Plant Biol (Stuttg) 2004; 6(1): 91-99
DOI: 10.1055/s-2003-44718
Original Paper

Georg Thieme Verlag Stuttgart · New York

Compatible and Incompetent Paxillus involutus Isolates for Ectomycorrhiza Formation in vitro with Poplar (Populus × canescens) Differ in H2O2 Production

A. Gafur 1 , A. Schützendübel 2 , R. Langenfeld-Heyser 2 , E. Fritz 2 , A. Polle 2
  • 1Department of Plant Protection, University of Lampung, Bandar Lampung, Indonesia
  • 2Forstbotanisches Institut, Georg-August University Göttingen, Göttingen, Germany
Further Information

Publication History

Publication Date:
17 February 2004 (online)

Abstract

Isolates of Paxillus involutus (Batsch) Fr. collected from different hosts and environmental conditions were screened for their ability to form ectomycorrhizal symbiosis with hybrid poplar P. × canescens (= Populus tremula L. × P. alba) in vitro. The ability to form ectomycorrhiza varied between the fungal isolates and was not correlated with the growth rate of the fungi on agar-based medium. The isolate MAJ, which was capable of mycorrhiza synthesis under axenic conditions, and the incompetent isolate NAU were characterized morphologically and anatomically. MAJ formed a typical hyphal mantle and a Hartig net, whereas NAU was not able to penetrate the host cell walls and caused thickenings of the outer cell walls of the host. MAJ, but not NAU, displayed strong H2O2 accumulation in the outer hyphal mantle. Increases in H2O2 in the outer epidermal walls and adjacent hyphae of the incompetent isolate were moderate. No increases of H2O2 in response to the mycobionts were found inside roots. Suggested functions of H2O2 production in the outer hyphal mantle of the compatible interaction are: growth regulation of the host's roots, defence against other invading microbes, or increasing plant-innate immunity. The system established here for P. × canescens compatible and incompetent fungal associations will be useful to take advantage of genomic information now available for poplar to study tree-fungal interactions at the molecular and physiological level.

References

  • 1 Agerer R.. Color Atlas of Ectomycorrhizae. Plate 27. Einhorn Verlag, Germany (1990)
  • 2 Albrecht C., Burgess T., Dell B., Lapeyrie F.. Chitinase and peroxidase activities are induced in Eucalyptus roots according to aggressiveness of Australian ectomycorrhizal strains of Pisolithus sp.  New Phytol.. (1994);  127 217-222
  • 3 Alvarez M. E., Pennell R., Meijer P.-J., Ishikawa A., Dixon R. A., Lamb C.. Reactive oxygen intermediates mediate a systemic signal network in the establishment of plant immunity.  Cell. (1998);  92 773-784
  • 4 Barker S. J., Duplessis S., Tagu D.. The application of genetic approaches for investigations of mycorrhizal symbioses.  Plant and Soil. (2002);  244 85-95
  • 5 Baum C., Makeschin F.. Effects of nitrogen and phosphorus fertilization on mycorrhizal formation of two poplar clones (Populus trichocarpa and P. tremula × tremuloides).  J. Plant Nutr. Soil Sci.. (2000);  163 491-497
  • 6 Baum C., Schmid K., Makeschin F.. Interactive effects of substrates and ectomycorrhizal colonization on growth of a poplar clone.  J. Plant Nutr. Soil Sci.. (2000);  163 221-226
  • 7 Bradshaw H. D., Ceulemans R., Davis J., Stettler R.. Emerging model systems in plant biology: poplar (Populus) as a model forest tree.  J. Plant Growth Reg.. (2000);  19 306-313
  • 8 Cairney J. W. G.. Intraspecific physiological variation: implications for understanding functional diversity in ectomycorrhizal fungi.  Mycorrhiza. (1999);  9 125-135
  • 9 Cripps C. L., Miller O. K.. Ectomycorrhizae formed in vitro by quaking aspen: including Inocybe lacera and Amanita pantherina. .  Mycorrhiza. (1995);  5 357-370
  • 10 Cripps C. L., Miller O. K.. Ectomycorrhizal fungi associated with aspen on three sites in the north-central Rocky Mountains.  Can. J. Bot.. (1993);  71 1414-1420
  • 11 Duddridge J. A.. Specificity and recognition in ectomycorrhizal association. Pegg, G. F. and Ayres, P. G., eds. Fungal Infection of Plants. England; Cambridge University Press (1987): 25-44
  • 12 Esau K.. Plant Anatomy. New York; John Wiley and Sons (1965): 735
  • 13 Fritz E., Jentschke G.. Agar standards for quantitative X-ray microanalysis of resin-embedded plant tissues.  J. Microsc.. (1994);  174 47-50
  • 14 Garcia-Garrido J. M., Ocampo J. A.. Regulation of the plant defence response in arbuscular mycorrhizal symbiosis.  J. Exp. Bot.. (2002);  53 1377-1386
  • 15 Gianninazzi-Pearson V., Dumas-Gaudot E., Golotte A., Tahiri-Alaoui A., Gianninazzi S.. Cellular and molecular defense related root responses to invasion by arbuscular mycorrhizal fungi.  New Phytol.. (1996);  133 45-57
  • 16 Godbout C., Fortin J. A.. Synthesized ectomycorrhizae of aspen: fungal genus level of structural characterization.  Can. J. Bot.. (1985);  63 252-262
  • 17 Hampp R., Ecke M., Schaeffer C., Wallenda T., Wingler A., Kottke I., Sundberg B.. Axenic mycorrhization of wild type and transgenic hybrid aspen expressing T-DNA indoleacetic acid-biosynthetic genes.  Trees. (1996);  11 59-64
  • 18 Hebe G., Hager A., Salzer P.. Initial signalling processes induced by elicitors of ectomycorrhiza-forming fungi in spruce cells can also be triggered by G-protein-activating mastoparan and protein-phosphatase-inhibiting cantharidin.  Planta. (1999);  207 418-425
  • 53 Heslin M. C., Douglas G. C.. Effects of ectomycorrhizal fungi on growth and development of poplar plants derived from tissue culture.  Sci. Hort.. (1986);  30 143-149
  • 19 Hönig K., Riefler M., Kottke I.. Survey of Paxillus involutus (Batsch) Fr. inoculum and fruitbodies in a nursery by IGS-RFLPs and IGS sequences.  Mycorrhiza. (2000);  9 315-322
  • 20 Ingleby K., Mason P. A., Last F. T., Fleming L. V.. Identification of Ectomycorrhizas. HMSO, England; ITE Research Publication (1990)
  • 21 Jarosch M., Bresinsky A.. Speciation and phylogenetic distances within Paxillus s. str. (Basidiomycetes, Boletales).  Plant Biol.. (1999);  1 701-706
  • 22 Jenschke G., Godbold D. L.. Metal toxicity and ectomycorrhizas.  Physiol. Plant. (2000);  109 107-116
  • 23 Kieliszewska-Rokicka B.. Effect of nitrogen level on acid phosphatase activity of eight isolates of the ectomycorrhizal fungus Paxillus involutus cultured in vitro.  Plant Soil. (1992);  139 229-238
  • 24 Klironomos J. N., Kendrick B. W.. Research on mycorrhizas: trends in the past 40 years as expressed in the “MYCOLIT” database.  New Phytol. (1993);  125 595-600
  • 25 Lei J., Lapeyrie F., Malajczuk N., Dexheimer J.. 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 mycorrhizal formation.  New Phytol.. (1990);  116 115-122
  • 26 LeQuéré A., Johansson T., Tunlid A.. Size and complexity of the nuclear genome of the ectomycorrhizal fungus Paxillus involutus. .  Fungal Gen Biol.. (2002);  36 234-241
  • 27 Littke W. R., Bledsoe C. S., Edmonds R. L.. Nitrogen uptake and growth in vitro by Hebeloma crustuliniforme and other Pacific Northwest mycorrhizal fungi.  Can. J. Bot.. (1984);  62 647-652
  • 28 Loewe A., Einig W., Shi-Lan B., Dizengremel P., Hampp R., Shi L. B.. Mycorrhiza formation and elevated CO2 both increase the capacity for sucrose synthesis in source leaves of spruce and aspen.  New Phytol.. (2000);  145 565-574
  • 29 Malajczuk N., Lapeyrie F., Garbaye J.. Infectivity of pine and eucalypt isolates of Pisolithus tinctorius on roots of Eucalyptus urophylla in vitro. I. Ectomycorrhiza formation in model systems.  New Phytol.. (1990);  114 627-631
  • 30 Martin F., Duplessis S., Ditengou F., Lagrange H., Voiblet C., Lapeyrie F.. Developmental cross talking in the ectomycorrhizal symbiosis: signals and communication genes.  New Phytol.. (2001);  151 145-154
  • 31 Mensen R., Hager A., Salzer P.. Elicitor-induced changes of wall-bound and secreted peroxidase activities in suspension-cultured spruce (Picea abies) cells are attenuated by auxins.  Physiol. Plant. (1998);  102 539-546
  • 32 Miller S. L., Koo C. D., Molina R.. Characterization of red alder ectomycorrhizae: a preface to monitoring below-ground ecological responses.  Can. J. Bot.. (1991);  69 516-531
  • 33 Molina R., Trappe J. M.. Patterns of ectomycorrhizal host specificity and potential among Pacific Northwest conifers and fungi.  Forest Sci.. (1982);  28 423-458
  • 34 Morashige T., Skoog F.. A revised medium for rapid growth and bioassays with tobacco tissue culture.  Physiol. Plant. (1962);  15 472-479
  • 35 Münzenberger B., Otter T., Wüstrich D., Polle A.. Peroxidase and lactase activities in mycorrhizal and non-mycorrhizal roots of Norway spruce (Picea abies L.) and larch (Larix decidua). .  Can. J. Bot.. (1997);  75 932-938
  • 36 Olson P. D., Varner J. E.. Hydrogen peroxide and lignification.  Plant J.. (1993);  4 887-892
  • 37 Orozco-Cardenas M. L., Narvaez-Vasquez J., Ryan C. A.. Hydrogen peroxide acts as a second messenger for the induction of defense genes in tomato plants in response to wounding, systemic, and methyl jasmonate.  Plant Cell. (2001);  13 179-191
  • 38 Pardo A. G., Hanif M., Raudaskoski M., Gorfer M.. Genetic transformation of ectomycorrhizal fungi mediated by Agrobacterium tumefaciens. .  Mycol. Res.. (2002);  106 132-137
  • 39 Polle A., Schützendübel A.. Heavy metal signalling in plants: linking cellular and organismic responses. Hirt, H. and Shinozaki, K., eds. Topics in Current Genetics. Plant Responses to Abiotic Stress, Vol. 4. Berlin; Springer Verlag (2003): 187-216
  • 40 Salzer P., Hebe G., Hager A.. Cleavage of chitinous elicitors from the ectomycorrhizal fungus Hebeloma crustuliniforme by host chitinases prevents induction of K+ and Cl- release, extracellular alkalinization and H2O2 synthesis of Picea abies cells.  Planta. (1997);  203 470-479
  • 41 Salzer P., Corbière H., Boller T.. Hydrogen peroxide accumulation in Medicago truncatula roots colonized by the arbuscular mycorrhiza-forming fungus Glomus intraradices. .  Planta. (1999);  208 319-325
  • 42 Schützendübel A., Polle A.. Plant responses to abiotic stresses: heavy metal-induced oxidative stress and protection by mycorrhization.  J. Exp. Bot.. (2002);  53 1351-1365
  • 43 Schützendübel A., Nikolova P., Rudolf C., Polle A.. Cadmium and H2O2-induced oxidative stress in Populus × canescens roots.  Plant Physiol. Biochem.. (2002);  40 577-584
  • 44 Smith S. E.. Discoveries, discussions and directions in mycorrhizal research. Varma, A. and Hock, B., eds Mycorrhiza: Structure, Function, Molecular Biology and Biotechnology. Berlin; Springer-Verlag (1999): 3-24
  • 45 Spurr A. R.. A low-viscosity epoxy resin embedding medium for electron microscopy.  J. Ultrastruct. Res.. (1969);  26 31-43
  • 46 Tarkka M., Nyman T. A., Kalkkinen N., Raudaskoski M.. Scots pine expresses short-root-specific peroxidases during development.  Eur. J. Biochem.. (2001);  268 86-92
  • 47 Taylor G.. Populus: Arabidopsis for forestry. Do we need a model tree?.  Ann. Bot.. (2002);  90 681-689
  • 48 Tenhaken R., Levine A., Brisson L. F., Dixon R. A., Lamb C.. Function of the oxidative burst in hypersensitive disease resistance.  Proc. Natl. Acad. Sci. USA. (1995);  92 4158-4163
  • 49 Voiblet C., Duplessis S., Encelot N., Martin F.. Identification of symbiosis-regulated genes in Eucalytus-Pisolithus tinctorius ectomycorrhiza by differential hybridization of arrayed cDNA.  Plant J.. (2001);  25 181-191
  • 50 Wallander H., Söderström B.. Paxillus. . Cairney, J. W. G. and Chamber, S. M., eds. Ectomycorrhizal Fungi Key Genera in Profile. Berlin; Springer Verlag (1999): 231-252
  • 51 Wojtaszek P.. Oxidative burst: an early plant response to pathogen infection.  Biochem. J.. (1997);  322 681-692
  • 52 Wullschleger S. D., Tuskan G. A., DiFazio S. P.. Genomics and the tree physiologist.  Tree Physiol.. (2002);  22 1273-1276

A. Polle

Forstbotanisches Institut
Georg-August-Universität Göttingen

Büsgenweg 2

37077 Göttingen

Germany

Email: apolle@gwdg.de

Section Editor: H. Rennenberg

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