Advanced transcriptome sequencing has revealed that the majority of eukaryotic genes undergo alternative splicing (AS). Nonetheless, little effort has been dedicated to investigating the functional relevance of particular splicing events, even those in the key developmental and hormonal regulators. Combining approaches of genetics, biochemistry and advanced confocal microscopy, we describe the impact of alternative splicing on the PIN7 gene in the model plant Arabidopsis thaliana. PIN7 encodes a polarly localized transporter for the phytohormone auxin and produces two evolutionarily conserved transcripts, PIN7a and PIN7b. PIN7a and PIN7b, differing in a four amino acid stretch, exhibit almost identical expression patterns and subcellular localization. We reveal that they are closely associated and mutually influence each other's mobility within the plasma membrane. Phenotypic complementation tests indicate that the functional contribution of PIN7b per se is minor, but it markedly reduces the prominent PIN7a activity, which is required for correct seedling apical hook formation and auxin-mediated tropic responses. Our results establish alternative splicing of the PIN family as a conserved, functionally relevant mechanism, revealing an additional regulatory level of auxin-mediated plant development.

Department of Plant Biotechnology and Bioinformatics Ghent University Ghent 9052 Belgium

Functional Genomics and Proteomics of Plants Central European Institute of Technology and National Centre for Biomolecular Research Masaryk University Brno 62500 Czech Republic

Institute of Biotechnology University of Helsinki Helsinki 00014 Finland

Institute of Organic Chemistry and Biochemistry Czech Academy of Sciences Prague 6 166 10 Czech Republic

Institute of Science and Technology Klosterneuburg 3400 Austria

Laboratory of Hormonal Regulations in Plants Institute of Experimental Botany Czech Academy of Sciences Prague 16502 Czech Republic

VIB Center for Plant Systems Biology Ghent 9052 Belgium

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Abas L, Kolb M, Stadlmann J, Janacek DP, Lukic K, Schwechheimer C, Sazanov LA, Mach L, Friml J, Hammes UZ. 2021. Naphthylphthalamic acid associates with and inhibits PIN auxin transporters. Proceedings of the National Academy of Sciences, USA 118: e2020857118.

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

Barbosa ICR, Hammes UZ, Schwechheimer C. 2018. Activation and polarity control of PIN-FORMED auxin transporters by phosphorylation. Trends in Plant Science 23: 523-538.

Bashandy H, Jalkanen S, Teeri TH. 2015. Within leaf variation is the largest source of variation in agroinfiltration of Nicotiana benthamiana. Plant Methods 11: 47.

Bazin J, Romero N, Rigo R, Charon C, Blein T, Ariel F, Crespi M. 2018. Nuclear Speckle RNA binding proteins remodel alternative splicing and the non-coding Arabidopsis transcriptome to regulate a cross-talk between auxin and immune responses. Frontiers in Plant Science 9: 1209.

Bennett SRM, Alvarez J, Bossinger G, Smyth DR. 1995. Morphogenesis in pinoid mutants of Arabidopsis thaliana. The Plant Journal 8: 505-520.

Bennett T, Brockington SF, Rothfels C, Graham SW, Stevenson D, Kutchan T, Rolf M, Thomas P, Wong G-S, Leyser O et al. 2014. Paralogous radiations of PIN proteins with multiple origins of noncanonical PIN structure. Molecular Biology and Evolution 31: 2042-2060.

Bennett T, Hines G, van Rongen M, Waldie T, Sawchuk MG, Scarpella E, Ljung K, Leyser O. 2016. Connective auxin transport in the shoot facilitates communication between shoot apices. PLoS Biology 14: e1002446.

Bishopp A, Help H, El-Showk S, Weijers D, Scheres B, Friml J, Benková E, Mähönen AP, Helariutta Y. 2011. A mutually inhibitory interaction between auxin and cytokinin specifies vascular pattern in roots. Current Biology 21: 917-926.

Blencowe BJ. 2017. The relationship between alternative splicing and proteomic complexity. Trends in Biochemical Sciences 42: 407-408.

Blilou I, Xu J, Wildwater M, Willemsen V, Paponov I, Friml J, Heidstra R, Aida M, Palme K, Scheres B. 2005. The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots. Nature 433: 39-44.

Boutté Y, Crosnier M-T, Carraro N, Traas J, Satiat-Jeunemaitre B. 2006. The plasma membrane recycling pathway and cell polarity in plants: studies on PIN proteins. Journal of Cell Science 119: 1255-1265.

Buljan M, Chalancon G, Dunker AK, Bateman A, Balaji S, Fuxreiter M, Babu MM. 2013. Alternative splicing of intrinsically disordered regions and rewiring of protein interactions. Current Opinion in Structural Biology 23: 443-450.

Casson SA, Topping JF, Lindsey K. 2009. MERISTEM-DEFECTIVE, an RS domain protein, is required for the correct meristem patterning and function in Arabidopsis. The Plant Journal 57: 857-869.

Chamala S, Feng G, Chavarro C, Barbazuk WB. 2015. Genome-wide identification of evolutionarily conserved alternative splicing events in flowering plants. Frontiers in Bioengineering and Biotechnology 3: 33.

Cheng C-Y, Krishnakumar V, Chan AP, Thibaud-Nissen F, Schobel S, Town CD. 2017. Araport11: a complete reannotation of the Arabidopsis thaliana reference genome. The Plant Journal 89: 789-804.

Cucinotta M, Cavalleri A, Guazzotti A, Astori C, Manrique S, Bombarely A, Oliveto S, Biffo S, Weijers D, Kater MM et al. 2020. Alternative splicing generates a MONOPTEROS isoform required for ovule development. Current Biology 31: 892-899.

Darracq A, Adams KL. 2013. Features of evolutionarily conserved alternative splicing events between Brassica and Arabidopsis. New Phytologist 199: 252-263.

Delbarre A, Muller P, Imhoff V, Guern J. 1996. Comparison of mechanisms controlling uptake and accumulation of 2,4-dichlorophenoxy acetic acid, naphthalene-1-acetic acid, and indole-3-acetic acid in suspension-cultured tobacco cells. Planta 198: 532-541.

Ding Z, Galván-Ampudia CS, Demarsy E, Łangowski Ł, Kleine-Vehn J, Fan Y, Morita MT, Tasaka M, Fankhauser C, Offringa R et al. 2011. Light-mediated polarization of the PIN3 auxin transporter for the phototropic response in Arabidopsis. Nature Cell Biology 13: 447-452.

Dubrovsky JG, Soukup A, Napsucialy-Mendivil S, Jeknic Z, Ivanchenko MG. 2009. The lateral root initiation index: an integrative measure of primordium formation. Annals of Botany 103: 807-817.

Feraru E, Feraru MI, Kleine-Vehn J, Martinière A, Mouille G, Vanneste S, Vernhettes S, Runions J, Friml J. 2011. PIN polarity maintenance by the cell wall in Arabidopsis. Current Biology 21: 338-343.

Friml J, Vieten A, Sauer M, Weijers D, Schwarz H, Hamann T, Offringa R, Jürgens G. 2003. Efflux-dependent auxin gradients establish the apical-basal axis of Arabidopsis. Nature 426: 147-153.

Friml J, Wiśniewska J, Benková E, Mendgen K, Palme K. 2002. Lateral relocation of auxin efflux regulator PIN3 mediates tropism in Arabidopsis. Nature 415: 806-809.

Furutani M, Kajiwara T, Kato T, Treml BS, Stockum C, Torres-Ruiz RA, Tasaka M. 2007. The gene MACCHI-BOU 4/ENHANCER OF PINOID encodes a NPH3-like protein and reveals similarities between organogenesis and phototropism at the molecular level. Development 134: 3849-3859.

Ganguly A, Park M, Kesawat MS, Cho H-T. 2014. Functional analysis of the hydrophilic loop in intracellular trafficking of Arabidopsis PIN-FORMED proteins. Plant Cell 26: 1570-1585.

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

Ghelli R, Brunetti P, Napoli N, Paolis AD, Cecchetti V, Tsuge T, Serino G, Matsui M, Mele G, Rinaldi G et al. 2018. A newly identified flower-specific splice variant of AUXIN RESPONSE FACTOR 8 regulates stamen elongation and endothecium lignification in Arabidopsis. Plant Cell 30: 620-637.

Glanc M, Fendrych M, Friml J. 2019. PIN2 polarity establishment in Arabidopsis in the absence of an intact cytoskeleton. Biomolecules 9: 222.

Glanc M, Gelderen KV, Hoermayer L, Tan S, Naramoto S, Zhang X, Domjan D, Včelařová L, Hauschild R, Johnson A et al. 2021. AGC kinases and MAB4/MEL proteins maintain PIN polarity by limiting lateral diffusion in plant cells. Current Biology 31: 1918-1930.

Grabov A, Ashley MK, Rigas S, Hatzopoulos P, Dolan L, Vicente-Agullo F. 2005. Morphometric analysis of root shape. New Phytologist 165: 641-651.

Greb T, Clarenz O, Schafer E, Muller D, Herrero R, Schmitz G, Theres K. 2003. Molecular analysis of the LATERAL SUPPRESSOR gene in Arabidopsis reveals a conserved control mechanism for axillary meristem formation. Genes & Development 17: 1175-1187.

Grones P, Abas M, Hajný J, Jones A, Waidmann S, Kleine-Vehn J, Friml J. 2018. PID/WAG-mediated phosphorylation of the Arabidopsis PIN3 auxin transporter mediates polarity switches during gravitropism. Scientific Reports 8: 10279.

Horák J, Grefen C, Berendzen KW, Hahn A, Stierhof Y-D, Stadelhofer B, Stahl M, Koncz C, Harter K. 2008. The Arabidopsis thaliana response regulator ARR22 is a putative AHP phospho-histidine phosphatase expressed in the chalaza of developing seeds. BMC Plant Biology 8: 77.

Hrtyan M, Šliková E, Hejátko J, Růžička K. 2015. RNA processing in auxin and cytokinin pathways. Journal of Experimental Botany 66: 4897-4912.

Kalyna M, Lopato S, Barta A. 2003. Ectopic expression of atRSZ33 reveals its function in splicing and causes pleiotropic changes in development. Molecular Biology of the Cell 14: 3565-3577.

Kashkan I, Timofeyenko K, Kollárová E, Růžička K. 2020. In vivo reporters for visualizing alternative splicing of hormonal genes. Plants 9: 868.

Kelemen O, Convertini P, Zhang Z, Wen Y, Shen M, Falaleeva M, Stamm S. 2013. Function of alternative splicing. Gene 514: 1-30.

Keren H, Lev-Maor G, Ast G. 2010. Alternative splicing and evolution: diversification, exon definition and function. Nature Reviews Genetics 11: 345-355.

Kleine-Vehn J, Ding Z, Jones AR, Tasaka M, Morita MT, Friml J. 2010. Gravity-induced PIN transcytosis for polarization of auxin fluxes in gravity-sensing root cells. Proceedings of the National Academy of Sciences, USA 107: 22344-22349.

Kleine-Vehn J, Łangowski Ł, Wiśniewska J, Dhonukshe P, Brewer PB, Friml J. 2008. Cellular and molecular requirements for polar PIN targeting and transcytosis in plants. Molecular Plant 1: 1056-1066.

Klepikova AV, Kasianov AS, Gerasimov ES, Logacheva MD, Penin AA. 2016. A high resolution map of the Arabidopsis thaliana developmental transcriptome based on RNA-seq profiling. The Plant Journal 88: 1058-1070.

Krejčí J, Stixová L, Pagáčová E, Legartová S, Kozubek S, Lochmanová G, Zdráhal Z, Sehnalová P, Dabravolski S, Hejátko J et al. 2015. Post-translational modifications of histones in human sperm: epigenetics of human sperm. Journal of Cellular Biochemistry 116: 2195-2209.

Kriechbaumer V, Wang P, Hawes C, Abell BM. 2012. Alternative splicing of the auxin biosynthesis gene YUCCA4 determines its subcellular compartmentation. The Plant Journal 70: 292-302.

Kumar S, Stecher G, Li M, Knyaz C, Tamura K. 2018. Mega X: molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution 35: 1547-1549.

Laňková M, Humpolíčková J, Vosolsobě S, Cit Z, Lacek J, Čovan M, Čovanová M, Hof M, Petrášek J. 2016. Determination of dynamics of plant plasma membrane proteins with fluorescence recovery and raster image correlation spectroscopy. Microscopy and Microanalysis 22: 290-299.

Lee JH, Ryu H-S, Chung KS, Posé D, Kim S, Schmid M, Ahn JH. 2013. Regulation of temperature-responsive flowering by MADS-box transcription factor repressors. Science 342: 628-632.

Leitner J, Petrášek J, Tomanov K, Retzer K, Pařezová M, Korbei B, Bachmair A, Zažímalová E, Luschnig C. 2012. Lysine63-linked ubiquitylation of PIN2 auxin carrier protein governs hormonally controlled adaptation of Arabidopsis root growth. Proceedings of the National Academy of Sciences, USA 109: 8322-8327.

Li H, Wangenheim D, Zhang X, Tan S, Darwish-Miranda N, Naramoto S, Wabnik K, De Rycke R, Kaufmann WA, Gütl D et al. 2021. Cellular requirements for PIN polar cargo clustering in Arabidopsis thaliana. New Phytologist 229: 351-369.

Li H-T, Yi T-S, Gao L-M, Ma P-F, Zhang T, Yang J-B, Gitzendanner MA, Fritsch PW, Cai J, Luo Y et al. 2019. Origin of angiosperms and the puzzle of the Jurassic gap. Nature Plants 5: 461-470.

Liao C-Y, Smet W, Brunoud G, Yoshida S, Vernoux T, Weijers D. 2015. Reporters for sensitive and quantitative measurement of auxin response. Nature Methods 12: 207.

Marquez Y, Brown JWS, Simpson C, Barta A, Kalyna M. 2012. Transcriptome survey reveals increased complexity of the alternative splicing landscape in Arabidopsis. Genome Research 22: 1184-1195.

Marquez Y, Höpfler M, Ayatollahi Z, Barta A, Kalyna M. 2015. Unmasking alternative splicing inside protein-coding exons defines exitrons and their role in proteome plasticity. Genome Research 25: 995-1007.

Martín G, Márquez Y, Mantica F, Duque P, Irimia M. 2021. Alternative splicing landscapes in Arabidopsis thaliana across tissues and stress conditions highlight major functional differences with animals. Genome Biology 22: 1-26.

Martiniere A, Lavagi I, Nageswaran G, Rolfe DJ, Maneta-Peyret L, Luu D-T, Botchway SW, Webb SED, Mongrand S, Maurel C et al. 2012. Cell wall constrains lateral diffusion of plant plasma-membrane proteins. Proceedings of the National Academy of Sciences, USA 109: 12805-12810.

Men S, Boutté Y, Ikeda Y, Li X, Palme K, Stierhof Y-D, Hartmann M-A, Moritz T, Grebe M. 2008. Sterol-dependent endocytosis mediates post-cytokinetic acquisition of PIN2 auxin efflux carrier polarity. Nature Cell Biology 10: 237-244.

Müller K, Hošek P, Laňková M, Vosolsobě S, Malínská K, Čarná M, Fílová M, Dobrev PI, Helusová M, Hoyerová K et al. 2019. Transcription of specific auxin efflux and influx carriers drives auxin homeostasis in tobacco cells. The Plant Journal 100: 627-640.

Nakabayashi K, Bartsch M, Ding J, Soppe WJJ. 2015. Seed dormancy in Arabidopsis requires self-binding ability of DOG1 protein and the presence of multiple isoforms generated by alternative splicing. PLoS Genetics 11: e1005737.

Nodzyński T, Vanneste S, Zwiewka M, Pernisová M, Hejátko J, Friml J. 2016. Enquiry into the topology of plasma membrane-localized PIN auxin transport components. Molecular Plant 9: 1504-1519.

O’Leary NA, Wright MW, Brister JR, Ciufo S, Haddad D, McVeigh R, Rajput B, Robbertse B, Smith-White B, Ako-Adjei D et al. 2016. Reference sequence (RefSeq) database at NCBI: current status, taxonomic expansion, and functional annotation. Nucleic Acids Research 44: D733-D745.

Ogura T, Goeschl C, Filiault D, Mirea M, Slovak R, Wolhrab B, Satbhai SB, Busch W. 2019. Root system depth in Arabidopsis is shaped by EXOCYST70A3 via the dynamic modulation of auxin transport. Cell 178: 400-412 e16.

Pernisova M, Prat T, Grones P, Harustiakova D, Matonohova M, Spichal L, Nodzynski T, Friml J, Hejatko J. 2016. Cytokinins influence root gravitropism via differential regulation of auxin transporter expression and localization in Arabidopsis. New Phytologist 212: 497-509.

Petrasek J, Mravec J, Bouchard R, Blakeslee JJ, Abas M, Seifertová D, Wisniewska J, Tadele Z, Kubes M, Covanová M et al. 2006. PIN proteins perform a rate-limiting function in cellular auxin efflux. Science 312: 914-918.

Posé D, Verhage L, Ott F, Yant L, Mathieu J, Angenent GC, Immink RGH, Schmid M. 2013. Temperature-dependent regulation of flowering by antagonistic FLM variants. Nature 503: 414-417.

Rademacher EH, Offringa R. 2012. Evolutionary adaptations of plant agc kinases: from light signaling to cell polarity regulation. Frontiers in Plant Science 3: 250.

Rakusová H, Abbas M, Han H, Song S, Robert HS, Friml J. 2016. Termination of shoot gravitropic responses by auxin feedback on PIN3 polarity. Current Biology 26: 3026-3032.

Rakusová H, Gallego-Bartolomé J, Vanstraelen M, Robert HS, Alabadí D, Blázquez MA, Benková E, Friml J. 2011. Polarization of PIN3-dependent auxin transport for hypocotyl gravitropic response in Arabidopsis thaliana. The Plant Journal 67: 817-826.

Reddy ASN, Marquez Y, Kalyna M, Barta A. 2013. Complexity of the alternative splicing landscape in plants. Plant Cell 25: 3657-3683.

Remy E, Cabrito TR, Baster P, Batista RA, Teixeira MC, Friml J, Sá-Correia I, Duque P. 2013. A major facilitator superfamily transporter plays a dual role in polar auxin transport and drought stress tolerance in Arabidopsis. Plant Cell 25: 901-926.

Retzer K, Butt H, Korbei B, Luschnig C. 2014. The far side of auxin signaling: fundamental cellular activities and their contribution to a defined growth response in plants. Protoplasma 251: 731-746.

Robert HS, Grones P, Stepanova AN, Robles LM, Lokerse AS, Alonso JM, Weijers D, Friml J. 2013. Local auxin sources orient the apical-basal axis in Arabidopsis embryos. Current Biology 23: 2506-2512.

Rosquete MR, von Wangenheim D, Marhavý P, Barbez E, Stelzer EHK, Benková E, Maizel A, Kleine-Vehn J. 2013. An auxin transport mechanism restricts positive orthogravitropism in lateral roots. Current Biology 23: 817-822.

Rosquete MR, Waidmann S, Kleine-Vehn J. 2018. PIN7 auxin carrier has a preferential role in terminating radial root expansion in Arabidopsis thaliana. International Journal of Molecular Sciences 19: 1238.

Roychoudhry S, Kieffer M, Del Bianco M, Liao C-Y, Weijers D, Kepinski S. 2017. The developmental and environmental regulation of gravitropic setpoint angle in Arabidopsis and bean. Scientific Reports 7: 42664.

Rueden CT, Schindelin J, Hiner MC, DeZonia BE, Walter AE, Arena ET, Eliceiri KW. 2017. ImageJ2: ImageJ for the next generation of scientific image data. BMC Bioinformatics 18: 529.

Ruzicka K, Zhang M, Campilho A, Bodi Z, Kashif M, Saleh M, Eeckhout D, El-Showk S, Li H, Zhong S et al. 2017. Identification of factors required for m6A mRNA methylation in Arabidopsis reveals a role for the conserved E3 ubiquitin ligase HAKAI. New Phytologist 215: 157-172.

Shang X, Cao Y, Ma L. 2017. Alternative splicing in plant genes: a means of regulating the environmental fitness of plants. International Journal of Molecular Sciences 18: 432.

Sibout R, Sukumar P, Hettiarachchi C, Holm M, Muday GK, Hardtke CS. 2006. Opposite root growth phenotypes of hy5 versus hy5 hyh mutants correlate with increased constitutive auxin signaling. PLoS Genetics 2: e202.

Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K, Li W, Lopez R, McWilliam H, Remmert M, Söding J et al. 2011. Fast, scalable generation of high-quality protein multiple sequence alignments using clustal omega. Molecular Systems Biology 7: 539.

Šimášková M, O’Brien JA, Khan M, Van Noorden G, Ötvös K, Vieten A, De Clercq I, Van Haperen JMA, Cuesta C, Hoyerová K et al. 2015. Cytokinin response factors regulate PIN-FORMED auxin transporters. Nature Communications 6: 8717.

Sprague BL, McNally JG. 2005. FRAP analysis of binding: proper and fitting. Trends in Cell Biology 15: 84-91.

Staiger D, Brown JWS. 2013. Alternative splicing at the intersection of biological timing, development, and stress responses. Plant Cell 25: 3640-3656.

Stamm S, Ben-Ari S, Rafalska I, Tang Y, Zhang Z, Toiber D, Thanaraj TA, Soreq H. 2005. Function of alternative splicing. Gene 344: 1-20.

Swarup K, Benková E, Swarup R, Casimiro I, Péret B, Yang Y, Parry G, Nielsen E, De Smet I, Vanneste S et al. 2008. The auxin influx carrier LAX3 promotes lateral root emergence. Nature Cell Biology 10: 946-954.

Szakonyi D, Duque P. 2018. Alternative splicing as a regulator of early plant development. Frontiers in Plant Science 9: 1174.

Teale WD, Pasternak T, Dal Bosco C, Dovzhenko A, Kratzat K, Bildl W, Schwörer M, Falk T, Ruperti B, Schaefer V et al. 2020. Flavonol-mediated stabilization of PIN efflux complexes regulates polar auxin transport. EMBO Journal 40: e104416.

Tress ML, Abascal F, Valencia A. 2017. Alternative splicing may not be the key to proteome complexity. Trends in Biochemical Sciences 42: 98-110.

Tseng Q, Duchemin-Pelletier E, Deshiere A, Balland M, Guillou H, Filhol O, Théry M. 2012. Spatial organization of the extracellular matrix regulates cell-cell junction positioning. Proceedings of the National Academy of Sciences, USA 109: 1506-1511.

Tsugeki R, Tanaka-Sato N, Maruyama N, Terada S, Kojima M, Sakakibara H, Okada K. 2015. CLUMSY VEIN, the Arabidopsis DEAH-box Prp16 ortholog, is required for auxin-mediated development. The Plant Journal 81: 183-197.

Waidmann S, De-Araujo L, Kleine-Vehn J, Korbei B. 2018. Immunoprecipitation of Membrane proteins from Arabidopsis thaliana root tissue. In: Ristova D, Barbez E, eds. Methods in molecular biology. Root development. New York, NY, USA: Springer New York, 209-220.

Waldie T, Leyser O. 2018. Cytokinin targets auxin transport to promote shoot branching. Plant Physiology 177: 803-818.

Weller B, Zourelidou M, Frank L, Barbosa ICR, Fastner A, Richter S, Jürgens G, Hammes UZ, Schwechheimer C. 2017. Dynamic PIN-FORMED auxin efflux carrier phosphorylation at the plasma membrane controls auxin efflux-dependent growth. Proceedings of the National Academy of Sciences, USA 114: E887-E896.

Willige BC, Ahlers S, Zourelidou M, Barbosa ICR, Demarsy E, Trevisan M, Davis PA, Roelfsema MRG, Hangarter R, Fankhauser C et al. 2013. D6PK AGCVIII kinases are required for auxin transport and phototropic hypocotyl bending in Arabidopsis. Plant Cell 25: 1674-1688.

Zadnikova P, Petrášek J, Marhavý P, Raz V, Vandenbussche F, Ding Z, Schwarzerová K, Morita MT, Tasaka M, Hejátko J et al. 2010. Role of PIN-mediated auxin efflux in apical hook development of Arabidopsis thaliana. Development 137: 607-617.

Zadnikova P, Wabnik K, Abuzeineh A, Gallemi M, Straeten DVD, Smith RS, Inzé D, Friml J, Prusinkiewicz P, Benková E. 2016. A model of differential growth-guided apical hook formation in plants. Plant Cell 28: 2464-2477.

Zourelidou M, Absmanner B, Weller B, Barbosa IC, Willige BC, Fastner A, Streit V, Port SA, Colcombet J, de la Bentem S et al. 2014. Auxin efflux by PIN-FORMED proteins is activated by two different protein kinases, D6 PROTEIN KINASE and PINOID. eLife 3: e02860.

Zwiewka M, Bilanovičová V, Seifu YW, Nodzyński T. 2019. The nuts and bolts of PIN auxin efflux carriers. Frontiers in Plant Science 10: 985.

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