The phytohormone auxin is a master regulator of plant growth and development in response to many endogenous and environmental signals. The underlying coordination of growth is mediated by the formation of auxin maxima and concentration gradients. The visualization of auxin dynamics and distribution can therefore provide essential information to increase our understanding of the mechanisms by which auxin orchestrates these growth and developmental processes. Several auxin reporters have been developed to better perceive the auxin distribution and signaling machinery in vivo. This review focuses on different types of auxin reporters and biosensors used to monitor auxin distribution and its dynamics, as well as auxin signaling, at the cellular and tissue levels in different plant species. We provide a brief history of each reporter and biosensor group and explain their principles and utilities.

CEITEC MU Central European Institute of Technology Masaryk University Brno Czech Republic

Faculty of Science National Centre for Biomolecular Research Masaryk University Brno Czech Republic

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Abbas M, Hernández-García J, Pollmann S, Samodelov SL, Kolb M, Friml J, Hammes UZ, Zurbriggen MD, Blázquez MA, Alabadí D (2018) Auxin methylation is required for differential growth in Arabidopsis. Proc Natl Acad Sci USA 115: 6864–6869 PubMed PMC

Band LR, Wells DM, Larrieu A, Sun J, Middleton AM, French AP, Brunoud G, Sato EM, Wilson MH, Péret B, et al (2012) Root gravitropism is regulated by a transient lateral auxin gradient controlled by a tipping-point mechanism. Proc Natl Acad Sci USA 109: 4668–4673 PubMed PMC

Bence M, Jankovics F, Lukácsovich T, Erdélyi M (2017) Combining the auxin-inducible degradation system with CRISPR/Cas9-based genome editing for the conditional depletion of endogenous Drosophila melanogaster proteins. FEBS J 284: 1056–1069 PubMed

Benková E, Michniewicz M, Sauer M, Teichmann T, Seifertová D, Jürgens G, Friml J (2003) Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell 115: 591–602 PubMed

Bieleszová K, Parízková B, Kubes M, Husicková A, Kubala M, Ma Q, Sedlárová M, Robert S, Dolezal K, Strnad M, et al (2019) New fluorescently labeled auxins exhibit promising anti-auxin activity. New Biotechnol 48: 44–52 PubMed

Boer DR, Freire-Rios A, van den Berg WAM, Saaki T, Manfield IW, Kepinski S, López-Vidrieo I, Franco-Zorrilla JM, de Vries SC, Solano R, et al (2014) Structural basis for DNA binding specificity by the auxin-dependent ARF trans cription factors. Cell 156: 577–589 PubMed

Brown KM, Long S, Sibley LD (2017) Plasma membrane association by N-acylation governs PKG function in Toxoplasma gondii .mBio 8: e00375–17 PubMed PMC

Brumos J, Robles LM, Yun JJ, Vu TC, Jackson S, Alonso JM, Stepanova AN (2018) Local auxin biosynthesis is a key regulator of plant development. Dev Cell 47: 306–318.e5 PubMed

Brunoud G, Wells DM, Oliva M, Larrieu A, Mirabet V, Burrow AH, Beeckman T, Kepinski S, Traas J, Bennett MJ, et al (2012) A novel sensor to map auxin response and distribution at high spatio-temporal resolution. Nature 482: 103–106 PubMed

Chaabouni S, Jones B, Delalande C, Wang H, Li Z, Mila I, Frasse P, Latché A, Pech JC, Bouzayen M (2009) Sl-IAA3, a tomato Aux/IAA at the crossroads of auxin and ethylene signalling involved in differential growth. J Exp Bot 60: 1349–1362 PubMed PMC

Chen Y, Yordanov YS, Ma C, Strauss S, Busov VB (2013) DR5 as a reporter system to study auxin response in Populus. Plant Cell Rep 32: 453–463 PubMed

Cheng Y, Dai X, Zhao Y (2006) Auxin biosynthesis by the YUCCA flavin monooxygenases controls the formation of floral organs and vascular tissues in Arabidopsis. Genes Dev 20: 1790–1799 PubMed PMC

Cucinotta M, Cavalleri A, Chandler JW, Colombo L (2021) Auxin and flower development: a blossoming field. Cold Spring Harb Perspect Biol 13: a039974. PubMed PMC

Dai X, Mashiguchi K, Chen Q, Kasahara H, Kamiya Y, Ojha S, DuBois J, Ballou D, Zhao Y (2013) The biochemical mechanism of auxin biosynthesis by an Arabidopsis YUCCA flavin-containing monooxygenase. J Biol Chem 288: 1448–1457 PubMed PMC

de Felipe P, Luke GA, Hughes LE, Gani D, Halpin C, Ryan MD (2006) E unum pluribus: multiple proteins from a self-processing polyprotein. Trends Biotechnol 24: 68–75 PubMed

Deltcheva E, Chylinski K, Sharma CM, Gonzales K, Chao Y, Pirzada ZA, Eckert MR, Vogel J, Charpentier E (2011) CRISPR RNA maturation by trans-encoded small RNA and host factor RNase III. Nature 471: 602–607 PubMed PMC

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

Di Mambro R, De Ruvo M, Pacifici E, Salvi E, Sozzani R, Benfey PN, Busch W, Novak O, Ljung K, Di Paola L, et al (2017) Auxin minimum triggers the developmental switch from cell division to cell differentiation in the Arabidopsis root. Proc Natl Acad Sci USA 114: E7641–E7649 PubMed PMC

Doudna JA, Charpentier E (2014) Genome editing. The new frontier of genome engineering with CRISPR-Cas9. Science 346: 1258096. PubMed

Dreher KA, Brown J, Saw RE, Callis J (2006) The Arabidopsis Aux/IAA protein family has diversified in degradation and auxin responsiveness. Plant Cell 18: 699–714 PubMed PMC

Figueiredo DD, Batista RA, Roszak PJ, Köhler C (2015) Auxin production couples endosperm development to fertilization. Nat Plants 1: 15184. PubMed

Finet C, Jaillais Y (2012) Auxology: when auxin meets plant evo-devo. Dev Biol 369: 19–31 PubMed

Friml J, Benková E, Blilou I, Wisniewska J, Hamann T, Ljung K, Woody S, Sandberg G, Scheres B, Jürgens G, et al (2002a) AtPIN4 mediates sink driven auxin gradients and patterning in Arabidopsis roots. Cell 108: 661–673 PubMed

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

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

Gallavotti A, Yang Y, Schmidt RJ, Jackson D (2008) The relationship between auxin transport and maize branching. Plant Physiol 147: 1913–1923 PubMed PMC

Galli M, Khakhar A, Lu Z, Chen Z, Sen S, Joshi T, Nemhauser JL, Schmitz RJ, Gallavotti A (2018) The DNA binding landscape of the maize AUXIN RESPONSE FACTOR family. Nat Commun 9: 4526. PubMed PMC

Galvan-Ampudia CS, Cerutti G, Legrand J, Brunoud G, Martin-Arevalillo R, Azais R, Bayle V, Moussu S, Wenzl C, Jaillais Y, et al (2020) Temporal integration of auxin information for the regulation of patterning. Elife 9: e55832. PubMed PMC

Gee MA, Hagen G, Guilfoyle TJ (1991) Tissue-specific and organ-specific expression of soybean auxin-responsive transcripts GH3 and SAURs. Plant Cell 3: 419–430 PubMed PMC

Geisler M (2021) A retro-perspective on auxin transport. Front Plant Sci 12: 756968. PubMed PMC

Geisler M, Wang B, Zhu J (2014) Auxin transport during root gravitropism: transporters and techniques. Plant Biol 16: 50–57 PubMed

Gilbert LA, Larson MH, Morsut L, Liu Z, Brar GA, Torres SE, Stern-Ginossar N, Brandman O, Whitehead EH, Doudna JA, et al (2013) CRISPR-mediated modular RNA-guided regulation of transcription in eukaryotes. Cell 154: 442–451 PubMed PMC

Gray WM, del Pozo JC, Walker L, Hobbie L, Risseeuw E, Banks T, Crosby WL, Yang M, Ma H, Estelle M (1999) Identification of an SCF ubiquitin-ligase complex required for auxin response in Arabidopsis thaliana. Genes Dev 13: 1678–1691 PubMed PMC

Gray WM, Kepinski S, Rouse D, Leyser O, Estelle M (2001) Auxin regulates SCFTIR1-dependent degradation of AUX/IAA proteins. Nature 414: 271–276 PubMed

Grieneisen VA, Xu J, Marée AF, Hogeweg P, Scheres B (2007) Auxin transport is sufficient to generate a maximum and gradient guiding root growth. Nature 449: 1008–1013 PubMed

Hagen G, Guilfoyle TJ (1985) Rapid induction of selective transcription by auxins. Mol Cell Biol 5: 1197–1203 PubMed PMC

Hagen G, Kleinschmidt A, Guilfoyle T (1984) Auxin-regulated gene expression in intact soybean hypocotyl and excised hypocotyl sections. Planta 162: 147–153 PubMed

Hagen G, Martin G, Li Y, Guilfoyle TJ (1991) Auxin-induced expression of the soybean GH3 promoter in transgenic tobacco plants. Plant Mol Biol 17: 567–579 PubMed

He Y, Zhang T, Sun H, Zhan H, Zhao Y (2020) A reporter for noninvasively monitoring gene expression and plant transformation. Hortic Res 7: 152. PubMed PMC

Heisler MG, Ohno C, Das P, Sieber P, Reddy GV, Long JA, Meyerowitz EM (2005) Patterns of auxin transport and gene expression during primordium development revealed by live imaging of the Arabidopsis inflorescence meristem. Curr Biol 15: 1899–1911 PubMed

Herud-Sikimić O, Stiel AC, Kolb M, Shanmugaratnam S, Berendzen KW, Feldhaus C, Höcker B, Jürgens G (2021) A biosensor for the direct visualization of auxin. Nature 592: 768–772 PubMed PMC

Hum JM, Siegel AP, Pavalko FM, Day RN (2012) Monitoring biosensor activity in living cells with fluorescence lifetime imaging microscopy. Int J Mol Sci 13: 14385–14400 PubMed PMC

Jinek M, Chylinski K, Fonfara I, Hauer M, Doudna JA, Charpentier E (2012) A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 337: 816–821 PubMed PMC

Jones AM, Danielson JA, Manojkumar SN, Lanquar V, Grossmann G, Frommer WB (2014) Abscisic acid dynamics in roots detected with genetically encoded FRET sensors. eLife 3: e01741. PubMed PMC

Jones AR, Kramer EM, Knox K, Swarup R, Bennett MJ, Lazarus CM, Leyser HM, Grierson CS (2009) Auxin transport through non-hair cells sustains root-hair development. Nat Cell Biol 11: 78–84 PubMed PMC

Kaper T, Looger LL, Takanaga H, Platten M, Steinman L, Frommer WB (2007) Nanosensor detection of an immunoregulatory tryptophan influx/kynurenine efflux cycle. PLoS Biol 5: e257. PubMed PMC

Kasahara H (2015) Current aspects of auxin biosynthesis in plants. Biosci Biotechnol Biochem 80: 34–42 PubMed

Kebrom TH (2017) A growing stem inhibits bud outgrowth – the overlooked theory of apical dominance. Front Plant Sci 8: 1874. PubMed PMC

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

Khakhar A, Bolten NJ, Nemhauser J, Klavins E (2016) Cell-Cell communication in yeast using auxin biosynthesis and auxin responsive CRISPR transcription factors. ACS Synth Biol 5: 279–286 PubMed

Khakhar A, Leydon AR, Lemmex AC, Klavins E, Nemhauser JL (2018) Synthetic hormone-responsive transcription factors can monitor and re-program plant development. eLife 7: e34702. PubMed PMC

Khakhar A, Wang C, Swanson R, Stokke S, Rizvi F, Sarup S, Hobbs J, Voytas DF (2021) VipariNama: RNA viral vectors to rapidly elucidate the relationship between gene expression and phenotype. Plant Physiol 186: 2222–2238 PubMed PMC

Korasick DA, Westfall CS, Lee SG, Nanao MH, Dumas R, Hagen G, Guilfoyle TJ, Jez JM, Strader LC (2014) Molecular basis for AUXIN RESPONSE FACTOR protein interaction and the control of auxin response repression. Proc Natl Acad Sci USA 111: 5427–5432 PubMed PMC

Kramer EM, Ackelsberg EM (2015) Auxin metabolism rates and implications for plant development. Front Plant Sci 6: 150. PubMed PMC

Lavy M, Estelle E (2016) Mechanisms of auxin signaling. Development 143: 3226–3229 PubMed PMC

Leyser O (2018) Auxin signaling. Plant Physiol 176: 465–479 PubMed PMC

Li L, Gallei M, Friml J (2022) Bending to auxin: fast acid growth for tropisms. Trends Plant Sci 27: 440–449 PubMed

Li Y, Hagen G, Guilfoyle T (1991) An auxin-responsive promoter is differentially induced by auxin gradients during tropisms. Plant Cell 3: 1167–1175 PubMed PMC

Liao CY, Smet W, Brunoud G, Yoshida S, Vernoux T, Weijers D (2015) Reporters for sensitive and quantitative measurement of auxin response. Nat Methods 12: 207–210 PubMed PMC

Lieberman-Lazarovich M, Yahav C, Israeli A, Efroni I (2019) Deep conservation of cis-element variants regulating plant hormonal responses. Plant Cell 31: 2559–2572 PubMed PMC

Mashiguchi K, Tanaka K, Sakai T, Sugawara S, Kawaide H, Natsume M, Hanada A, Yaeno T, Shirasu K, Yao H, et al (2011) The main auxin biosynthesis pathway in Arabidopsis. Proc Natl Acad Sci USA 108: 18512–18517 PubMed PMC

McClure BA, Guilfoyle T (1987) Characterization of a class of small auxin-inducible soybean polyadenylated RNAs. Plant Mol Biol 9: 611–623 PubMed

McClure BA, Hagen G, Brown CS, Gee MA, Guilfoyle TJ (1989) Transcription, organization, and sequence of an auxin-regulated gene cluster in soybean. Plant Cell 1: 229–239 PubMed PMC

McClure CD, Hassan A, Aughey GN, Butt K, Estacio-Gómez A, Duggal A, Sia CY, Barber AF, Southall TD (2022) An auxin-inducible, GAL4-compatible, gene expression system for Drosophila. Elife 11: e67598. PubMed PMC

Mendoza-Ochoa GI, Barrass JD, Terlouw BR, Maudlin IE, de Lucas S, Sani E, Aslanzadeh V, Reid JAE, Beggs JD (2019) A fast and tuneable auxin-inducible degron for depletion of target proteins in budding yeast. Yeast 36: 75–81 PubMed PMC

Mir R, Aranda LZ, Biaocchi T, Luo A, Sylvester AW, Rasmussen CG (2017) A DII domain-based auxin reporter uncovers low auxin signaling during telophase and early G1. Plant Physiol 173: 863–871 PubMed PMC

Mironova VV, Omelyanchuk NA, Wiebe DS, Levitsky VG (2014) Computational analysis of auxin responsive elements in the Arabidopsis thaliana L. genome. BMC Genom 15: S4 PubMed PMC

Moreno-Risueno MA, Van Norman JM, Moreno A, Zhang J, Ahnert SE, Benfey PN (2010) Oscillating gene expression determines competence for periodic Arabidopsis root branching. Science 329: 1306–1311 PubMed PMC

Moss BL, Mao H, Guseman JM, Hinds TR, Hellmuth A, Kovenock M, Noorassa A, Lanctot A, Villalobos LI, Zheng N, et al (2015) Rate motifs tune auxin/indole-3-acetic acid degradation dynamics. Plant Physiol 169: 803–813 PubMed PMC

Nagai T, Ibata K, Park ES, Kubota M, Mikoshiba K, Miyawaki A (2002) A variant of yellow fluorescent protein with fast and efficient maturation for cell-biological applications. Nat Biotechnol 20: 87–90 PubMed

Natsume T, Kiyomitsu T, Saga Y, Kanemaki MT (2016) Rapid protein depletion in human cells by auxin-inducible degron tagging with short homology donors. Cell Rep 15: 210–218 PubMed

Niemeyer M, Moreno Castillo E, Ihling CH, Iacobucci C, Wilde V, Hellmuth A, Hoehenwarter W, Samodelov SL, Zurbriggen MD, Kastritis PL, et al (2020) Flexibility of intrinsically disordered degrons in AUX/IAA proteins reinforces auxin co-receptor assemblies. Nat Commun 11: 2277. PubMed PMC

Nishimura K, Fukagawa T, Takisawa H, Kakimoto T, Kanemaki M (2009) An auxin-based degron system for the rapid depletion of proteins in non-plant cells. Nat Methods 6: 917–922 PubMed

Oh E, Zhu JY, Bai MY, Arenhart RA, Sun Y, Wang ZY (2014) Cell elongation is regulated through a central circuit of interacting transcription factors in the Arabidopsis hypocotyl. Elife 3: e03031 PubMed PMC

O’Malley RC, Huang SC, Song L, Lewsey MG, Bartlett A, Nery JR, Galli M, Gallavotti A, Ecker JR (2016) Cistrome and epicistrome features shape the regulatory DNA landscape. Cell 165: 1280–1292 PubMed PMC

Pacios-Bras C, Schlaman HR, Boot K, Admiraal P, Langerak JM, Stougaard J, Spaink HP (2003) Auxin distribution in Lotus japonicus during root nodule development. Plant Mol Biol 52: 1169–1180 PubMed

Pařízková B, Žukauskaitė A, Vain T, Grones P, Raggi S, Kubeš MF, Kieffer M, Doyle SM, Strnad M, Kepinski S, et al (2021) New fluorescent auxin probes visualise tissue‐specific and subcellular distributions of auxin in Arabidopsis. New Phytol 230: 535–549 PubMed

Petersson SV, Johansson AI, Kowalczyk M, Makoveychuk A, Wang JY, Moritz T, Grebe M, Benfey PN, Sandberg G, Ljung K (2009) An auxin gradient and maximum in the Arabidopsis root apex shown by high-resolution cell-specific analysis of IAA distribution and synthesis. Plant Cell 21: 1659–1668 PubMed PMC

Philip N, Waters AP (2015) Conditional degradation of plasmodium calcineurin reveals functions in parasite colonization of both host and vector. Cell Host Microbe 18: 122–131 PubMed PMC

Pierre-Jerome E, Jang SS, Havens KA, Nemhauser JL, Klavins E (2014) Recapitulation of the forward nuclear auxin response pathway in yeast. Proc Natl Acad Sci USA 111: 9407–9412 PubMed PMC

Piston DW, Kremers GJ (2007) Fluorescent protein FRET: the good, the bad and the ugly. Trends Biochem Sci 32: 407–414 PubMed

Qi J, Wang Y, Yu T, Cunha A, Wu B, Vernoux T, Meyerowitz E, Jiao Y (2014) Auxin depletion from leaf primordia contributes to organ patterning .Proc Natl Acad Sci USA 111: 18769–18774 PubMed PMC

Qi L, Yan J, Li Y, Jiang H, Sun J, Chen Q, Li H, Chu J, Yan C, Sun X, et al (2012) Arabidopsis thaliana plants differentially modulate auxin biosynthesis and transport during defense responses to the necrotrophic pathogen Alternaria brassicicola. New Phytol 195: 872–882 PubMed

Qi LS, Larson MH, Gilbert LA, Doudna JA, Weissman JS, Arkin AP, Lim WA (2013) Repurposing CRISPR as an RNA-guided platform for sequence-specific control of gene expression. Cell 152: 1173–1183 PubMed PMC

Ramos JA, Zenser N, Leyser O, Callis J (2001) Rapid degradation of auxin/indoleacetic acid proteins requires conserved amino acids of domain II and is proteasome dependent. Plant Cell 13: 2349–2360 PubMed PMC

Reissaus CA, Day KH, Mirmira RG, Dunn KW, Pavalko FM, Day RN (2020) PIE-FLIM measurements of two different FRET-based biosensor activities in the same living cells. Biophys J 118: 1820–1829 PubMed PMC

Rizza A, Walia A, Lanquar V, Frommer WB, Jones AM (2017) In vivo gibberellin gradients visualized in rapidly elongating tissues. Nat Plants 3: 803–813 PubMed

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. Curr Biol 23: 2506–2512 PubMed

Robert HS, Grunewald W, Sauer M, Cannoot B, Soriano M, Swarup R, Weijers D, Bennett MJ, Boutilier K, Friml J (2015) Plant embryogenesis requires AUX/LAX-mediated auxin influx. Development 142: 702–711 PubMed

Sabatini S, Beis D, Wolkenfelt H, Murfett J, Guilfoyle T, Malamy J, Benfey P, Leyser O, Bechtold N, Weisbeek P, et al (1999) An auxin-dependent distal organizer of pattern and polarity in the Arabidopsis root. Cell 99: 463–472 PubMed

Salehin M, Bagchi R, Estelle M (2015) SCFTIR1/AFB-based auxin perception: mechanism and role in plant growth and development. Plant Cell 27: 9–19 PubMed PMC

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

Serre NBC, Kralík D, Yun P, Slouka Z, Shabala S, Fendrych M (2021) AFB1 controls rapid auxin signalling through membrane depolarization in Arabidopsis thaliana root. Nat Plants 7: 1229–1238 PubMed PMC

Simon S, Petrášek J (2011) Why plants need more than one type of auxin. Plant Sci 180: 454–460 PubMed

Skalický V, Vojtková T, Pěnčík A, Vrána J, Juzoń K, Koláčková V, Sedlářová M, Kubeš MF, Novák O (2021) Auxin metabolite profiling in isolated and intact plant nuclei .Int J Mol Sci 22: 12369. PubMed PMC

Sokołowska K, Kizinska J, Szewczuk Z, Banasiak A (2014) Auxin conjugated to fluorescent dyes–a tool for the analysis of auxin transport pathways. Plant Biol 16: 866–877 PubMed

Spicer R, Tisdale-Orr T, Talavera C (2013) Auxin-responsive DR5 promoter coupled with transport assays suggest separate but linked routes of auxin transport during woody stem development in populus. PLoS One 8: e72499. PubMed PMC

Stepanova AN, Robertson-Hoyt J, Yun J, Benavente LM, Xie DY, Dolezal K, Schlereth A, Jürgens G, Alonso JM (2008) TAA1-mediated auxin biosynthesis is essential for hormone crosstalk and plant development. Cell 133: 177–191 PubMed

Stepanova AN, Yun JJ, Robles LM, Novak O, He W, Guo H, Ljung K, Alonso JM (2011) The Arabidopsis YUCCA1 flavin monooxygenase functions in the indole-3-pyruvic acid branch of auxin biosynthesis. Plant Cell 23: 3961–3973 PubMed PMC

Su SH, Gibbs NM, Jancewicz AL, Masson PH (2017) Molecular mechanisms of root gravitropism. Curr Biol 27: R964–R972 PubMed

Tan X, Calderon Villalobos LIA, Sharon M, Zheng C, Robinson CV, Estelle M, Zheng N (2007) Mechanism of auxin perception by the TIR1 ubiquitin ligase. Nature 446: 640–645 PubMed

Tao Y, Ferrer JL, Ljung K, Pojer F, Hong F, Long JA, Li L, Moreno JE, Bowman ME, Ivans LJ, et al (2008) Rapid synthesis of auxin via a new tryptophan-dependent pathway is required for shade avoidance in plants. Cell 133: 164–176 PubMed PMC

Thelander M, Landberg K, Sundberg E (2019) Minimal auxin sensing levels in vegetative moss stem cells revealed by a ratiometric reporter. New Phytol 224: 775–788 PubMed

Ulmasov T, Murfett J, Hagen G, Guilfoyle TJ (1997) Aux/lAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response element. Plant Cell 9: 1963–1971 PubMed PMC

Ulmasov T, Liu ZB, Hagen G, Guilfoyle TJ (1995) Composite structure of auxin response elements. Plant Cell 7: 1611–1623 PubMed PMC

Včelařová L, Skalický V, Chamrád I, Lenobel R, Kubeš MF, Pěnčík A, Novák O (2021) Auxin metabolome profiling in the Arabidopsis endoplasmic reticulum using an optimised organelle isolation protocol. Int J Mol Sci 22: 9370. PubMed PMC

Verma S, Attuluri VPS, Robert HS (2021) An essential function for auxin in embryo development. CSH Perspect Biol 13: a039966 PubMed PMC

Vernoux T, Brunoud G, Farcot E, Morin V, Van den Daele H, Legrand J, Oliva M, Das P, Larrieu A, Wells D, et al (2011) The auxin signalling network translates dynamic input into robust patterning at the shoot apex. Mol Syst Biol 7: 508. PubMed PMC

Völker A, Stierhof YD, Jürgens G (2001) Cell cycle-independent expression of the Arabidopsis cytokinesis-specific syntaxin KNOLLE results in mistargeting to the plasma membrane and is not sufficient for cytokinesis. J Cell Sci 114: 3001–3012 PubMed

Waadt R, Hitomi K, Nishimura N, Hitomi C, Adams SR, Getzoff ED, Schroeder JI (2014) FRET-based reporters for the direct visualization of abscisic acid concentration changes and distribution in Arabidopsis. eLife 3: e01739. PubMed PMC

Wang R, Estelle M (2014) Diversity and specificity: auxin perception and signaling through the TIR1/AFB pathway. Curr Opin Plant Biol 21: 51–58 PubMed PMC

Wang S, Shen B, Ren S, Zhao Y, Zhang S, Qu J, Liu L (2019) Implementation and application of FRET-FLIM technology. J Innov Opt Health Sci 12: 1930010.

Ware A, Walker CH, Šimura J, González-Suárez P, Ljung K, Bishopp A, Wilson ZA, Bennett T (2020) Auxin export from proximal fruits drives arrest in temporally competent inflorescences. Nat Plants 6: 699–707 PubMed

Weijers D, Franke-van Dijk M, Vencken RJ, Quint A, Hooykaas P, Offringa R (2001) An Arabidopsis minute-like phenotype caused by a semi-dominant mutation in a RIBOSOMAL PROTEIN S5 gene. Development 128: 4289–4299 PubMed

Weijers D, Wagner D (2016) Transcriptional responses to the auxin hormone. Annu Rev Plant Biol 67: 539–574 PubMed

Wend S, Bosco CD, Kämpf MM, Ren F, Palme K, Weber W, Dovzhenko A, Zurbriggen MD (2013) A quantitative ratiometric sensor for time-resolved analysis of auxin dynamics. Sci Rep 3: 2052. PubMed PMC

Willems AR, Schwab M, Tyers M (2004) A hitchhiker’s guide to the cullin ubiquitin ligases: SCF and its kin. Biochim Biophys Acta 1695: 133–170 PubMed

Won C, Shen X, Mashiguchi K, Zheng Z, Dai X, Cheng Y, Kasahara H, Kamiya Y, Chory J, Zhao Y (2011) 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 PubMed PMC

Xiao X, Li X, Chen C, Guo W. (2020) DR5 is a suitable system for studying the auxin response in the Poncirus trifoliata-Xanthomonas axonopodis pv. citri Interaction. Hortic Plant J 6: 277–283

Yang J, Yuan Z, Meng Q, Huang G, Perin C, Bureau C, Meunier AC, Ingouff M, Bennett MJ, Liang W (2017) Dynamic regulation of auxin response during rice development revealed by newly established hormone biosensor markers. Front Plant Sci 8: 256. PubMed PMC

Yesbolatova A, Saito Y, Kitamoto N, Makino-Itou H, Ajima R, Nakano R, Nakaoka H, Fukui K, Gamo K, Tominari Y, et al (2020) The auxin-inducible degron 2 technology provides sharp degradation control in yeast, mammalian cells, and mice. Nat Commun 11: 5701. PubMed PMC

Žádníková 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 PubMed

Zhang L, Ward JD, Cheng Z, Dernburg AF (2015) The auxin-inducible degradation (AID) system enables versatile conditional protein depletion in C. elegans. Development 142: 4374–4384 PubMed PMC

Zhao Y, Christensen SK, Fankhauser C, Cashman JR, Cohen JD, Weigel D, Chory J (2001) A role for flavin monooxygenase-like enzymes in auxin biosynthesis. Science 291: 306–309 PubMed

Zimmermann T, Rietdorf J, Girod A, Georget V, Pepperkok R (2002) Spectral imaging and linear un-mixing enables improved FRET efficiency with a novel GFP2-YFP FRET pair. FEBS Lett 531: 245–249 PubMed

Transcriptome analysis of thermomorphogenesis in ovules and during early seed development in Brassica napus