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Mosaic stunting in bareroot Pinus banksiana seedlings is unrelated to colonization by mycorrhizal fungi

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Abstract

Mosaic stunting, the occurrence of random patches of chlorotic seedlings with reduced shoot and diameter growth amidst more robust cohorts within bareroot nurseries, is classically associated with poor colonization by mycorrhizal fungi. We examined possible relationships among soil fertility, mycorrhizas, and random patches of mosaic stunting in bareroot Pinus banksiana Lamb. and suggest this paradigm is not universal. Stunted seedlings were distributed among healthy seedlings, occupied field space for 2–3 years, and used nursery resources (i.e. irrigation, fertilization); consequently high rates of culling at harvest resulted in an economic stress for the nursery. Thus, an understanding of the cause(s) of stunting was necessary. Stunted 1 + 0 seedlings had significantly lower levels of nitrogen, phosphorus, potassium, and zinc than their healthy cohorts, despite similar soil nutrient levels. The numbers of mycorrhizal root tips on stunted and healthy seedlings were similar, and the taxa of mycorrhizal fungi, determined by isolations and DNA sequencing, were not consistently associated with stunted or healthy seedlings. We conclude that differences in Pinus banksiana mycorrhizas are not responsible for mosaic stunting, but may be caused by localized low soil N availability due to uneven distribution of added organic matter amendments.

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References

  • Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucl Acids Res 25(17):3389–3402

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Amaranthus MP, Perry DA (1987) Effect of soil transfer on ectomycorrhiza formation and the survival and growth of conifer seedlings on old, nonreforested clear-cuts. Can J For Res 17:944–950

    Article  Google Scholar 

  • Berger KC (1962) Micronutrient shortages, micronutrient deficiencies in the United States. J Agric Food Chem 10(3):178–181

    Article  CAS  Google Scholar 

  • Browning MHR, Whitney RD (1992) The influence of phosphorus concentration and frequency of fertilization on ectomycorrhizal development in containerized black spruce and jack pine seedlings. Can J For Res 22:1263–1270

    Article  CAS  Google Scholar 

  • Bubner B, Morgner C, Stark W, Münzenberger B (2014) Proof of ectomycorrhizal status of Sistotrema confluens Pers., the type species of the polyphyletic genus Sistotrema. Mycol Progress 1–5

  • Campagna JP, White DP (1969) Phosphorus deficiency of white spruce and red pine seedlings following nursery soil fumigation. Michigan Academician 2:105–112

    Google Scholar 

  • Colombo SJ (1986) Second-year shoot development in black spruce Picea mariana (Mill.) B.S.P. container seedlings. Can J For Res 16:68–73

    Article  Google Scholar 

  • Colpaert JV (1999) Thelephora. In: Cairney JWG, Chambers SM (eds) Ectomycorrhizal fungi key Genera in profile. Springer, Berlin, pp 325–345

    Chapter  Google Scholar 

  • Croghan CF, LaMadeleine LA (1982) The impact of stunting of white spruce at Eveleth nursery. Tree Planters’ Notes 33(4):19–22

    Google Scholar 

  • Croghan CF, Palmer MA, Wolosiewicz M (1987) Stunting of white spruce (Picea glauca (Moench) Voss) associated with ectomycorrhizal deficiency. Tree Planters’ Notes 38(1):22–23

    Google Scholar 

  • Dahlberg A, Finlay RD (1999) Suillus. In: Cairney JWG, Chambers SM (eds) Ectomycorrhizal fungi key Genera in profile. Springer, Berlin, pp 33–64

    Chapter  Google Scholar 

  • Domisch T, Finér L, Lehto T, Smolander A (2002) Effect of soil temperature on nutrient allocation and mycorrhizas in Scots pine seedlings. Plant Soil 239:173–185

    Article  CAS  Google Scholar 

  • Dumroese RK, James RL (2005) Root diseases in bareroot and container nurseries of the Pacific Northwest: epidemiology, management, and effects on outplanting performance. New For 30(2–3):185–202

    Article  Google Scholar 

  • Eriksson J, Hjortstam K, Ryvarden L (1984) The Corticiaceae of northern Europe, Schizophora-Suillosporium. In: Fungiflora, vol 7 Oslo, Norway

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

    Article  PubMed  CAS  Google Scholar 

  • Grand LF, Harvey AE (1982) Quantitative measurement of ectomycorrhizae on plant roots. In: Schenk NC (ed) Methods and principles of mycorrhizal research. The American Phytopathological Society, St. Paul, pp 157–174

    Google Scholar 

  • Henderson GS, Stone EL Jr (1970) Interactions of phosphorus availability, mycorrhizae and soil fumigation on coniferous seedlings. Soil Sci Soc Am Proc 34:314–318

    Article  CAS  Google Scholar 

  • Ho I, Zak B (1979) Acid phosphatase activity of six ectomycorrhizal fungi. Can J Bot 57:1203–1205

    Article  CAS  Google Scholar 

  • Horneck DA, Miller RO (1998) Determination of total nitrogen in plant tissue. In: Kalra YP (ed) Handbook and reference methods for plant analysis. CRC Press, New York, pp 75–84

    Google Scholar 

  • Hung LL, Chien C-Y, Ying S-l (1982) Effects of soil fumigation and mycorrhizal inoculation on ectomycorrhizal formation and growth of Taiwan red pine containerized seedlings. Quart J Chin For 15:13–19

    Google Scholar 

  • Hutchison LJ (1991) Description and identification of cultures of ectomycorrhizal fungi found in North America. Mycotaxon 42:387–504

    Google Scholar 

  • Islam MA, Apostol KG, Jacobs DF, Dumroese RK (2009) Fall fertilization of Pinus resinosa seedlings: nutrient uptake, cold hardiness, and morphological development. Ann For Sci 66(704):9

  • Koide RT, Shumway DL, Xu B, Sharda JN (2007) On temporal partitioning of a community of ectomycorrhizal fungi. New Phytol 174:420–429

    Article  PubMed  Google Scholar 

  • Koll P, Jurgensen MF, Dumroese RK (2010) Effects of pine sawdust, hardwood sawdust, and peat on bareroot soil properties. In: Riley LE, Pinto JR, Dumroese RK (Tech Coords) (eds) National proceedings, forest and conservation nursery associations 2009. Fort Collins, CO: USDA Forest Service, Rocky Mountain Research Station. Proceedings RMRS-P-62, pp 69–73

  • Kozlowski TT, Torrie JH, Marshall PE (1973) Predictability of shoot length from bud size in Pinus resinosa Ait. Can J For Res 3:34–38

    Article  Google Scholar 

  • Landeweert R, Leeflang P, Kuyper TW, Hoffland E, Rosling A, Wernars K, Smit E (2003) Molecular identification of ectomycorrhizal mycelium in soil horizons. Appl Environ Microbiol 69:327–333

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Landis TD (1985) Mineral nutrition as an index of seedling quality. In: Duryea ML (ed) Evaluating seedling quality: principles, procedures, and predictive abilities of major tests. Oregon State University, Corvallis, pp 29–48

    Google Scholar 

  • Landis TD (1998) Mosaic-pattern stunting. In: Forest Nursery Notes, Summer 1998. USDA Forest Service, Pacific Northwest Region, State and Private Forestry Cooperative Programs. R6-CP-TP-03-98. Portland, OR

  • Landis TD, van Steenis E (2003) Macronutrients-nitrogen: part 1. In: Forest Nursery Notes, Summer 2003. USDA Forest Service, Pacific Northwest Region, State and Private Forestry Cooperative Programs. R6-CP-TP-04-03. Portland, OR

  • Lilleskov EA, Fahey TJ, Horton TR, Lovett GM (2002) Belowground ectomycorrhizal fungal community change over a nitrogen deposition gradient in Alaska. Ecology 83:104–115

    Article  Google Scholar 

  • Linderman RG, Russell KW, Tanaka Y (2007) Investigations of the cause of first-year stunting of Douglas-fir seedlings in bareroot conifer nurseries. Tree Planters’ Notes 52(1):19–25

    Google Scholar 

  • Marx DH (1969) The influence of ectotrophic mycorrhizal fungi on the resistance of pine roots to pathogenic infection. I. Antagonism of mycorrhizal fungi to root pathogenic fungi and soil bacteria. Phytopathology 59:153–163

    Google Scholar 

  • Marx DH, Morris WG, Mexal JG (1978) Growth and ectomycorrhizal development of loblolly pine seedlings in fumigated and nonfumigated nursery soil infested with different fungal symbionts. For Sci 24:193–203

    Google Scholar 

  • Menkis A, Vasiliauskas R, Taylor AFS, Stenlid J, Finlay R (2005) Fungal communities in mycorrhizal roots of conifer seedlings in forest nurseries under different cultivation systems, assessed by morphotyping, direct sequencing and mycelial isolation. Mycorrhiza 16:33–41

    Article  PubMed  Google Scholar 

  • Michigan Climatological Resources Program (2009) Climatological summary tables. http://climate.geo.msu.edu/. Accessed 03 Aug 2009

  • Miller RO (1998) High-temperature oxidation: dry ashing. In: Kalra YP (ed) Handbook and reference methods for plant analysis. CRC Press, New York, pp 53–56

    Google Scholar 

  • Molina R, Trappe JG (1982) Isolation, maintenance, and pure culture manipulation of ectomycorrhizal fungi. In: Schenck NC (ed) Methods and principles of mycorrhizal research. American Phytopathological Society, St. Paul, pp 115–129

    Google Scholar 

  • Nilsson RH, Larsson K-H, Larsson E, Koljalg U (2006) Fruiting body-guided molecular identification of root-tip mantle mycelia provides strong indications of ectomycorrhizal associations in two species of Sistotrema (Basidiomycota). Mycol Res 110(12):1426–1432

    Article  PubMed  CAS  Google Scholar 

  • Natural Resources Conservation Service (NRCS) (2007) US Department of Agriculture Web Soil Survey. http://websoilsurvey.nrcs.usda.gov/app/. Accessed Oct 2007

  • Potvin LR, Richter DL, Jurgensen MF, Dumroese RK (2012) Association of Pinus banksiana Lamb. and Populus tremuloides Michx. seedling fine roots with Sistotrema brinkmannii (Bres.) J. Erikss. (Basidiomycotina). Mycorrhiza 22:631–638

    Article  PubMed  Google Scholar 

  • Richter DL, Bruhn JN (1989) Field survival of containerized red and jack pine seedlings inoculated with mycelial slurries of ectomycorrhizal fungi. New Forest 3:247–258

    Article  Google Scholar 

  • Richter DL, Bruhn JN (1993) Mycorrhizal fungus colonization of Pinus resinosa Ait. transplanted on northern hardwood clearcuts. Soil Biol Biochem 25:355–369

    Article  Google Scholar 

  • Ridge EH, Theodorou C (1972) The effect of soil fumigation on microbial recolonization and mycorrhizal infection. Soil Biol Biochem 4:295–305

    Article  CAS  Google Scholar 

  • Smith SE, Read DJ (1997) Mycorrhizal symbiosis. Academic Press, Harcourt Brace and Company, Great Britain

    Google Scholar 

  • Stewart H, Swan D (1970) Relationships between nutrient supply, growth, and nutrient concentrations in the foliage of black spruce and jack pine. Pulp Paper Res Inst Canada. Woodlands Paper 19

  • Taylor JH, Peterson CA (2005) Ectomycorrhizal impacts on nutrient uptake pathways in woody roots. New For 30:203–214

    Article  Google Scholar 

  • Theodorou C (1978) Soil moisture and the mycorrhizal association of Pinus radiata. Soil Biol Biochem 10:33–38

    Article  CAS  Google Scholar 

  • Timmer VR, Armstrong G, Miller BD (1991) Steady-state nutrient preconditioning and early outplanting performance of containerized black spruce seedlings. Can J For Res 21:585–594

    Article  CAS  Google Scholar 

  • Trappe JM, Strand RF (1969) Mycorrhizal deficiency in a Douglas-fir region nursery. For Sci 15:381–389

    Google Scholar 

  • Trappe JM, Molina R, Castellano M (1984) Reactions of mycorrhizal fungi and mycorrhiza formations to pesticides. Annu Rev Phytopathol 22:331–359

    Article  CAS  Google Scholar 

  • Tyminska A, LeTacon F, Chadoeuf J (1986) Effect of three ectomycorrhizal fungi on growth and phosphorus uptake of Pinus sylvestris seedlings at increasing phosphorus levels. Can J Bot 64:2753–2757

    Article  CAS  Google Scholar 

  • White TJ, Bruns TD, Lee SB, Taylor JW (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, New York, pp 315–322

    Google Scholar 

  • Zak B, Bryan WC (1963) Isolation of fungal symbionts from pine mycorrhizae. For Sci 9:270–278

    Google Scholar 

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Acknowledgments

We thank A. Holland, C. Makuck, P. Koll, and the J.W. Toumey Nursery staff for assistance with field work and E. Lilleskov, L. vanDiepen, and C. Andrew for assistance with molecular methodology. This work was supported by Michigan Technological University and the USDA Forest Service: J.W. Toumey Nursery; National Center for Reforestation, Nursery, and Genetic Resources and the Rocky Mountain Research Station.

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Authors and Affiliations

  1. USDA Forest Service, Northern Research Station, 410 MacInnes Drive, Houghton, MI, 49931, USA

    Lynette R. Potvin

  2. School of Forest Resources and Environmental Science, Michigan Technological University, 1400 Townsend Drive, Houghton, MI, 49931, USA

    Martin F. Jurgensen & Dana L. Richter

  3. USDA Forest Service, Rocky Mountain Research Station, 1221 South Main St., Moscow, ID, 83843, USA

    R. Kasten Dumroese & Deborah S. Page-Dumroese

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  1. Lynette R. Potvin
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  2. Martin F. Jurgensen
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  3. R. Kasten Dumroese
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  4. Dana L. Richter
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  5. Deborah S. Page-Dumroese
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Correspondence to Lynette R. Potvin.

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Potvin, L.R., Jurgensen, M.F., Dumroese, R.K. et al. Mosaic stunting in bareroot Pinus banksiana seedlings is unrelated to colonization by mycorrhizal fungi. New Forests 45, 893–903 (2014). https://doi.org/10.1007/s11056-014-9438-4

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