Bacterially produced Pt-GFP as ratiometric dual-excitation sensor for in planta mapping of leaf apoplastic pH in intact Avena sativa and Vicia faba

Plant Methods

Volumn 10, Issue 1, 2014, Pages

  Geilfus, Christoph Martin ^a   Mühling, Karl H ^a   Kaiser, Hartmut ^a   Plieth, Christoph ^a  

^a UNIVERSITY OF KIEL   (Germany)

Author keywords

Apoplast; Genetically encoded biosensor; GFP; Nitrogen forms; pH; Plant bioimaging; Ptilosarcus gurneyi; Salinity; Signaling; Stress; Three channel ratio imaging

Indexed keywords

EID: 84907609273     PISSN: None     EISSN: 17464811     Source Type: Journal    
DOI: 10.1186/1746-4811-10-31     Document Type: Article

References (64)

1. Schulte A, Lorenzen I, Bötcher M, Plieth C. A novel fluorescent pH probe for expression in plants. Plant Methods 2006, 2:7. 10.1186/1746-4811-2-7, 1475855, 16600023.
2. Monshausen GB, Miller ND, Murphy AS, Gilroy S. Dynamics of auxin-dependent Ca2+ and pH signalling in root growth revealed by integrating high-resolution imaging with automated computer vision-based analysis. Plant J 2011, 65:309-318. 10.1111/j.1365-313X.2010.04423.x, 21223394.
3. Sanders D. Generalized kinetic analysis of ion driven cotransport systems: II. random ligand binding as a simple explanation for non-Michaelis kinetics. J Membr Biol 1986, 90:67-87. 10.1007/BF01869687, 2422385.
4. Lemoine R, Delrot S. Proton-motive-force-driven sucrose uptake in sugar beet plasma membrane vesicles. FEBS Lett 1989, 249:129.
5. Bush DR. Proton-coupled sugar and amino acid transporters in plants. Annu Rev Plant Physiol Plant Mol Biol 1993, 44:513-542.
6. Marschner H. Mineral nutrition of higher plants 1995, London: Academic, 2.
7. Maathuis FJ, Sanders D. Plasma membrane transport in context - making sense out of complexity. Cur Opin Plant Biol 1999, 2:236-243.
8. Ben-Shimon A, Shalev DE, Niv MY. Protonation States in molecular dynamics simulations of peptide folding and binding. Curr Pharm Des 2013, 19(23):4173-4181. 10.2174/1381612811319230003, 23170889.
9. Hartung W. Die intrazelluläre Verteilung von Phytohormonen in Pflanzenzellen. Hahenheimer Arbeiten 1983, 129:64-80.
10. Hartung W, Solvik S. Physicochemical properties of plant growth regulators and plant tissues determine their distribution and redistribution: stomatal regulation by abscisic acid in leaves. New Phytol 1991, 119:361-382.
11. Daeter W, Slovik S, Hartung W. The pH-gradients in the root system and the abscisic acid concentration in xylem and apoplastic saps. Philos T Roy Soc B 1993, 341:49-56.
12. Swanson SJ, Choi WG, Chanoca A, Gilroy S. In vivo imaging of Ca2+, pH, and reactive oxygen species using fluorescent probes in plants. Annu Rev Plant Biol 2011, 62:273-297. 10.1146/annurev-arplant-042110-103832, 21370977.
13. Gerendás J, Ratcliffe RG. Intracellular pH regulation in maize root tips exposed to ammonium at high external pH. J Exp Bot 2000, 51(343):207-219. 10.1093/jexbot/51.343.207, 10938827.
14. Mühling KH, Läuchli A. Influence of chemical form and concentration of nitrogen on apoplastic pH of leaves. J Plant Nutr 2001, 24:399-411.
15. Van Volkenburgh E, Boyer JS. Inhibitory effects of water deficit on maize leaf elongation. Plant Physiol 1985, 77:190-194. 10.1104/pp.77.1.190, 1064480, 16664006.
16. Hartung W, Radin JW, Hendrix DL. Abscisic acid movement into the apoplastic solution of water-stressed cotton leaves: role of apoplastic pH. Plant Physiol 1988, 86:908-913. 10.1104/pp.86.3.908, 1054593, 16666007.
17. Wilkinson S, Davies WJ. Xylem sap pH increase: a drought signal received at the apoplastic face of the guard cell that involves the suppression of saturable abscisic acid uptake by the epidermal symplast. Plant Physiol 1997, 113:559-573. 158172, 12223626.
18. Felle HH, Hermann A, Hückelhoven R, Kogel KH. Root-to-shoot signalling: apoplastic alkalinization, a general stress response and defence factor in barley (Hordeum vulgare). Protoplasma 2005, 227:17-24. 10.1007/s00709-005-0131-5, 16389490.
19. Felle HH. pH regulation in anoxic plants. Ann Bot 2005, 96:519-532. 10.1093/aob/mci207, 16024558.
20. Geilfus CM, Mühling KH. Transient alkalinization in the leaf apoplast of Viciafaba L. depends on NaCl stress intensity: an in situ ratio imaging study. Plant Cell Environ 2012, 35(3):578-587. 10.1111/j.1365-3040.2011.02437.x, 21954856.
21. Geilfus CM, Mühling KH. Microscopic and macroscopic monitoring of adaxial- abaxial pH gradients in the leaf apoplast of Vicia faba L. as primed by NaCl stress at the roots. Plant Sci 2014, 223:109-115.
22. Felle HH, Herrmann A, Hanstein S, Hückelhoven R, Kogel KH. Apoplastic pH signalling in barley leaves attacked by the powdery mildew fungus Blumeria graminis f.sp. hordei. Mol Plant Microbe In 2004, 17:118-123.
23. Schäfer P, Pfiffi S, Voll LM, Zajic D, Chandler PM, Waller F, Scholz U, Pons-Kühnemann J, Sonnewald S, Sonnewald U, Kogel KH. Manipulation of plant innate immunity and gibberellin as factor of compatibility in the mutualistic association of barley roots with Piriformospora indica. Plant J 2009, 59:461-474. 10.1111/j.1365-313X.2009.03887.x, 19392709.
24. Hager A, Menzel H, Krauss A. Versuche und Hypothese zur Primärwirkung des Auxins beim Streckenwachstum. Planta 1971, 100:47-75. 10.1007/BF00386886, 24488103.
25. Raven JA, Farquhar GD. Leaf apoplast pH estimation in Phaseolus vulgaris. Plant membrane transport: the current position 1989, 607-610. Amsterdam: Elsevier, Dainty J, De Michelis MI, Marre E, Rasi-Caldogno F.
26. Ullrich WR. Transport of nitrate and ammonium through plant membranes. Nitrogen Metabolism in Plants 1992, 121-137. Oxford, UK: Oxford University Press, Mengel K, Pilbeam DJ.
27. Mühling KH, Plieth C, Hansen UP, Sattelmacher B. Apoplastic pH of intact leaves of Vicia faba as influenced by light. J Exp Bot 1995, 16:377-382.
28. Mühling KH, Läuchli A. Light-induced pH and K + changes in the apoplast of intact leaves. Planta 2000, 212:9-15. 10.1007/s004250000374, 11219588.
29. Monshausen GB, Bibikova TN, Messerli MA, Shi C, Gilroy S. Oscillations in extracellular pH and reactive oxygen species modulate tip growth of Arabidopsis root hairs. Proc Natl Acad Sci U S A 2007, 104(52):20996-21001. 10.1073/pnas.0708586104, 2409255, 18079291.
30. Toyota M, Gilroy S. Gravitropism and mechanical signaling in plants. Am J Bot 2012, 100(1):111-125.
31. Fricker MD, Plieth C, Knight H, Blancaflor E, Knight MR, White NS, Gilroy S. Fluorescent and luminescent techniques to probe ion activities in living plant cells. Fluorescent and luminescent probes 1999, 569-596. London: Academic, Mason WT.
32. Fricker MD, Parsons A, Tlalka M, Blancaflor E, Gilroy S, Meyer A, Plieth C. Fluorescent probes for living plant cells. Plant Cell Biology: A Practical Approach 2001, 35-84. Oxford: University Press, Hawes C, Satiat- Jeunemaitre B, 2.
33. Gilroy S. Fluorescence microscopy of living plant cells. Annu Rev Plant Physiol Plant Mol Biol 1997, 48:165-190. 10.1146/annurev.arplant.48.1.165, 15012261.
34. Geilfus CM, Mühling KH. Real-time imaging of leaf apoplastic pH dynamics in response to NaCl stress. Front Plant Sci 2011, 2:13. 3355670, 22639578.
35. Grignon C, Sentenac H. pH and ionic conditions in the apoplast. Annu Rev Plant Physiol Plant Mol Biol 1991, 42:103-128.
36. Gao D, Trewavas AJT, Knight MR, Sattelmacher B, Plieth C. Selfreporting Arabidopsis thaliana expressing pH- and [Ca 2+]-indicators unveil ion dynamics in the cytoplasm and in the apoplast under abiotic stress. Plant Physiol 2004, 134:898-908. 10.1104/pp.103.032508, 389913, 15020753.
37. Geilfus CM, Mühling KH. Ratiometric monitoring of transient apoplastic alkalinizations in the leaf apoplast of living Vicia faba plants: chloride primes and PM-H+-ATPase shapes NaCl-induced systemic alkalinizations. New Phytol 2013, 197(4):1117-1129. doi:10.1111/nph.12046, 10.1111/nph.12046, 23176077.
38. Hoffmann B, Kosegarten H. FITC-dextran for measuring apoplast pH and apoplastic pH gradients between various cell types in sunflower leaves. Physiol Plant 1995, 95:327-335.
39. Mahmoudi AR, Shaban E, Ghods R, Jeddi-Tehrani M, Emami S, Rabbani H, Zarnani AH, Mahmoudian J. Comparison of photostability and photobleaching properties of FITC- and dylight 488 conjugated Herceptin. Int J Green Nanotech 2011, 3(3):264-270.
40. Han JY, Burgess K. Fluorescent Indicators for Intracellular pH. Chem Rev 2010, 110:2709-2728. 10.1021/cr900249z, 19831417.
41. Shen J, Zeng Y, Zhuang X, Sun L, Yao X, Pimpl P, Jiang L. Organelle pH in the Arabidopsis endomembrane system. Mol Plant 2013, doi:10.1093/mp/sst079.
42. Geilfus CM, Zörb C, Neuhaus C, Hansen T, Lüthen H, Mühling KH. Differential transcript expression of wall-loosening candidates in leaves of maize cultivars differing in salt resistance. J Plant Growth Regul 2011, doi:10.1007/s00344-011-9201-4.
43. Zörb C, Geilfus CM, Mühling KH, Ludwig-Müller J. The influence of salt stress on ABA and auxin concentrations in two maize cultivars differing in salt resistance. J Plant Physiol 2013, 170(2):220-224. 10.1016/j.jplph.2012.09.012, 23181973.
44. Bibikova TN, Jacob T, Dahse I, Gilroy S. Localized changes in apoplastic and cytoplasmic pH are associated with root hair development in Arabidopsis thaliana. Development 1998, 125:2925-2934.
45. Felle HH. pH: signal and messenger in plant cells. Plant Biol 2001, 3:577-591.
46. Choi WG, Swanson SJ, Gilroy S. High-resolution imaging of Ca2+, redox status, ROS and pH using GFP biosensors. Plant J 2012, 70:118-128. 10.1111/j.1365-313X.2012.04917.x, 22449047.
47. Bacon MA, Wilkinson S, Davies WJ. pH-regulated leaf cell expansion in droughted plants is abscisic acid dependent. Plant Physiol 1998, 118:1507-1511. 10.1104/pp.118.4.1507, 34769, 9847127.
48. Wilkinson S. pH as a stress signal. Plant Growth Regul 1999, 29:89-99.
49. Casey JR, Grinstein S, Orlowski J. Sensors and regulators of intracellular pH. Nat Rev Mol Cell Biol 2010, 11:50-61. 10.1038/nrm2820, 19997129.
50. Monshausen GB. Visualizing Ca2+ signatures in plants. Curr Opin Plant Biol 2012, 15(6):677-682. 10.1016/j.pbi.2012.09.014, 23044039.
51. Fricker MD, Errington RJ, Wood JL, Tlalka M, May M, White NS. Quantitative confocal fluorescence measurements in living tissues. Signal Transduction - Single Cell Research 1997, 569-596. Heidelberg: Springer- Verlag, Van Duijn B, Wiltnik A.
52. Sanders D, Hansen UP. Mechanism of Cl - transport at the plasma membrane of Chara corallina. part II. transinhibition and the determination of H+/Cl - binding order from a reaction kinetic model. J Membrane Biol 1981, 58:139-153.
53. Felle HH. The H+/CI- -symporter in root-hair cells of Sinapis alba. an electrophysiological study using ion-selective microelectrodes. Plant Physiol 1994, 106:1131-1136. 159640, 12232395.
54. Lorenzen I, Aberle T, Plieth C. Salt stress-induced chloride flux: a study using transgenic Arabidopsis expressing a fluorescent anion probe. Plant J 2004, 38:539-544. 10.1111/j.0960-7412.2004.02053.x, 15086798.
55. Rayle DL. Auxin-induced hydrogen-ion secretion in Avena coleoptiles and its implications. Planta 1973, 114(1):63-73. 10.1007/BF00390285, 24458665.
56. DiCiccio JE, Steinberg BE. Lysosomal pH and analysis of the counter ion pathways that support acidification. J Gen Physiol 2011, 137:385-390. doi:10.1085/jgp.201110596, 10.1085/jgp.201110596, 3068279, 21402887.
57. Miesenböck G, de Angelis DA, Rothman JE. Visualizing secretion and synaptic transmission with pH-sensitive green fluorescent protein. Nature 1998, 394:192-195. 10.1038/28190, 9671304.
58. Hanson GT, McAnaney TB, Park ES, Rendell MEP, Yarbrough DK, Chu SY, Xi LX, Boxer SG, Montrose MH, Remington SJ. Green fluorescent protein variants as ratiometric dual emission pH sensors. 1. structural characterization and preliminary application. Biochemistry 2002, 41:15477-15488. 10.1021/bi026609p, 12501176.
59. Bizzarri R, Arcangeli C, Arosio D, Ricci F, Faraci P, Cardarelli F, Beltram F. Development of a novel GFP-based ratiometric excitation and emission pH indicator for intracellular studies. Biophys J 2006, 90:3300-3314. doi:10.1529/biophysj.105.074708, 10.1529/biophysj.105.074708, 1432127, 16603505.
60. Meyer AJ, Brach T, Marty L, Kreye S, Rouhier N, Jacquot JP, Hell R. Redox- sensitive GFP in Arabidopsis thaliana is a quantitative biosensor for the redox potential of the cellular glutathione redox buffer. Plant J 2007, 52:973-986. 10.1111/j.1365-313X.2007.03280.x, 17892447.
61. Young B, Wightman R, Blanvillain R, Purcel SB, Gallois P. pH-sensitivity of YFP provides an intracellular indicator of programmed cell death. Plant Methods 2010, 6:27. 10.1186/1746-4811-6-27, 3009963, 21118545.
62. Gjetting KS, Ytting K, Karkov C, Schulz A, Fuglsang AT. Live imaging of intra- and extracellular pH in plants using pHusion, a novel genetically encoded biosensor. J Exp Bot 2012, 63(8):3207-3218. 10.1093/jxb/ers040, 3350929, 22407646.
63. Gjetting KS, Schulz A, Fuglsang AT. Perspectives for using genetically encoded fluorescent biosensors in plants. Front Plant Sci 2013, 4:234. 3709170, 23874345.
64. Martinière A, Desbrosses G, Sentenac H, Paris N. Development and properties of genetically encoded pH sensors in plants. Front Plant Sci 2013, 4:523. doi:10.3389/fpls.2013.00523, 3866548, 24391657.