A pH signaling mechanism involved in the spatial distribution of calcium and anion fluxes in ectomycorrhizal roots

New Phytologist

Volumn 181, Issue 2, 2009, Pages 448-462

  Ramos, Alessandro C ^a   Lima, Pedro T ^a   Dias, Pedro N ^a   Kasuya, Maria Catarina M ^b   Feijó, José A ^a,c  

^a INSTITUTO GULBENKIAN DE CIÊNCIA   (Portugal)

^b FEDERAL UNIVERSITY OF VIÇOSA   (Brazil)

^c UNIVERSITY OF LISBON   (Portugal)

Author keywords

Anion; Calcium; Ectomycorrhizas; Ion selective vibrating probe; pH signaling; Pisolithus microcarpus; Proton

Indexed keywords

ANION; CALCIUM;

ANION; CALCIUM; ECTOMYCORRHIZA; EVERGREEN TREE; FUNGUS; HOST-PATHOGEN INTERACTION; IMMUNE RESPONSE; NUTRIENT UPTAKE; OSMOREGULATION; PH; PROBE; RHIZOSPHERE; SPATIAL DISTRIBUTION; WAVELET;

ARTICLE; EUCALYPTUS; FUNGUS; ION TRANSPORT; METABOLISM; MYCELIUM; MYCORRHIZA; PH; PHYSIOLOGY; PLANT ROOT; SEEDLING; SIGNAL TRANSDUCTION; SYMBIOSIS;

ANIONS; CALCIUM; EUCALYPTUS; FUNGI; HYDROGEN-ION CONCENTRATION; ION TRANSPORT; MYCELIUM; MYCORRHIZAE; PLANT ROOTS; SEEDLING; SIGNAL TRANSDUCTION; SYMBIOSIS;

EUCALYPTUS; EUCALYPTUS GLOBULUS; FUNGI; PISOLITHUS; PISOLITHUS MICROCARPUS;

EID: 57649223982     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/j.1469-8137.2008.02656.x     Document Type: Article

References (84)

1. Ahonen-Jonnarth U, Van Hees PAW, Lundstrom US, Finlay RD. 2000. Organic acids produced by mycorrhizal Pinus sylvestris exposed to elevated aluminium and heavy metal concentrations. New Phytologist 146 : 557 567.
2. Allen GJ, Sanders D. 1994. Two voltage-gated calcium release channels coreside in the vacuolar membrane of guard cells. Plant Cell 6 : 685 694.
3. Antoine AF, Faure JE, Cordeiro S, Dumas C, Rougier M, Feijó JA. 2000. A calcium influx is triggered and propagates as a wavefront in the zygote after in vitro fertilization of flowering plants. Proceedings of the National Academy of Sciences, USA 97 : 10643 10648.
4. Antoine AF, Faure JE, Dumas C, Feijó JA. 2001. Differential contributions of free cytosolic and extracellular fluxes of calcium to gamete fusion and egg activation in flowering plants. Nature-Cell Biology 3 : 1120 1124.
5. Assmann SM, Simoncini L, Schroeder JI. 1985. Blue light activates electrogenic ion pumping in guard cell protoplasts of Vicia faba. Nature 318 : 285 287.
6. Béguiristain T, Lapeyrie F. 1997. Host plant stimulates hypaphorine accumulation in Pisolithus tinctorius hyphae during ectomycorrhizal infection while excreted fungal hypaphorine controls root hair development. New Phytologist 136 : 525 532.
7. Boukcim H, Plassard C. 2003. Juvenile nitrogen uptake capacities and root architecture of two open-pollinated families of Picea abies. Effects of nitrogen source and ectomycorrhizal symbiosis. Journal of Plant Physiology 10 : 1211 1218.
8. Bowman BJ. 1982. Vanadate uptake in Neurospora crassa occurs via phosphate transport system II. Journal of Bacteriology 153 : 286 291.
9. Bowman BJ, Allen KE, Slayman CW. 1983. Vanadate-resistant mutants of Neurospora crassa are deficient in a high-affinity phosphate transport system. Journal of Bacteriology 153 : 292 296.
10. Brundrett M, Bougher NM, Dell B, Grove T, Malajczuck N. 1996. Working with mycorrhizas in forestry and agriculture. Camberra, Australia : Pirie Printers.
11. Bücking H, Hans R, Heyser W. 2007. The apoplast of ectomycorrhizal roots - site of nutrient uptake and nutrient exchange between the symbiotic partners. In : Sattelmacher B, Horst WJ, eds. The apoplast of higher plants: compartment of storage, transport and reactions. Dordrecht, the Netherlands : Springer-Verlag, 97 108.
12. Bücking H, Heyser W. 2000. Subcellular compartmentation of elements in nonmycorrhizal and mycorrhizal roots of Pinus sylvestris: an X-ray microanalytical study. II. The distribution of calcium, potassium and sodium. New Phytologist 145 : 321 331.
13. Bücking H, Kuhn AJ, Schröder WH, Heyser W. 2002. The fungal sheath of ectomycorrhizal pine roots: an apoplastic barrier for the entry of calcium, magnesium, and potassium into the root cortex? Journal of Experimental Botany 53 : 1659 1669.
14. Caldwell RA, Clemo HF, Baumgarten CM. 1998. Using gadolinium to identify stretch-activated channels: technical considerations. American Journal of Physiology - Cell Physiology 275 : 619 621.
15. +-pumping ATPases from oat roots. Plant Physiology 73 : 921 928.
16. -, and a disulfonic stilbene. Plant Physiology 76 : 490 497.
17. Clark RB. 1975. Characterization of phosphatase of intact maize roots. Journal of Agricultural and Food Chemistry 23 : 458 460.
18. + transporter from the Trk family in the ectomycorrhizal fungus Hebeloma cylindrosporum. Journal of Biological Chemistry. 282 : 26057 26066.
19. Courty PE, Pouysegur R, Buee M, Garbaye J. 2006. Laccase and phosphatase activities of the dominant ectomycorrhizal types in a lowland oak forest. Soil Biology & Biochemistry 38 : 1219 1222.
20. Crawford NM. 1995. Nitrate: nutrient and signal for plant growth. Plant Cell 7 : 859 868.
21. Dauphin A, Gérard J, Lapeyrie F, Legué V. 2007. Fungal hypaphorine reduces growth and induces cytosolic calcium increase in root hairs of Eucalyptus globulus. Protoplasma 231 : 83 88.
22. +-ATPase of maize embryos localizes in regions that are critical during the onset of germination. Plant Science 169 : 11 19.
23. Evans ML, Mulkey TJ, Vesper MJ. 1980. Auxin action on proton influx in corn roots and its correlation with growth. Planta 148 : 510 512.
24. Feijó JA, Sainhas J, Hackett GR, Kunkel JG, Hepler PK. 1999. Growing pollen tubes posses a constitutive alkaline band in the clear zone and a growth-dependent acidic tip. Journal of Cell Biology 144 : 483 496.
25. Felle HH. 2001. pH: signal and messenger in plant cells. Plant Biology 3 : 577 591.
26. +-ATPase gene expression in tomato plants. Journal of Experimental Botany 53 : 1683 1687.
27. Forde BG. 2000. Nitrate transporters in plants: structure, function and regulation. Biochimica et Biophysica Acta 1465 : 219 235.
28. Foster JF. 1990. Influence of pH and plant nutrient status on ion fluxes between tomato plants and simulated acid mists. New Phytologist 116 : 475 485.
29. Garnett TP, Shabala SN, Smethurst PJ, Newman IA. 2001. Kinetics of ammonium and nitrate uptake by eucalypt roots and associated proton fluxes measured using ion selective microelectrodes. Functional Plant Biology 30 : 1165 1176.
30. Garnett TP, Shabala SN, Smethurst PJ, Newman IA. 2003. Simultaneous measurement of ammonium, nitrate and proton fluxes along the length of eucalypt roots. Plant and Soil 236 : 55 62.
31. Garnett TP, Smethurst PJ. 1999. Ammonium and nitrate uptake by Eucalyptus nitens: effects of pH and temperature. Plant and Soil 214 : 133 140.
32. Glass AD, Shaff JE, Kochian LV. 1992. Studies of the uptake of nitrate in barley. IV. Electrophysiology. Plant Physiology 99 : 456 463.
33. Gobert A, Plassard C. 2002. Differential dependent patterns of uptake in Pinus pinaster, Rhizopogon roseolus and their ectomycorrhizal association. New Phytologist 154 : 509 516.
34. +-ATPase in auxin induced elongation growth. Historical and new aspects. Journal of Plant Research 116 : 483 505.
35. Hawkins BJ, Boukcim H, Plassard C. 2008. A comparison of ammonium, nitrate and proton net fluxes along seedling roots of Douglas-fir and lodgepole pine grown and measured with different inorganic nitrogen sources. Plant, Cell & Environment 31 : 278 287.
36. 2+ and nucleotide dependent regulation of voltage dependent anion channels in the plasma membrane of guard cells. EMBO Journal 9 : 3889 3892.
37. Ihaka R, Gentleman R. 1996. R: a language for data analysis and graphics. Journal of Computational and Graphical Statistics 5 : 299 314.
38. +-ATPase in the root apex: evidence for strong expression in xylem parenchyma and asymmetric localization within cortical and epidermal cells. Physiologia Plantarum 104 : 311 316.
39. Javelle A, Andre B, Marini AM, Chalot M. 2003. High-affinity ammonium transporters and nitrogen sensing in mycorrhizas. Trends in Microbiology 11 : 53 55.
40. Klüsener B, Boheim G, Liss H, Engelberth J, Weiler EW. 1995. Gadolinium-sensitive, voltage-dependent calcium release channels in the endoplasmic reticulum of a higher plant mechanoreceptor organ. EMBO Journal 14 : 2708 2714.
41. Knight H, Trewavas AJ, Knight MR. 1996. Cold calcium signaling in Arabidopsis involves two cellular pools and a change in calcium signature after acclimation. Plant Cell 8 : 489 50.
42. 2+ fluxes in maize suspension cells. Planta 188 : 601 610.
43. Kuhn AJ, Schröder WH, Bauch J. 2000. The kinetics of calcium and magnesium entry into mycorrhizal spruce roots. Planta 210 : 488 96.
44. Kunkel JG, Cordeiro S, Xu J, Shipley AM, Feijó JA. 2006. The use of noninvasive ion-selective microelectrode techniques for the study of plant development. In : Volkov V, ed. Plant electrophysiology - theory and methods. Berlin, Germany : Springer-Verlag, 109 137.
45. Lecourieux D, Ranjeva R, Pugin A. 2006. Calcium in plant defence-signalling pathways. New Phytologist 171 : 249 69.
46. Lei J, Dexheimer J. 1988. Ultrastructural localization of ATPase activity in the Pinus sylvestris/Laccaria laccata ectomycorrhizal association. New Phytologist 108 : 329 334.
47. +-ATPase from beet root is inhibited by a calcium-dependent phosphorylation. Planta 204 : 352 359.
48. Malajczuk N, Cromack K Jr. 1982. Accumulation of calcium oxalate in the mantle of ectomycorrhizal roots of Pinus radiata and Eucalyptus marginata. New Phytologist 92 : 527 531.
49. Marchner H, Dell B. 1994. Nutrient uptake in mycorhizal symbiosis. Plant and Soil 159 : 89 102.
50. Martin F, Aerts A, Ahrén D, Brun A, Danchin EGJ, Duchaussoy F, Gibon J, Kohler A, Lindquist E, Pereda V et al. 2008. The genome of Laccaria bicolor provides insights into mycorrhizal symbiosis. Nature 452 : 88 92.
51. Martin F, Kohler A, Duplessis S. 2007. Living in harmony in the wood underground: ectomycorrhizal genomics. Current Opinion in Plant Biology 10 : 204 210.
52. Marx DH. 1969. The influence of ectotrophic mycorrhizal fungi on the resistance of pine roots to pathogenic fungi and soil bacteria. I. Antagonism of mycorrhizal fungi to root pathogenic fungi and soil bacteria. Phytopathology 59 : 153 163.
53. Messerli MA, Smith PJS, Lewis RC, Robinson KR. 2004. Chloride fluxes in lily pollen tubes: a critical reevaluation. Plant Journal 40 : 799 812.
54. Michard E, Dias P, Feijó JA. 2008. Tobacco pollen tubes as cellular models for ion dynamics: improved spatial and temporal resolution of extracellular flux and free cytosolic concentration of calcium and protons using pHluorin and YC3.1 CaMeleon. Sexual Plant Reproduction 21 : 169 181.
55. Moloney MM, Elliott MC, Cleland RE. 1981. Acid growth effects in maize roots: evidence for a link between auxin economy and proton extrusion in the control of root growth. Planta 152 : 285 291.
56. Müller T, Avolioa M, Olivia M, Benjdiab M, Rikirschb E, Kasarasa A, Fitza M, Chalotc M, Wipfa D. 2007. Nitrogen transport in the ectomycorrhiza association: the Hebeloma cylindrosporum-Pinus pinaster model. Phytochemistry 68 : 41 51.
57. Nemchinov LG, Shabala L, Shabala S. 2008. Calcium efflux as a component of the hypersensitive response of Nicotiana benthamiana to Pseudomonas syringae. Plant and Cell Physiology 49 : 40 46.
58. +-ATPases: powerhouses for nutrient uptake. Annual Review of Plant Physiology and Plant Molecular Biology 52 : 817 845.
59. Parker DR, Chaney RL, Norvell WA. 1995. Chemical equilibrium models: applications to plant nutrition research. In : RH Loeppert, AP Schwab, S Goldberg, eds. Chemical equilibrium and reaction models. Madison, WI, USA : Soil Science Society of America, Inc, 163 200, 253 269.
60. Pasqualini S, Panara F, Antonielli M. 1992. Acid-phosphatase-activity in Pinus-pinea-Tuber-albidum ectomycorrhizal association. Canadian Journal of Botany 70 : 1377 1383.
61. Peterson CA, Enstone DE. 1996. Functions of passage cells in the endodermis and exodermis of roots. Physiologia Plantarum 97 : 592 598.
62. Plassard C, Guérin-Laguette A, Véry AA, Casarin V, Thibaud JB. 2002. Local measurements of nitrate and potassium fluxes along roots of maritime pine. Effects of ectomycorrhizal symbiosis. Plant, Cell & Environment 25 : 75 84.
63. +-ATPase in fungi and plants. Biochimica et Biophysica Acta 1469 : 31 42.
64. +) flux signature for the presymbiotic development of the arbuscular mycorrhizal fungi. New Phytologist 178 : 177 188.
65. Ramos AC, Façanha AR, Feijó JA. 2008b. Ion dynamics during the polarized growth of arbuscular mycorrhizal fungi: from presymbiosis to symbiosis. In : Varma A, ed. Mycorrhiza: structure function and biotechnology. Heidelberg, Germany : Springer-Verlag, 241 261.
66. Ramos AC, Martins MA, Façanha AR. 2005. ATPase and pyrophosphatase activities in corn root microsomes colonized with arbuscular mycorrhizal fungi. Brazilian Journal of Soil Science 29 : 207 213.
67. Rayle DL, Cleland RE. 1992. The acid growth theory of auxin-induced cell elongation is alive and well. Plant Physiology 99 : 1271 1274.
68. Rosewarne GM, Smith FA, Schachtman DP, Smith SE. 2007. Localization of proton-ATPase genes expressed in arbuscular mycorrhizal tomato plants. Mycorrhiza 17 : 249 258.
69. Rygiewicz PT, Bledsoe CS. 1984. Mycorrhizal effects on potassium fluxes by northwest coniferous seedlings. Plant Physiology 76 : 918 923.
70. van Scholl L, Hoffland E, van Breemen N. 2006. Organic anion exudation by ectomycorrhizal fungi and Pinus sylvestris in response to nutrient deficiencies. New Phytologist 170 : 153 163.
71. Schroeder JI, Schmidt C, Sheaffer J. 1993. Identification of high-affinity slow anion channel blockers and evidence for stomatal regulation by slow anion channels in guard cells. Plant Cell 5 : 1831 1841.
72. Schwartz A, Ilan N, Schwarz M, Scheaffer J, Assmann SM, Schroeder JI. 1995. Anion-channel blockers inhibit S-type anion channels and abscisic-acid responses in guard cells. Plant Physiology 109 : 651 658.
73. 2+ transporters in bean leaf mesophyll: masking role of the cell wall. Annals of Botany 85 : 681 686.
74. Shipley AM, Feijó JA. 1999. The use of the vibrating probe technique to study steady extracellular currents during pollen germination and tube growth. In : Cresti M, Cai G, Moscatelli S, eds. Fertilization in higher plants: molecular and cytological aspects. Heidelberg, Germany : Springer-Verlag, 235 252.
75. Taylor JH, Peterson CA. 2005. Ectomycorrhizal impacts on nutrient uptake pathways in woody roots. New Forests 30 : 203 214.
76. + pump, Journal of Plant Research 116 : 419 442.
77. -, uptake and fusicoccin in root hairs of Limnobium storoniferum. Plant Physiology 94 : 1561 1567.
78. + pumping by Leishmania major Promastigotes. Journal of Biological Chemistry 270 : 5299 5304.
79. Ward JT, Lahner B, Yakubova E, Salt DE, Raghothama KG. 2008. The effect of iron on the primary root elongation of Arabidopsis during phosphate deficiency. Plant Physiology 147 : 1181 1191.
80. Winch S, Pritchard J. 1999. Acid-induced cell wall loosening is confined to the accelerating region of the root growing zone. Journal of Experimental Botany 50 : 1481 1487.
81. Yang X-C, Sachs F. 1989. Block of stretch-activated ion channels in Xenopus oocytes by gadolinium and calcium ions. Science. 243 : 1068 1071.
82. Zimmermann S, Thomine S, Guern J, Barbier-Brygoo H. 1994. An anion current at the plasma membrane of tobacco protoplasts shows ATP-dependent voltage regulation and is modulated by auxin. Plant Journal 6 : 707 716.
83. Zonia L, Cordeiro S, Feijó JA. 2001. Ion dynamics and the control of hydrodynamics in the regulation of pollen tube growth. Sexual Plant Reproduction 14 : 111 116.
84. Zonia L, Cordeiro S, Tupy J, Feijó JA. 2002. Oscillatory chloride efflux at the pollen tube apical tip has a role in growth and osmoregulation and is linked to inositol polyphosphate signaling pathways. Plant Cell 14 : 2233 2249.