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Impact of Heterobasidion root-rot on fine root morphology and associated fungi in Picea abies stands on peat soils

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Abstract

We examined differences in fine root morphology, mycorrhizal colonisation and root-inhabiting fungal communities between Picea abies individuals infected by Heterobasidion root-rot compared with healthy individuals in four stands on peat soils in Latvia. We hypothesised that decreased tree vitality and alteration in supply of photosynthates belowground due to root-rot infection might lead to changes in fungal communities of tree roots. Plots were established in places where trees were infected and in places where they were healthy. Within each stand, five replicate soil cores with roots were taken to 20 cm depth in each root-rot infected and uninfected plot. Root morphological parameters, mycorrhizal colonisation and associated fungal communities, and soil chemical properties were analysed. In three stands root morphological parameters and in all stands root mycorrhizal colonisation were similar between root-rot infected and uninfected plots. In one stand, there were significant differences in root morphological parameters between root-rot infected versus uninfected plots, but these were likely due to significant differences in soil chemical properties between the plots. Sequencing of the internal transcribed spacer of fungal nuclear rDNA from ectomycorrhizal (ECM) root morphotypes of P. abies revealed the presence of 42 fungal species, among which ECM basidiomycetes Tylospora asterophora (24.6 % of fine roots examined), Amphinema byssoides (14.5 %) and Russula sapinea (9.7 %) were most common. Within each stand, the richness of fungal species and the composition of fungal communities in root-rot infected versus uninfected plots were similar. In conclusion, Heterobasidion root-rot had little or no effect on fine root morphology, mycorrhizal colonisation and composition of fungal communities in fine roots of P. abies growing on peat soils.

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References

  • Agerer R (1986–2006) Colour atlas of ectomycorrhizae. Einhorn-Verlag, Schwäbisch Gmünd, München, Germany

  • Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Arhipova N, Gaitnieks T, Donis J, Stenlid J, Vasaitis R (2011) Butt rot incidence, causal fungi, and related yield loss in Picea abies stands of Latvia. Can J For Res 41:2337–2345. doi:10.1139/x11-141

    Article  Google Scholar 

  • Bendz-Hellgren M, Stenlid J (1995) Long-term reduction in the diameter growth of butt rot affected Norway spruce, Picea abies. Forest Ecol Manag 74:239–243. doi:10.1016/0378-1127(95)03530-N

    Article  Google Scholar 

  • Bendz-Hellgren M, Stenlid J (1997) Decreased volume growth of Picea abies in response to Heterobasidion annosum infection. Can J For Res 27:1519–1524. doi:10.1139/x97-104

    Article  Google Scholar 

  • Bendz-Hellgren M, Brandtberg P-O, Johansson M, Swedjemark G, Stenlid J (1999) Growth Rate of Heterobasidion annosum in Picea abies established on forest land and arable land. Scand J For Res 14:402–407. doi:10.1080/02827589950154104

    Article  Google Scholar 

  • Bergemann SE, Kordesch NC, VanSant-Glass W, Garbelotto M, Metz TA (2013) Implications of tanoak decline in forests impacted by Phytophthora ramorum: girdling decreases the soil hyphal abundance of ectomycorrhizal fungi associated with Notholithocarpus densiflorus. Madroño 60:95–106. doi:10.3120/0024-9637-60.2.95

    Article  Google Scholar 

  • Bücking E (1979) Fichten-Mykorrhizen auf Standorten der Schwäbischen Alb und ihre Beziehung zum Befall durch Fomes annosus. Eur J Forest Pathol 9:19–35

    Article  Google Scholar 

  • Dalman K, Olson Å, Stenlid J (2010) Evolutionary history of the conifer root rot fungus Heterobasidion annosum sensu lato. Mol Ecol 19:4979–4993. doi:10.1111/j.1365-294X.2010.04873.x

    Article  CAS  PubMed  Google Scholar 

  • Eberhardt U, Walter L, Kottke I (1999) Molecular and morphological discrimination between Tylospora fibrillosa and Tylospora asterophora mycorrhizae. Can J Botany 77:11–21. doi:10.1139/b98-182

    CAS  Google Scholar 

  • Eichhorn J, Roskams P, Ferretti M, Mues V, Szepesi A, Durrant D (2010) Visual assessment of crown condition and damaging agents. Manual part IV. Manual on methods and criteria for harmonized sampling, assessment, monitoring and analysis of the effects of air pollution on forests. In. UNECE ICP Forests programme co-ordinating centre, Hamburg, pp 1–49 (available at: http://icp-forests.net/page/icp-forests-manual)

  • Gaitnieks T (2005) Vitality of Norway spruce fine roots in stands infected by Heterobasidion annosum. In: Solheim H, Hietala AM (eds) Proceedings of the SNS meeting in forest pathology: Forest pathology research in Nordic and Baltic countries 2005. Skogbrukets Kursinstitutt, Biri, Norway, pp 79–82 (available at: http://www.skogoglandskap.no/filearchive/a-2006-1.pdf)

  • Gaitnieks T, Liepa I, Rokjanis B, Indriksons A (2000) Development of Norway spruce mycorrhiza in mixed Norway spruce and grey alder stands infected by Heterobasidion annosum. Metsanduslikud Uurimused 34:44–51

    Google Scholar 

  • Gaitnieks T, Arhipova N, Donis J, Stenlid J, Vasaitis R (2008) Butt rot incidence and related losses in Latvian Picea abies (L.) Karst. stands. Proceedings of 12th international conference on root and butt rots, Berkley, California, pp 177–179

  • Garbelotto M, Gonthier P (2013) Biology, epidemiology, and control of Heterobasidion species worldwide. Annu Rev Phytopathol 51:39–59. doi:10.1146/annurev-phyto-082712-102225

    Article  CAS  PubMed  Google Scholar 

  • Gardes M, Bruns T (1993) ITS primers with enhanced specificity for basidiomycetes—application to the identification of mycorrhizae and rusts. Mol Ecol 2:113–118

    Article  CAS  PubMed  Google Scholar 

  • Hall T (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for windows 95/98/NT. Nucleic Acid S 41:95–98

    CAS  Google Scholar 

  • Helmisaari HS, Saarsalmi A, Kukkola M (2009) Effects of wood ash and nitrogen fertilization on fine root biomass and soil and foliage nutrients in a Norway spruce stand in Finland. Plant Soil 314:121–132. doi:10.1007/s11104-008-9711-4

    Article  CAS  Google Scholar 

  • Högberg P, Nordgren A, Buchmann N, Taylor AFS, Ekblad A, Högberg MN, Nyberg G, Ottosson-Lofvenius M, Read DJ (2001) Large-scale forest girdling shows that current photosynthesis drives soil respiration. Nature 411:789–792. doi:10.1038/35081058

    Article  PubMed  Google Scholar 

  • Jansons J (2011) Statistical inventory of Latvia’s forest resources (results of cycle I), Latvian State Forest Research Institute “Silava”. (In Latvian), (available at: http://www.silava.lv/22/section.aspx/View/13)

  • Klavina D, Gaitnieks T, Menkis A (2013) Survival, growth and ectomycorrhizal community development of container- and bare-root grown Pinus sylvestris and Picea abies seedlings outplanted on a forest clear-cut. Balt For 19:39–49

    Google Scholar 

  • Kõljalg U, Dahlberg A, Taylor AFS, Larsson E, Hallenberg N, Stenlid J, Larsson KH, Fransson PM, Karen O, Jonsson L (2000) Diversity and abundance of resupinate thelephoroid fungi as ectomycorrhizal symbionts in Swedish boreal forests. Mol Ecol 9:1985–1996

    Article  PubMed  Google Scholar 

  • Kõljalg U, Nilsson RH, Abarenkov K, Tedersoo L, Taylor AFS, Bahram M, Bates ST, Bruns TD, Bengtsson-Palme J, Callaghan TM, Douglas B, Drenkhan T, Eberhardt U, Dueñas M, Grebenc T, Griffith GW, Hartmann M, Kirk PM, Kohout P, Larsson E, Lindahl BD, Lücking R, Martín MP, Matheny PB, Nguyen NH, Niskanen T, Oja J, Peay KG, Peintner U, Peterson M, Põldmaa K, Saag L, Saar I, Schüßler A, Scott JA, Senés C, Smith ME, Suija A, Taylor DL, Telleria MT, Weiss M, Larsson K-H (2013) Towards a unified paradigm for sequence-based identification of fungi. Mol Ecol 22:5271–5277. doi:10.1111/mec.12481

    Article  PubMed  Google Scholar 

  • Kranabetter J (2004) Ectomycorrhizal community effects on hybrid spruce seedling growth and nutrition in clearcuts. Can J Botany 82:983–991. doi:10.1139/x05-095

    Article  Google Scholar 

  • Коротков ГП (1974) Распространение микориз в сосновых насаждениях, зараженных корневой губкой [Distribution of mycorrhiza in the pine stands damaged by Heterobasidion root-rot]. Лесоведение 5:63–67

  • Magurran AE (1988) Ecological diversity and its measurement. Princeton University Press, Princeton

    Book  Google Scholar 

  • Menkis A, Vasiliauskas R, Taylor AFS, Stenlid J, Finlay R (2007) Afforestation of abandoned farmland with conifer seedlings inoculated with three ectomycorrhizal fungi—impact on plant performance and ectomycorrhizal community. Mycorrhiza 17:337–348. doi:10.1007/s00572-007-0110-0

    Article  CAS  PubMed  Google Scholar 

  • Menkis A, Bakys R, Lygis V, Vasaitis R (2011) Mycorrhization, establishment and growth of outplanted Picea abies seedlings produced under different cultivation systems. Silva Fenn 45:283–289. doi:10.14214/sf.118

    Article  Google Scholar 

  • Napierala-Filipiak A, Werner A (2000) Antagonism of higher fungi to Heterobasidion annosum (Fr.) Bref. in laboratory conditions. Dendrobiology 45:65–81

    Google Scholar 

  • Oliva J, Julio Camarero J, Stenlid J (2012) Understanding the role of sapwood loss and reaction zone formation on radial growth of Norway spruce (Picea abies) trees decayed by Heterobasidion annosum s.l. Forest Ecol Manag 274:201–209. doi:10.1016/j.foreco.2012.02.026

    Article  Google Scholar 

  • Piri T (2003) Early development of root rot in young Norway spruce planted on sites infected by Heterobasidion in southern Finland. Can J For Res 33:604–611. doi:10.1139/x02-200

    Article  Google Scholar 

  • Piri T, Korhonen K (2001) Infection of advance regeneration of Norway spruce by Heterobasidion parviporum. Can J For Res 31:937–942. doi:10.1139/x01-021

    Article  Google Scholar 

  • Rishbeth J (1951) Observations on the biology of Fomes annosus, with particular reference to East Anglian pine plantations. III. Natural and experimental infection of pines, and some factorsaffecting severity of the disease. Ann Bot 15:221–246

    Google Scholar 

  • Saravesi K, Aikio S, Wali PR, Ruotsalainen AL, Kaukonen M, Huusko K, Suokas M, Brown SP, Jumpponen A, Tuomi J, Markkola A (2015) Moth outbreaks alter root-associated fungal communities in subarctic mountain birch forests. Microb Ecol 69:788–797. doi:10.1007/s00248-015-0577-8

    Article  CAS  PubMed  Google Scholar 

  • Shannon CE (1948) A mathematical theory of communication. Bell Syst Tech J 27:379–423

    Article  Google Scholar 

  • Sinclair WA, Sylvia DM, Larsen AO (1982) Disease suppression and growth promotion in Douglas-fir seedlings by the ectomycorrhizal fungus Laccaria laccata. Forest Sci 28:191–201

    Google Scholar 

  • Smith SE, Read DJ (1997) Mycorrhizal symbiosis. Academic, London

    Google Scholar 

  • Stenlid J (1987) Controlling and predicting the spread of Heterobasidion annosum from infected stumps and trees of Picea abies. Scand J For Res 2:187–198. doi:10.1080/02827588709382457

    Article  Google Scholar 

  • Stivriņa B, Kenigsvalde K, Korhonen K, Gaitnieks T (2010) Importance of large dimension decaying logging residues of spruce in the spread of Heterobasidion root rot. Mežzinātne 22:88–102 (In Latvian)

    Google Scholar 

  • Swedjemark G, Stenlid J (1993) Population dynamics of the root rot fungus Heterobasidion annosum following thinning of Picea abies. Oikos 66:247–254

    Article  Google Scholar 

  • ter Braak CJF, Smilauer P (1998) Canoco reference manual and user’s guide to Canoco for Windows: software for canonical community ordination, Version 4. Microcomputer Power, Ithaca

    Google Scholar 

  • Treu R, Karst J, Randall M, Pec GJ, Cigan PW, Simard SW, Cooke JEK, Erbilgin N, Cahill JF (2014) Decline of ectomycorrhizal fungi following a mountain pine beetle epidemic. Ecology 95:1096–1103. doi:10.1890/13-1233.1

    Article  PubMed  Google Scholar 

  • Vaario LM, Tervonen A, Haukioja K, Haukioja M, Pennanen T, Timonen S (2009) The effect of nursery substrate and fertilization on the growth and ectomycorrhizal status of containerized and outplanted seedlings of Picea abies. Can J For Res 39:64–75. doi:10.1139/x08-156

    Article  Google Scholar 

  • Vainio J, Korhonen K, Hantula J (1998) Genetic variation in Phlebia gigantea as detected with random amplified microsatellite (RAMS) markers. Mycol Res 102:187–192

    Article  Google Scholar 

  • Vogt KA, Persson H (1991) Root methods. In: Lassoie JP, Hinckley TM (eds) Techniques and approaches in forest tree ecophysiology. CRC Press, Boca Raton, pp 477–502

    Google Scholar 

  • White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic Press, Inc, San Diego, pp 315–322

    Google Scholar 

  • Woodward S, Stenlid J, Karjalainen R, Hüttermann A (1998) Heterobasidion annosum: biology, ecology, impact and control. CAB International, Wallingford

    Google Scholar 

  • Zālītis P (2006) Preconditions for forest management. SIA, Riga (In Latvian)

    Google Scholar 

Download references

Acknowledgments

The study was supported by the JSC “Latvian State Forests”, ERDF funded project (no. L-KC-11-0004) “Methods and technologies for increasing forest capital value”, research direction “Investigation of the factors limiting the spread of root rot”, grant project no.426/2012 of Latvian Council of Science “Evaluation of factors affecting the efficacy of Phlebiopsis gigantea against Heterobasidion root rot” and the Swedish Energy Agency (Energimyndigheten).

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Correspondence to Audrius Menkis.

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Gaitnieks, T., Klavina, D., Muiznieks, I. et al. Impact of Heterobasidion root-rot on fine root morphology and associated fungi in Picea abies stands on peat soils. Mycorrhiza 26, 465–473 (2016). https://doi.org/10.1007/s00572-016-0685-4

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