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Decomposition and Fungi of Needle Litter from Slow- and Fast-growing Norway Spruce (Picea abies) Clones

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Abstract

The fungal species involved in the decomposition of needle litter and their response to intraspecific genetic variation of trees are poorly known. First, we compared the needle decomposition and fungal decomposers underneath eight different Norway spruce clones in situ. This experiment revealed 60−70% loss of needle mass in two years. Although spruce clones differed considerably in growth (twofold height difference) and their needles differed in chemical composition, no significant difference was found for loss of needle mass under the spruce clones. Furthermore, the spruce clones did not affect the community structure of the fungal decomposers. Fungi inhabiting needle litter were identified by extracting ribosomal RNA (rRNA) and sequencing complementary DNA (cDNA) of internal trascribed spacer 1 (ITS1) region. The most frequent identifications were Lophodermium, Pezizales, Mycena, and Marasmius, suggesting that endophytic fungi were involved in the decomposition process. Second, we evaluated the potential of endophytes to decompose needle material in a microcosm experiment in which all other fungi than endophytes were excluded. Within 2 years, the endophytes had decomposed 35−45% of the needle mass. Sequences of Mollisia, Lophodermium, Lachnum, and Phialocephala were most frequently found in rRNA and rDNA extracted from the needles at the end of the microcosm experiment. The dominant needle endophyte in fresh, green needles was Lophodermium piceae, and this species was also found frequently in the needle material after 2 years of decay both in the field and laboratory experiments. Moreover, the relative abundance of Lophodermium-derived denaturing gradient gel electrophoresis (DGGE) bands correlated positively with the decomposition in the microcosm experiment. Hence, our results suggest a significant role of endophytic fungi, and particularly L. piceae, in the process of needle decomposition in boreal forests.

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References

  1. 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 Acid Res 25:3389–3402

    Article  PubMed  CAS  Google Scholar 

  2. Anderson IC, Parkin PI (2007) Detection of active soil fungi by RT-PCR amplification of precursor rRNA molecules. J Microbiol Methods 68:248–253

    Article  PubMed  CAS  Google Scholar 

  3. Aneja MK, Sharma S, Munch JC, Schloter M (2004) RNA fingerprinting—a new method to screen for differences in plant litter degrading microbial communities. J Microbiol Methods 59:223–231

    Article  PubMed  CAS  Google Scholar 

  4. Aneja MK, Sharma S, Fleischmann F, Stich S, Heller W, Bahnweg G, Munch JC, Schloter M (2006) Microbial colonization of beech and spruce litter—influence of decomposition site and plant litter species on the diversity of microbial community. Microb Ecol 52:127–135

    Article  PubMed  Google Scholar 

  5. Barklund P (1987) Occurrence and pathogenicity of Lophodermium piceae appearing as an endophyte in needles of Picea abies. Trans Br Mycol Soc 89:307–313

    Google Scholar 

  6. Berg B, Hannus K, Popoff T, Theander O (1982) Changes in organic chemical components of needle litter during decomposition. Long-term decomposition in a Scots pine forest. I. Can J Bot 60:1310–1319

    CAS  Google Scholar 

  7. Bergemann SE, Garbelotto M (2006) High diversity of fungi recovered from the roots of mature tanoak (Lithocarpus densiflorus) in northern California. Can J Bot 84:1380–1394

    Article  CAS  Google Scholar 

  8. Bocock KL, Gilbert OJW (1957) The disappearance of leaf litter under different woodland conditions. Plant Soil 9:179–185

    Article  Google Scholar 

  9. Cajander AK (1949) Forest types and their significance. Acta For Fenn 56:1–71

    Google Scholar 

  10. Carroll F, Muller E, Sutton B (1977) Preliminary studies on the incidence of needle endophytes in some European conifers. Sydowia 29:87–103

    Google Scholar 

  11. Carroll GC, Carroll FE (1978) Studies on the incidence of coniferous needle endophytes in the Pacific Northwest. Can J Bot 56:3034–3043

    Article  Google Scholar 

  12. Dix NJ, Webster J (1995) Fungal ecology. Chapman & Hall, London, UK

    Google Scholar 

  13. Fioretto A, Papa S, Pellegrino A, Fuggi A (2007) Decomposition dynamics of Myrtus communis and Quercus ilex leaf litter: mass loss, microbial activity and quality change. App Soil Ecol 36:32–40

    Article  Google Scholar 

  14. Ganley RJ, Newcombe G (2006) Fungal endophytes in seeds and needles of Pinus monticola. Mycol Res 110:318–327

    Article  PubMed  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  16. Ghimire SR, Hyde KD (2004) Fungal endophytes. In: Varma A, Abbott L, Werner D, Hampp R (eds) Plant surface microbiology. Springer, Berlin, pp 281–292

    Google Scholar 

  17. Girvan M, Bullimore J, Ball A, Pretty J, Osborn AM (2004) Responses of active bacterial and fungal communities in soils under winter wheat to different fertilizer and pesticide regimens. Appl Environ Microbiol 70:2692–2701

    Article  PubMed  CAS  Google Scholar 

  18. Hata K, Futai K (1996) Variation in fungal endophyte populations in needles of the genus Pinus. Can J Bot 74:103–114

    Article  Google Scholar 

  19. Herdina NS, Jabaji-Hare S, Ophel-Keller K (2004) Persistence of DNA of Gaeumannomyces graminis var. tritici in soil as measured by a DNA-based assay. FEMS Microbiol Ecol 47:143–152

    Article  CAS  PubMed  Google Scholar 

  20. Killham K (1994) Soil ecology. Cambridge University Press, Cambridge

    Google Scholar 

  21. Korkama T, Fritze H, Kiikkilä O, Pennanen T (2007) Do same-aged but different height Norway spruce (Picea abies) clones affect soil microbial community? Soil Biol Biochem 39:2420–2423

    Article  CAS  Google Scholar 

  22. 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 Phytol 173:798–807

    Article  PubMed  CAS  Google Scholar 

  23. Korkama T, Pakkanen A, Pennanen T (2006) Ectomycorrhizal community structure varies among Norway spruce (Picea abies) clones. New Phytol 171:815–824

    Article  PubMed  CAS  Google Scholar 

  24. Lindahl BD, Ihrmark K, Boberg J, Trumbore SE, Högberg P, Stenlid J, Finlay RD (2007) Spatial separation of litter decomposition and mycorrhizal nitrogen uptake in a boreal forest. New Phytol 173:611–620

    Article  PubMed  CAS  Google Scholar 

  25. Livsey S (1995) Ecology of endophytic microfungi in Norway spruce crows. Thesis, Swedish University of Agricultural Sciences, Uppsala.

  26. Livsey S, Barklund P (1992) Lophodermium piceae and Rhizosphaera kalkhoffii in fallen needles of Norway spruce (Picea abies). Eur J For Pathol 22:204–216

    Article  Google Scholar 

  27. Manefield M, Whiteley AS, Griffiths RI, Bailey MJ (2002) RNA stable isotope probing, a novel means of linking microbial community function to Phylogeny. Appl Environ Microbiol 68:5367–5373

    PubMed  CAS  Google Scholar 

  28. McCune B, Mefford MJ (1999) PC-ORD. Multivariate Analysis of Ecological Data, version 5. MjM Software Design, Gleneden Beach

    Google Scholar 

  29. Melillo JM, Aber JD, Muratore JF (1982) Nitrogen and lignin control of hardwood leaf litter decomposition dynamics. Ecology 63:621–626

    Article  CAS  Google Scholar 

  30. Menkis A, Vasiliauskas R, Taylor AFS, Stenström E, Stenlid J, Finlay R (2006) Fungi in decayed roots of conifer seedlings in forest nurseries, afforested clear-cuts and abandoned farmland. Plant Pathol 55:117–129

    Article  CAS  Google Scholar 

  31. Minter DW (1981) Lophodermium on pines. Mycol Papers 147:1–54

    Google Scholar 

  32. Mitchell CP, Millar CS, Minter DW (1978) Studies on decomposition of Scots pine needles. Trans Br Mycol Soc 71:343–348

    Article  Google Scholar 

  33. Müller M, Valjakka R, Suokko A, Hantula J (2001) Diversity of endophytic fungi of single Norway spruce needles and their role as pioneer decomposers. Mol Ecol 10:1801–1810

    Article  PubMed  Google Scholar 

  34. Müller MM, Valjakka R, Hantula J (2007) Genetic diversity of Lophodermium piceae in South Finland. For Pathol 37:329–337

    Google Scholar 

  35. Müller MM, Hallaksela AM (1998) Diversity of Norway spruce needle endophytes in various mixed and pure Norway spruce stands. Mycol Res 102:1183–1189

    Article  Google Scholar 

  36. Müller MM, Kantola R, Kitunen V (1994) Combining sterol and fatty-acid profiles for the characterization of fungi. Mycol Res 98:593–603

    Google Scholar 

  37. Murphy KL, Klopatek JM, Klopatek CC (1998) The effects of litter quality and climate on decomposition along an elevation gradient. Ecol Appl 8:1061–1071

    Article  Google Scholar 

  38. Pennanen T, Caul S, Daniell TJ, Griffiths BS, Ritz K, Wheatley RE (2004) Community-level responses of metabolically-active soil microorganisms to the quantity and quality of substrate inputs. Soil Biol Biochem 36:841–848

    Article  CAS  Google Scholar 

  39. Pennanen T, Liski J, Bååth E, Kitunen V, Uotila J, Westman CJ, Fritze H (1999) Structure of microbial communities in coniferous forest soils in relation to site fertility and stand development stage. Microb Ecol 38:168–179

    Article  PubMed  Google Scholar 

  40. Rosset R, Julien J, Monier R (1966) Ribonucleic acid composition of bacteria as a function of growth rate. J Mol Biol 18:308–320

    PubMed  CAS  Google Scholar 

  41. Saetre P, Bååth E (2000) Spatial variation and patterns of soil microbial community structure in a mixed spruce-birch stand. Soil Biol Biochem 32:909–917

    Article  CAS  Google Scholar 

  42. Saikkonen K, Helander ML, Rousi M (2003) Endophytic foliar fungi in Betula spp. and their F1 hybrids. For Pathol 33:215–222

    Google Scholar 

  43. Sieber T (1988) Endophytic fungi in needles of healthy-looking and diseased Norway spruce (Picea abies (L.) Karsten). Eur J For Pathol 18:321–342

    Article  Google Scholar 

  44. Sieber TN (1989) Endophytic fungi in twigs of healthy and diseased Norway spruce and White fir. Mycol Res 92:322–326

    Article  Google Scholar 

  45. Smolander A, Kitunen V, Paavolainen L, Mälkönen E (1996) Decomposition of Norway spruce and Scots pine needles: effects of liming. Plant Soil 179:1–7

    Article  CAS  Google Scholar 

  46. Stephan BR, Osorio M (1995) Lophodermium piceae and zone lines on spruce needles and in culture. In: Capretti P, Heiniger U, Stephen R (eds) Shoot and Foliage Diseases in Forest Trees. Instituto di Patologia e Zoologia Forestale e Agraria, Universita degli Studi di Firenze, pp 6–10

    Google Scholar 

  47. Taylor BR, Parkinson D, Parsons WFJ (1989) Nitrogen and lignin content as predictors of litter decay-rates - a microcosm test. Ecology 70:97–104

    Article  Google Scholar 

  48. Todd D (1988) The effects of host genotype, growth rate, and needle age on the distribution of a mutualistic, endophytic fungus in Douglas-fir plantations. Can J For Res 18:601–605

    Article  Google Scholar 

  49. Vainio E, 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 

  50. Wagner R (1994) The regulation of ribosomal RNA synthesis and bacterial cell growth. Arch Microbiol 161:100–109

    Article  PubMed  CAS  Google Scholar 

  51. White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfaud DE, Sninsky JJ, White TJ (eds) PCR Protocols: a guide to methods and applications. Academic, SanDiego, pp 315–322

    Google Scholar 

  52. Wilkinson SC, Anderson JM, Scardelis SP, Tisiafouli M, Taylor A, Wolters V (2002) PLFA profiles of microbial communities in decomposing conifer litters subject to moisture stress. Soil Biol Biochem 34:189–200

    Article  CAS  Google Scholar 

  53. Wilson D (1995) Endophyte—the evolution of a term, and clarification of its use and definition. Oikos 73:274–276

    Article  Google Scholar 

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Acknowledgments

We thank M. Sinkkonen, K. Pihlajamaa, and B. Sultan for technical assistance, A. Siika for help with the illustration, M. Hardman for revising the text and three anonymous reviewers for useful comments. The study was funded by the Academy of Finland (project no. 201178) and The Finnish Society of Forest Research.

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  1. Vantaa Research Unit, Finnish Forest Research Institute (Metla), P.O. Box, 18, 01301, Vantaa, Finland

    Tiina Korkama-Rajala, Michael M. Müller & Taina Pennanen

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  1. Tiina Korkama-Rajala
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  3. Taina Pennanen
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Correspondence to Tiina Korkama-Rajala.

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Korkama-Rajala, T., Müller, M.M. & Pennanen, T. Decomposition and Fungi of Needle Litter from Slow- and Fast-growing Norway Spruce (Picea abies) Clones. Microb Ecol 56, 76–89 (2008). https://doi.org/10.1007/s00248-007-9326-y

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