Plant hormones are a group of naturally occurring, low-abundance organic compounds that influence physiological processes in plants. Our knowledge of the distribution profiles of phytohormones in plant organs, tissues, and cells is still incomplete, but advances in mass spectrometry have enabled significant progress in tissue- and cell-type-specific analyses of phytohormones over the last decade. Mass spectrometry is able to simultaneously identify and quantify hormones and their related substances. Biosensors, on the other hand, offer continuous monitoring; can visualize local distributions and real-time quantification; and, in the case of genetically encoded biosensors, are noninvasive. Thus, biosensors offer additional, complementary technologies for determining temporal and spatial changes in phytohormone concentrations. In this review, we focus on recent advances in mass spectrometry–based quantification, describe monitoring systems based on biosensors, and discuss validations of the various methods before looking ahead at future developments for both approaches.


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Literature Cited

  1. Al-Babili S, Bouwmeester HJ. 1.  2015. Strigolactones, a novel carotenoid-derived plant hormone. Annu. Rev. Plant Biol. 66:161–86 [Google Scholar]
  2. Antoniadi I, Plačková L, Simonovik B, Doležal K, Turnbull C. 2.  et al. 2015. Cell-type specific cytokinin distribution within the Arabidopsis primary root apex. Plant Cell 27:1955–67Describes a method of combining fluorescence-activated cell-type-specific sorting with MS to measure CKs in specific cell types of Arabidopsis roots. [Google Scholar]
  3. Arrivault S, Guenther M, Florian A, Encke B, Feil R. 3.  et al. 2014. Dissecting the subcellular compartmentation of proteins and metabolites in Arabidopsis leaves using non-aqueous fractionation. Mol. Cell. Proteom. 13:2246–59 [Google Scholar]
  4. Badescu GO, Marsh A, Smith TR, Thompson AJ, Napier RM. 4.  2016. Kinetic characterisation of a single chain antibody against the hormone abscisic acid: comparison with its parental monoclonal. PLOS ONE 11:e0152148 [Google Scholar]
  5. Balcke GU, Handrick V, Bergau N, Fichtner M, Henning A. 5.  et al. 2012. An UPLC-MS/MS method for highly sensitive high-throughput analysis of phytohormones in plant tissues. Plant Methods 8:47 [Google Scholar]
  6. Band LR, Wells DM, Larrieu A, Sun J, Middleton AM. 6.  et al. 2012. Root gravitropism is regulated by a transient lateral auxin gradient controlled by a tipping-point mechanism. PNAS 109:4668–73 [Google Scholar]
  7. Benková E, Witters E, Van Dongen W, Kolár J, Motyka V. 7.  et al. 1999. Cytokinins in tobacco and wheat chloroplasts. Occurrence and changes due to light/dark treatment. Plant Physiol 121:245–52 [Google Scholar]
  8. Bielach A, Podlešáková K, Marhavy P, Duclercq J, Cuesta C. 8.  et al. 2012. Spatiotemporal regulation of lateral root organogenesis in Arabidopsis by cytokinin. Plant Cell 24:3967–81 [Google Scholar]
  9. Bing T, Chang T, Yang X, Mei H, Liu X, Shangguan D. 9.  2011. G-quadruplex DNA aptamers generated for systemin. Bioorg. Med. Chem 194211–19 [Google Scholar]
  10. Brunoud G, Wells DM, Oliva M, Larrieu A, Mirabet V. 10.  et al. 2012. A novel sensor to map auxin response and distribution at high spatio-temporal resolution. Nature 482:103–108 [Google Scholar]
  11. Cai BD, Ye EC, Yuan BF, Feng YQ. 11.  2015. Sequential solvent induced phase transition extraction for profiling of endogenous phytohormones in plants by liquid chromatography-mass spectrometry. J. Chromatogr. B 1004:23–29 [Google Scholar]
  12. Cai BD, Yin J, Hao YH, Li YN, Yuan BF, Feng YQ. 12.  2015. Profiling of phytohormones in rice under elevated cadmium concentration levels by magnetic solid-phase extraction coupled with liquid chromatography tandem mass spectrometry. J. Chromatogr. A 1406:78–86 [Google Scholar]
  13. Cai BD, Zhu JX, Gao Q, Luo D, Yuan BF, Feng YQ. 13.  2014. Rapid and high-throughput determination of endogenous cytokinins in Oryza sativa by bare Fe3O4 nanoparticles-based magnetic solid-phase extraction. J. Chromatogr. A 1340:146–50 [Google Scholar]
  14. Cai BD, Zhu JX, Shi ZG, Yuan BF, Feng YQ. 14.  2013. A simple sample preparation approach based on hydrophilic solid-phase extraction coupled with liquid chromatography-tandem mass spectrometry for determination of endogenous cytokinins. J. Chromatogr. B 942–43:31–36 [Google Scholar]
  15. Cao ZY, Sun LH, Mou RX, Zhang LP, Lin XY. 15.  et al. 2016. Profiling of phytohormones and their major metabolites in rice using binary solid-phase extraction and liquid chromatography-triple quadrupole mass spectrometry. J. Chromatogr. A 1451:67–74 [Google Scholar]
  16. Chen ML, Huang YQ, Liu JQ, Yuan BF, Feng YQ. 16.  2011. Highly sensitive profiling assay of acidic plant hormones using a novel mass probe by capillary electrophoresis-time of flight-mass spectrometry. J. Chromatogr. B 879:938–44 [Google Scholar]
  17. Chen S, Yuan R, Chai Y, Hu F. 17.  2013. Electrochemical sensing of hydrogen peroxide using metal nanoparticles: a review. Microchim. Acta 180:15–32 [Google Scholar]
  18. Chiwocha SDS, Abrams SR, Ambrose SJ, Cutler AJ, Loewen M. 18.  et al. 2003. A method for profiling classes of plant hormones and their metabolites using liquid chromatography-electrospray ionization tandem mass spectrometry: an analysis of hormone regulation of thermodormancy of lettuce (Lactuca sativa L.) seeds. Plant J 35:405–17 [Google Scholar]
  19. Corbesier L, Prinsen E, Jacqmard A. 19.  2003. Cytokinin levels in leaves, leaf exudate and shoot apical meristem of Arabidopsis thaliana during floral transition. J. Exp. Bot. 54:2511–17 [Google Scholar]
  20. Cristescu SM, Mandon J, Arslanov D, De Pessemier J, Hermans C, Harren FJM. 20.  2013. Current methods for detecting ethylene in plants. Ann. Bot. 111:347–60 [Google Scholar]
  21. 21.  Davies PJ. 2010. Plant Hormones: Biosynthesis, Signal Transduction, Action! Dordrecht, Neth.: Kluwer Acad, 3rd. [Google Scholar]
  22. Deng T, Wu D, Duan C, Guan Y. 22.  2016. Ultrasensitive quantification of endogenous brassinosteroids in milligram fresh plant with a quaternary ammonium derivatization reagent by pipette-tip solid-phase extraction coupled with ultra-high-performance liquid chromatography tandem mass spectrometry. J. Chromatogr. A 1456:105–12 [Google Scholar]
  23. Dewitte W, Chiappetta A, Azmi A, Witters E, Strnad M. 23.  et al. 1999. Dynamics of cytokinins in apical shoot meristems of a day-neutral tobacco during floral transition and flower formation. Plant Physiol 119:111–21 [Google Scholar]
  24. Ding J, Mao LJ, Yuan BF, Feng YQ. 24.  2013. A selective pretreatment method for determination of endogenous active brassinosteroids in plant tissues: double layered solid phase extraction combined with boronate affinity polymer monolith microextraction. Plant Methods 9:13 [Google Scholar]
  25. Ding J, Wu JH, Liu JF, Yuan BF, Feng YQ. 25.  2014. Improved methodology for assaying brassinosteroids in plant tissues using magnetic hydrophilic material for both extraction and derivatization. Plant Methods 10:39 [Google Scholar]
  26. Du F, Ruan G, Liang S, Xie F, Liu H. 26.  2012. Monolithic molecularly imprinted solid-phase extraction for the selective determination of trace cytokinins in plant samples with liquid chromatography-electrospray tandem mass spectrometry. Anal. Bioanal. Chem. 404:489–501 [Google Scholar]
  27. Du F, Ruan G, Liu H. 27.  2012. Analytical methods for tracing plant hormones. Anal. Bioanal. Chem. 403:55–74 [Google Scholar]
  28. Ellington AD, Szostak JW. 28.  1990. In vitro selection of RNA molecules that bind specific ligands. Nature 346:818–22 [Google Scholar]
  29. Esser B, Schnorr JM, Swager TM. 29.  2012. Selective detection of ethylene gas using carbon nanotube-based devices: utility in determination of fruit ripeness. Angew. Chem. Int. Ed. 51:5752–56 [Google Scholar]
  30. Floková K, Tarkowská D, Miersch O, Strnad M, Wasternack C, Novák O. 30.  2014. UHPLC-MS/MS based target profiling of stress-induced phytohormones. Phytochemistry 105:147–57 [Google Scholar]
  31. Fu C, Li JP. 31.  2014. A molecular imprinted sensor for trace detection of gibberellin based on ferrocenecarboxylic acid multiply marked dendrimer. Chin. J. Anal. Chem. 42:315–19 [Google Scholar]
  32. Fu J, Sun X, Wang J, Chu J, Yan C. 32.  2011. Progress in quantitative analysis of plant hormones. Chin. Sci. Bull. 56:355–66 [Google Scholar]
  33. Fujii T, Matsuda S, Tejedor ML, Esaki T, Sakane I. 33.  et al. 2015. Direct metabolomics for plant cells by live single-cell mass spectrometry. Nat. Protoc. 10:1445–56 [Google Scholar]
  34. Galbraith DW.34.  2010. Flow cytometry and fluorescence-activated cell sorting in plants: the past, present and future. Biomédica 30:65–70 [Google Scholar]
  35. Gan T, Hua C, Chen Z, Hua S. 35.  2010. Fabrication and application of a novel plant hormone sensor for the determination of methyl jasmonate based on self-assembling of phosphotungstic acid-graphene oxide nanohybrid on graphite electrode. Sens. Actuators B 151:8–14 [Google Scholar]
  36. Gan T, Hua C, Chen Z, Hua S. 36.  2011. A disposable electrochemical sensor for the determination of indole-3-acetic acid based on poly(safranine T)-reduced graphene oxide nanocomposite. Talanta 85:310–16 [Google Scholar]
  37. Gan T, Hua C, Chen Z, Hua S. 37.  2011. Novel electrocatalytic system for the oxidation of methyl jasmonate based on layer-by-layer assembling of montmorillonite and phosphotungstic acid nanohybrid on graphite electrode. Electrochim. Acta 56:4512–17 [Google Scholar]
  38. Gan T, Shi Z, Liu N, Lv Z, Sun J, Wang H. 38.  2015. A novel electrochemical sensing strategy for rapid and ultrasensitive detection of 6-benzylaminopurine in sprout vegetables by hollow core/shell-structured CuO@SiO2 microspheres. Food Anal. Methods 8:2504–14 [Google Scholar]
  39. Geilfus CM, Mithöfer A, Ludwig-Müller J, Zörb C, Muehling KH. 39.  2015. Chloride-inducible transient apoplastic alkalinizations induce stomata closure by controlling abscisic acid distribution between leaf apoplast and guard cells in salt-stressed Vicia faba. New Phytol. 208:803–16 [Google Scholar]
  40. Goble AM, Fan H, Sali A, Raushel FM. 40.  2011. Discovery of a cytokinin deaminase. ACS Chem. Biol. 6:1036–40 [Google Scholar]
  41. Grojean J, Downes B. 41.  2010. Riboswitches as hormone receptors: hypothetical cytokinin-binding riboswitches in Arabidopsis thaliana. Biol. Direct 5:60–72Provides a treatise on naturally occurring riboswitches and illustrates the potential of using synthetic riboswitches as biosensors. [Google Scholar]
  42. Hauserová E, Swaczynová J, Doležal K, Lenobel R, Popa I. 42.  et al. 2005. Batch immunoextraction method for efficient purification of aromatic cytokinins. J. Chromatogr. A 1100:116–25 [Google Scholar]
  43. Holčapek M, Jirásko R, Lísa M. 43.  2012. Recent developments in liquid chromatography-mass spectrometry and related techniques. J. Chromatogr. A 1259:3–15 [Google Scholar]
  44. Huang L, Tang X, Zhang W, Jiang R, Chen D. 44.  et al. 2016. Imaging of endogenous metabolites of plant leaves by mass spectrometry based on laser activated electron tunneling. Sci. Rep. 6:24164 [Google Scholar]
  45. Iinuma R, Ke Y, Jungmann R, Schlichthaerle T, Woehrstein JB, Yin P. 45.  2014. Polyhedra self-assembled from DNA tripods and characterized with 3D DNA-PAINT. Science 344:65–69 [Google Scholar]
  46. Immanen J, Nieminen K, Smolander OP, Kojima M, Alonso Serra J. 46.  et al. 2016. Cytokinin and auxin display distinct but interconnected distribution and signaling profiles to stimulate cambial activity. Curr. Biol. 26:1990–97 [Google Scholar]
  47. Israelsson M, Sundberg B, Moritz T. 47.  2005. Tissue-specific localization of gibberellins and expression of gibberellin-biosynthetic and signaling genes in wood-forming tissues in aspen. Plant J 44:494–504 [Google Scholar]
  48. Janssen S, Schmitt K, Blanke M, Bauersfeld ML, Wöllenstein J, Lang W. 48.  2014. Ethylene detection in fruit supply chains. Philos. Trans. A 372:20130311 [Google Scholar]
  49. Jin X, Wang RS, Zhu M, Jeon BW, Albert R. 49.  et al. 2013. Abscisic acid-responsive guard cell metabolomes of Arabidopsis wild-type and. gpa1 G-protein mutants. Plant Cell 25:4789–811Describes the phytohormone profiles in the Arabidopsis stomata, providing the first example of single-cell-resolution analysis using LC-MS/MS. [Google Scholar]
  50. Jiskrová E, Novák O, Pospíšilová H, Holubová K, Karády M. 50.  et al. 2016. Extra- and intracellular distribution of cytokinins in the leaves of monocots and dicots. New Biotechnol 33:735–42 [Google Scholar]
  51. Johnson A, Song Q, Ko Ferrigno P, Bueno PR, Davis JJ. 51.  2012. Sensitive affimer and antibody based impedimetric label-free assays for C-reactive protein. Anal. Chem. 84:6553–60 [Google Scholar]
  52. Jones AM.52.  2016. A new look at stress: abscisic acid patterns and dynamics at high-resolution. New Phytol 210:38–44Provides an insider's perspective on the case for genetically encoded biosensors, focusing on work creating and applying the ABACUS ABA FRET biosensors. [Google Scholar]
  53. Jones AM, Danielson JÅH, ManojKumar SN, Lanquar V, Grossmann G, Frommer WB. 53.  2014. Abscisic acid dynamics in roots detected with genetically encoded FRET sensors. eLife 3:e01741 [Google Scholar]
  54. Jungmann R, Avendaño MS, Maier S, Woehrstein JB, Dai M. 54.  et al. 2014. Multiplexed 3D cellular super-resolution imaging with DNA-PAINT and exchange-PAINT. Nat. Methods 11:313–18 [Google Scholar]
  55. Kathirvelan J, Vijayaraghavan R. 55.  2014. Development of prototype laboratory setup for selective detection of ethylene based on multiwalled carbon nanotubes. J. Sens. 2014:395035 [Google Scholar]
  56. Kim SK, Abe H, Little CH, Pharis RP. 56.  1990. Identification of two brassinosteroids from the cambial region of Scots pine (Pinus silverstris) by gas chromatography-mass spectrometry, after detection using a dwarf rice lamina inclination bioassay. Plant Physiol 94:1709–13 [Google Scholar]
  57. Kojima M, Kamada-Nobusada T, Komatsu H, Takei K, Kuroha T. 57.  et al. 2009. Highly sensitive and high-throughput analysis of plant hormones using MS-probe modification and liquid chromatography-tandem mass spectrometry: an application for hormone profiling in Oryza sativa. Plant Cell Physiol. 50:1201–14 [Google Scholar]
  58. Koo Y, Wang J, Zhang Q, Zhu H, Chehab EW. 58.  et al. 2015. Fluorescence reports intact quantum dot uptake into roots and translocation to leaves of Arabidopsis thaliana and subsequent ingestion by insect herbivores. Environ. Sci. Technol. 49:626–32 [Google Scholar]
  59. Kowalska M, Tian F, Šmehilová M, Galuszka P, Frébort I. 59.  et al. 2011. Prussian Blue acts as a mediator in a reagentless cytokinin biosensor. Anal. Chim. Acta 701:218–23 [Google Scholar]
  60. Kramer EM, Ackelsberg EM. 60.  2015. Auxin metabolism rates and implications for plant development. Front. Plant Sci. 6:150 [Google Scholar]
  61. Kruger NJ, Ratcliffe RG. 61.  2012. Pathways and fluxes: exploring the plant metabolic network. J. Exp. Bot. 63:2243–46 [Google Scholar]
  62. Kueger S, Steinhauser D, Willmitzer L, Giavalisco P. 62.  2012. High-resolution plant metabolomics: from plant spectral features to metabolites and from whole-cell analysis to subcellular metabolite distributions. Plant J 70:39–50 [Google Scholar]
  63. Larrieu A, Champion A, Legrand J, Lavenus J, Mast D. 63.  et al. 2015. A fluorescent hormone biosensor reveals the dynamics of jasmonate signalling in plants. Nat. Commun. 6:6043Describes the construction of the Jas9-VENUS biosensor and some beautifully delicate work using it to define the speed of signal movement. [Google Scholar]
  64. Li D, Guo Z, Chen Y. 64.  2016. Direct derivatization and quantitation of ultra-trace gibberellins in sub-milligram fresh plant organs. Mol. Plant 9:175–77 [Google Scholar]
  65. Li J, Li S, Wei X, Tao H, Pan H. 65.  2012. Molecularly imprinted electrochemical luminescence sensor based on signal amplification for selective determination of trace gibberellin A3. Anal. Chem. 84:9951–55 [Google Scholar]
  66. Li J, Xiao LT, Zeng GM, Huang GH, Shen GL. 66.  et al. 2003. Amperometric immunosensor based on polypyrrole/poly(m-pheylenediamine) multilayer on glassy carbon electrode for cytokinin N6-(Δ2-isopentenyl) adenosine assay. Anal. Biochem. 321:89–95 [Google Scholar]
  67. Li J, Yin W, Tan Y, Pan H. 67.  2014. A sensitive electrochemical molecularly imprinted sensor based on catalytic amplification by silver nanoparticles for 3-indoleacetic acid determination. Sensor. Actuat. B 197:109–15 [Google Scholar]
  68. Li YW, Xia K, Wang RZ. 68.  2008. An impedance immunosensor for the detection of the phytohormone abscisic acid. Anal. Bioanal. Chem. 391:2869–74 [Google Scholar]
  69. Liao CY, Smet W, Brunoud G, Yoshida S, Vernoux T, Weijers D. 69.  2015. Reporters for sensitive and quantitative measurement of auxin response. Nat. Methods 12:207–12Describes the careful development of some elegant biosensors that (semi-)quantify temporal changes in auxin concentrations in vivo. [Google Scholar]
  70. Liu C, Chen J, Mao G, Su C, Ji X, He Z. 70.  2016. Target-induced structure switching of a hairpin aptamer for the fluorescence detection of zeatin. Anal. Methods 8:5957–61 [Google Scholar]
  71. Liu H, Li X, Xiao J, Wang S. 71.  2012. A convenient method for simultaneous quantification of multiple phytohormones and metabolites: application in study of rice-bacterium interaction. Plant Methods 8:2 [Google Scholar]
  72. Liu JT, Hu LS, Liu YL, Chen RS, Cheng Z. 72.  et al. 2014. Real-time monitoring of auxin vesicular exocytotic efflux from single plant protoplasts by nanowires. Angew. Chem. Int. Ed. Engl. 53:2643–47 [Google Scholar]
  73. Liu X, Hegeman AD, Gardner G, Cohen JD. 73.  2012. Protocol: high-throughput and quantitative assays of auxin and auxin precursors from minute tissue samples. Plant Methods 8:31 [Google Scholar]
  74. Liu Z, Cai BD, Feng YQ. 74.  2012. Rapid determination of endogenous cytokinins in plant samples by combination of magnetic solid phase extraction with hydrophilic interaction chromatography-tandem mass spectrometry. J. Chromatogr. B 891–92:27–35 [Google Scholar]
  75. Ljung K, Bhalerao RP, Sandberg G. 75.  2001. Sites and homeostatic control of auxin biosynthesis in Arabidopsis during vegetative growth. Plant J 28:465–74 [Google Scholar]
  76. Ljung K, Hull AK, Celenza J, Yamada M, Estelle M. 76.  et al. 2005. Sites and regulation of auxin biosynthesis in Arabidopsis roots. Plant Cell 17:1090–94 [Google Scholar]
  77. Ljung K, Sandberg G, Moritz T. 77.  2004. Methods of plant hormone analysis. Plant Hormones: Biosynthesis, Signal Transduction, Action! PJ Dawies 671–94 Dordrecht, Neth.: Kluwer Acad. [Google Scholar]
  78. Llaudet E, Hatz S, Droniou M, Dale N. 78.  2005. Microelectrode biosensor for real-time measurement of ATP in biological tissue. Anal. Chem. 77:3267–73 [Google Scholar]
  79. Lockhart J.79.  2015. Measuring cytokinin levels in the root tip by the zeptomole. Plant Cell 27:1819 [Google Scholar]
  80. Mancuso S, Marras AM, Magnus V, Baluska F. 80.  2005. Noninvasive and continuous recordings of auxin fluxes in intact root apex with a carbon nanotube-modified and self-referencing microelectrode. Anal. Biochem. 341:344–51 [Google Scholar]
  81. Mauriat M, Sandberg LG, Moritz T. 81.  2011. Proper gibberellin localization in vascular tissue is required to control auxin-dependent leaf development and bud outgrowth in hybrid aspen. Plant J 67:805–16 [Google Scholar]
  82. McLafferty FW.82.  2011. A century of progress in molecular mass spectrometry. Annu. Rev. Anal. Chem. 4:1–22 [Google Scholar]
  83. McLamore ES, Diggs A, Calvo Marzal P, Shi J, Blakeslee JJ. 83.  et al. 2010. Non-invasive quantification of endogenous root auxin transport using an integrated flux microsensor technique. Plant J 63:1004–16 [Google Scholar]
  84. Moritz T, Olsen JE. 84.  1995. Comparison between high-resolution selected-ion monitoring, selected reaction monitoring, and 4-sector tandem mass-spectrometry in quantitative-analysis of gibberellins in milligram amounts of plant-tissue. Anal. Chem. 67:1711–16 [Google Scholar]
  85. Müller A, Düchting P, Weiler EW. 85.  2002. A multiplex GC-MS/MS technique for the sensitive and quantitative single-run analysis of acidic phytohormones and related compounds, and its application to Arabidopsis thaliana. Planta 216:44–56Uses multiple GC-MS/MS to create organ-distribution maps for the levels of several phytohormones in Arabidopsis at the flowering stage. [Google Scholar]
  86. Müller B, Sheen J. 86.  2008. Cytokinin and auxin interplay in root stem-cell specification during early embryogenesis. Nature 453:1094–97 [Google Scholar]
  87. Müller M, Munné-Bosch S. 87.  2011. Rapid and sensitive hormonal profiling of complex plant samples by liquid chromatography coupled to electrospray ionization tandem mass spectrometry. Plant Methods 7:37 [Google Scholar]
  88. Nakamura A, Higuchi K, Goda H, Fujiwara MT, Sawa S. 88.  et al. 2003. Brassinolide induces IAA5, IAA19, and DR5, a synthetic auxin response element in Arabidopsis, implying a cross talk point of brassinosteroid and auxin signaling. Plant Physiol 133:1843–53 [Google Scholar]
  89. Nonhebel HM, Cooney TP. 89.  1990. Measurement of the in vivo rate of indole-acetic acid turnover. Plant Growth Substances 1988 RP Pharis, SB Rood 333–40 Berlin: Springer [Google Scholar]
  90. Novák J, Černý M, Pavlů J, Zemánková J, Skalák J. 90.  et al. 2015. Roles of proteome dynamics and cytokinin signaling in root-to-hypocotyl ratio changes induced by shading roots of Arabidopsis seedlings. Plant Cell Physiol 56:1006–18 [Google Scholar]
  91. Novák O, Hauserová E, Amakorová P, Doležal K, Strnad M. 91.  2008. Cytokinin profiling in plant tissues using ultra-performance liquid chromatography-electrospray tandem mass spectrometry. Phytochemistry 69:2214–24 [Google Scholar]
  92. Novák O, Hényková E, Sairanen I, Kowalczyk M, Pospíšil T, Ljung K. 92.  2012. Tissue specific profiling of the Arabidopsis thaliana auxin metabolome. Plant J 72:523–36 [Google Scholar]
  93. Novák O, Pěnčík A, Ljung K. 93.  2014. Identification and profiling of auxin and auxin metabolites. Auxin and Its Role in Plant Development E Zažímalová, J Petrášek, E Benková 39–60 Vienna: Springer [Google Scholar]
  94. Nováková L.94.  2013. Challenges in the development of bioanalytical liquid chromatography-mass spectrometry method with emphasis on fast analysis. J. Chromatogr. A 1292:25–37 [Google Scholar]
  95. Oikawa A, Saito K. 95.  2012. Metabolite analyses of single cells. Plant J 70:30–38 [Google Scholar]
  96. Okumoto S, Jones A, Frommer WB. 96.  2012. Quantitative imaging with fluorescent biosensors. Annu. Rev. Plant Biol. 63:663–706 [Google Scholar]
  97. Pan X, Welti R, Wang X. 97.  2008. Simultaneous quantification of major phytohormones and related compounds in crude plant extracts by liquid chromatography-electrospray tandem mass spectrometry. Phytochemistry 69:1773–82 [Google Scholar]
  98. Pěnčík A, Simonovik B, Petersson SV, Henyková E, Simon S. 98.  et al. 2013. Regulation of auxin homeostasis and gradients in Arabidopsis roots through the formation of the IAA catabolite oxIAA. Plant Cell 25:3858–70 [Google Scholar]
  99. Petersson SV, Johansson AI, Kowalczyk M, Makoveychuk A, Wang JY. 99.  et al. 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 21:1659–68 [Google Scholar]
  100. Polanská L, Vicánková A, Nováková M, Malbeck J, Dobrev PI. 100.  et al. 2007. Altered cytokinin metabolism affects cytokinin, auxin, and abscisic acid contents in leaves and chloroplasts, and chloroplast ultrastructure in transgenic tobacco. J. Exp. Bot. 58:637–49 [Google Scholar]
  101. Porco S, Pěnčík A, Rashed A, Voß U, Casanova-Sáez R. 101.  et al. 2016. The dioxygenase-encoding AtDAO1 gene controls IAA oxidation and homeostasis in Arabidopsis. PNAS 113:11016–21 [Google Scholar]
  102. Porfírio S, Gomes da Silva MDR, Peixe A, Cabrita MJ, Azadi P. 102.  2016. Current analytical methods for plant auxin quantification—a review. Anal. Chim. Acta 902:8–21 [Google Scholar]
  103. Pothoulakis G, Ceroni F, Reeve B, Ellis T. 103.  2014. The spinach RNA aptamer as a characterization tool for synthetic biology. ACS Synth. Biol. 3:182–87 [Google Scholar]
  104. Qi C, Bing T, Mei H, Yang X, Liu X, Shangguan D. 104.  2013. G-quadruplex DNA aptamers for zeatin recognizing. Biosens. Bioelectron. 41:157–62Describes the selection of aptamers that adopt a hairpin-G-quadruplex structure for binding to zeatin and shows that the fluorescence aptasensor is selective for zeatin. [Google Scholar]
  105. Ranocha P, Dima O, Nagy R, Felten J, Corratgé-Faillie C. 105.  et al. 2013. Arabidopsis WAT1 is a vacuolar auxin transport facilitator required for auxin homoeostasis. Nat. Commun. 4:2625 [Google Scholar]
  106. Romanov GA, Kieber JJ, Schmülling T. 106.  2002. A rapid cytokinin response assay in Arabidopsis indicates a role for phospholipase D in cytokinin signalling. FEBS Lett 515:39–43 [Google Scholar]
  107. Sadanandom A, Napier RM. 107.  2010. Biosensors in plants. Curr. Opin. Plant Biol. 13:736–43 [Google Scholar]
  108. Sandberg G, Gardeström P, Sitbon F, Olsson O. 108.  1990. Presence of indole-3-acetic acid in chloroplasts of Nicotiana tabacum. Pinus sylvestris. Planta 180:562–68 [Google Scholar]
  109. Schäfer M, Brütting C, Baldwin IT, Kallenbach M. 109.  2016. High-throughput quantification of more than 100 primary- and secondary-metabolites, and phytohormones by a single solid-phase extraction based sample preparation with analysis by UHPLC–HESI–MS/MS. Plant Methods 12:30 [Google Scholar]
  110. Schütze T, Wilhelm B, Greiner N, Braun H, Peter F. 110.  et al. 2011. Probing the SELEX process with next-generation sequencing. PLOS ONE 6:e29604 [Google Scholar]
  111. Seo H, Kriechbaumer V, Park WJ. 111.  2016. Modern quantitative analytical tools and biosensors for functional studies of auxin. J. Plant Biol. 59:93–104 [Google Scholar]
  112. Shimizu T, Miyakawa S, Esaki T, Mizuno H, Masujima T. 112.  et al. 2015. Live single-cell plant hormone analysis by video-mass spectrometry. Plant Cell Physiol 56:1287–96Describes experiments in which a nano-electrospray ionization tip under a microscope was subjected to direct single-cell analysis of ABA and JA-Ile. [Google Scholar]
  113. Slavkovic S, Altunisik M, Reinstein O, Johnson PE. 113.  2015. Structure-affinity relationship of the cocaine-binding aptamer with quinine derivatives. Bioorg. Med. Chem 232593–97 [Google Scholar]
  114. Stirk WA, Van Staden J, Novák O, Doležal K, Strnad M. 114.  et al. 2011. Changes in endogenous cytokinin concentrations in Chlorella (Chlorophyceae) in relation to light and the cell cycle. J. Phycol. 47:291–301 [Google Scholar]
  115. Su C, Liu C, Chen J, Chen Z, He Z. 115.  2016. Simultaneous determination of zeatin and systemin by coupling graphene oxide-protected aptamers with catalytic recycling of DNase I. Sens. Actuators B 230:442–48 [Google Scholar]
  116. Sugawara S, Hishiyama S, Jikumaru Y, Hanada A, Nishimura T. 116.  et al. 2009. Biochemical analyses of indole-3-acetaldoxime-dependent auxin biosynthesis in Arabidopsis. PNAS 106:5430–35 [Google Scholar]
  117. Sun B, Chen L, Xu Y, Liu M, Yin H, Ai S. 117.  2014. Ultrasensitive photoelectrochemical immunoassay of indole-3-acetic acid based on the MPA-modified CdS/RGO nanocomposites decorated ITO electrode. Biosens. Bioelectron. 51:164–69 [Google Scholar]
  118. Svačinová J, Novák O, Plačková L, Lenobel R, Holík J. 118.  et al. 2012. A new approach for cytokinin isolation from Arabidopsis tissues using miniaturized purification: pipette tip solid-phase extraction. Plant Methods 8:17 [Google Scholar]
  119. Svatos A.119.  2010. Mass spectrometric imaging of small molecules. Trends Biotechnol 28:425–34 [Google Scholar]
  120. Tanaka M, Takei K, Kojima M, Sakakibara H, Mori H. 120.  2006. Auxin controls local cytokinin biosynthesis in the nodal stem in apical dominance. Plant J 45:1028–36 [Google Scholar]
  121. Tarkowská D, Filek M, Biesaga-Kościelniak J, Marcińska I, Macháčková I. 121.  et al. 2012. Cytokinins in shoot apices of Brassica napus plants during vernalization. Plant Sci 187:105–12 [Google Scholar]
  122. Tarkowská D, Novák O, Floková K, Tarkowski P, Turečková V. 122.  et al. 2014. Quo vadis plant hormone analysis?. Planta 240:55–76 [Google Scholar]
  123. Tarkowski P, Floková K, Václavíková K, Jaworek P, Rauset M. 123.  et al. 2010. An improved in vivo deuterium labeling method for measuring the biosynthetic rate of cytokinins. Molecules 15:9214–29 [Google Scholar]
  124. Tian F, Greplová M, Frébort I, Dale N, Napier RM. 124.  2014. A highly selective biosensor with nanomolar sensitivity based on cytokinin dehydrogenase. PLOS ONE 9:e90877 [Google Scholar]
  125. Tuominen H, Puech L, Fink S, Sundberg B. 125.  1997. A radial concentration gradient of indole-3-acetic acid is related to secondary xylem development in hybrid aspen. Plant Physiol 115:577–85 [Google Scholar]
  126. Uggla C, Moritz T, Sandberg G, Sundberg B. 126.  1996. Auxin as a positional signal in pattern formation in plants. PNAS 93:9282–86 [Google Scholar]
  127. Uslu VV, Grossmann G. 127.  2016. The biosensor toolbox for plant developmental biology. Curr. Opin. Plant Biol. 29:138–47 [Google Scholar]
  128. Van Meulebroek L, Vanden Bussche J, Steppe K, Vanhaecke L. 128.  2012. Ultra-high performance liquid chromatography coupled to high resolution Orbitrap mass spectrometry for metabolomic profiling of the endogenous phytohormonal status of the tomato plant. J. Chromatogr. A 1260:67–80 [Google Scholar]
  129. Waadt R, Hitomi K, Nishimura N, Hitomi C, Adams SR. 129.  et al. 2014. FRET-based reporters for the direct visualization of abscisic acid concentration changes and distribution in Arabidopsis. eLife 3:e01739 [Google Scholar]
  130. Wachter A, Tunc-Ozdemir M, Grove BC, Green PJ, Shintani DK, Breaker RR. 130.  2007. Riboswitch control of gene expression in plants by splicing and alternative end processing of mRNAs. Plant Cell 19:3437–50 [Google Scholar]
  131. Wang HC, Lee AR. 131.  2014. Recent developments in blood glucose sensors. J. Food Drug Anal. 23:191–200 [Google Scholar]
  132. Wang J.132.  2001. Glucose biosensors: 40 years of advances and challenges. Electroanalysis 13:983–88 [Google Scholar]
  133. Wells DM, Laplaze L, Bennett MJ, Vernoux T. 133.  2013. Biosensors for phytohormone quantification: challenges, solutions, and opportunities. Trends Plant Sci 18:244–49 [Google Scholar]
  134. Wend S, Dal Bosco C, Kämpf MM, Ren F, Palme K. 134.  et al. 2013. A quantitative ratiometric sensor for time-resolved analysis of auxin dynamics. Sci. Rep. 3:2052 [Google Scholar]
  135. Xiao C, Liu YL, Xu JQ, Lv SW, Guo S, Huang WH. 135.  2015. Real-time monitoring of H2O2 release from single cells using nanoporous gold microelectrodes decorated with platinum nanoparticles. Analyst 140:3753–58 [Google Scholar]
  136. Yang X, Han Q, Zhang Y. 136.  2015. Determination of free tryptophan in serum with aptamer—comparison of two aptasensors. Talanta 131:672–77 [Google Scholar]
  137. Yates JR III. 137.  2011. A century of mass spectrometry: from atoms to proteomes. Nat. Methods 8:633–37 [Google Scholar]
  138. Yaxley JR, Ross JJ, Sherriff LJ, Reid JB. 138.  2001. Gibberellin biosynthesis mutations and root development in pea. Plant Physiol 125:627–33 [Google Scholar]
  139. Yin H, Xu Z, Zhou Y, Wang M, Ai S. 139.  2013. An ultrasensitive electrochemical immunosensor platform with double signal amplification for indole-3-acetic acid determinations in plant seeds. Analyst 138:1851–57 [Google Scholar]
  140. Yokota T, Higuchi K, Takahashi N, Kamuro Y, Watanabe T, Takatsuto S. 140.  1998. Identification of brassinosteroids with epimerized substituents and/or the 23-oxo group in pollen and anthers of Japanese cedar. Biosci. Biotechnol. Biochem. 62:526–31 [Google Scholar]
  141. Yu P, Eggert K, von Wiren N, Li CJ, Hochholdinger F. 141.  2015. Cell type-specific gene expression analyses by RNA sequencing reveal local high nitrate-triggered lateral root initiation in shoot-borne roots of maize by modulating auxin-related cell cycle regulation. Plant Physiol 169:690–704 [Google Scholar]
  142. Zhang J, Nodzyńskia T, Pěnčík A, Rolčík J, Friml J. 142.  2010. PIN phosphorylation is sufficient to mediate PIN polarity and direct auxin transport. PNAS 107:918–22 [Google Scholar]
  143. Zhang K, Novak O, Wei Z, Gou M, Zhang X. 143.  et al. 2014. Arabidopsis ABCG14 protein controls the acropetal translocation of root-synthesized cytokinins. Nat. Commun. 5:3274 [Google Scholar]
  144. Zhang LM, Wei XP, Wei YX, Li JP, Zeng Y. 144.  2014. Determination of trace gibberellin A3 by magnetic self‐assembly molecularly imprinted electrochemical sensor. Chin. J. Anal. Chem. 42:1580–85 [Google Scholar]
  145. Zhang Q, Li G, Xiao X, Zhan S, Cao Y. 145.  2016. Efficient and selective enrichment of ultratrace cytokinins in plant samples by magnetic perhydroxy-cucurbit[8]uril microspheres. Anal. Chem. 88:4055–62 [Google Scholar]
  146. Zhang Y, Li Y, Hu Y, Li G, Chen Y. 146.  2010. Preparation of magnetic indole-3-acetic acid imprinted polymer beads with 4-vinylpyridine and β-cyclodextrin as binary monomer via microwave heating initiated polymerization and their application to trace analysis of auxins in plant tissues. J. Chromatogr. A 1217:7337–44 [Google Scholar]
  147. Zhao Z, Andersen SU, Ljung K, Dolezal K, Miotk A. 147.  et al. 2010. Hormonal control of the shoot stem-cell niche. Nature 465:1089–92 [Google Scholar]
  148. Zhou Y, Xua Z, Wang M, Meng X, Yina H. 148.  2013. Electrochemical immunoassay platform for high sensitivity detection of indole-3-acetic acid. Electrochim. Acta 96:66–73 [Google Scholar]
  149. Zürcher E, Tavor-Deslex D, Lituiev D, Enkerli K, Tarr PT, Müller B. 149.  2013. A robust and sensitive synthetic sensor to monitor the transcriptional output of the cytokinin signaling network in planta. Plant Physiol 161:1066–75 [Google Scholar]

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