 in Arabidopsis. Plant Cell 25 1740–1755. 10.1105/tpc.113.112789 PubMed DOI PMC

Locascio A., Blázquez M. A., Alabadí D. (2013). Dynamic regulation of cortical microtubule organization through prefoldin-DELLA interaction. Curr. Biol. 23 804–809. 10.1016/j.cub.2013.03.053 PubMed DOI

Lopez-Obando M., de Villiers R., Hoffmann B., Ma L., de Saint Germain A., Kossmann J., et al. (2018). Physcomitrella patens MAX2 characterization suggests an ancient role for this F-box protein in photomorphogenesis rather than strigolactone signalling. New Phytol. 219 743–756. 10.1111/nph.15214 PubMed DOI

Louveaux M., Rochette S., Beauzamy L., Boudaoud A., Hamant O. (2016). The impact of mechanical compression on cortical microtubules in Arabidopsis: a quantitative pipeline. Plant J. 88 328–342. 10.1111/tpj.13290 PubMed DOI PMC

Ma Q., Sun J., Mao T. (2016). Microtubule bundling plays a role in ethylene-mediated cortical microtubule reorientation in etiolated Arabidopsis hypocotyls. J. Cell Sci. 15 2043–2051. 10.1242/jcs.184408 PubMed DOI

Ma Q., Wang X., Sun J., Mao T. (2018). Coordinated regulation of hypocotyl cell elongation by light and ethylene through a microtubule destabilizing protein. Plant Physiol. 176 678–690. 10.1104/pp.17.01109 PubMed DOI PMC

Marc J., Granger C. L., Brincat J., Fisher D. D., Kao, Th, McCubbin A. G., et al. (1998). A GFP-MAP4 reporter gene for visualizing cortical microtubule rearrangements in living epidermal cells. Plant Cell 10 1927–1940. 10.1105/tpc.10.11.1927 PubMed DOI PMC

Mayzlish-Gati E., Laufer D., Grivas C. F., Shaknof J., Sananes A., Bier A., et al. (2015). Strigolactone analogs act as new anti-cancer agents in inhibition of breast cancer in xenograft model. Cancer Biol. Ther. 16 1682–1688. 10.1080/15384047.2015.1070982 PubMed DOI PMC

McAdam E. L., Hugill C., Fort S., Samain E., Cottaz S., Davies N. W., et al. (2017). Determining the site of action of strigolactones during nodulation. Plant Physiol. 175 529–542. 10.1104/pp.17.00741 PubMed DOI PMC

Meijering E. (2010). Neuron tracing in perspective. Cytometry A 77 693–704. 10.1002/cyto.a.20895 PubMed DOI

Min Z., Li R., Chen L., Zhang Y., Li Z., Liu M., et al. (2019). Alleviation of drought stress in grapevine by foliar-applied strigolactones. Plant Physiol. Biochem. 135 99–110. 10.1016/j.plaphy.2018.11.037 PubMed DOI

Montesinos J. C., Abuzeineh A., Kopf A., Juanes-Garcia A., Ötvös K., Petrášek J., et al. (2020). Phytohormone cytokinin guides microtubule dynamics during cell progression from proliferative to differentiated stage. EMBO J. 39:e104238. 10.15252/embj.2019104238 PubMed DOI PMC

Nelson D. C., Scaffidi A., Dun E. A., Waters M. T., Flematti G. R., Dixon K. W., et al. (2011). F-box protein MAX2 has dual roles in karrikin and strigolactone signaling in Arabidopsis thaliana. Proc. Natl. Acad. Sci. U.S.A. 108 8897–8902. 10.1073/pnas.1100987108 PubMed DOI PMC

Pan X., Fang L., Liu J., Senay-Aras B., Lin W., Zheng S., et al. (2020). Auxin-induced signaling protein nanoclustering contributes to cell polarity formation. Nat. Commun. 11:3914. 10.1038/s41467-020-17602-w PubMed DOI PMC

Pandya-Kumar N., Shema R., Kumar M., Mayzlish-Gati E., Levy D., Zemach H., et al. (2014). Strigolactone analog GR24 triggers changes in PIN2 polarity, vesicle trafficking and actin filament architecture. New Phytol. 202 1184–1196. 10.1111/nph.12744 PubMed DOI

Podolec R., Ulm R. (2018). Photoreceptor-mediated regulation of the COP1/SPA E3 ubiquitin ligase. Curr. Opin. Plant Biol. 45 18–25. 10.1016/j.pbi.2018.04.018 PubMed DOI

Roumeliotis E., Kloosterman B., Oortwijn M., Kohlen W., Bouwmeester H. J., Visser R. G. F., et al. (2012). The effects of auxin and strigolactones on tuber initiation and stolon architecture in potato. J. Exp. Bot. 63 4539–4547. 10.1093/jxb/ers132 PubMed DOI PMC

Ruan Y., Wasteneys G. O. (2014). CLASP: a microtubule-based integrator of the hormone-mediated transitions from cell division to elongation. Curr. Opin. Plant Biol. 22 149–158. 10.1016/j.pbi.2014.11.003 PubMed DOI

Ruyter-Spira C., Kohlen W., Charnikhova T., van Zeijl A., van Bezouwen L., de Ruijter N., et al. (2011). Physiological effects of the synthetic strigolactone analog GR24 on root system architecture in Arabidopsis: another belowground role for strigolactones? Plant Physiol. 155 721–734. 10.1104/pp.110.166645 PubMed DOI PMC

Ruyter-Spira C., Al-Babili S., van der Krol S., Bouwmeester H. (2013). The biology of strigolactones. Trends Plant Sci. 18 72–83. 10.1016/j.tplants.2012.10.003 PubMed DOI

Sambade A., Pratap A., Buschmann H., Morris R. J., Lloyd C. (2012). The influence of light on microtubule dynamics and alignment in the Arabidopsis hypocotyl. Plant Cell 24 192–201. 10.1105/tpc.111.093849 PubMed DOI PMC

Sampathkumar A., Krupinski P., Wightman R., Milani P., Berquand A., Boudaoud A., et al. (2014). Subcellular and supracellular mechanical stress prescribes cytoskeleton behavior in Arabidopsis cotyledon pavement cells. eLife 3:e01967. 10.7554/eLife.01967 PubMed DOI PMC

Scaffidi A., Waters M. T., Sun Y. K., Skelton B. W., Dixon K. W., Ghisalberti E. L., et al. (2014). Strigolactone hormones and their stereoisomers signal through two related receptor proteins to induce different physiological responses in Arabidopsis. Plant Physiol. 165 1221–1232. 10.1104/pp.114.240036 PubMed DOI PMC

Schneider C. A., Rasband W. S., Eliceiri K. W. (2012). NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9 671–675. 10.1038/nmeth.2089 PubMed DOI PMC

Seto Y., Yasui R., Kameoka H., Tamiru M., Cao M., Terauchi R., et al. (2019). Strigolactone perception and deactivation by a hydrolase receptor DWARF14. Nat. Commun. 10:191. PubMed PMC

Sheerin D. J., Hiltbrunner A. (2017). Molecular mechanisms and ecological function of far-red light signalling. Plant Cell Environ. 40 2509–2529. 10.1111/pce.12915 PubMed DOI

Shen H., Luong P., Huq E. (2007). The F-box protein MAX2 functions as a positive regulator of photomorphogenesis in Arabidopsis. Plant Physiol. 145 1471–1483. 10.1104/pp.107.107227 PubMed DOI PMC

Shinohara N., Taylor C., Leyser O. (2013). Strigolactone can promote or inhibit shoot branching by triggering rapid depletion of the auxin efflux protein PIN1 from the plasma membrane. PLoS Biol. 11:e1001474. 10.1371/journal.pbio.1001474 PubMed DOI PMC

Shoji T., Suzuki K., Abe T., Kaneko Y., Shi H., Zhu J. K., et al. (2006). Salt stress affects cortical microtubule organization and helical growth in Arabidopsis. Plant Cell Physiol. 47 1158–1168. 10.1093/pcp/pcj090 PubMed DOI

Soundappan I., Bennett T., Morffy N., Liang Y., Stanga J. P., Abbas A., et al. (2015). SMAX1-LIKE/D53 family members enable distinct MAX2-dependent responses to strigolactones and karrikins in Arabidopsis. Plant Cell 27 3143–3159. 10.1105/tpc.15.00562 PubMed DOI PMC

Stanga J. P., Smith S. M., Briggs W. R., Nelson D. C. (2013). SUPPRESSOR OF MORE AXILLARY GROWTH2 1 controls seed germination and seedling development in Arabidopsis. Plant Physiol. 163 318–330. 10.1104/pp.113.221259 PubMed DOI PMC

Stirnberg P., van de Sande K., Leyser H. M. O. (2002). MAX1 and MAX2 control shoot lateral branching in Arabidopsis. Development 129 1131–1141. PubMed

Struk S., De Cuyper C., Jacobs A., Braem L., Walton A., De Keyser A., et al. (2021). Unraveling the MAX2 protein network in Arabidopsis thaliana: identification of the protein phosphatase PAPP5 as a novel MAX2 interactor. Mol. Cell. Proteom. 20:100040. 10.1074/mcp.RA119.001766 PubMed DOI PMC

Sun H., Xu F., Guo X., Wu D., Zhang X., Lou M., et al. (2019). A strigolactone signal inhibits secondary lateral root development in rice. Front. Plant Sci. 10:1527. 10.3389/fpls.2019.01527 PubMed DOI PMC

Sun S., Wang T., Wang L., Li X., Jia Y., Liu C., et al. (2018). Natural selection of a GSK3 determines rice mesocotyl domestication by coordinating strigolactone and brassinosteroid signaling. Nat. Commun. 9:2523. 10.1038/s41467-018-04952-9 PubMed DOI PMC

Swarbreck S. M., Mohammad-Sidik A., Davies J. M. (2020). Common components of the strigolactone and karrikin signaling pathways suppress root branching in Arabidopsis thaliana. Plant Physiol. 184 18–22. 10.1104/pp.19.00687 PubMed DOI PMC

Takatani S., Verger S., Okamoto T., Takahashi T., Hamant O., Motose H. (2020). Microtubule response to tensile stress is curbed by NEK6 to buffer growth variation in the Arabidopsis hypocotyl. Curr. Biol. 30 1491–1503. 10.1016/j.cub.2020.02.024 PubMed DOI

Taulera Q., Lauressergues D., Martin K., Cadoret M., Servajean V., Boyer F.-D., et al. (2020). Initiation of arbuscular mycorrhizal symbiosis involves a novel pathway independent from hyphal branching. Mycorrhiza 30 491–501. 10.1007/s00572-020-00965-9 PubMed DOI

Toh S., McCourt P., Tsuchiya Y. (2012). HY5 is involved in strigolactone-dependent seed germination in Arabidopsis. Plant Signal. Behav. 7 556–558. 10.4161/psb.19839 PubMed DOI PMC

True J. H., Shaw S. L. (2020). Exogenous auxin induces transverse microtubule arrays through TRANSPORT INHIBITOR RESPONSE1/AUXIN SIGNALING F-BOX receptors. Plant Physiol. 182 892–907. 10.1104/pp.19.00928 PubMed DOI PMC

Tsuchiya Y., Vidaurre D., Toh S., Hanada A., Nambara E., Kamiya Y., et al. (2010). A small-molecule screen identifies new functions for the plant hormone strigolactone. Nat. Chem. Biol. 6 741–749. 10.1038/nchembio.435 PubMed DOI

Ueda H., Kusaba M. (2015). Strigolactone regulates leaf senescence in concert with ethylene in Arabidopsis. Plant Physiol. 169 138–147. 10.1104/pp.15.00325 PubMed DOI PMC

Ueda K., Sakaguchi S., Kumagai F., Hasezawa S., Quader H., Kristen U. (2003). Development and disintegration of phragmoplasts in living cultured cells of a GFP:: TUA6 transgenic Arabidopsis thaliana plant. Protoplasma 220 111–118. 10.1007/s00709-002-0049-0 PubMed DOI

Umehara M., Hanada A., Yoshida S., Akiyama K., Arite T., Takeda-Kamiya N., et al. (2008). Inhibition of shoot branching by new terpenoid plant hormones. Nature 455 195–200. 10.1038/nature07272 PubMed DOI

van Zeijl A., Liu W., Xiao T. T., Kohlen W., Yang W. C., Bisseling T., et al. (2015). The strigolactone biosynthesis gene DWARF27 is co-opted in rhizobium symbiosis. BMC Plant Biol. 15:260. 10.1186/s12870-015-0651-x PubMed DOI PMC

Vavrdová T., Křenek P., Ovečka M., Šamajová O., Floková P., Illešová P., et al. (2020). Complementary superresolution visualization of composite plant microtubule organization and dynamics. Front. Plant Sci. 11:693. 10.3389/fpls.2020.00693 PubMed DOI PMC

Villaécija-Aguilar J. A., Hamon-Josse M., Carbonnel S., Kretschmar A., Schmid C., Dawid C., et al. (2019). SMAX1/SMXL2 regulate root and root hair development downstream of KAI2-mediated signalling in Arabidopsis. PLoS Genet. 15:e1008327. 10.1371/journal.pgen.1008327 PubMed DOI PMC

Vineyard L., Elliott A., Dhingra S., Lucas J. R., Shaw S. L. (2013). Progressive transverse microtubule array organization in hormone-induced Arabidopsis hypocotyl cells. Plant Cell 25 662–676. 10.1105/tpc.112.107326 PubMed DOI PMC

Wan Y., Yokawa K., Baluška F. (2019). Arabidopsis roots and light: complex interactions. Mol. Plant 12 1428–1430. 10.1016/j.molp.2019.10.001 PubMed DOI

Wang C., Zhang L., Yuan M., Ge Y., Liu Y., Fan J., et al. (2010). The microfilament cytoskeleton plays a vital role in salt and osmotic stress tolerance in Arabidopsis. Plant Biol. 12 70–78. 10.1111/j.1438-8677.2009.00201.x PubMed DOI

Wang L., Hart B. E., Khan G. A., Cruz E. R., Persson S., Wallace I. S. (2020a). Associations between phytohormones and cellulose biosynthesis in land plants. Ann. Bot. 126 807–824. 10.1093/aob/mcaa121 PubMed DOI PMC

Wang L., Wang B., Jiang L., Liu X., Li X., Lu Z., et al. (2015). Strigolactone signaling in Arabidopsis regulates shoot development by targeting d53-like SMXL repressor proteins for ubiquitination and degradation. Plant Cell 27 3128–3142. 10.1105/tpc.15.00605 PubMed DOI PMC

Wang L., Xu Q., Yu H., Ma H., Li X., Yang J., et al. (2020b). Strigolactone and karrikin signaling pathways elicit ubiquitination and proteolysis of SMXL2 to regulate hypocotyl elongation in Arabidopsis. Plant Cell 32 2251–2270. 10.1105/tpc.20.00140 PubMed DOI PMC

Wang L., Xu Q., Yu H., Ma H., Li X., Yang J., et al. (2020c). Submergence stress-induced hypocotyl elongation through ethylene signaling-mediated regulation of cortical microtubules in Arabidopsis. J. Exp. Bot. 71 1067–1077. 10.1093/jxb/erz453 PubMed DOI

Wang X., Zhang J., Yuan M., Ehrhardt D. W., Wang Z., Mao T. (2012). Arabidopsis microtubule destabilizing protein40 is involved in brassinosteroid regulation of hypocotyl elongation. Plant Cell 24 4012–4025. 10.1105/tpc.112.103838 PubMed DOI PMC

Wang Y., Sun S., Zhu W., Jia K., Yang H., Wang X. (2013). Strigolactone/MAX2-induced degradation of brassinosteroid transcriptional effector BES1 regulates shoot branching. Dev. Cell 27 681–688. 10.1016/j.devcel.2013.11.010 PubMed DOI

Waters M. T., Scaffidi A., Sun Y. K., Flematti G. R., Smith S. M. (2014). The karrikin response system of Arabidopsis. Plant J. 79 623–631. 10.1111/tpj.12430 PubMed DOI

Waters M. T., Smith S. M. (2013). KAI2-and MAX2-mediated responses to karrikins and strigolactones are largely independent of HY5 in Arabidopsis seedlings. Mol. Plant 6 63–75. 10.1093/mp/sss127 PubMed DOI

Wigchert S. C. M., Kuiper E., Boelhouwer G. J., Nefkens G. H. L., Verkleij J. A. C., Zwanenburg B. (1999). Dose response of seeds of the parasitic weeds Striga and Orobanche toward the synthetic germination stimulants GR 24 and Nijmegen 1. J. Agric. Food Chem. 47 1705–1710. 10.1021/jf981006z PubMed DOI

Xie Y., Liu Y., Ma M., Zhou Q., Zhao Y., Zhao B., et al. (2020). Arabidopsis FHY3 and FAR1 integrate light and strigolactone signaling to regulate branching. Nat. Commun. 11:1955. 10.1038/s41467-020-15893-7 PubMed DOI PMC

Yao L., Zheng Y., Zhu Z. (2017). Jasmonate suppresses seedling soil emergence in Arabidopsis thaliana. Plant Signal. Behav. 12:e1330239. 10.1080/15592324.2017.1330239 PubMed DOI PMC

Yoneyama K., Xie X., Kusumoto D., Sekimoto H., Sugimoto Y., Takeuchi Y., et al. (2007). Nitrogen deficiency as well as phosphorus deficiency in sorghum promotes the production and exudation of 5-deoxystrigol, the host recognition signal for arbuscular mycorrhizal fungi and root parasites. Planta 227 125–132. 10.1007/s00425-007-0600-5 PubMed DOI

Yu Y., Huang R. (2017). Integration of ethylene and light signaling affects hypocotyl growth in Arabidopsis. Front. Plant Sci. 8:57. 10.3389/fpls.2017.00057 PubMed DOI PMC

Zandomeni K., Schopfer P. (1993). Reorientation of microtubules at the outer epidermal wall of maize coleoptiles by phytochrome, blue-light photoreceptor, and auxin. Protoplasma 173 103–112. 10.1007/BF01378999 DOI

Zhang J., Mazur E., Balla J., Gallei M., Kalousek P., Medved’ová Z., et al. (2020). Strigolactones inhibit auxin feedback on PIN-dependent auxin transport canalization. Nat. Commun. 11:3508. 10.1038/s41467-020-17252-y PubMed DOI PMC

Zhong S., Shi H., Xue C., Wei N., Guo H., Deng X. W. (2014). Ethylene-orchestrated circuitry coordinates a seedling’s response to soil cover and etiolated growth. Proc. Natl. Acad. Sci. U.S.A. 111 3913–3920. 10.1073/pnas.1402491111 PubMed DOI PMC

Zhu Q., Gallemí M., Pospíšil J., Žádníková P., Strnad M., Benková E. (2019). Root gravity response module guides differential growth determining both root bending and apical hook formation in Arabidopsis. Development 12:dev175919. 10.1242/dev.175919 PubMed DOI

Knockout of MITOGEN-ACTIVATED PROTEIN KINASE 3 causes barley root resistance against Fusarium graminearum