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Sensors for Plant Sciences

Compiled by Yuuma Ishikawa, Mayuri Sadoine & Wolf B. Frommer

These lists were compiled for an “update” section for Plant Physiology (Sadoine et al., 2021). Please contact us if you would like to add information or add comments.  


Table 1. List of ion and metabolite and transporter sensors for plant sciences*

* extensive list, but far from being comprehensive

m, mutant; smMLCK, smooth-muscle myosin light-chain kinase; p, peptide


Table 2. Calcium sensors


Ahmad M, Anjum NA, Asif A, Ahmad A (2020) Real-time monitoring of glutathione in living cells using genetically encoded FRET-based ratiometric nanosensor. Sci Rep 10: 1–9

Ahmad M, Mohsin M, Iqrar S, Manzoor O, Siddiqi TO, Ahmad A (2018) Live cell imaging of vitamin B12 dynamics by genetically encoded fluorescent nanosensor. Sens Actuators B Chem 257: 866–874

Akerboom J, Rivera JDV, Guilbe MMR, Malavé ECA, Hernandez HH, Tian L, Hires SA, Marvin JS, Looger LL, Schreiter ER (2009) Crystal structures of the GCaMP calcium sensor reveal the mechanism of fluorescence signal change and aid rational design. J Biol Chem 284: 6455–6464

Ali HM, Ahmad M, Salem MZ, Ahmad A (2020) Construction of a nanosensor for non-invasive imaging of hydrogen peroxide levels in living cells. Biology 9: 430

Ameen S, Ahmad M, Mohsin M, Qureshi MI, Ibrahim MM, Abdin MZ, Ahmad A (2016) Designing, construction and characterization of genetically encoded FRET-based nanosensor for real time monitoring of lysine flux in living cells. J Nanobiotechnology 14: 49

Arce-Molina R, Cortés-Molina F, Sandoval PY, Galaz A, Alegría K, Schirmeier S, Barros LF, San Martín A (2020) A highly responsive pyruvate sensor reveals pathway-regulatory role of the mitochondrial pyruvate carrier MPC. eLife 9: e53917

Ast C, De Michele R, Kumke MU, Frommer WB (2015) Single-fluorophore membrane transport activity sensors with dual-emission read-out. eLife 4: e07113

Ast C, Foret J, Oltrogge LM, Michele RD, Kleist TJ, Ho C-H, Frommer WB (2017) Ratiometric Matryoshka biosensors from a nested cassette of green- and orange-emitting fluorescent proteins. Nat Comm 8: 431

Baird GS, Zacharias DA, Tsien RY (1999) Circular permutation and receptor insertion within green fluorescent proteins. Proceedings of the National Academy of Sciences of the United States of America 96: 11241–6

Belousov VV, Fradkov AF, Lukyanov KA, Staroverov DB, Shakhbazov KS, Terskikh AV, Lukyanov S (2006) Genetically encoded fluorescent indicator for intracellular hydrogen peroxide. Nat Methods 3: 281–286

Berg J, Hung YP, Yellen G (2009) A genetically encoded fluorescent reporter of ATP: ADP ratio. Nat Methods 6: 161–166

Bilan DS, Pase L, Joosen L, Gorokhovatsky AY, Ermakova YG, Gadella TW, Grabher C, Schultz C, Lukyanov S, Belousov VV (2013) HyPer-3: a genetically encoded H2O2 probe with improved performance for ratiometric and fluorescence lifetime imaging. ACS Chem Biol 8: 535–542

Bischof H, Rehberg M, Stryeck S, Artinger K, Eroglu E, Waldeck-Weiermair M, Gottschalk B, Rost R, Deak AT, Niedrist T (2017) Novel genetically encoded fluorescent probes enable real-time detection of potassium in vitro and in vivo. Nat Commun 8: 1–12

Bogner M, Ludewig U (2007) Visualization of arginine influx into plant cells using a specific FRET-sensor. J Fluoresc 17: 350–360

Bulusu V, Prior N, Snaebjornsson MT, Kuehne A, Sonnen KF, Kress J, Stein F, Schultz C, Sauer U, Aulehla A (2017) Spatiotemporal analysis of a glycolytic activity gradient linked to mouse embryo mesoderm development. Dev Cell 40: 331-341. e4

Chen T-W, Wardill TJ, Sun Y, Pulver SR, Renninger SL, Baohan A, Schreiter ER, Kerr RA, Orger MB, Jayaraman V, et al (2013) Ultrasensitive fluorescent proteins for imaging neuronal activity. Nature 499: 295–300

Dana H, Sun Y, Mohar B, Hulse BK, Kerlin AM, Hasseman JP, Tsegaye G, Tsang A, Wong A, Patel R, et al (2019) High-performance calcium sensors for imaging activity in neuronal populations and microcompartments. Nat Methods 16: 649–657

De Michele R, Ast C, Loqué D, Ho C-H, Andrade SL, Lanquar V, Grossmann G, Gehne S, Kumke MU, Frommer WB (2013) Fluorescent sensors reporting the activity of ammonium transceptors in live cells. eLife 2: e00800

Deuschle K (2006) Rapid metabolism of glucose detected with FRET glucose nanosensors in epidermal cells and intact roots of Arabidopsis RNA-silencing mutants. Plant Cell 18: 2314–2325

Deuschle K, Okumoto S, Fehr M, Looger LL, Kozhukh L, Frommer WB (2005) Construction and optimization of a family of genetically encoded metabolite sensors by semirational protein engineering. Protein Sci 14: 2304–2314

DíazGarcía CM, Lahmann C, MartínezFrançois JR, Li B, Koveal D, Nathwani N, Rahman M, Keller JP, Marvin JS, Looger LL (2019) Quantitative in vivo imaging of neuronal glucose concentrations with a genetically encoded fluorescence lifetime sensor. J Neurosci Res 97: 946–960

Ding Y, Li J, Enterina JR, Shen Y, Zhang I, Tewson PH, Mo GCH, Zhang J, Quinn AM, Hughes TE, et al (2015) Ratiometric biosensors based on dimerization-dependent fluorescent protein exchange. Nat Methods 12: 195–198

Ermakova YG, Bilan DS, Matlashov ME, Mishina NM, Markvicheva KN, Subach OM, Subach FV, Bogeski I, Hoth M, Enikolopov G (2014) Red fluorescent genetically encoded indicator for intracellular hydrogen peroxide. Nat Commun 5: 5222

Ewald JC, Reich S, Baumann S, Frommer WB, Zamboni N (2011) Engineering genetically encoded nanosensors for real-time in vivo measurements of citrate concentrations. PLoS One 6: e28245

Fehr M, Frommer WB, Lalonde S (2002) Visualization of maltose uptake in living yeast cells by fluorescent nanosensors. Proc Natl Acad Sci USA 99: 9846–9851

Gruenwald K, Holland JT, Stromberg V, Ahmad A, Watcharakichkorn D, Okumoto S (2012) Visualization of glutamine transporter activities in living cells using genetically encoded glutamine sensors. PLoS One 7: e38591

Gu H, Lalonde S, Okumoto S, Looger LL, Scharff-Poulsen AM, Grossman AR, Kossmann J, Jakobsen I, Frommer WB (2006) A novel analytical method for in vivo phosphate tracking. FEBS Lett 580: 5885–5893

Gutscher M, Pauleau A-L, Marty L, Brach T, Wabnitz GH, Samstag Y, Meyer AJ, Dick TP (2008) Real-time imaging of the intracellular glutathione redox potential. Nat Methods 5: 553–559

Gutscher M, Sobotta MC, Wabnitz GH, Ballikaya S, Meyer AJ, Samstag Y, Dick TP (2009) Proximity-based protein thiol oxidation by H2O2-scavenging peroxidases. J Biol Chem 284: 31532–31540

Hendel T, Mank M, Schnell B, Griesbeck O, Borst A, Reiff DF (2008) Fluorescence changes of genetic calcium indicators and OGB-1 correlated with neural activity and calcium in vivo and in vitro. J Neurosci 28: 7399–411

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

Ho C-H, Frommer WB (2014) Fluorescent sensors for activity and regulation of the nitrate transceptor CHL1/NRT1. 1 and oligopeptide transporters. eLife 3: e01917

Horikawa K, Yamada Y, Matsuda T, Kobayashi K, Hashimoto M, Matsu-ura T, Miyawaki A, Michikawa T, Mikoshiba K, Nagai T (2010) Spontaneous network activity visualized by ultrasensitive Ca2+ indicators, yellow Cameleon-Nano. Nat Methods 7: 729–732

Hu H, Gu Y, Xu L, Zou Y, Wang A, Tao R, Chen X, Zhao Y, Yang Y (2017) A genetically encoded toolkit for tracking live-cell histidine dynamics in space and time. Sci Rep 7: 1–9

Imamura H, Nhat KPH, Togawa H, Saito K, Iino R, Kato-Yamada Y, Nagai T, Noji H (2009) Visualization of ATP levels inside single living cells with fluorescence resonance energy transfer-based genetically encoded indicators. Proc Natl Acad Sci USA 106: 15651–15656

Inoue M, Takeuchi A, Manita S, Horigane S, Sakamoto M, Kawakami R, Yamaguchi K, Otomo K, Yokoyama H, Kim R, et al (2019) Rational Engineering of XCaMPs, a Multicolor GECI Suite for In Vivo Imaging of Complex Brain Circuit Dynamics. Cell 177: 1346-1360.e24

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

Kaper T, Lager I, Looger LL, Chermak D, Frommer WB (2008) Fluorescence resonance energy transfer sensors for quantitative monitoring of pentose and disaccharide accumulation in bacteria. Biotechnol Biofuels 1: 1–10

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

Kausar H, Ambrin G, Okla MK, Alamri SA, Soufan WH, Ibrahim EI, Abdel-Maksoud MA, Ahmad A (2021) FRET-based genetically encoded nanosensor for real-time monitoring of the flux of α-tocopherol in living cells. ACS omega 6: 9020–9027

Krebs M, Held K, Binder A, Hashimoto K, Den Herder G, Parniske M, Kudla J, Schumacher K (2012) FRET-based genetically encoded sensors allow high-resolution live cell imaging of Ca2+ dynamics. The Plant journal : for cell and molecular biology 69: 181–92

Lager I, Fehr M, Frommer WB, Lalonde S (2003) Development of a fluorescent nanosensor for ribose. FEBS Lett 553: 85–89

Lager I, Looger LL, Hilpert M, Lalonde S, Frommer WB (2006) Conversion of a putative Agrobacterium sugar-binding protein into a FRET sensor with high selectivity for sucrose. J Biol Chem 281: 30875–30883

Lanquar V, Grossmann G, Vinkenborg JL, Merkx M, Thomine S, Frommer WB (2014) Dynamic imaging of cytosolic zinc in Arabidopsis roots combining FRET sensors and RootChip technology. New Phytol 202: 198–208

Lindenburg LH, Vinkenborg JL, Oortwijn J, Aper SJ, Merkx M (2013) MagFRET: the first genetically encoded fluorescent Mg2+ sensor. PloS one 8: e82009

Mank M, Santos AF, Direnberger S, Mrsic-Flogel TD, Hofer SB, Stein V, Hendel T, Reiff DF, Levelt C, Borst A (2008) A genetically encoded calcium indicator for chronic in vivo two-photon imaging. Nat Methods 5: 805–811

Markvicheva KN, Bilan DS, Mishina NM, Gorokhovatsky AY, Vinokurov LM, Lukyanov S, Belousov VV (2011) A genetically encoded sensor for H2O2 with expanded dynamic range. Bioorg Med Chem 19: 1079–1084

Marvin JS, Borghuis BG, Tian L, Cichon J, Harnett MT, Akerboom J, Gordus A, Renninger SL, Chen T-W, Bargmann CI (2013) An optimized fluorescent probe for visualizing glutamate neurotransmission. Nat Methods 10: 162

Marvin JS, Shimoda Y, Magloire V, Leite M, Kawashima T, Jensen TP, Kolb I, Knott EL, Novak O, Podgorski K (2019) A genetically encoded fluorescent sensor for in vivo imaging of GABA. Nat Methods 16: 763–770

Miyawaki A, Griesbeck O, Heim R, Tsien RY (1999) Dynamic and quantitative Ca2+ measurements using improved cameleons. Proceedings of the National Academy of Sciences of the USA 96: 2135–40

Miyawaki A, Llopis J, Heim R, McCaffery JM, Adams JA, Ikura M, Tsien RY (1997) Fluorescent indicators for Ca2+ based on green fluorescent proteins and calmodulin. Nature 388: 882–7

Mohsin M, Abdin MZ, Nischal L, Kardam H, Ahmad A (2013) Genetically encoded FRET-based nanosensor for in vivo measurement of leucine. Biosens Bioelectron 50: 72–77

Mohsin M, Ahmad A (2014) Genetically-encoded nanosensor for quantitative monitoring of methionine in bacterial and yeast cells. Biosens Bioelectron 59: 358–364

Morgan B, Van Laer K, Owusu TN, Ezeriņa D, Pastor-Flores D, Amponsah PS, Tursch A, Dick TP (2016) Real-time monitoring of basal H2O2 levels with peroxiredoxin-based probes. Nat Chem Biol 12: 437–443

Nagai T, Yamada S, Tominaga T, Ichikawa M, Miyawaki A (2004) Expanded dynamic range of fluorescent indicators for Ca2+ by circularly permuted yellow fluorescent proteins. Proceedings of the National Academy of Sciences of the United States of America 101: 10554–9

Ngo QA, Vogler H, Lituiev DS, Nestorova A, Grossniklaus U (2014) A calcium dialog mediated by the FERONIA signal transduction pathway controls plant sperm delivery. Dev Cell 29: 491–500

Nietzel T, Mostertz J, Ruberti C, Née G, Fuchs P, Wagner S, Moseler A, Müller-Schüssele SJ, Benamar A, Poschet G (2020) Redox-mediated kick-start of mitochondrial energy metabolism drives resource-efficient seed germination. Proc Natl Acad Sci USA 117: 741–751

Okada S, Ota K, Ito T (2009) Circular permutation of ligand‐binding module improves dynamic range of genetically encoded FRET‐based nanosensor. Protein Sci 18: 2518–2527

Okumoto S, Looger LL, Micheva KD, Reimer RJ, Smith SJ, Frommer WB (2005) Detection of glutamate release from neurons by genetically encoded surface-displayed FRET nanosensors. Proc Natl Acad Sci USA 102: 8740–8745

Palmer AE, Giacomello M, Kortemme T, Hires SA, Lev-Ram V, Baker D, Tsien RY (2006) Ca2+ indicators based on computationally redesigned calmodulin-peptide pairs. Chem Biol 13: 521–30

Park J, Chavez TM, Frommer W, Cheung LS (2020) Quantitative analysis of transporter activity biosensors. bioRxiv. doi: 10.1101/2020.09.03.282301

Pei Z-M, Murata Y, Benning G, Thomine S, Klusener B, Allen GJ, Grill E, Schroeder JI (2000) Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cells. Nature 406: 731–714

Rizza A, Tang B, Stanley CE, Grossmann G, Owen MR, Band LR, Jones AM (2021) Differential biosynthesis and cellular permeability explain longitudinal gibberellin gradients in growing roots. Proc Natl Acad Sci USA 118: e1921960118

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

Romoser VA, Hinkle PM, Persechini A (1997) Detection in living cells of Ca2+-dependent changes in the fluorescence emission of an indicator composed of two green fluorescent protein variants linked by a calmodulin-binding sequence. Journal of Biological Chemistry 272: 13270–13274

Sadoine M., Ishikawa M., Kleist T., Wudick M.W., Nakamura M., Grossmann G., Frommer W.B.& Ho C.H. (2021) Designs, applications, and limitations of genetically encoded fluorescent sensors to explore plant biology. Plant Physiol. online. doi.org/10.1093/plphys/kiab353

Sahu A, Banerjee S, Raju AS, Chiou T-J, Garcia LR, Versaw WK (2020) Spatial profiles of phosphate in roots indicate developmental control of uptake, recycling, and sequestration. Plant Physiol 184: 2064–2077

San Martín A, Ceballo S, Ruminot I, Lerchundi R, Frommer WB, Barros LF (2013) A genetically encoded FRET lactate sensor and its use to detect the Warburg effect in single cancer cells. PloS one 8: e57712

Singh S, Sharma MP, Ahmad A (2020) Construction and characterization of protein-based cysteine nanosensor for the real time measurement of cysteine level in living cells. Int J Biol Macromol 143: 273–284

Singh S, Sharma MP, Alqarawi AA, Hashem A, Abd_Allah EF, Ahmad A (2019) Real-time optical detection of isoleucine in living cells through a genetically-encoded nanosensor. Sensors 20: 146

Tantama M, Yellen G (2014) Imaging changes in the cytosolic ATP-to-ADP ratio. Methods Enzymol 547: 355–371

Thestrup T, Litzlbauer J, Bartholomäus I, Mues M, Russo L, Dana H, Kovalchuk Y, Liang Y, Kalamakis G, Laukat Y (2014) Optimized ratiometric calcium sensors for functional in vivo imaging of neurons and T lymphocytes. Nat Methods 11: 175–182

Tian L, Hires SA, Mao T, Huber D, Chiappe ME, Chalasani SH, Petreanu L, Akerboom J, McKinney SA, Schreiter ER, et al (2009) Imaging neural activity in worms, flies and mice with improved GCaMP calcium indicators. Nature Methods 6: 875–81

Toyota M, Spencer D, Sawai-Toyota S, Jiaqi W, Zhang T, Koo AJ, Howe GA, Gilroy S (2018) Glutamate triggers long-distance, calcium-based plant defense signaling. Science 361: 1112–1115

Voon CP, Guan X, Sun Y, Sahu A, Chan MN, Gardeström P, Wagner S, Fuchs P, Nietzel T, Versaw WK (2018) ATP compartmentation in plastids and cytosol of Arabidopsis thaliana revealed by fluorescent protein sensing. Proc Natl Acad Sci USA 115: E10778–E10787

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

Waadt R, Köster P, Andrés Z, Waadt C, Bradamante G, Lampou K, Kudla J, Schumacher K (2020) Dual-reporting transcriptionally linked genetically encoded fluorescent indicators resolve the spatiotemporal coordination of cytosolic abscisic acid and second messenger dynamics in Arabidopsis. Plant Cell 32: 2582–2601

Yaginuma H, Kawai S, Tabata KV, Tomiyama K, Kakizuka A, Komatsuzaki T, Noji H, Imamura H (2014) Diversity in ATP concentrations in a single bacterial cell population revealed by quantitative single-cell imaging. Sci Rep 4: 1–7

Yang H, Bogner M, Stierhof Y-D, Ludewig U (2010) H+-independent glutamine transport in plant root tips. PLoS One 5: e8917

Yang Y, Liu N, He Y, Liu Y, Ge L, Zou L, Song S, Xiong W, Liu X (2018) Improved calcium sensor GCaMP-X overcomes the calcium channel perturbations induced by the calmodulin in GCaMP. Nature Communications 9: 1504

Zarowny L, Aggarwal A, Rutten VM, Kolb I, Project G, Patel R, Huang H-Y, Chang Y-F, Phan T, Kanyo R (2020) Bright and high-performance genetically encoded Ca2+ indicator based on mNeonGreen fluorescent protein. ACS sens 5: 1959–1968

Zhang C, Ye B-C (2014) A single fluorescent protein-based sensor for in vivo 2-oxogluatarate detection in cell. Biosens Bioelectron 54: 15–19

Zhang WH, Herde MK, Mitchell JA, Whitfield JH, Wulff AB, Vongsouthi V, Sanchez-Romero I, Gulakova PE, Minge D, Breithausen B (2018) Monitoring hippocampal glycine with the computationally designed optical sensor GlyFS. Nat Chem Biol 14: 861–869

Zhao Y, Araki S, Wu J, Teramoto T, Chang Y-F, Nakano M, Abdelfattah AS, Fujiwara M, Ishihara T, Nagai T (2011) An expanded palette of genetically encoded Ca2+ indicators. Science 333: 1888–1891