Ectomycorrhizal fungal communities associated with Masson pine (Pinus massoniana Lamb.) in Pb-Zn mine sites of central south China

Mycorrhiza

Volumn 22, Issue 8, 2012, Pages 589-602

  Huang, Jian ^a   Nara, Kazuhide ^a   Lian, Chunlan ^a   Zong, Kun ^a   Peng, Kejian ^b   Xue, Shengguo ^c   Shen, Zhenguo ^d  

^a UNIVERSITY OF TOKYO   (Japan)

^b Hunan Research Academy of Environmental Sciences   (China)

^c CENTRAL SOUTH UNIVERSITY   (China)

^d NANJING AGRICULTURAL UNIVERSITY   (China)

Author keywords

Ectomycorrhizal fungal community; Heavy metal contamination; Mine tailing; Mineland; Pinus massoniana Lamb

Indexed keywords

CADMIUM; COPPER; FUNGAL DNA; HEAVY METAL; LEAD; RIBOSOMAL SPACER DNA; ZINC;

CONIFEROUS TREE; ECTOMYCORRHIZA; FUNGUS; LEAD; SPECIES DIVERSITY; SPECIES RICHNESS; TAILINGS; ZINC;

ARTICLE; BASIDIOMYCETES; CHEMISTRY; CHINA; CLASSIFICATION; DNA SEQUENCE; ENVIRONMENTAL MONITORING; GENETICS; GROWTH, DEVELOPMENT AND AGING; ISOLATION AND PURIFICATION; MICROBIOLOGY; MINING; MOLECULAR GENETICS; MYCORRHIZA; NUCLEOTIDE SEQUENCE; PINE; PLANT LEAF; PLANT ROOT; POLYMERASE CHAIN REACTION; RESTRICTION FRAGMENT LENGTH POLYMORPHISM; RHIZOSPHERE; SOIL; SOIL POLLUTANT; SYMBIOSIS;

BASE SEQUENCE; BASIDIOMYCOTA; CADMIUM; CHINA; COPPER; DNA, FUNGAL; DNA, RIBOSOMAL SPACER; ENVIRONMENTAL MONITORING; LEAD; METALS, HEAVY; MINING; MOLECULAR SEQUENCE DATA; MYCORRHIZAE; PINUS; PLANT LEAVES; PLANT ROOTS; POLYMERASE CHAIN REACTION; POLYMORPHISM, RESTRICTION FRAGMENT LENGTH; RHIZOSPHERE; SEQUENCE ANALYSIS, DNA; SOIL; SOIL POLLUTANTS; SYMBIOSIS; ZINC;

CHINA;

FUNGI; INOCYBE CURVIPES; PINUS MASSONIANA; RHIZOPOGON BUENOI; SUILLUS GRANULATUS; TOMENTELLA ELLISII;

EID: 84868003306     PISSN: 09406360     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00572-012-0436-0     Document Type: Article

References (58)

1. Adriaensen K, van der Lelie D, van Laere A, Vangronsveld J, Colpaert JV (2004) A zinc-adapted fungus protects pines from zinc stress. New Phytol 161(2): 549-555. doi: 10. 1046/j. 1469-8137. 2003. 00941. x.
2. Adriaensen K, Vangronsveld J, Colpaert JV (2006) Zinc-tolerant Suillus bovinus improves growth of Zn-exposed Pinus sylvestris seedlings. Mycorrhiza 16(8): 553-558. doi: 10. 1007/s00572-006-0072-7.
3. Adriaensen K, Vralstad T, Noben JP, Vangronsveld J, Colpaert JV (2005) Copper-adapted Suillus luteus, a symbiotic solution for pines colonizing Cu mine spoils. Appl Environ Microbiol 71(11): 7279-7284. doi: 10. 1128/AEM. 71. 11. 7279-7284. 2005.
4. Agerer R (1987-1993) Colour atlas of Ectomycorrhizae, vol 1-7th del. Einhorn-Verlag Eduard Dietenberger, Schwäbisch Gmünd, Germany.
5. Bell R, Evans C, Roberts E (1988) Decreased incidence of mycorrhizal root tips associated with soil heavy-metal enrichment. Plant Soil 106(1): 143-145. doi: 10. 1007/bf02371206.
6. Blaudez D, Jacob C, Turnau K, Colpaert JV, Ahonen-Jonnarth U, Finlay R, Botton B, Chalot M (2000) Differential responses of ectomycorrhizal fungi to heavy metals in vitro. Mycol Res 104(11): 1366-1371. doi: 10. 1017/s0953756200003166.
7. Bradshaw AD, Johnson M (1992) Revegetation of metalliferous mine wastes: the range of practical techniques used in Western Europe. Elsevier, Manchester.
8. Buscardo E, Rodriguez-Echeverria S, Martin MP, De Angelis P, Pereira JS, Freitas H (2010) Impact of wildfire return interval on the ectomycorrhizal resistant propagules communities of a Mediterranean open forest. Fungal Biol 114(8): 628-636. doi: 10. 1016/j. funbio. 2010. 05. 004.
9. Chappelka AH, Kush JS, Runion GB, Meier S, Kelley WD (1991) Effects of soil-applied lead on seedling growth and ectomycorrhizal colonization of loblolly pine. Environ Pollut 72(4): 307-316. doi: 10. 1016/0269-7491(91)90004-g.
10. Chen LQ (1989) Studies on symbiotic mycorrhiza fungi with Masson pine. Forest Res 2(4): 357-362 (in Chinese).
11. Colpaert JV, Wevers JHL, Krznaric E, Adriaensen K (2011) How metal-tolerant ecotypes of ectomycorrhizal fungi protect plants from heavy metal pollution. Ann For Sci 68(1): 17-24. doi: 10. 1007/s13595-010-0003-9.
12. Colwell RK (2006) EstimateS: statistical estimation of species richness and shared species from samples. Version 8. 0. doi: http://viceroy. eeb. uconn. edu/EstimateSPages/.
13. Cripps CL (1997) The genus Inocybe in Montana aspen stands. Mycologia 89(4): 670-688. doi: 10. 2307/3761005.
14. Cripps CL (2003) Native mycorrhizal fungi with aspen on smelter-impacted sites in the northern Rocky Mountains: occurrence and potential use in reclamation. Paper presented at the National Meeting of the American Society of Mining and Reclamation and the 9th Billings Land Reclamation Symposium, Billings MT, June 3-6, 2003.
15. Dickinson NM, Turner AP, Watmough SA, Lepp NW (1992) Acclimation of trees to pollution stress-cellular metal tolerance traits. Ann Bot 70(6): 569-572.
16. Dixon R (1988) Response of ectomycorrhizal Quercus rubra to soil cadmium, nickel and lead. Soil Biol Biochem 20(4): 555-559. doi: 10. 1016/0038-0717(88)90072-7.
17. Dixon R, Buschena C (1988) Response of ectomycorrhiza Pinus banksiana and Picea glauca to heavy metals in soil. Plant Soil 105(2): 265-271. doi: 10. 1007/bf02376791.
18. Dora S (1976) Determination of ammonia and Kjeldahl nitrogen by indophenol method. Water Res 10(1): 31-36. doi: 10. 1016/0043-1354(76)90154-8.
19. Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes-application to the identification of mycorrhizae and rusts. Mol Ecol 2(2): 113-118. doi: 10. 1111/j. 1365-294X. 1993. tb00005. x.
20. Gebhardt S, Neubert K, Wollecke J, Munzenberger B, Huttl RF (2007) Ectomycorrhiza communities of red oak (Quercus rubra L.) of different age in the Lusatian lignite mining district, East Germany. Mycorrhiza 17(4): 279-290. doi: 10. 1007/s00572-006-0103-4.
21. Gardner JH, Malajczuk N (1988) Recolonisation of rehabilitated bauxite mine sites in western Australia by mycorrhizal fungi. Forest Ecol Manag 24(1): 27-42. doi: 10. 1016/0378-1127(88)90022-9.
22. Glen M, Bougher NL, Colquhoun IJ, Vlahos S, Loneragan WA, O'Brien PA, Hardy GESJ (2008) Ectomycorrhizal fungal communities of rehabilitated bauxite mines and adjacent, natural jarrah forest in Western Australia. Forest Ecol Manag 255(1): 214-225. doi: 10. 1016/j. foreco. 2007. 09. 007.
23. Guo J, Wu F, Xie S, Yao L, Xie Y (2007) Environmental conditions and exploitation of lead-zinc tailings in Linxiang County, Hunan Province. Chin J Soil Sci 38: 553-557 (in Chinese).
24. Hartley-Whitaker J, Cairney J, Meharg A (2000) Sensitivity to Cd or Zn of host and symbiont of ectomycorrhizal Pinus sylvestris L. (Scots pine) seedlings. Plant Soil 218(1): 31-42. doi: 10. 1023/a: 1014989422241.
25. Hartley J, Cairney JWG, Freestone P, Woods C, Meharg AA (1999) The effects of multiple metal contamination on ectomycorrhizal Scots pine (Pinus sylvestris) seedlings. Environ Pollut 106(3): 413-424. doi: 10. 1016/s0269-7491(99)00095-0.
26. Horton TR, Bruns TD (2001) The molecular revolution in ectomycorrhizal ecology: peeking into the black-box. Mol Ecol 10(8): 1855-1871. doi: 10. 1046/j. 0962-1083. 2001. 01333. x.
27. Hrynkiewicz K, Haug I, Baum C (2008) Ectomycorrhizal community structure under willows at former ore mining sites. Eur J Soil Biol 44(1): 37-44. doi: 10. 1016/j. ejsobi. 2007. 10. 004.
28. Hui N, Jumpponen A, Niskanen T, Liimatainen K, Jones KL, Koivula T, Romantschuk M, Strommer R (2011) EcM fungal community structure, but not diversity, altered in a Pb-contaminated shooting range in a boreal coniferous forest site in Southern Finland. FEMS Microbiol Ecol 76(1): 121-132. doi: 10. 1111/j. 1574-6941. 2010. 01038. x.
29. Ishida TA, Nara K, Tanaka M, Kinoshita A, Hogetsu T (2008) Germination and infectivity of ectomycorrhizal fungal spores in relation to their ecological traits during primary succession. New Phytol 180(2): 491-500. doi: 10. 1111/j. 1469-8137. 2008. 02572. x.
30. Jentschke G, Godbold DL (2000) Metal toxicity and ectomycorrhizas. Physiol Plantarum 109(2): 107-116. doi: 10. 1034/j. 1399-3054. 2000. 100201. x.
31. Johansson L, Xydas C, Messios N, Stoltz E, Greger M (2005) Growth and Cu accumulation by plants grown on Cu containing mine tailings in Cyprus. Appl Geochem 20(1): 101-107. doi: 10. 1016/j. apgeochem. 2004. 07. 003.
32. Jones MD, Hutchinson TC (1986) The effect of mycorrhizal infection on the response of Betula papyrifera to nickel and copper. New Phytol 102(3): 429-442. doi: 10. 1111/j. 1469-8137. 1986. tb00820. x.
33. Kalin M, Stokes PM (1981) Macrofungi on uranium mill tailings-associations and metal content. Sci Total Environ 19(1): 83-94. doi: 10. 1016/0048-9697(81)90120-0.
34. Ke LX, Liu BR (2005) Resource and ecological distribution of ectomycorrhizal fungi under pine forests of Huangshan Mountain district. Chin J Appl Ecol 2005(16): 445-458 (in Chinese).
35. Koljalg U, Larsson KH, Abarenkov K, Nilsson RH, Alexander IJ, Eberhardt U, Erland S, Hoiland K, Kjoller R, Larsson E, Pennanen T, Sen R, Taylor AF, Tedersoo L, Vralstad T, Ursing BM (2005) UNITE: a database providing web-based methods for the molecular identification of ectomycorrhizal fungi. New Phytol 166(3): 1063-1068. doi: 10. 1111/j. 1469-8137. 2005. 01376. x.
36. Krpata D, Peintner U, Langer I, Fitz WJ, Schweiger P (2008) Ectomycorrhizal communities associated with Populus tremula growing on a heavy metal contaminated site. Mycol Res 112(Pt 9): 1069-1079. doi: 10. 1016/j. mycres. 2008. 02. 004.
37. Li MS (2006) Ecological restoration of mineland with particular reference to the metalliferous mine wasteland in China: a review of research and practice. Sci Total Environ 357(1-3): 38-53. doi: 10. 1016/j. scitotenv. 2005. 05. 003.
38. Lian C, Hogetsu T, Matsushita N, Guerin-Laguette A, Suzuki K, Yamada A (2003) Development of microsatellite markers from an ectomycorrhizal fungus, Tricholoma matsutake, by an ISSR-suppression-PCR method. Mycorrhiza 13(1): 27-31. doi: 10. 1007/s00572-002-0193-6.
39. Lindsay WL, Norvell WA (1978) Development of a DTPA soil test for zinc, iron, manganese, and copper. Soil Sci Soc Am J 42(3): 421-428. doi: 10. 2136/sssaj1978. 03615995004200030009x.
40. Liu YG, Zhang HZ, Zeng GM, Huang BR, Li X, Xu WH (2005) Characteristics of tailings from metal mines in Hunan Province, China. J Cent South Univ Technol 12(2): 225-228.
41. Malloch D (1982) An undescribed species of Inocybe from mine wastes in Ontario. Can J Bot 60(1): 40-45. doi: 10. 1139/b82-006.
42. Martin KJ, Rygiewicz PT (2005) Fungal-specific PCR primers developed for analysis of the ITS region of environmental DNA extracts. BMC Microbiol (5). doi: 10. 1186/1471-2180-5-28.
43. Meharg AA, Cairney JWG (2000) Ectomycorrhizas-extending the capabilities of rhizosphere remediation? Soil Biol Biochem 32(11-12): 1475-1484. doi: 10. 1016/s0038-0717(00)00076-6.
44. Nara K (2006) Ectomycorrhizal networks and seedling establishment during early primary succession. New Phytol 169(1): 169-178. doi: 10. 1111/j. 1469-8137. 2005. 01545. x.
45. Nara K, Nakaya H, Wu B, Zhou Z, Hogetsu T (2003) Underground primary succession of ectomycorrhizal fungi in a volcanic desert on Mount Fuji. New Phytol 159(3): 743-756. doi: 10. 1046/j. 1469-8137. 2003. 00844. x.
46. Olsen SR, Sommers LE (1982) Phosphorus. In: Page AL, Miller RH, Keeney DR (eds) Methods of soil analysis. Part 2. Chemical and microbiological properties. Agronomy, No. 9. American Society of Agronomy and Soil Science Society of America, Madison, pp 403-430.
47. Peay KG, Garbelotto M, Bruns TD (2009) Spore heat resistance plays an important role in disturbance-mediated assemblage shift of ectomycorrhizal fungi colonizing Pinus muricata seedlings. J Ecol 97(3): 537-547. doi: 10. 1111/j. 1365-2745. 2009. 01489. x.
48. Ruotsalainen AL, Markkola AM, Kozlov MV (2009) Mycorrhizal colonisation of mountain birch (Betula pubescens ssp. czerepanovii) along three environmental gradients: does life in harsh environments alter plant-fungal relationships? Environ Monit Assess 148(1-4): 215-232. doi: 10. 1007/s10661-007-0152-y.
49. Pestana Nieto M, Santolamazza Carbone S (2009) Characterization of juvenile maritime pine (Pinus pinaster Ait.) ectomycorrhizal fungal community using morphotyping, direct sequencing and fruitbodies sampling. Mycorrhiza 19(2): 91-98. doi: 10. 1007/s00572-008-0207-0.
50. Shu WS, Ye ZH, Zhang ZQ, Lan CY, Wong MH (2005) Natural colonization of plants on five lead/zinc mine tailings in Southern China. Restor Ecol 13(1): 49-60. doi: 10. 1111/j. 1526-100X. 2005. 00007. x.
51. Staudenrausch S, Kaldorf M, Renker C, Luis P, Buscot F (2005) Diversity of the ectomycorrhiza community at a uranium mining heap. Biol Fert Soils 41(6): 439-446. doi: 10. 1007/s00374-005-0849-4.
52. Tedersoo L, Kõljalg U, Hallenberg N, Larsson K-H (2003) Fine scale distribution of ectomycorrhizal fungi and roots. New Phytol 159: 153-165. doi: 10. 1046/j. 0028-646x. 2003. 00792. x.
53. Tedersoo L, Jairus T, Horton BM, Abarenkov K, Suvi T, Saar I, Koljalg U (2008) Strong host preference of ectomycorrhizal fungi in a Tasmanian wet sclerophyll forest as revealed by DNA barcoding and taxon-specific primers. New Phytol 180(2): 479-490. doi: 10. 1111/j. 1469-8137. 2008. 02561. x.
54. Turnau K, Kottke I, Dexheimer J (1996) Toxic element filtering in Rhizopogon roseolus/Pinus sylvestris mycorrhizas collected from calamine dumps. Mycol Res 100(1): 16-22. doi: 10. 1016/s0953-7562(96)80094-3.
55. Vrålstad T, Myhre E, Schumacher T (2002) Molecular diversity and phylogenetic affinities of symbiotic root-associated ascomycetes of the Helotiales in burnt and metal polluted habitats. New Phytol 155(1): 131-148. doi: 10. 1046/j. 1469-8137. 2002. 00444. x.
56. White TJ, Bruns TD, Lee S, Taylor J (1990) Analysis of phylogenetic relationships by amplification and direct sequencing of ribosomal RNA genes. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic, San Diego, pp 315-322.
57. Wilkinson DM, Dickinson NM (1995) Metal resistance in trees-the role of mycorrhizae. Oikos 72(2): 298-300. doi: 10. 2307/3546233.
58. Zhu LH, Wu XQ, Qu HY, Ji J, Ye JR (2010) Micropropagation of Pinus massoniana and mycorrhiza formation in vitro. Plant Cell Tiss Org 102(1): 121-128. doi: 10. 1007/s11240-010-9711-y.