The spatial distribution of acid phosphatase activity in ectomycorrhizal tissues depends on soil fertility and morphotype, and relates to host plant phosphorus uptake

Plant, Cell and Environment

Volumn 35, Issue 1, 2012, Pages 126-135

  Alvarez, Maricel ^a   Huygens, Dries ^a,b   Díaz, Leila Milena ^a   Villanueva, Claudia Añazco ^a   Heyser, Wolfgang ^c   Boeckx, Pascal ^b  

^a UNIVERSIDAD AUSTRAL DE CHILE   (Chile)

^b GHENT UNIVERSITY   (Belgium)

^c UNIVERSITY OF BREMEN   (Germany)

Author keywords

Confocal laser scanning microscopy; Digital image processing; Ectomycorrhiza; Enzyme labelled fluorescence (ELF 97); Nothofagus obliqua

Indexed keywords

ACID PHOSPHATASE; PHOSPHORUS;

BIOLOGICAL UPTAKE; DIGITAL IMAGE; ECTOMYCORRHIZA; ENZYME ACTIVITY; HOST PLANT; IMAGE PROCESSING; MICROSCOPY; MOBILIZATION; MORPHOTYPE; PHOSPHORUS; ROOT COLONIZATION; SOIL FERTILITY; SPATIAL DISTRIBUTION;

ANGIOSPERM; ARTICLE; ASCOMYCETES; BASIDIOMYCETES; CHEMISTRY; ENZYMOLOGY; METABOLISM; MICROBIOLOGY; MYCELIUM; MYCORRHIZA; PHYSIOLOGY; PLANT; PLANT ROOT; SEEDLING; SOIL; STATISTICAL MODEL; SYMBIOSIS; TRANSPORT AT THE CELLULAR LEVEL;

ACID PHOSPHATASE; ANGIOSPERMS; ASCOMYCOTA; BASIDIOMYCOTA; BIOLOGICAL TRANSPORT; LINEAR MODELS; MYCELIUM; MYCORRHIZAE; PHOSPHORUS; PLANT ROOTS; PLANT SHOOTS; SEEDLING; SOIL; SYMBIOSIS;

FUNGI; NOTHOFAGUS OBLIQUA;

EID: 83255185067     PISSN: 01407791     EISSN: 13653040     Source Type: Journal    
DOI: 10.1111/j.1365-3040.2011.02422.x     Document Type: Article

References (51)

1. Agerer R. (1995) Anatomical characteristics of identified ectomycorrhizae: An attempt towards a natural classification. In Mycorrhiza: Structure, Function, Molecular Biology and Biotechnology (eds A. Varma & B. Hock ), pp. 685-734. Springer-Verlag, Berlin, Germany.
2. Agerer R. (2001) Exploration types of ectomycorrhizae. A proposal to classify ectomycorrhizal mycelial systems according to their patterns of differentiation and putative ecological importance. Mycorrhiza 11, 107-114.
3. Ali M.A., Louche J., Legname E., Duchemin M. & Plassard C. (2009) Pinus pinaster seedlings and their fungal symbionts show high plasticity in phosphorus acquisition in acidic soils. Tree Physiology 29, 1587-1597.
4. Alvarez M., Godoy R., Heyser W. & Hartel S. (2004) Surface-bound phosphatase activity in living hyphae of ectomycorrhizal fungi of Nothofagus obliqua. Mycologia 96, 479-487.
5. Alvarez M., Godoy R., Heyser W. & Hartel S. (2005) Anatomical-physiological determination of surface bound phosphatase activity in ectomycorrhizae of Nothofagus obliqua. Soil Biology & Biochemistry 37, 125-132.
6. Alvarez M., Gieseke A., Godoy R. & Hartel S. (2006) Surface-bound phosphatase activity in ectomycorrhizal fungi: a comparative study between a colorimetric and a microscope-based method. Biology and Fertility of Soils 42, 561-568.
7. Ashford A.E. & Allaway W.G. (2002) The role of motile tubular vacuole system in mycorrhizal fungi. Plant and Soil 244, 177-187.
8. Bartlett E.M. & Lewis D.H. (1973) Surface phosphatase activity of mycorrhizal roots of beech. Soil Biology & Biochemistry 5, 249-257.
9. Borie F., Zunino H. & Martinez L. (1989) Macromolecule-P associations and inositol phosphates in some Chilean volcanic soils of temperate regions. Communications in Soil Science and Plant Analysis 20, 1881-1984.
10. Bougher N.L., Grove T.S. & Malajczuk N. (1990) Growth and phosphorus acquisition of karri Eucalyptus diversicolor F. Muell. seedlings inoculated with ectomycorrhizal fungi in relation to phosphorus supply. New Phytologist 114, 77-85.
11. Box G.E.P. & Cox D.R. (1964) An analysis of transformations (with discussion). Journal of the Royal Statistical Society B 26, 211-252.
12. Bücking H. & Heyser W. (1999) Elemental composition and function of polyphosphates in ectomycorrhizal fungi - an X-ray microanalytical study. Mycological Research 103, 31-39.
13. Burns G.B. & Dick R.P. (2002) Enzymes in the Environment: Activity, Ecology and Applications. Marcel Dekker, New York.
14. Cairney J.W.G. (2011) Ectomycorrhizal fungi: the symbiotic route to the root for phosphorus in forest soils. Plant and Soil 344, 51-71.
15. Colpaert J.V., Van Tichelen K.K., Van Assche J.A. & Van Laere A. (1999) Short-term phosphorus uptake rates in mycorrhizal and non-mycorrhizal roots of intact Pinus sylvestris seedlings. New Phytologist 143, 589-597.
16. Courty P.E., Buee M., Diedhiou A.G., Frey-Klett P., Le Tacon F., Rineau F., Turpault M.P., Uroz S. & Garbaye J. (2010) The role of ectomycorrhizal communities in forest ecosystem processes: new perspectives and emerging concepts. Soil Biology & Biochemistry 42, 679-698.
17. Debaud J.C., Gay G., Prevost A., Lei J. & Dexheimer J. (1988) Ectomycorrhizal ability of genetically different homokaryotic and dikaryotic mycelia of Hebloma cylindrosporum. New Phytologist 108, 323-328.
18. Dexheimer J., Aubert-Dufresne M.-P., Gérard J., LeTacon F. & Mousain D. (1986) Étude de la localization ultrastructurale des activités phosphatasiques acides dans deux types d'ectomycorhizes: Pinus nigra nigricans/Hebeloma crustuliniforme et Pinus pinaster/Pisolithus tinctorius. Bulletin de la Societé Botanique de France 133, 343-352.
19. Ezawa T., Smith S.E. & Smith F.A. (2002) P metabolism and transport in arbuscular mycorrhizal fungi. Plant and Soil 244, 221-230.
20. Ezawa T., Hayatsu M. & Saito M. (2005) A new hypothesis on the strategy for acquisition of phosphorus in arbuscular mycorrhiza: up-regulation of secreted acid phosphatase gene in the host plant. Molecular Plant-Microbe Interactions 18, 1046-1053.
21. 31P-NMR. Mycorrhiza 7, 101-106.
22. Hinsinger P. (2001) Bioavailability of soil inorganic P in the rhizosphere as affected by root-induced chemical changes: a review. Plant and Soil 237, 173-195.
23. Hobbie E.A. & Agerer R. (2010) Nitrogen isotopes in ectomycorrhizal sporocaps correspond to belowground exploration types. Plant and Soil 327, 71-83.
24. Huygens D., Boeckx P., Templer P., Paulino L., Van Cleemput O., Oyarzún C., Müller C. & Godoy R. (2008) Mechanisms for retention of bioavailable nitrogen in volcanic rainforest soils. Nature Geoscience 1, 543-548.
25. Kottke I., Gutenberger M., Hampp R. & Oberwinkler F. (1987) An in vitro method for establishing mycorrhizae on coniferous tree seedlings. Trees 1, 191-194.
26. Lapeyrie F., Lei J., Malajczuk N. & Dexheimer J. (1989) Ultrastructural and biochemical changes at the prinfection stage of mycorrhizal formation by two isolates of Pisolithus tinctorius. Annals of Fores Science 46, 154s-757s.
27. Lei J., Lapeyrie F., Malajczuk N. & Dexheimer J. (1990) Infectivity of pine and eucalypt isolates of Pisolithus tinctorius (Pers.) Coker and Couch on roots of Eucalyptus urophylla S.T. Blake in vitro. II. Ultrastructural and biochemical changes at the early stage of mycorrhiza formation. New Phytologist 116, 115-122.
28. McElhinney C. & Mitchell D.T. (1993) Phosphatase-activity of 4 ectomycorrhizal fungi found in a Sitka spruce Japanese larch plantation in Ireland. Mycological Research 97, 725-732.
29. MacFall J.S., Slack S.A. & Wehrli S. (1992) Phosphorus distribution in red pine roots and the ectomycorrhizal fungus Hebloma arenosa. Plant Physiology 100, 713-717.
30. Molina R. & Palmer J.G. (1982) Isolation, maintenance, and pure culture manipulation of ectomycorrhizal fungi. In Methods and Principles of Mycorrhizal Research (ed. N.C. Schenck ), pp. 115-129. The American Phytopathological Society, St Paul, MN, USA.
31. Pasqualini S., Panara F. & Antonielli M. (1992) Acid phosphatase activity in Pinus pinea -Tuber albidum ectomycorrhizal association. Canadian Journal of Botany-Revue Canadienne De Botanique 70, 1377-1383.
32. Peterson R.L. & Massicotte H.B. (2004) Exploring structural definitions of mycorrhizas, with emphasis on nutrient-exchange interfaces. Canadian Journal of Botany - Revue Canadienne De Botanique 82, 1074-1088.
33. Peterson R.L., Massicotte H.B. & Melville L.H. (2004) Mycorrhizas: Anatomy and Cell Biology. CABI, Wallingford, CT, USA.
34. Plassard C. & Dell B. (2010) Phosphorus nutrition of mycorrhizal trees. Tree Physiology 30, 1129-1139.
35. R Development Core Team (2009) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna.
36. Redel Y., Rubio R., Godoy R. & Borie F. (2008) Phosphorus fractions and phosphatase activity in an Andisol under different forest ecosystems. Geoderma 145, 216-221.
37. Scheidegger C. & Brunner I. (1998) Electron microscopy of ectomycorrhiza: methods, applications, and findings. In Mycorrhiza: Function, Molecular Biology and Biotechnology (eds A. Varma & B. Hock ), pp. 205-228. Springer-Verlag, Berlin, Germany.
38. Smith S.E. & Read D.J. (2008) Mycorrhizal Symbiosis. Academic Press, San Diego, CA, USA.
39. Smith S.E. & Smith F.A. (1989) Membrane transport at the biotrophic interface: an overview. Australian Journal of Plant Physiology 16, 33-43.
40. Solomon C. & Breckon T. (2011) Fundamentals of Digital Image Processing - A Practical Approach with Examples in Matlab. John Wiley & Sons, Ltd, Oxford, UK.
41. Straker C.J. & Mitchell D.T. (1986) The activity and characterisation of acid phosphatases in endomycorrhizal fungi of the Ericaceae. New Phytologist 104, 243-256.
42. Taniguchi T., Kataoka R. & Futai K. (2008) Plant growth and nutrition in pine (Pinus thunbergii) seedlings and dehydrogenase and phosphatase activity of ectomycorrhizal root tips inoculated with seven individual ectomycorrhizal fungal species at high and low nitrogen conditions. Soil Biology & Biochemistry 40, 1235-1243.
43. Tibbett M., Sanders F.E. & Cairney J.W.G. (1998) The effect of temperature and inorganic phosphorus concentration on acid phosphatase production and growth rate in arctic and temperate isolates of the ectomycorrhizal fungi Hebeloma spp. in axenic culture. Mycological Research 102, 129-135.
44. Timonen S. & Sen R. (1998) Heterogeneity of fungal and plant enzyme expression in intact Scots pine-Suillus bovinus and -Paxillus involutus mycorrhizospheres developed in natural forest humus. New Phytologist 138, 355-366.
45. Unestam T. & Sun Y.P. (1995) Extrametrical structures of hydrophobic and hydrophilic ectomycorrhizal fungi. Mycorrhiza 5, 301-311.
46. Van Aarle I.M. (2009) Assessment of phosphatase activity associated with mycorrhizal fungi by epi-fluorescent microscopy. In Symbiotic Fungi, Soil Biology 18 (eds A. Varma & A.C. Kharkwal ), pp. 89-99. Springer-Verlag, Berlin.
47. Van Aarle I.M. & Plassard C. (2010) Spatial distribution of phosphatase activity with ectomycorrhizal plants is related to soil type. Soil Biology & Biochemistry 42, 324-330.
48. Van Aarle I.M., Rouhier H. & Saito M. (2002) Phosphatase activities of arbuscular mycorrhizal intraradical and extraradical mycelium, and their relation to phosphorus availability. Mycological Research 106, 1224-1229.
49. Werner T.P., Amrhein N. & Freimoser F.M. (2007) Specific localization of inorganic polyphosphate (poly P) in fungal cell walls by selective extraction and immunohistochemistry. Fungal Genetics and Biology 44, 845-852.
50. Yang X.J. & Finnegan P.M. (2010) Regulation of phosphate starvation responses in higher plants. Annals of Botany 105, 513-526.
51. Ziegler H. (1998) Physiology. In Lerbuch Der Botanik (eds P. Sitte, H. Ziegler, F. Ehrendorfer & A. Bresinky ), p. 318. Gustav Fisher, Stuttgart-Jena-Lübeck-Ulm, Germany.