Development and properties of genetically encoded pH sensors in plants

Frontiers in Plant Science

Volumn 4, Issue DEC, 2013, Pages

  Martinière, Alexandre ^a   Desbrosses, Guilhem ^b   Sentenac, Hervé ^a   Paris, Nadine ^a  

^a UNIV MONTPELLIER   (France)

^b LABORATOIRE DES SYMBIOSES TROPICALES ET MÉDITERRANÉENNES   (France)

Author keywords

Acidic gowth theory; Endomembrane trafficking; GFP; Ion transport; pH; pHluorin; Vacuoles

Indexed keywords

EID: 84901018717     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2013.00523     Document Type: Article

References (61)

1. Ahmed, S. U., Rojo, E., Kovaleva, V., Venkataraman, S., Dombrowski, J. E., Matsuoka, K., et al. (2000). The plant vacuolar sorting receptor AtELP is involved in transport of NH(2)-terminal propeptide-containing vacuolar pro-teins in Arabidopsis thaliana. J. Cell Biol. 149, 1335-1344. doi: 10.1083/jcb.149. 7.1335
2. Alberts, P., Rudge, R., Irinopoulou, T., Danglot, L., Gauthier-Rouviere, C., and Galli, T. (2006). Cdc42 and actin control polarized expression of TI-VAMP vesicles to neuronal growth cones and their fusion with the plasma membrane. Mol. Biol. Cell 17, 1194-1203. doi: 10.1091/mbc.E05-07-0643
3. Arosio, D., Garau, G., Ricci, F., Marchetti, L., Bizzarri, R., Nifosi, R., et al. (2007). Spectroscopic and structural study of proton and halide ion cooperative binding to gfp. Biophys. J. 93,232-244. doi: 10.1529/biophysj.106.102319
4. Bagar, T., Altenbach, K., Read, N. D., and Bencina, M. (2009). Live-Cell imaging and measurement of intracellular pH in filamentous fungi usingageneticallyencoded ratiometric probe. Eukaryot. Cell 8, 703-712. doi: 10.1128/EC.00333-08
5. Bassil, E., Ohto, M., Esumi, T., Tajima, H., Zhu, Z., Cagnac, O., et al. (2011). The Arabidopsis intracellular Na+/H+ antiporters NHX5 and NHX6 are endosome associated and necessary for plant growth and development. PlantCell 23, 224-239. doi: 10.1105/tpc.110.079426
6. Bizzarri, R., Arcangeli, C., Arosio, D., Ricci, F., Farad, P., Cardarelli, F., et al. (2006). Development of a novel GFP-based ratiometric excitation and emission pH indicator for intracellular studies. Biophys. J. 90, 3300-3314. doi: 10.1529/biophysj.105.074708
7. Bizzarri, R., Serresi, M., Luin, S., and Beltram, F. (2009). Green fluorescent protein based pH indicators for in vivo use: a review. Anal. Bioanal. Chem. 393, 1107-1122. doi: 10.1007/s00216-008-2515-9
8. daSilva, L. L. P., Foresti, O., and Denecke, J. (2006). Targeting of the plant vacuolar sorting receptor BP80 is dependent on multiple sorting signals in the cytosolic tail. PlantCell18, 1477-1497. doi: 10.1105/tpc.105.040394
9. Davis, S. J., andVierstra, R. D. (1998). Soluble, highly fluorescent variants of green fluorescent protein (GFP) for use in higher plants. Plant Mol. Biol. 36, 521-528. doi: 10.1023/A:1005991617182
10. Demaurex, N. (2002). pH Homeostasis of cellular organelles. News Physiol. Sci. 17, 1-5
11. Dettmer, J., Hong-Hermesdorf, A., Stierhof, Y.-D., and Schumacher, K. (2006). Vacuolar H+-ATPase activity is required for endocytic and secretory trafficking in Arabidopsis. PlantCell 18,715-730. doi: 10.1105/tpc.105.037978
12. Esposito, A., Gralle, M., Dani, M. A. C., Lange, D., and Wouters, F. S. (2008). pHlameleons: a family of FRET-based protein sensors for quantitative pH imaging. Biochemistry 47,13115-13126. doi: 10.1021/bi8009482
13. Felle, H.H.(1998). The apoplastic pH of the Zea mays root cortexas measuredwith pH-sensitive microelectrodes: aspects of regulation. J. Exp. Bot. 49, 987-995. doi: 10.1093/jxb/49.323.987
14. Gandhi, S. P., and Stevens, C. F. (2003). Three modes of synaptic vesicu-lar recycling revealed by single-vesicle imaging. Nature 423, 607-613. doi: 10.1038/nature01677
15. Gao, D., Knight, M. R., Trewavas, A. J., Sattelmacher, B., and Plieth, C. (2004). Self-reporting Arabidopsis expressing pH and [Ca2+] indicators unveil ion dynamics in the cytoplasm and in the apoplast under abiotic stress. Plant Physiol. 134, 898-908. doi: 10.1104/pp.103.032508
16. Geilfus, C.-M., and Muhling, K. H. (2012). Transient alkalinization in the leaf apoplast of Viciafaba L. depends on NaCl stress intensity: an in situ ratio imaging study. PlantCellEnviron. 35,578-587. doi: 10.1111/j.1365-3040.2011.02437.x
17. Gjetting, K.S.K., Ytting, C. K., Schulz, A., and Fuglsang, A. T. (2012). Liveimaging of intra-and extracellular pH in plants using pHusion, a novel genetically encoded biosensor. J. Exp. Bot. 63, 3207-3218. doi: 10.1093/jxb/ers040
18. Gjetting, S. K., Schulz, A., and Fuglsang, A. T. (2013). Perspectives for using geneticallyencoded fluorescent biosensors in plants. Front. PlantSci. 4:234. doi: 10.3389/fpls.2013.00234
19. Grignon, C., and Sentenac, H. (1991). pH and ionic conditions in the apoplast. Annu. Rev. Plant Physiol. Plant Mol. Biol. 42, 103-128. doi: 10.1146/annurev.pp.42.060191.000535
20. Hanson, G. T., McAnaney, T. B., Park, E. S., Rendell, M. E. P., Yarbrough, D. K., Chu, S., et al. (2002). Green fluorescent protein variants as ratiometric dual emission pH sensors. 1. Structural characterization and preliminaryapplication. Biochemistry 41, 15477-15488. doi: 10.1021/bi026609p
21. Jones, A. M., Grossmann, G., Danielson, J. A., Sosso, D., Chen, L.-Q., Ho, C.-H., et al. (2013). In vivo biochemistry: applications for small molecule biosensors in plant biology. Curr. Opin. Plant Biol. 16, 389-395. doi: 10.1016/j.pbi.2013. 02.010
22. Kirsch, T., Paris, N., Butler, J. M., Beevers, L., and Rogers, J. C. (1994). Purification and initial characterization of a potential plant vacuolar targeting receptor. Proc. Natl. Acad. Sci. U.S.A. 91, 3403-3407. doi: 10.1073/pnas.91. 8.3403
23. Kneen, M., Farinas, J., Li, Y., and Verkman, A. S. (1998). Green fluorescent pro-tein as a noninvasive intracellular pH indicator. Biophys. J. 74, 1591-1599. doi: 10.1016/S0006-3495(98)77870-1
24. Krebs, M., Beyhl, D., Gorlich, E., Al-Rasheid, K. A. S., Marten, I., Stierhof, Y.-D., et al. (2010). ArabidopsisV-ATPase activityat the tonoplast is required for efficient nutrient storage butnotfor sodium accumulation. Proc. Natl. Acad. Sci. U.S.A. 107, 3251-3256. doi: 10.1073/pnas.0913035107
25. Llopis, J., McCaffery, J. M., Miyawaki, A., Farquhar, M. G., and Tsien, R.Y. (1998). Measurement of cytosolic, mitochondrial, and Golgi pH in single living cells with green fluorescent proteins. Proc. Natl. Acad. Sci. U.S.A. 95, 6803-6808. doi: 10.1073/pnas.95.12.6803
26. Mahon, M. J. (2011). pHluorin2: an enhanced, ratiometric, pH-sensitive green florescent protein. Adv. Biosci. Biotechnol. 2, 132-137. doi: 10.4236/abb.2011. 23021
27. Martiniere, A., Bassil, E., Jublanc, E., Alcon, C., Reguera, M., Sentenac, H., et al. (2013). In vivo intracellular pH measurements in Tobacco and Arabidopsis reveal an unexpected pH gradient in the endomembrane system. Plant Cell 25, 4028-4043. doi: 10.1105/tpc.113.116897
28. Miesenbock, G., DeAngelis, D. A., and Rothman, J. E. (1998).Visualizing secretion and synaptic transmission with pH-sensitive green fluorescent proteins. Nature 394, 192-195. doi: 10.1038/28190
29. Miyawaki, A., Llopis, J., Heim, R., McCaffery, J. M., Adams, J. A., Ikura, M., et al. (1997). Fluorescent indicators for Ca2+ based on green fluorescent proteins and calmodulin. Nature 388, 882-887. doi: 10.1038/42264
30. Monshausen, G. B., Bibikova, T. N., Weisenseel, M. H., and Gilroy, S. (2009). Ca2+ regulates reactive oxygen species production and pH during mechanosens-ing in Arabidopsis roots. Plant Cell 21, 2341-2356. doi: 10.1105/tpc.109. 068395
31. Monshausen, G. B., Miller, N. D., Murphy, A. S., and Gilroy, S. (2011). Dynamics of auxin-dependent Ca2+ and pH signaling in root growth revealed by integrating high-resolution imaging with automated computer vision-based analysis. Plant J. 65, 309-318. doi: 10.1111/j.1365-313X.2010.04423.x
32. Moseyko, N., and Feldman, L. J. (2001). Expression of pH-sensitive green fluo-rescent protein in Arabidopsis thaliana. Plant Cell Environ. 24, 557-563. doi: 10.1046/j.1365-3040.2001.00703.x
33. Muhling, K. H., and Sattelmacher, B. (1995). Apoplastic ion concentration of intact leaves of fieldbean (Viciafaba) as influencedbyammoniumandnitrate nutrition. J. PlantPhysiol. 147, 81-86. doi: 10.1016/S0176-1617(11)81417-3
34. O'Neill, R. A., and Scott, T. K. (1983). Proton flux and elongation in primary roots of barley (Hordeum vulgare L.). PlantPhysiol. 73, 199-201. doi: 10.1104/pp.73. 1.199
35. Quintero, F. J., Martinez-Atienza, J., Villalta, I., Jiang, X., Kim, W.-Y., Ali, Z., et al. (2011). Activation of the plasma membrane Na/H antiporter Salt-Overly-Sensitive 1 (SOS1) by phosphorylation of an auto-inhibitory C-terminal domain. Proc. Natl. Acad. Sci. U.S.A. 108, 2611-2616. doi: 10.1073/pnas. 1018921108
36. Rayle, D. L., and Cleland, R. E. (1992). The Acid Growth Theory of auxin-induced cell elongation is alive and well. Plant Physiol. 99, 1271-1274. doi: 10.1104/pp.99.4.1271
37. Rink, T. J., Tsien, R. Y., and Pozzan, T. (1982). Cytoplasmic pH and free Mg2+ in lymphocytes. J. CellBiol. 95, 189-196. doi: 10.1083/jcb.95.1.189
38. Robinson, D. G., and Pimpl, P. (2013). Receptor-mediated transport of vacuolar proteins: a critical analysis and a new model. Protoplasma doi: 10.1007/s00709-013-0542-7 [Epub ahead of print].
39. Robinson, D. G., Pimpl, P., Scheuring, D., Stierhof, Y.-D., Sturm, S., and Viotti, C. (2012). Trying to make sense of retromer. Trends Plant Sci. 17, 431-439. doi: 10.1016/j.tplants.2012.03.005
40. Romoser, V. A., Hinkle, P. M., and Persechini, A. (1997). Detection in living cells of Ca2 +-dependent changes in the fluorescence emission of an indicator com-posed of two green fluorescent protein variants linked by a calmodulin-binding sequence.Anewclass of fluorescentindicators. J. Biol. Chem. 272, 13270-13274. doi: 10.1074/jbc.272.20.13270
41. Saint-Jean, B., Seveno-Carpentier, E., Alcon, C., Neuhaus, J.-M., and Paris, N. (2010). The cytosolic tail dipeptide Ile-Met of the pea receptor BP80 is required for recycling from the prevacuole and for endocytosis. PlantCell 22, 2825-2837. doi: 10.1105/tpc.109.072215
42. Sankaranarayanan, S., De Angelis, D., Rothman, J. E., and Ryan, T. A. (2000). The use of pHluorins for optical measurements of presynaptic activity. Biophys. J. 79, 2199-2208. doi: 10.1016/S0006-3495(00)76468-X
43. Sankaranarayanan, S., and Ryan, T. A. (2001). Calcium accelerates endocytosis of vSNAREs athippocampalsynapses. Nat. Neurosci. 4,129-136. doi: 10.1038/83949
44. Scheuring, D., Viotti, C., Kruger, F., Kunzl, F., Sturm, S., Bubeck, J., et al. (2011). Multivesicular bodies mature from the trans-Golgi network/early endosome in Arabidopsis. PlantCell 23, 3463-3481. doi: 10.1105/tpc.111.086918
45. Schulte, A., Lorenzen, I., Bottcher, M., and Plieth, C. (2006).A novel fluorescent pH probe for expression in plants. PlantMethods 2, 7. doi: 10.1186/1746-4811-2-7
46. Sentenac, H., and Grignon, C. (1987). Effect of H excretion on the surface pH of corn root cells evaluated by using weak zacid influx as apH probe. PlantPhysiol. 84, 1367-1372. doi: 10.1104/pp.84.4.1367
47. Shen, J., Zeng, Y., Zhuang, X., Sun, L., Yao, X., Pimpl, P., et al. (2013). Organelle pH in the Arabidopsis endomembrane system. Mol. Plant 6, 1419-1437. doi: 10.1093/mp/sst079
48. Shimada, T., Fuji, K., Tamura, K., Kondo, M., Nishimura, M., and Hara-Nishimura, I. (2003). Vacuolar sorting receptor for seed storage proteins in Arabidopsis thaliana. Proc. Natl. Acad. Sci. U.S.A. 100, 16095-16100. doi: 10.1073/pnas.2530568100
49. Sieberer, B. J., Chabaud, M., Fournier, J., Timmers, A. C. J., and Barker, D. G. (2012). A switch in Ca2+ spiking signature is concomitant with endosymbiotic microbe entry into cortical root cells of Medicago truncatula. Plant J. 69, 822-830. doi: 10.1111/j.1365-313X.2011.04834.x
50. Singh, S., and Parniske, M. (2012). Activation of calcium-and calmodulin-dependent protein kinase (CCaMK), the central regulator of plant root endosym-biosis. Curr. Opin. PlantBiol. 15, 444-453. doi: 10.1016/j.pbi.2012.04.002
51. Staal, M., De Cnodder, T., Simon, D., Vandenbussche, F., Van der Straeten, D., Verbelen, J.-P., et al. (2011). Apoplastic alkalinization is instrumental for the inhibition of cell elongation in the Arabidopsis root by the ethylene precur-sor 1-aminocyclopropane-1-carboxylic acid. Plant Physiol. 155, 2049-2055. doi: 10.1104/pp.110.168476
52. Tamura, K., Shimada, T., Ono, E., Tanaka, Y., Nagatani, A., Higashi, S.-I., et al. (2003). Why green fluorescent fusion proteins have not been observed in the vacuoles of higher plants. Plant J.35, 545-555. doi: 10.1046/j.1365-313X.2003.01822.x
53. Taylor, D. P., Slattery, J., and Leopold, A. C. (1996). Apoplastic pH in corn root gravitropism: a laser scanning confocal microscopy measurement. Physiol. Plant. 97, 35-38. doi: 10.1111/j.1399-3054.1996.tb00475.x
54. Taylor, M. J., Perrais, D., and Merrifield, C. J. (2011). A high precision survey of the molecular dynamics of mammalian clathrin-mediated endocytosis. PLoS Biol. 9:e1000604. doi: 10.1371/journal.pbio.1000604
55. Thibaud, J. B., Davidian, J. C., Sentenac, H., Soler, A., and Grignon, C. (1988). H+ cotransports in corn roots as related to the surface pH shift induced by active H+ excretion. PlantPhysiol. 88, 1469-1473. doi: 10.1104/pp.88.4.1469
56. Toulon, V., Sentenac, H., Thibaud, J. B., Davidian, J. C., Moulineau, C., and Grignon, C. (1992). Role of apoplast acidification by the H(+) pump: effect on the sensitivity to pH and CO2 of iron reduction by roots of Brassica napus L. Planta 186, 212-218. doi: 10.1007/BF00196250
57. Toulon, V., Sentenac, H., Thibaud, J.-B., Soler, A., Clarkson, D., and Grignon, C. (1989). Effect of HCO-concentration in the absorption solution on the energetic coupling of H+-cotransports in roots of Zea mays L. Planta 179, 235-241. doi: 10.1007/BF00393694
58. Wachter, R. M. (2007). Chromogenic cross-link formation in green fluorescent protein. Acc. Chem. Res. 40, 120-127. doi: 10.1021/ar040086r
59. Watanabe, E., Shimada, T., Kuroyanagi, M., Nishimura, M., and Hara-Nishimura, I. (2002). Calcium-mediated association of a putative vacuolar sorting receptor PV72 with a propeptide of 2S albumin. J. Biol. Chem. 277, 8708-8715. doi: 10.1074/jbc.M109346200
60. Watanabe, E., Shimada, T., Tamura, K., Matsushima, R., Koumoto, Y., Nishimura, M., et al. (2004). An ER-localized form of PV72, a seed-specific vacuolar sorting receptor, interferes the transport of an NPIR-containing proteinase in Arabidopsis leaves. PlantCellPhysiol. 45, 9-17. doi: 10.1093/pcp/pch012
61. Zhang, Y., Xie, Q., Robertson, J. B., and Johnson, C. H. (2012). pHlash: a new genetically encoded and ratiometric luminescence sensor of intracellular pH. PLoS ONE 7:e43072. doi: 10.1371/journal.pone.0043072