The effect of Cylindrocarpon destructans on the growth of Eucalyptus regnans seedlings in air-dried and undried forest soil
T. M. Iles A C , D. H. Ashton A B D , K. J. Kelliher B and P. J. Keane AA Department of Botany, La Trobe University, Bundoora, Vic. 3083, Australia.
B School of Botany, The University of Melbourne, Parkville, Vic. 3052, Australia.
C Corresponding author. Email: tuula.iles@optusnet.com.au
D Deceased.
Australian Journal of Botany 58(2) 133-140 https://doi.org/10.1071/BT08124
Submitted: 10 July 2008 Accepted: 20 January 2010 Published: 29 March 2010
Abstract
The growth of Eucalyptus regnans F.Muell. (mountain ash) seedlings is poor in natural forest soil, where purple coloration of the foliage indicates P deficiency and where the fungus Cylindrocarpon destructans (Zinsm.) Scholten is commonly isolated from the roots of the seedlings. When forest soil is air-dried, P acquisiton and growth of seedlings are markedly improved, although the degree of growth stimulation varies considerably at different times, as does the frequency of occurrence of C. destructans on the roots. C. destructans has been implicated as a possible reason for suppressed growth of seedlings in undried natural soil. To find out whether C. destructans contributes to growth inhibition of E. regnans seedlings in undried forest soil, the effect of three isolates of C. destructans on the root growth of E. regnans seedlings was tested in Petri dish experiments in vitro and the effect of C. destructans inoculation on seedling growth both in air-dried and undried forest soil was tested in pot experiments. The frequency of occurrence of C. destructans on the roots varied at different times, and was not consistently higher in undried than in air-dried soil, even though the growth of the seedlings was always poor in undried soil compared with that in air-dried soil. In vitro, C. destructans decreased the root growth significantly and caused blackening of root tips. This effect was removed by adding natural air-dried or undried soil. In pot experiments using undried forest soil, there was no evidence of either direct toxic effect or any other adverse effect on the roots when soil was inoculated with this fungus, even when the growth of the seedlings was reduced to ~1/2 of that in uninoculated undried soil. In air-dried soil, inoculation with the fungus did not significantly reduce seedling growth. Although potentially pathogenic and able to cause blackening of root tips, C. destructans is unlikely to be the main reason for poor seedling growth in undried forest soil. It appears to be antagonistic rather than pathogenic, suppressing seedling growth only under unfavourable conditions, such as in undried soil, possibly by competing for limited nutrients, or by suppressing other beneficial micro-organisms. The results are discussed in the context of field conditions.
Acknowledgements
This paper reports some results from BSc(Honours) and PhD work by TMI and from earlier work done by DHA and KJK. The PhD part of the work was funded by an Australian Postgraduate Award. An Australian Research Council grant provided funding for the work done by DHA and KJK. Melbourne Water allowed access to Wallaby Creek catchment area. Dick Williams and two anonymous referees helped improve the paper.
Ashton DH, Chinner JH
(1999) Problems of regeneration of the mature E. regnans (the Big Ash) in the absence of fire at Wallaby Creek, Victoria. Australian Forestry 62, 265–280.
Ashton DH, Kelliher KJ
(1996a) Effects of forest soil desiccation on the growth of Eucalyptus regnans F.Muell. seedlings. Vegetation Science 7, 487–496.
| Crossref | GoogleScholarGoogle Scholar |
Ashton DH, Kelliher KJ
(1996b) The effect of soil desiccation on the nutrient status of Eucalyptus regnans F.Muell. seedlings. Plant and Soil 179, 45–56.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Attiwill PM
(1980) Nutrient cycling in a Eucalyptus obliqua L’Herit forest. IV. Nutrient uptake and nutrient return. Australian Journal of Botany 28, 199–222.
|
CAS |
Crossref |
Bending GD, Read DJ
(1995a) The structure and function of the vegetative mycelium of ectomycorrhizal plants. V. Foraging behaviour and translocation of nutrients from exploited litter. New Phytologist 130, 401–409.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Bending GD, Read DJ
(1995b) The structure and function of the vegetative mycelium of ectomycorrhizal plants. VI. Activities of nutrient mobilizing enzymes in birch litter colonized by Paxillus-involutus (Fr.) Fr. New Phytologist 130, 411–417.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Birch HF
(1958) The effect of soil drying on humus decomposition and nitrogen availability. Plant and Soil 10, 9–31.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Bolan NS
(1991) A critical review on the role of mycorrhizal fungi in the uptake of phosphorus by plants. Plant and Soil 134, 189–207.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Booth C
(1966) The genus Cylindrocarpon. Mycological papers 104, 1–56.
Borken W, Matzner E
(2009) Reappraisal of drying and wetting effects on C and N mineralisation and fluxes in soils. Global Change Biology 15, 808–824.
| Crossref | GoogleScholarGoogle Scholar |
Bottner P
(1985) Response of microbial biomass to alternate moist and dry conditions in a soil incubated with 14C- and 15N-labelled plant material. Soil Biology & Biochemistry 17, 329–337.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Buscot F,
Weber G, Oberwinkler F
(1992) Interactions between Cylindrocarpon destructans and ectomycorrhizas of Picea abies with Laccaria laccata and Paxillus involutus. Trees—Structure and Function 6, 83–90.
Chakravarty C,
Peterson RL, Ellis BE
(1991) Interaction between the ectomycorrhizal fungus Paxillus involutus, damping-off fungi and Pinus resinosa seedlings. Journal of Phytopathology 132, 207–218.
| Crossref | GoogleScholarGoogle Scholar |
Chambers DP, Attiwill PM
(1994) The ash-bed effect in Eucalyptus regnans forest: chemical, physical and microbiological changes in soil after heating or partial sterilisation. Australian Journal of Botany 42, 739–749.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Denef K,
Six J,
Bossuyt H,
Frey SD,
Elliott ET,
Merckx R, Paustian K
(2001) Influence of the dry–wet cycles on the interrelationship between aggregate, particulate organic matter, and microbial community dynamics. Soil Biology & Biochemistry 33, 2145–2153.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Evans G,
Cartwright JB, White NH
(1967) The production of a phytotoxin, nectrolide, by some root-surface isolates of Cylindrocarpon radicicola, Wr. Plant and Soil 26, 253–260.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Fierer N,
Schimel JP, Holden PA
(2003) Influence of drying–rewetting frequency on soil bacterial community structure. Microbial Ecology 45, 63–71.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Finlay RD, Read DJ
(1986) The structure and function of the vegetative mycelium of ectomycorrhizal plants. II. The uptake and distribution of phosphorus by mycelial strands interconnecting host plants. New Phytologist 103, 157–165.
| Crossref | GoogleScholarGoogle Scholar |
Florence RG, Crocker RL
(1962) Analysis of blackbutt (Eucalyptus pilularis Sm.) seedling growth in a blackbutt forest soil. Ecology 43, 670–679.
| Crossref | GoogleScholarGoogle Scholar |
Greenhalgh FC, Lucas SE
(1984) Effect of soil pasteurization on damping-off and root rot of subterranean clover caused by Fusarium avenaceum and Pythium spp. Soil Biology & Biochemistry 16, 87–88.
| Crossref | GoogleScholarGoogle Scholar |
Kim SI,
Shim JO,
Shin HS,
Choi HJ, Lee MW
(1992) Suppressive mechanism of soil-borne disease development and its practical application: isolation and identification of species of Trichoderma antagonistic to soil diseases and its activities in the rhizosphere. Korean Journal of Mycology 20, 337–346.
Kluge E
(1966) Pathogenität gegenüber Kiefernsämlingen und Toxinbildung bei Cylindrocarpon radicicola Wr. Phytopathology 55, 368–388.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Korkama T,
Fritze H,
Pakkanen A, Pennanen T
(2007) Interactions between extraradical ectomycorrhizal mycelia, microbes associated with the mycelia and growth rate of Norway spruce (Picea abies) clones. New Phytologist 173, 798–807.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Kowalski S
(1980) Influence of soil fungi community in selected mountain stands on the development of Cylindrocarpon destructans (Zins.) Scholt. Acta Societe Botanicae Poland 49(4), 487–492.
Launonen TM,
Ashton DH, Keane PJ
(1999) The effect of regeneration burns on the growth, nutrient acquisition and mycorrhizae of Eucalyptus regnans F.Muell. (mountain ash) seedlings. Plant and Soil 210, 273–283.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Launonen TM,
Ashton DH,
Kelliher KJ, Keane PJ
(2004) The growth and P acquisition of Eucalyptus regnans F.Muell seedlings in air-dried and undried forest soil in relation to seedling age and ectomycorrhizal infection. Plant and Soil 267, 179–189.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Launonen TM,
Ashton DH, Keane PJ
(2005) Growth, nutrient acquisition and ectomycorrhizae of Eucalyptus regnans F.Muell. seedlings in fertilized or diluted air-dried and undried forest soil. Plant and Soil 268, 221–231.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Liu Y,
Yao H, Huang C
(2009) Assessing the effect of air-drying and storage on microbial biomass and community structure in paddy soils. Plant and Soil 317, 213–221.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Marx DH
(1969) The influence of ectotropic mycorrhizal fungi on the resistance of pine roots to pathogenic infections. I. Antgonism of mycorrhizal fungi to root pathogenic fungi and soil bacteria. Phytopathology 59, 153–163.
Qian XM,
El-Ashker A,
Kottke I, Oberwinkler F
(1998) Studies of pathogenic and antagonistic microfungal populations and their potential interactions in the mycorrhizoplane of Norway spruce (Picea abies (L.) Karst.) and beech (Fagus sylvatica L.) on acidified and limed plots. Plant and Soil 199, 111–116.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Rab MA
(1996) Soil physical and hydrological properties following logging and slash burning in the Eucalyptus regnans forest of southeastern Australia. Forest Ecology and Management 84, 159–176.
| Crossref | GoogleScholarGoogle Scholar |
Raison RJ
(1979) Modification of the soil environment by vegetation fires, with particular reference to nitrogen transformations: a review. Plant and Soil 51, 73–108.
|
CAS |
Crossref |
Renbuss MA,
Chilvers GA, Pryor LD
(1973) Microbiology of an ashbed. Proceedings of the Linnean Society of New South Wales 97, 302–310.
Samuels GJ, Brayford D
(1990) Variation in Nectria radicicola and its anamorph Cylindrocarpon destructans. Mycological Research 94, 433–442.
Schelkle M, Peterson RL
(1996) Suppression of common root pathogens by helper bacteria and ectomycorrhizal fungi in vitro. Mycorrhiza 6, 481–485.
| Crossref |
Schimel JP,
Gulledge JM,
Clein-Curley JS,
Lindstrom JE, Braddock JS
(1999) Moisture effects on microbial activity and community structure in decomposing birch litter in the Alaskan taiga. Soil Biology & Biochemistry 31, 831–838.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Sparling GP,
Speir TW, Whale KN
(1986) Changes in microbial biomass-C, ATP content, soil phospho-monoesterase and phospho-diesterase activity following air-drying of soils. Soil Biology & Biochemistry 18, 363–370.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Taylor GS, Parkinson D
(1964) Studies on fungi in the root region. II. The effect of certain environmental conditions on the development of root surface mycoflora of dwarf bean seedlings. Plant and Soil 20, 34–42.
| Crossref | GoogleScholarGoogle Scholar |
Tomkins IB,
Kellas JD,
Tolhurst KG, Oswin DA
(1991) Effects of fire intensity on soil chemistry in a eucalypt forest. Australian Journal of Soil Research 29, 25–47.
|
CAS |
Crossref |
Unestam T,
Bayer-Ericsson L, Strand M
(1989) Involvement of Cylindrocarpon destructans in root death of Scotch pine seedlings: pathogenic behavior and predisposing factors. Scandinavian Journal of Forest Research 4, 521–535.
| Crossref | GoogleScholarGoogle Scholar |
Van Gestel M,
Merckx R, Vlassak K
(1993a) Microbial biomass and activity in soils with fluctuating water contents. Geoderma 56, 617–626.
| Crossref | GoogleScholarGoogle Scholar |
Van Gestel M,
Merckx R, Vlassak K
(1993b) Microbial biomass responses to soil drying and rewetting: the fate of fast- and slow-growing microorganisms in soils from different climates. Soil Biology & Biochemistry 25, 109–123.
| Crossref | GoogleScholarGoogle Scholar |
Warcup JH
(1991) The fungi forming mycorrhizas on eucalypt seedlings in regeneration coupes in Tasmania. Mycological Research 95, 329–332.
| Crossref | GoogleScholarGoogle Scholar |
