Neutral red as a probe for confocal laser scanning microscopy studies of plant roots

Annals of Botany

Volumn 97, Issue 6, 2006, Pages 1127-1138

  Dubrovsky, Joseph G ^a   Guttenberger, Martin ^c   Saralegui, Andres ^b   Napsucialy Mendivil, Selene ^a   Voigt, Boris ^d   Baluška, František ^d   Menzel, Diedrik ^d  

^a Departamento de Biología Molecular de Plantas   (Mexico)

^b INSTITUTO DE BIOTECNOLOGÍA   (Mexico)

^c UNIVERSITY OF TÜBINGEN   (Germany)

^d UNIVERSITY OF BONN   (Germany)

Author keywords

Casparian band; CLSM; Lateral root development; Neutral red; Root development; Vacuole biogenesis; Xylem

Indexed keywords

ALLIUM CEPA; ARABIDOPSIS; ARABIDOPSIS THALIANA; ARBUSCULAR; FUNGI;

NEUTRAL RED;

ARTICLE; CELL VACUOLE; CONFOCAL MICROSCOPY; CYTOLOGY; GENETIC PROCEDURES; GROWTH, DEVELOPMENT AND AGING; HISTOLOGY; METHODOLOGY; MYCORRHIZA; PLANT ROOT; ULTRASTRUCTURE;

MICROSCOPY, CONFOCAL; MOLECULAR PROBE TECHNIQUES; MYCORRHIZAE; NEUTRAL RED; PLANT ROOTS; VACUOLES;

EID: 33947301745     PISSN: 03057364     EISSN: 10958290     Source Type: Journal    
DOI: 10.1093/aob/mcl045     Document Type: Article

References (75)

1. Abrahams S, Lee E, Walker AR, Tanner GJ, Larkin PJ, Ashton AR. 2003. The Arabidopsis TDS4 gene encodes leucoaiithocyanidin dioxygenase (LDOX) and is essential for proanthocyanidin synthesis and vacuole development. The Plant Journal 35: 624-636. (Pubitemid 37110717)
2. Baluška F, Parker JS, Barlow PW. 1993. The microtubular cytoskeleton in cells of cold-treated roots of maize (Zea mays L.) shows tissues-pecific responses. Protoplasma 172: 84-96.
3. Baluška F, Barlow PW, Volkmann D. 1996. Complete disintegration of the microtubular cytoskeleton precedes its auxin-mediated reconstruction in postmitotic maize root cells. Plant Cell Physiology 37:1013-1021. (Pubitemid 27050254)
4. Baluška F, Vitha S, Barlow PW, Volkmann D. 1997. Rearrangements of F-actin arrays in growing cells of intact maize root apex tissues: a major developmental switch occurs in the postmitotic transition region.European Journal of Cell Biology 72: 113-121. (Pubitemid 27095994)
5. Baluška F, Jásik J, Edelmann HG, Salajová T, Volkmann D. 2001a.Latrunculin B induced plant dwarfism: plant cell elongation is F-actin dependent. Developmental Biology 231: 113-124. (Pubitemid 32198391)
6. Baluška F, Volkmann D, Barlow PW. 20016. A polarity crossroad in the transition growth, zone of maize root apices: cytoskeletal and developmental implications. Journal of Plant Growth Regulation 20: 170-181.
7. Barlow PW, Baluška F. 2000. Cytoskeletal perspectives on root growth and morphogenesis. Annual Revew of Plant Physiology and Plant Molecular Biology 51: 289-322. (Pubitemid 32160867)
8. Bates TR, Lynch JP. 2000. Plant growth and phosphorus accumulation of wild type and two root hair mutants of Arabidopsis thaliana (Brassicaceae). American Journal of Botany 87: 958-963.
9. Benková E, Michniewicz MSM, Teichmann T, Seifertova D, Jürgens G, Friml J. 2003. Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell 115: 591-602. (Pubitemid 37506047)
10. 2 concentration does not affect growth or root respiration in bean or citrus.Plant, Cell and Environment 20: 1495-1.505.
11. Bouma TJ, Nielsen KL, Koutstaal B. 2000. Sample preparation and scanning protocol for computerized analysis of root length and diameter.Plant and Soil 218: 185-196. (Pubitemid 30144147)
12. Cárdenas L, Alemán E, Nava N, Santana O, Sánchez F, Quinto C. 2006. Early responses to nod-factors and mycorhizal colonization in a nonnodulated Phaseolm vulgaris mutant. Planta DOI 10.1007/s00425005-0132-9.
13. Caño-Delgado AI, Metzlaff K, Bevan MW. 2000. The elil mutation reveals a link between cell expansion and secondary cell wall formation in Arabidopsis thaliana. Development 127: 3395-3405. (Pubitemid 30649549)
14. Chen G, Hanson CL, Ebner TJ. 1998. Optical responses evoked by cerebellar surface stimulation in vivo using neutral red. Neuroscience 84: 645-668. (Pubitemid 28137885)
15. Conn HJ. 1977. Conn's biological stains. A handbook on the nature and uses of the dyes employed in the biological laboratory. Baltimore, MD: Waverly Press.
16. Grippen RW, Perrier JL. 1974. The use of neutral, red and Evans blue for live-dead determinations of marine plankton. Stain Technology 49: 97-104.
17. a shifts. European Journal of Biochemistry 24: 566-576.
18. De Simone O, Müller E, Junk WJ, Richau K, Schmidt W. 2003a. Schmidt iron distribution in three central Amazon tree species from whitewater- inundation areas (várzea) subjected to different iron regimes. Trees 17: 535-541. (Pubitemid 37435905)
19. De Simone O, Haase K, Müller E, Junk WJ, Hartmann K, Schreiber L, Schmidt W. 20036. Apoplasmic barriers and oxygen transport properties of hypodermal cell walls in roots from four Amazonian tree species. Plant Physiology 132: 206-217.
20. Dickinson ME, Bearman G, Tille S, Lansford R, Fraser SE. 2001. Multispectral imaging and linear unmixing add a whole new dimension to laser scanning fluorescence microscopy. BioTechniques 31: 1272-1278. (Pubitemid 33131210)
21. Di Laurenzio L, Wysocka-Diller J, Malamy JE, Pysh L, Helariutta Y, Freshour G, et al. 1996. The SCARECROW gene regulates an asymmetric cell, division that is essential for generating the radial organization of the Arabidopsis root. Cell 86: 423-433. (Pubitemid 26272082)
22. Di Sansebastiano GP, Paris N, Marc-Martin S, Neuhaus J-M. 1998. Specific accumulation of GFP in a non-acidic vacuolar compartment via a C-terminal. propeptide-mediated sorting pathway. The Plant Journal 15: 449-457. (Pubitemid 28450832)
23. Dixon KP, Xu J-R, Smirnoff N, Talbot NJ. 1999. Independent signaling pathways regulate cellular turgor during hyperosmotic stress and appressorium-mediated plant infection by Magnaporthe grísea. Plant Cell 11: 2045-2058.
24. Dubrovsky JG, Doerner P, Colón-Carmona A, Rost TL. 2000. Pericycle cell proliferation and lateral root initiation in Arabidopsis thaliana. Plant Physiology 124: 1648-1657. (Pubitemid 32053499)
25. Dubrovsky JG, Colón-Carmona A, Rost TL, Doerner PW. 2001. Early primordium morphogenesis during lateral root initiation in Arabidopsis thaliana. Planta 214: 30-36.
26. Dubrovsky JG, Gambetta GA, Hernández-Barrera A, Shishkova S, González I. 2006. Lateral root initiation in Arabidopsis: developmental window, spatial patterning, density, and predictability. Annals of Botany 97: in press.
27. Ehara M, Noguchi T, Ueda K. 1996. Uptake of neutral, red by the vacuoles of a green alga, Micrasterias pinnatifida. Plant Cell Physiology 37:734-741.
28. Essig-Marcello JS, van Buskirk, RG. 1990. A double-label in situ cytotoxicity assay using the fluorescent probes neutral red and BCECF-AM. Toxicology In Vitro 3: 219-227.
29. Fahraeus G. 1957. The infection of clover root hairs by nodule bacteria studied by a simple glass slide technique. Journal of General Microbiology 16: 374-381.
30. Felle H. 1988. Cytoplasmatic free calcium, in Ricciafluitans L. and Zea mays L.: interactions of Ca2+ and pH? Planta 176: 248-255.
31. Fischer BB, Krieger-Liszkay A, Eggen RIL. 2005. Oxidative stress induced by the photosensitizers neutral, red (type I) or rose bengal (type II) in the light causes different molecular responses in Chlamydomonas reinhardtii. Plant Science 168: 747-759.
32. Flückiger R. De Caroli M, Piro G, Dalessandro G, Neuhaus J-M,Di Sansebastiano G-P. 2003. Vacuolar system distribution in Arabidopsis tissues, visualized using GFP fusion proteins. Journal of Experimental Botany 54: 1577-1584.
33. Fukaki H, Wysocka-Diller J, Kato T, Fujisawa H, Benfey PN, Tasaka M. 1998. Genetic evidence that the endodermis is essential for shoot gravitropism in Arabidopsis thaliana. The Plant Journal 14: 425-430.
34. Guilliermond A. 1929. The recent development of our idea of the vacuome of plant cells. American Journal of Botany 16: 1-22.
35. Guttenberger M. 2000a. Arbuscules of vesicular-arbuscular mycorrhizal fungi inhabit an acidic compartment within plant roots. Planta 211:299-304. (Pubitemid 30674691)
36. Guttenberger M. 20002b. A rapid staining procedure for arbuscules of living arbuscular mycorrhizas using neutral red as acidotropic dye. Plant and Soil. 226: 211-218.
37. Hugdahl JD, Morejohn LC. 1993. Rapid and reversible high-affinity binding of the dinitroaniline herbicide oryzalin to tubulin from Zea mays L. Plant Physiology 102: 725-740.
38. Kawai M, Samarajeewa PK, Barrero RA, Nishiguchi M, Uchimiya H. 1998. Cellular dissection of the degradation pattern of cortical. cell death during aerenchyma formation of rice roots. Planta 204: 277-287. (Pubitemid 28107267)
39. Ketelaar T, Allwood EG, Anthony R, Voigt B, Menzel D, Hussey PJ. 2004. The actin-interacting protein AIP1. is essential for actin organization and plant development. Current Biology 20:145-149. (Pubitemid 38211234)
40. Kost B, Spielhofer P, Chua N-H. 1998. GFP-mouse talin fusion protein labels plant actin filaments in vivo and visualizes the actin cytoskeleton in growing pollen tubes. The Plant Journal 16: 393-401. (Pubitemid 28560348)
41. LaManna JC, McCracken KA. 1984. The use of neutral red as an intracellular pH indicator in rat brain cortex in vivo. Analytical Biochemistry 142: 117-125.
42. Li QG, Ni YJ, Cao YI. 1991. The use of neutral red to monitor the surface potential of the purple membrane. Photochemistry and Photobiology 53: 653-657.
43. Lulai EC, Morgan WC. 1992. Histochemical probing of potato periderm with neutral red: a sensitive cytofluorochrome for the hydrophobic domain of suberin. Biotechnic and Histochemistry 67:185-195.
44. Malamy JE, Benfey PN. 1997. Organization and cell differentiation in lateral roots oí Arabidopsis thaliana. Development 124: 33-44.
45. Marc J, Granger CL, Brincat J, Fisher DD, Kao T, McCubbin AG,Cyr RJ. 1998. A GFP-MAP4 reporter gene for visualizing cortical microtubule rearrangements in living epidermal cells. The Plant Cell 1.0: 1927-1939.
46. Marty F. 1999. Plant vacuoles. The Plant Cell 11: 587-599.
47. Ngo DA, Garland PA, Mandoli DF. 2005. Development and organization of the central vacuole of Acetabularia acetabulum. New Phytologist 165: 731-746.
48. Nishimura M. 1982. pH in vacuoles isolated from castor bean endosperm. Plant Physiology 70: 742-746.
49. 2 exchange, cell viability and cultivation range for Agave tequilana. Journal of Arid Environment 39: 1-9.
50. Nonomura T, Tajima H, Kitagawa Y, Sekiya N, Shitomi K, Tanaka M, et al. 2003. Distinguishable staining with neutral red for GFP-marked and GFP-nonmarked Fusarium oxysporum strains simultaneously colonizing root surfaces. Journal of General Plant Pathology 69: 45-48.
51. Okada D. 2000. Neutral red as a hydrophobic probe for monitoring neuronal activity. Journal of Neuroscience Methods 101: 85-92. (Pubitemid 30680142)
52. Oparka KJ. 1991. Uptake and compartmentation of fluorescent probes by plant cells. Journal of Experimental Botany 42: 565-579.
53. Paddock SW. 1999. An introduction to confocal imaging. In: Paddock SW, ed. Confocal microscopy, methods and protocols. Totowa: Humana Press, 1-34.
54. Scheres B, Di Laurenzio L, Willemsen V, Hauser M.-T, Janmaat K, Weisbeek P, et al. 1995. Mutations affecting the radial organisation of the Arabidopsis root display specific defects throughout the embryonic axis. Development 121: 53-62.
55. Schumacher TE, Smucker AJ. 1984. Effect of localized anoxia on Phaseolus vulgaris L. root growth. Journal of Experimental Botany 35: 1039-1047.
56. Schumacher TE, Smucker AJM, Eshel A, Curry RB. 1983. Measurement of short-term, root growth by prestaining with neutral red. Crop Science 23: 1212-1215.
57. Sivaguru M, Baluška F, Volkmann D, Felle H, Horst WJ. 1999. Impacts of aluminum on cytoskeleton of maize root apex: short-term effects on distal part of transition zone. Plant Physiology 119:1073-1082. (Pubitemid 29388279)
58. Smith FA, Raven JA. 1979. Intracellular pH and its regulation. Annual Review of Plant Physiology 30: 289-311.
59. Soran V, Lazar G. 1965. Some data concerning the accumulation of neutral red in various tissues and regions of the maize root. Physiologia Plantarum 18: 329-336.
60. Sousa C, Sa e Melo T, Gaze M, Gaullier JM, Maziäre JC, Santus R. 1996. Solvent polarity and pH effects on the spectroscopic properties of neutral red: application to lysosomal microenvironment probing in living cells. Photochemistry and Photobiology 63: 601-607.
61. Stadelmann EJ, Kinzel H. 1972. Vital staining of plant cells. In: Prescott DM, ed. Methods in cell physiology. Vol.V. New York, NY: Academic Press, 325-372.
62. Strugger S. 1935. Beiträge zur Gewebephysiologie der Wurzel. Zur Analyse und Methodik der Vitalfärbung pflanzlicher Zellen mit Neutralrot. Protoplasma 24: 108-127.
63. Svendsen C, Spurgeon DJ, Hankard PK, Weeks JM. 2004. A review of lysosomal, membrane stability measured by neutral red retention: is it a workable earthworm, biomarker? Ecotoxicology and Environmental Safety 57: 20-29. (Pubitemid 37491382)
64. Thatcher FS. 1939. Osmotic and permeability relations in the nutrition of fungus parasite. American Journal of Botany 26: 449-458.
65. Timmers ACJ, Tirlapur UK, Schel JHN. 1995. Vacuolar accumulation of acridine orange and neutral red in zygotic and somatic embryos of carrot (Daucus carota L.). Protoplasma 188: 236-244.
66. Tsien RY, Wagooner A. 1995. Fluorophores for confocal microscopy. In: Pawley JB, ed. Handbook of biological confocal microscopy, 2nd edn. New York, NY: Plenum Press, 267-279.
67. Van den Berg C, Willemsen V, Hage W, Weisbeek P, Scheres B. 1995. Cell fate in the Arabidopsis root meristem determined by directional signalling. Nature 378: 62-65.
68. VanderWerf QM, Castro DJ, Nguyen RD, Paiva MB, Chao KH, Santillanes ME, et al. 1997. KTP laser and neutral red phototherapy of human squamous cell, carcinoma. Laryngoscope 107: 316-320.
69. Voigt B, Timmers T, Šamaj J, Müller J, Baluška F, Menzel D. 2005. GFP-FABD2 fusion construct allows in vivo visualization of the dynamic actin cytoskeleton in all cells of Arabidopsis seedlings. European Journal of Cell Biology 84: 595-608. (Pubitemid 40823299)
70. Watkin ELJ, Thomson CJ, Greenway H. 1998. Root development and aerenchyma formation in two wheat cultivara and one triticale cultivar grown in. stagnant agar and aerated nutrient solution. Annals of Botany 81: 349-354. (Pubitemid 28111397)
71. Weeks JM, Svendsen C. 1996. Neutral red retention by lysosomes from earthworm. (Lumbricus rubellus) coelomocytes: a simple biomarker of exposure to soil, copper. Environmental Toxicology and Chemistry 15: 1801-1805. (Pubitemid 26342344)
72. Wilson GH, Grolig F, Kosegarten H. 1998. Differential pH restoration after ammonia-elicited vacuolar alkalization in rice and maize root hairs as measured by fluorescence ratio. Planta 206: 154-161. (Pubitemid 28371623)
73. Zhang G, Shuang S, Dong C, Liu D, Choi MMF. 2004. Investigation on DNA assembly to neutral red-cyclodextrin complex by molecular spectroscopy. Journal of Photochemistry and Photobiology B: Biology 74: 127-134. (Pubitemid 38667454)
74. Zhang SZ, Lipsky MM, Trump BF, Hsu IC. 1990. Neutral red (NR) assay for cell viability and xenobiotic-induced cytotoxicity in primary cultures of human and rat hepatocytes. Cell Biology and Toxicology 6: 219-234.
75. Zhong R, Ripperger A, Ye Z-H. 2000. Ectopic deposition of lignin in the pith of stems of two Arabidopsis mutants. Plant Physiology 123: 59-70. (Pubitemid 30322817)