Effects of fungi isolated from Quercus robur roots on growth of oak seedlings

• Autorzy: Kwasna H. , Szewczyk W.
• Języki publikacji: EN

Abstrakty

EN

Effects of 62 isolates (of 41 taxa) of fungi on growth of 1-year-old oak (Quercus robur) seedlings were studied in an inoculation experiment. The fungi were isolated from roots of 80–96-year-old Q. robur that had been subjected to periodic flooding and had symptoms of oak decline. The fungal genera included Alternaria, Aspergillus, Calonectria, Chaetomium, Cladosporium, Clonostachys, Corynespora, Cylindrocarpon, Dicyma, Geotrichum, Ilyonectria, Isaria, Metarhizium, Oidiodendron, Ophiostoma, Pezicula, Phialocephala, Phialophora, Pyrenochaeta, Sporendocladia, Sporothrix, Thelonectria, Trichoderma and Trimmatostroma. Mycelial colonies of fungi growing in potato-dextrose broth were used for soil inoculation. Plant growth was assessed 2 years after inoculation, when the plants were 3 years old. Stem lengths, and dry weights of stems, roots and leaves were measured. Stem growth was inhibited by 31 isolates (50%) and root growth by 12 isolates (19%). Stem growth was stimulated by two isolates (3%) and root growth by 17 isolates (27%). The overall ratio of inhibitors to stimulants was 2.1. The proportion of taxa that inhibited stem growth was 16 times greater than that which promoted stem growth. The proportion of taxa that promoted root growth was only 1.5 times greater than that which inhibited root growth. The structure of the fungal communities in periodically flooded oak forests suggests that they are more likely to inhibit than to promote vigour in oaks.

Słowa kluczowe

EN

growth inhibition; fungi; endophyte; isolation; Quercus robur; root; plant growth; oak; seedling

• Wydawca: -
• Czasopismo: Dendrobiology
• Rocznik: 2016
• Tom: 75
• Opis fizyczny: p.99-112,ref.

Twórcy

autor

Kwasna H.

• Department of Forest Pathology, Poznan University of Life Sciences, Wojska Polskiego 71c, 60-625 Poznan, Poland

autor

Szewczyk W.

• Department of Forest Pathology, Poznan University of Life Sciences, Wojska Polskiego 71c, 60-625 Poznan, Poland

Bibliografia

• Aerts R, Chapin FS (2000) The mineral nutrition of wild plants revisited: a reevaluation of processes and patterns. Advances in Ecological Research 30:1–67.
• Alberton O, Kuyper TW & Summerbell RC (2010) Dark septate root endophytic increase growth of Scots pine seedlings under elevated CO2 through enhanced nitrogen use efficiency. Plant and Soil 328: 459–470.
• Anderson NA & Anderson GW (1964) White pine root rot at the Chittenden nursery. Lake States Forest Experiment Station, U.S. Department of Agriculture , Research Note LS-26J.
• Baltruschat H, Fodor J, Harrach BD, Niemczyk E, Barna B, Gullner G, Janeczko A, Kogel KH, Schäfer P, Schwarczinger I, Zuccaro A & Skoczowski A (2008) Salt tolerance of barley induced by the root endophyte Piriformospora indica is associated with a strong increase in antioxidants. New Phytologist 80: 501–510.
• Barrett LG, Kniskern JM, Bodenhausen N, Zhang W & Bergelson J (2009) Continua of specificity and virulence in plant host–pathogen interactions: causes and consequences. New Phytologist 183: 513–529.
• Carroll GC (1986) The biology of endophytism in plants with particular reference to woody perennials. Microbiology of the phyllosphere. (ed by NJ.Fokkema & J Van den Heuvel) Cambridge University Press, Cambridge, pp. 205–222.
• Clay K & Schardl C (2002) Evolutionary origins and ecological consequences of endophyte symbiosis with grasses. The American Naturalist 160: 99–127.
• Contreras-Cornejo HA, Macias-Rodriguez L, Cortes-Penagos C & Lopez-Bucio J. (2009) Trichoderma virens, a plant beneficial fungus, enhances biomass production and promotes lateral root growth through an auxin-dependent mechanism in Arabidopsis. Plant Physiology 149: 1579–1592.
• Das A, Kamal S, Shakil NA, Sherameti I, Oelmüller R, Dua M, Tuteja N, Johri AK & Varma A (2012) The root endophyte fungus Piriformospora indica leads to early flowering, higher biomass and altered secondary metabolites of the medicinal plant, Coleus forskohlii. Plant Signaling and Behavior 7(1): 103–112.
• Faeth SH (2002) Are endophytic fungi defensive plant mutualists? Oikos 98(1): 25–36.
• Faeth SH (2009) Asexual fungal symbionts alter reproductive allocation and herbivory over time in their native perennial grass hosts. The American Naturalist 173 (5): 554–565.
• Faeth SH & Sullivan TJ (2003) Mutualistic asexual endophytes in a native grass are usually parasitic. The American Naturalist 161: 310–325.
• Freeman S & Rodriguez RJ (1993) Genetic conversion of a fungal plant pathogen to a nonpathogenic, endophytic mutualist. Science 260:75–78.
• Grünig CR, Queloz V, Sieber TN & Holdenrieder O (2008) Dark septate endophytes (DSE) of the Phialocephala fortinii s.l. – Acephala applanata species complex in tree roots: classification, population biology, and ecology. Botany 86: 1355–1369.
• Halmschlager E & Kowalski T (2004) The mycobiota in non-mycorrhizal roots of healthy and declining oaks. Canadian Journal of Botany 82(10): 1446–1458.
• Hanada RE, Pomella AW, Costa HS, Bezerra JL, Loguercio LL & Pereira JO (2010) Endophytic fungal diversity in Theobroma cacao (cacao) and T. grandiflorum (cupuaçu) trees and their potential for growth promotion and biocontrol of black-pod disease. Fungal Biology 114: 901–910.
• Hodda M, Smith D, Smith I, Nambiar L, & Pascoe I (2008). Incursion management in the face of multiple uncertainties: A case study of an unidentified nematode associated with dying pines near Melbourne, Australia. Pine Wilt Disease: A Worldwide Threat to Forest Ecosystems, Mota MM & Vieira P (eds), Springer. pp. 15–40.
• Hoeksema JD, Chaudhary VB, Gehring CA, Johnson NC, Karst J, Koide RT, Pringle A, Zabinski C, Bever JD, Moore JC, Wilson GWT, Klironomos JN & Umbanhowar J (2010) A meta-analysis of context-dependency in plant response to inoculation with mycorrhizal fungi. Ecology Letters 13(3): 394–407.
• Hol WHG, Van Veen JA (2002) Pyrrolizidine alkaloids from Senecio jacobaea affect fungal growth. Journal of Chemical Ecology 28: 1763–1772.
• Hol WHG, Vrieling K & van Veen JA (2003) Nutrients decrease pyrrolizidine alkaloid concentrations in Senecio jacobaea. New Phytologist 158: 175–181.
• Johnson NC, Graham JH & Smith FA (1997) Functioning of mycorrhizal associations along the mutualism‐parasitism continuum. New Phytologist 135: 575–586.
• Joosten L, Mulder PPJ, Klinkhamer PGL, & van Veen JA (2009) Soil-borne microorganisms and soil-type affect pyrrolizidine alkaloids in Jacobaea vulgaris Plant and Soil 325:133–143.
• Jumpponen A, Mattson KG & Trappe JM (1998) Mycorrhizal functioning of Phialocephala fortinii with Pinus contorta on glacier forefront soil: interactions with soil nitrogen and organic matter. Mycorrhiza 7: 261–265.
• Jumpponen A & Trappe JM (1998) Dark septate endophytes: a review of facultative biotrophic root colonizing fungi. New Phytologist 140(2): 295–310.
• Karst J, Jones MD & Turkington R (2009) Ectomycorrhizal colonization and intraspecific variation in growth responses of lodgepole pine. Plant Ecology 200: 161–165.
• Kessler W (1988) Root rot in young plants of oak and beech caused by Cylindrocarpon destructans. Sozialistische Forstwirtschaft 38(4): 110–111.
• Klironomos JN (2003) Variation in plant response to native and exotic arbuscular mycorrhizal fungi. Ecology 84: 2292–2301.
• Koch AM, Croll D & Sanders IR (2006) Genetic variability in a population of arbuscular mycorrhizal fungi causes variation in plant growth. Ecology Letters 9: 103–110.
• Kowalchuk GA, Hol WHG, & van Veen JA (2006) Rhizosphere fungal communities are influenced by Senecio jacobaea pyrrolizidine alkaloid content and composition. Soil Biology and Biochemistry 38:2852–2859.
• Kwaśna H, Szewczyk W & Behnke-Borowczyk J (2016) Fungal root endophytes of Quercus robur subjected to flooding. Forest Pathology 46:35–46.
• Larimer AL, Bever JD & Clay K (2010) The interactive effects of plant microbial symbionts: a review and meta analysis. Symbiosis 51:139–148.
• Liarzi O & Ezra D (2014) Endophyte-mediated biocontrol of herbaceous and non-herbaceous plants. Advances in Endophytic Research (ed by VC Verma & AC Gange) Springer, pp. 335–369.
• Macia’-Vicente JG, Jansson HB, Mendgen K & Lopez-Llorca LV (2008 a) Colonization of barley roots by endophytic fungi and their reduction of take-all caused by Gaeumannomyces graminis var. tritici. Canadian Journal of Microbiology 54(8): 600–609.
• Macia’-Vicente JG, Jansson HB, Samir K, Abdullah SK, Descals E, Salinas J & Lopez-Llorca LV (2008 b) Fungal root endophytes from natural vegetation in Mediterranean environments with special reference to Fusarium spp. FEMS Microbiological Ecology 64: 90–105.
• Mandyam KG, Fox C & Jumpponen A (2012) Septate endophyte colonization and host responses of grasses and forbs native to a tallgrass prairie. Mycorrhiza 22: 109–119.
• Mandyam K & Jumpponen A (2005) Seeking the elusive function of the root-colonising dark septate endophytic fungi. Studies in Mycology 53: 173–189.
• Mandyam KG., Roe J & Jumpponen A (2013) Arabidopsis thaliana model system reveals a continuum of responses to root endophyte colonization. Fungal Biology 117(4): 250–60.
• Mayerhofer MS, Kernaghan G & Harper KA (2013) The effects of fungal root endophytes on plant growth: a meta-analysis. Mycorrhiza 23(2): 119–128.
• Melin E (1922) On the mycorrhizas of Pinus silvestris L. and Picea abies Karst: a preliminary note. Journal of Ecology 9: 254–257.
• Munkvold L, Kjøller R, Vestberg M, Rosendahl S & Jakobsen I (2004) High functional diversity within species of arbuscular mycorrhizal fungi. New Phytologist 164: 357–364.
• Newsham KK (1994) First record of intracellular sporulation by a coelomycete fungus. Mycological Research 98: 1390–1392.
• Newsham KK (2011) A meta-analysis of plant responses to dark septate root endophytes. New Phytologist 190: 783–793.
• Paz Z, Burdman S, Gerson U & Sztejnberg A (2007) Antagonistic effects of the endophytic fungus Meira geulakonigii on the citrus rust mite Phyllocoptruta oleivora. Journal of Applied Microbiology 103 (6): 2570–2579.
• Piculell BJ, Hoeksema JD & Thompson JN (2008) Interactions of biotic and abiotic environmental factors in an ectomycorrhizal symbiosis, and the potential for selection mosaics. BMC Biology 6: 23.
• Redman RS, Dunigan DD & Rodriguez RJ (2001) Fungal symbiosis from mutualism to parasitism: who controls the outcome, host or invader? New Phytologist 151: 705–716.
• Reininger V, Grünig CR & Sieber TN (2012) Host species and strain combination determine growth reduction of spruce and birch seedlings colonized by root-associated dark septate endophytes. Environmental Microbiology 14: 1064–1076.
• Reininger V & Sieber TN (2012) Mycorrhiza reduces adverse effects of dark septate endophytes (DSE) on growth of Conifers. Plos one. DOI: 10.1371/journal.pone.0042865
• Richard C & Fortin A (1974) Distribution géographique, écologie, physiologie, pathogenicité et sporulation du Mycelium radicis atrovirens. Phytoprotection 55: 67–88.
• Richard C, Fortin J-A & Fortin A (1971) Protective effect of an ectomycorrhizal fungus against the root pathogen Mycelium radicis atrovirens. Canadian Journal of Forest Research 1: 246–251.
• Ridge EH & Rovira AD (1971) Phosphatase activity of intact young wheat roots under sterile and non-sterile conditions. New Phytologist 70: 1017–1026.
• Robin C & Desprez-Loustau M-L (1998) Testing variability in pathogenicity of Phytophthora cinnamomi. European Journal of Plant Pathology 104: 465–475.
• Rodriguez RJ, Freeman DC , McArthur ED, Kim JO & Redman RS (2009 a) Symbiotic regulation of plant growth, development and reproduction. Communicative and Integrative Biology 2(2): 141–143.
• Rodriguez RJ & Redman R (2008) More than 400 million years of evolution and some plants still can’t make it on their own: Plant stress tolerance via fungal symbiosis. Journal of Experimental Botany 59: 1109–1114.
• Rodriguez RJ, Redman RS & Henson JM (2004) The role of fungal symbioses in the adaptation of plants to high stress environments. Mitigation and Adaptation Strategies for Global Change 9: 261–272.
• Rodriguez RJ, Redman RS & Henson JM (2005) Symbiotic lifestyle expression by fungal endophytes and the adaptation of plants to stress: Unravelling the complexities of intimacy. The fungal community: its organization and role in the ecosystem, Dighton J, White JF & Oudemans P(eds) 3rd Ed. CRC Press, Boca Raton, FL, USA, pp. 683–695.
• Rodriguez RJ, White JF, Jr Arnold AE & Redman RS (2009 b) Fungal endophytes: diversity and functional roles. New Phytologist 182: 314–330.
• Rowe HC & Kliebenstein DJ (2010) All mold is not alike: the importance of intraspecific diversity in necrotrophic plant pathogens. PLoS Pathog 6: e1000759.
• Ruotsalainen AL & Kytöviita M-M (2004) Mycorrhiza does not alter low temperature impact on Gnaphalium norvegicum. Oecologia 140: 226–233.
• Saikkonen K, Faeth SH, Helander M & Sullivan TJ (1998) Fungal endophytes: a continuum of interactions with host plants. Annual Review of Ecology and Systematics 29: 319–343.
• Sánchez ME, Lora F & Trapero A (2002) First report of Cylindrocarpon destructans as a root pathogen of Mediterranean Quercus species in Spain. Plant Diseases 86(6): 693.
• Scervino JM, Gottlieb A, SIlvani VA, Pérgola M, Fernández L & Godeas AM (2009) Exudates of dark septate endophyte (DSE) modulate the development of the arbuscular mycorrhizal fungus (AMF) Gigaspora rosea. Soil Biology and Biochemistry 41: 1753–1756.
• Schulz B & Boyle C (2005) The endophytic continuum. Mycological Research 109: 661–686.
• Schulz B, Rommert AK, Dammann U, Aust HJ & Strack D (1999) The endophyte-host interaction: a balanced antagonism? Mycological Research 10: 1275–1283.
• Schwartz MW & Hoeksema JD (1998) Specialization and resource trade: biological markets as a model of mutualisms. Ecology 79: 1029–1038.
• Sieber TN (2002) Fungal root endophytes. The hidden half. Plant Roots (ed by Y Waisel A, Eshel & U Kafkafi) 1st Ed. Marcel Dekker, New York, USA, pp. 887–917.
• Sieber TN (2007) Endophytic fungi in forest trees: are they mutualists? Fungal Biology Rev 21: 75–89.
• Sinclair JB & Cerkauskas RF (1997) Latent infection vs. endophytic colonization by fungi. Endophytic Fungi in Grasses and Woody Plants (ed by SC Redlin & LM Carris) APS Press, St. Paul, MN, USA, pp. 3–30.
• Srivastava PK, Shenoy BD, Gupta M, Vaish A, Mannan S, Singh N, Tewari SK & Tripathi RD (2012) Stimulatory effects of arsenic-tolerant soil fungi on plant growth promotion and soil properties. Microbes Environment 27(4): 477–482.
• Stoyke G & Currah RS (1993) Resynthesis in pure culture of a common sub-alpine fungus–root association using Phialocephala fortinii and Menziesia ferruginea (Ericaceae). Arctic and Alpine Research 25: 189–193.
• Sturz AV &Nowak J (2000) Endophytic communities of rhizobacteria and the strategies required to create yield enhancing associations with crops. Applied Soil Ecology 15: 183–190.
• Sylvia D, Fuhrmann J, Hartel P & Zuberer D (2005) Principles and applications of soil microbiology. Pearson Education Inc. New Jersey.
• Tanaka A, Christensen MJ, Takemoto D, Park P & Scott B (2006) Reactive oxygen species play a role in regulating a fungus–perennial ryegrass mutualistic interaction. The Plant Cell 18: 1052–1066.
• Tellenbach C, Grunig CR & Sieber TN (2011) Negative effects on survival and performance of Norway spruce seedlings colonized by dark septate root endophytes are primarily isolate-dependent. Environmental Microbiology 13: 2508–2517.
• Tsuneda A, Wang W, Tsuneda I & Currah RS (2009) Endomembrane system of aspen root cells plays a key role in defense against a common fungal root endophyte, Cryptosporiopsis radicicola. Mycologia 101(2): 182–189.
• Tudzynski B & Sharon A (2002) Biosynthesis, biological role and application of fungal hormones. The mycota X: Industrial applications (ed by HD Osiewacz) Springer, Berlin Heidelberg New York, 183–211.
• Upson R, Read DJ & Newsham KK (2009) Nitrogen form influences the response of Deschampsia antarctica to dark septate root endophytes. Mycorrhiza 20:1–11.
• van de Voorde TFJ, van der Putten WH & Bezemer TM (2011) Intra- and interspecific plant–soil interactions, soil legacies and priority effects during old-field succession. Journal of Ecology 99: 945–953.
• van de Voorde TFJ, Van der Putten WH & Bezemer TM (2012) Soil inoculation method determines the strength of plant–soil interactions. Soil Biology and Biochemistry 55: 1–6.
• Waller F, Achatz B, Baltruschat H, Fodor J, Becker K, Fischer M, Heier T, Hückelhoven R, Neumann C, von Wettstein D, Franken &, Kogel KH (2005) The endophytic fungus Piriformospora indica reprograms barley to salt-stress tolerance, disease resistance, and higher yield. Proceedings of the National Academy of Sciences of the United States of America 102 (38): 13386–13391.
• Waller F, Mukherjee K, Deshmukh SD, Achatz B, Sharma M, Schäfer P & Kogel KH (2008) Systemic and local modulation of plant responses by Piriformospora indica and related Sebacinales species. Journal of Plant Physiology 165 (1): 60–70.
• Wang W, Tsuneda A, Gibas CF & Currah RS (2007) Cryptosporiopsis species isolated from the roots of aspen in central Alberta: identification, morphology, and interactions with the host, in vitro. Canadian Journal of Botany 85(12): 1214–1226.
• Wilcox HE & Wang CJK (1987) Mycorrhizal and pathological associations of dematiaceous fungi in roots of 7-month-old tree seedlings. Canadian Journal of Forest Research 17(8): 884–899.

Identyfikatory

DOI

10.12657/denbio.075.010