Mycorrhizal Response to Experimental pH and P Manipulation in Acidic Hardwood Forests

PLoS ONE

Volumn 7, Issue 11, 2012, Pages

  Kluber, Laurel A ^a,b   Carrino Kyker, Sarah R ^a,b   Coyle, Kaitlin P ^a   DeForest, Jared L ^c   Hewins, Charlotte R ^b   Shaw, Alanna N ^c   Smemo, Kurt A ^b,d   Burke, David J ^a,b  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Holden Arboretum   (United States)

^c OHIO UNIVERSITY   (United States)

^d KENT STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PHOSPHORUS; RESIN;

ACER; ARBUSCULAR MYCORRHIZA; ARTICLE; BEECH; BIOMANIPULATION; CARBON SOURCE; COMMUNITY STRUCTURE; CONTROLLED STUDY; ECOSYSTEM; ECTOMYCORRHIZA; ENZYME ANALYSIS; FOREST; FUNGAL COLONIZATION; HARDWOOD FOREST; MICROBIAL ACTIVITY; MICROBIAL COMMUNITY; MYCORRHIZA; NONHUMAN; NUCLEOTIDE SEQUENCE; OAK; PH; PHYTOCHEMISTRY; PLANT COMMUNITY; PLANT ENVIRONMENT INTERACTION; PLANT FUNGUS INTERACTION; PLANT ROOT; POPULATION ABUNDANCE; SOIL ANALYSIS; SOIL CHEMISTRY; SPECIES DIFFERENCE; SPECIES RICHNESS; TEMPERATE DECIDUOUS FOREST; UNINDEXED SEQUENCE;

BIOMASS; ECOSYSTEM; HYDROGEN-ION CONCENTRATION; MYCORRHIZAE; OHIO; PHOSPHORUS; PLANT ROOTS; SOIL; SOIL MICROBIOLOGY; TREES;

ARBUSCULAR; ASCOMYCOTA;

EID: 84869028731     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0048946     Document Type: Article

References (68)

1. Vitousek PM, Horwarth RW, (1991) Nitrogen limitation on land and in the sea: how can it occur? Biogeochemistry 13: 87-115.
2. SanClements MD, Fernandez IJ, Norton SA, (2010) Phosphorus in Soils of Temperate Forests: Linkages to Acidity and Aluminum. Soil Science Society of America Journal 74: 2175.
3. Groffman PM, Fisk MC, (2011) Phosphate additions have no effect on microbial biomass and activity in a northern hardwood forest. Soil Biology and Biochemistry 43: 2441-2449.
4. Finzi AC, (2009) Decades of atmospheric deposition have not resulted in widespread phosphorus limitation or saturation of tree demand for nitrogen in southern New England. Biogeochemistry 92: 217-229.
5. Cairney JWG, (2011) Ectomycorrhizal fungi: the symbiotic route to the root for phosphorus in forest soils. Plant and Soil 344: 51-71.
6. DeForest JL, McCarthy BC, (2011) Diminished soil quality in an old-growth mixed mesophytic forest following chronic acid deposition. Northeastern Naturalist 18: 177-184.
7. Wood T, Bormann FH, Voight GK, (1984) Phosphorus Cycling in a Northern Hardwood Forest: Biological and Chemical Control. Science 223: 391-393.
8. Casson NJ, Eimers MC, Watmough SA (2011) An assessment of the nutrient status of sugar maple in Ontario: indications of phosphorus limitation. Environmental Monitoring and Assessment DOI: 10.1007/s10661-011-2390-2.
9. DeForest JL, Smemo KA, Burke DJ, Elliott HL, Becker JC, (2012) Soil microbial responses to elevated phosphorus and pH in acidic temperate deciduous forests. Biogeochemistry 109: 189-202.
10. Vance CP, Uhde-Stone C, Allan DL, (2003) Phosphorus acquisition and use: critical adaptations by plants for securing a nonrenewable resource. New Phytologist 157: 423-447.
11. Smith S, Read D (2008) Mycorrhizal Symbiosis. New York: Academic Press. 787 p.
12. 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.
13. Van Tichelen KK, Colpaert JV, (2000) Kinetics of phosphate absorption by mycorrhizal and non-mycorrhizal Scots pine seedlings. Physiologia Plantarum 110: 96-103.
14. Griffiths RP, Baham JE, Caldwell BA, (1994) Soil solution chemistry of ectomycorrhizal mats in forest soil. Soil Biology and Biochemistry 26: 331-337.
15. Tuason MMS, Arocena JM, (2009) Calcium oxalate biomineralization by Piloderma fallax in response to various levels of calcium and phosphorus. Applied and Environmental Microbiology 75: 7079-7085.
16. Jongmans AG, van Breemen N, Lundstrom U, van Hees PAW, Finlay RD, et al. (1997) Rock-eating fungi. Nature 389: 682-683.
17. Antunes PM, Schneider K, Hillis D, Klironomos JN, (2007) Can the arbuscular mycorrhizal fungus Glomus intraradices actively mobilize P from rock phosphates? Pedobiologia 51: 281-286.
18. Heijne B, Dam D, Heil G, Bobbink R, (1996) Acidification effects on vesicular-arbuscular mycorrhizal (VAM) infection, growth and nutrient uptake of established heathland herb species. Plant and Soil 179: 197-206.
19. Aguilera P, Borie F, Seguel A, Cornejo P, (2011) Fluorescence detection of aluminum in arbuscular mycorrhizal fungal structures and glomalin using confocal laser scanning microscopy. Soil Biology and Biochemistry 43: 2427-2431.
20. Dighton J, Skeffington R, (1987) Effects of artificial acid precipitation on the mycorrhizas of Scots pine seedlings. New Phytologist 107: 191-202.
21. Kjøller R, Clemmensen KE, (2009) Belowground ectomycorrhizal fungal communities respond to liming in three southern Swedish coniferous forest stands. Forest Ecology and Management 257: 2217-2225.
22. Roth DR, Fahey TJ, (1998) The effects of acid precipitation and ozone on the ectomycorrhizae of red spruce seedlings. Water, Air, & Soil Pollution 103: 263-276.
23. Rudawska M, Kieliszewska-Rokicka B, Leski T, Oleksyn J, (1995) Mycorrhizal status of a Scots pine (Pinus sylvestris L.) plantation affected by pollution from a phosphate fertilizer plant. Water, Air, & Soil Pollution 85: 1281-1286.
24. Erland S, Soderstrom B (1990) Effects of liming on ectomycorrhizal fungi infecting Pinus sylvestris L. I. mycorrhizal infection in limed humus in the laboratory and isolation of fungi from mycorrhizal roots. New Phytologist 115.
25. Wallander H, Arnebrant K, Östrand F, Kårén O, (1997) Uptake of 15N-labelled alanine, ammonium and nitrate in Pinus sylvestris L. ectomycorrhiza growing in forest soil treated with nitrogen, sulphur or lime. Plant and Soil 195: 329-338.
26. Qian XM, Kottke I, Oberwinkler F, (1998) Influence of liming and acidification on the activity of the mycorrhizal communities in a Picea abies (L.) Karst. stand. Plant and Soil 199: 99-109.
27. 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.
28. Treseder KK, (2004) A meta-analysis of mycorrhizal responses to nitrogen, phosphorus, and atmospheric CO2 in field studies. New Phytologist 164: 347-355.
29. Van Aarle IM, Olsson PA, Söderström B, (2002) Arbuscular mycorrhizal fungi respond to the substrate pH of their extraradical mycelium by altered growth and root colonization. New Phytologist 155: 173-182.
30. Coughlan A, Dalpe Y, Lapointe L, Piche Y, (2000) Soil pH-induced changes in root colonization, diversity, and reproduction of symbiotic arbuscular mycorrhizal fungi from healthy and declining maple forests. Canadian Journal of Forest Research 30: 1543-1554.
31. Dumbrell AJ, Nelson M, Helgason T, Dytham C, Fitter AH, (2010) Relative roles of niche and neutral processes in structuring a soil microbial community. The ISME Journal 4: 337-345.
32. Dickie IA, Richardson SJ, Wiser SK, (2009) Ectomycorrhizal fungal communities and soil chemistry in harvested and unharvested temperate Nothofagus rainforests. Canadian Journal of Forest Research 39: 1069-1079.
33. Morris MH, Smith ME, Rizzo DM, Rejmánek M, Bledsoe CS, (2008) Contrasting ectomycorrhizal fungal communities on the roots of co-occurring oaks (Quercus spp.) in a California woodland. New Phytologist 178: 167-176.
34. Baxter JW, Dighton J, (2001) Ectomycorrhizal diversity alters growth and nutrient acquisition of grey birch (Betula populifolia) seedlings in host-symbiont culture conditions. New Phytologist 152: 139-149.
35. DeForest JL, Scott LG, (2010) Available soil phosphorus has an important influence on microbial community composition. Soil Science Society of America Journal 74: 2059-2066.
36. DeForest JL, (2009) The influence of time, storage temperature, and substrate age on potential soil enzyme activity in acidic forest soils using MUB-linked substrates and l-DOPA. Soil Biology and Biochemistry 41: 1180-1186.
37. Agerer R (2002) Color atlas of ectomycorrhizae. Schwäbisch Gmünd, Germany: Einhorn Verlag.
38. Burke DJ, (2008) Effects of Alliaria petiolata (garlic mustard; Brassicaceae) on mycorrhizal colonization and community structure in three herbaceous plants in a mixed deciduous forest. American Journal of Botany 95: 1416-1425.
39. Helgason T, Daniell TJ, Husband R, Fitter AH, Young JPW, (1998) Ploughing up the wood-wide web? Nature 394: 431.
40. Simon L, LaLonde M, Bruns TD, (1992) Specific amplification of 18S fungal ribosomal genes from vesicular-arbuscular endomycorrhizal fungi colonizing roots. Applied and Environmental Microbiology 58: 291-295.
41. Avis PG, Feldheim KA, (2005) A method to size DNA fragments from 50 to 800 bp on a DNA analyser. Molecular Ecology Notes 5: 969-970.
42. Taylor DL, Booth MG, McFarland JW, Herriott IC, Lennon NJ, et al. (2008) Increasing ecological inference from high throughput sequencing of fungi in the environment through a tagging approach. Molecular Ecology Resources 8: 742-752.
43. Aponte C, García LV, Marañón T, Gardes M, (2010) Indirect host effect on ectomycorrhizal fungi: Leaf fall and litter quality explain changes in fungal communities on the roots of co-occurring Mediterranean oaks. Soil Biology and Biochemistry 42: 788-796.
44. Drummond A, Ashton B, Cheung M, Heled J, Kearse M, et al. (2009) Geneious v5.4. Available from http://www.geneious.com/.
45. Isayenkov S, Fester T, Hause B, (2004) Rapid determination of fungal colonization and arbuscule formation in roots of Medicago truncatula using real-time (RT) PCR. Journal of Plant Physiology 161: 1379-1383.
46. Alkan N, Gadkar V, Yarden O, Kapulnik Y, (2006) Analysis of quantitative interactions between two species of arbuscular mycorrhizal fungi, Glomus mosseae and G. intraradices, by real-time PCR. Applied and Environmental Microbiology 72: 4192-4199.
47. Bustin SA, Benes V, Garson JA, Hellemans J, Huggett J, et al. (2009) The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clinical Chemistry 55: 611-622.
48. Gardes M, Bruns TD, (1993) ITS primers with enhanced specificity for basidiomycetes- application to the identification of mycorrhizae and rusts. Molecular Ecology Notes 2: 113-118.
49. 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, T.J White, editors. PCR Protocols - a Guide to Methods and Applications. San Diego, CA Academic Press. 315-322.
50. Manter DK, Vivanco JM, (2007) Use of the ITS primers, ITS1F and ITS4, to characterize fungal abundance and diversity in mixed-template samples by qPCR and length heterogeneity analysis. Journal of Microbiological Methods 71: 7-14.
51. Burke DJ, Lopez-Gutierrez JC, Smemo KA, Chan CR, (2009) Vegetation and soil environment influence the spatial distribution of root-associated fungi in a mature beech-maple forest. Applied and Environmental Microbiology 75: 7639-7648.
52. R Development Core Team (2010) R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.
53. McCune B, Grace JB (2002) Analysis of Ecological Communities. Glendale Beach, Oregon: MjM Software Design.
54. Kluber LA, Smith JE, Myrold DD, (2011) Distinctive fungal and bacterial communities are associated with mats formed by ectomycorrhizal fungi. Soil Biology and Biochemistry 43: 1042-1050.
55. Kourtev PS, Ehrenfeld JG, Haggblom M, (2002) Exotic plant species alter the microbial community structure and function in the soil. Ecology 83: 3152-3166.
56. Colwell RK (2006) EstimateS: Statistical estimation of species richness and shared species from samples. Version 8: Persistent URL .
57. Sinsabaugh RL, M J Klung, H P Collins, P E Yeager, S O Peterson (1999) Characterizing soil microbial communities. In: Robertson GC, DC; Bledsoe, CS; Sollins, P, editor. Standard soil methods for long-term ecological research. New York: Oxford University Press. 318-348.
58. Boerner REJ, Brinkman JA, Smith A, (2005) Seasonal variations in enzyme activity and organic carbon in soil of a burned and unburned hardwood forest. Soil Biology and Biochemistry 37: 1419-1426.
59. Wang GM, Stribley DP, Tinker PB, Walker C, (1993) Effects of pH on arbuscular mycorrhiza I. Field observations on the long-term liming experiments at Rothamsted and Woburn. New Phytologist 124: 465-472.
60. Avis PG, Dickie IA, Mueller GM, (2006) A dirty business: testing the limitations of terminal restriction fragment length polymorphism (TRFLP) analysis of soil fungi. Molecular Ecology 15: 873-882.
61. Miller M, McGonigle T, Addy H, (1995) Functional ecology of vesicular-arbuscular mycorrhizas as influenced by phosphate fertilization and tillage in an agricultural ecosystem. Critical Reviews in Biotechnology 15: 241-255.
62. Ouimet R, Camire C, Furlan V, (1995) Endomycorrhizal status of sugar maple in relation to tree decline and foliar, fine-roots, and soil chemistry in the Beauce region, Quebec. Canadian Journal of Botany 73: 1168-1175.
63. Juice S, Fahey T, Siccama T, Driscoll C, Denny E, et al. (2006) Response of sugar maple to calcium addition to northern hardwood forest. Ecology 87: 1267-1280.
64. Avis PG, McLaughlin DJ, Dentinger BC, Reich PB, (2003) Long-term increase in nitrogen supply alters above- and below-ground ectomycorrhizal communities and increases the dominance of Russula spp. in a temperate oak savanna. New Phytologist 160: 239-253.
65. Kjøller R, Nilsson LO, Hansen K, Schmidt IK, Vesterdal L, et al. (2012) Dramatic changes in ectomycorrhizal community composition, root tip abundance and mycelial production along a stand-scale nitrogen deposition gradient. New phytologist 194: 278-286.
66. Rineau F, Maurice J-P, Nys C, Voiry H, Garbaye J, (2010) Forest liming durably impact the communities of ectomycorrhizas and fungal epigeous fruiting bodies. Annals of Forest Science 67: 110-110.
67. Hung L-L, Trappe JM, (1983) Growth variation between and within species of ectomycorrhizal fungi in response to pH in vitro. Mycologia 75: 234-241.
68. García-Montero LG, Quintana A, Valverde-Asenjo I, Díaz P, (2009) Calcareous amendments in truffle culture: A soil nutrition hypothesis. Soil Biology and Biochemistry 41: 1227-1232.