Pine microsatellite markers allow roots and ectomycorrhizas to be linked to individual trees

New Phytologist

Volumn 165, Issue 1, 2005, Pages 295-304

  Saari, S K ^a,b   Campbell, C D ^a   Russell, J ^a   Alexander, I J ^b   Anderson, I C ^a  

^a SCOTTISH CROP RESEARCH INSTITUTE   (United Kingdom)

^b UNIVERSITY OF ABERDEEN   (United Kingdom)

Author keywords

Ectomycorrhizas; Host genotype; Microsatellite fingerprinting; Root ecology; Scots pine (Pinus sylvestris)

Indexed keywords

MICROSATELLITE DNA;

ECTOMYCORRHIZA; GENETIC MARKER; IDENTIFICATION METHOD; ROOT;

ARTICLE; DNA FINGERPRINTING; GENETICS; MICROBIOLOGY; MYCORRHIZA; PLANT ROOT; POLYMERASE CHAIN REACTION; SCOTS PINE;

DNA FINGERPRINTING; MICROSATELLITE REPEATS; MYCORRHIZAE; PINUS SYLVESTRIS; PLANT ROOTS; POLYMERASE CHAIN REACTION;

FUNGI; PINUS SYLVESTRIS;

EID: 11144252229     PISSN: 0028646X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1469-8137.2004.01213.x     Document Type: Article

References (70)

1. Agerer R. 1991. Characterization of ectomycorrhiza. Methods in Microbiology 23: 25-73.
2. Ainsworth EA, Tranel PJ, Drake BG, Long SP. 2003. The clonal structure of Quercus geminata revealed by conserved microsatellite loci. Molecular Ecology 12: 527-532.
3. Albee SR, Mueller GM, Kropp BR. 1996. Polymorphisms in the large intergenic spacer of the nuclear ribosomal repeat identify Laccaria proxima strains. Mycologia 88: 970-976.
4. Attiwill PM, Adams MA. 1993. Nutrient cycling in forests. New Phytologist 124: 561-582.
5. Auckland LD, Bui T, Zhou Y, Shepherd M, Williams CG. 2002. Conifer Microsatellite Handbook. College Station, TX, USA: Texas A & M University.
6. Barker JHA, Pahlich A, Trybush S, Edwards KJ, Karp A. 2003. Microsatellite markers for diverse Salix species. Molecular Ecology Notes 3: 4-6.
7. Bending GD, Read DJ. 1996. Nitrogen mobilizarion from protein-polyphenol complex by ericoid and ectomycorrhizal fungi. Soil Biology and Biochemistry 28: 1603-1612.
8. Bending GD, Read DJ. 1997. Lignin and soluble phenolic degradation by ectomycorrhizal and ericoid mycorrhizal fungi. Mycological Research 101: 1348-1354.
9. Bobowski BR, Hole D, Wolf PG, Bryant L. 1999. Identification of roots of woody species using polymerase chain reaction (PCR) and restriction fragment length polymorphism (RFLP) analysis. Molecular Ecology 8: 485-491.
10. Brondani RPV, Brondani C, Grattapaglia D. 2002. Towards a genus-wide reference linkage map for Eucalyptus based exclusively on highly informative microsarellite markers. Molecular Genetics and Genomics 267: 338-347.
11. Brunner I, Brodbeck S, Buchler U, Sperisen C. 2001. Molecular identification of fine roots of trees from the Alps: reliable and fast DNA extraction and PCR-RFLP analyses of plastid DNA. Molecular Ecology 10: 2079-2087.
12. Cullings KW, Vogler DR, Parker VT, Finley SK. 2000. Ectomycorrhizal specificity patterns in a mixed Pinus contorta and Picea engelmannii forest in Yellowstone National Park. Applied and Environmental Microbiology 66: 4988-4991.
13. Dickie IA, Avis PG, McLaughlin DJ, Reich PB. 2003. Good-Enough RFLP Matcher (GERM) program. Mycorrhiza 13: 171-172.
14. Dickie IA, Xu B, Koide RT. 2002. Vertical distribution of ectomycorrhizal hyphae in soil as shown by T-RFLP analysis. New Phytologist 156: 527-535.
15. Dixon RK, Garrett HE, Stelzer HE. 1987. Growth and ectomycorrhizal development of Loblolly pine progenies inoculated with three isolates of Pisolithus tinctorius. Silvae Genetica 36: 240-245.
16. EspinosaGarcia FJ, Langenheim JH. 1991. Effect of some leaf essential oil phenotypes in coastal redwood on the growth of several fungi with endophytic stages. Biochemical Systematics and Ecology 19: 629-642.
17. Finlay RD, Read DJ. 1986a. The structure and function of the vegetative mycelium of ectomycorrhizal plants. 1. Translocation of C-14-labeled carbon between plants interconnected by a common mycelium. New Phytologist 103: 143-156.
18. Finlay RD, Read DJ. 1986B. The structure and function of the vegetative mycelium of ectomycorrhizal plants. 2. The uptake and distribution of phosphorus by mycelial strands interconnecting host plants. New Phytologist 103: 157-165.
19. Gardes M, Bruns TD. 1993. ITS primers with enhanced specificity for basidiomycetes - application to the identification of mycorrhizae and rusts. Molecular Ecology 2: 113-118.
20. Gonzalez-Martinez SC, Gerber S, Cervera MT, Martinez-Zapater JM, Gil L, Alia R. 2002. Seed gene flow and fine-scale structure in a Mediterranean pine (Pinus pinaster Ait.) using nuclear microsatellite markers. Theoretical and Applied Genetics 104: 1290-1297.
21. Guidot A, Lumini E, Debaud JC, Marmeisse R. 1999. The nuclear ribosomal DNA intergenic spacer as a target sequence to study intraspecific diversity of the ectomycorrhizal basidiomycete Hebeloma cylindrosporum directly on Pinus root systems. Applied and Environmental Microbiology 65: 903-909.
22. Heybroek HM, Stephan BR, von Weissenberg K, eds. 1982. Resistance to diseases and pests in forest trees. Wageningen, the Netherlands: Centre for Agricultural Publishing and Documentation (Pudoc).
23. Hill MO, Gauch HG. 1980. Detrended correspondence analysis: an improved ordination technique. Vegetatio 42: 47-58.
24. Horton TR, Bruns TD. 1998. Multiple-host fungi are the most frequent and abundant ectomycorrhizal types in a mixed stand of Douglas fit (Pseudotsuga menziesii) and Bishop pine (Pinus muricata). New Phytologist 139: 331-339.
25. Horton TR, Bruns TD. 2001. The molecular revolution in ectomycorrhizal ecology: peeking into the black-box. Molecular Ecology 10: 1855-1871.
26. Jonsson L, Dahlberg A, Nilsson MC, Karen O, Zackrisson O. 1999. Continuity of ectomycorrhizal fungi in self-regenerating boreal Pinus sylvestris forests studied by comparing mycobiont diversity on seedlings and mature trees. New Phytologist 142: 151-162.
27. Kalela EK. 1954. Mäntysiemenpuiden ja -puustojen juurisuhteista. Acta Forestalia Fennica 61: 1-16.
28. Kennedy PG, Izzo AD, Bruns TD. 2003. There is high potential for the formation of common mycorrhizal networks between understorey and canopy trees in a mixed evergreen forest. Journal of Ecology 91: 1071-1080.
29. Kretzer A, Li YN, Szaro T, Bruns TD. 1996. Internal transcribed spacer sequences from 38 recognized species of Suillus sensu lato: Phylogenetic and taxonomic implications. Mycologia 88: 776-785.
30. Kubis S, Schmidt T, Heslop-Harrison JS. 1998. Repetitive DNA elements as a major component of plant genomes. Annals of Botany 82: 45-55.
31. Kutil BL, Williams CG. 2001. Triplet-repeat microsatellites shared among hard and soft pines. Journal of Heredity 92: 327-332.
32. Laitakari E. 1927. Männyn juuristo, morphologinen tutkimus (The root system of pine, a morphological investigation). Acta Forestalia Fennica 33: 1-380.
33. Linder CR, Moore LA, Jackson RB. 2000. A universal molecular method for identifying underground plant parts to species. Molecular Ecology 9: 1549-1559.
34. Marx DH, Bryan WC. 1971. Formation of ectomycorrhizae on half-sib progenies of slash pine in aseptic culture. Forest Science 17: 488-492.
35. Melin E, Krupa SV. 1971. Studies on ectomycorrhizae of pine. II. Growth inhibition of mycorrhizal fungi by volatile organic constituents of Pinus sylvestris. Physiologia Plantarum 25: 337-340.
36. Mitchell SE, Kresovich S, Jester CA, Hernandez CJ, SzewcMcFadden AK. 1997. Application of multiplex PCR and fluorescence-based, semi-automated allele sizing technology for genotyping plant genetic resources. Crop Science 37: 617-624.
37. Morgante M, Pfeiffer A, Costacurta A, Olivieri AM. 1996. Molecular tools for population and ecological genetics in coniferous trees. Phyton 36: 129-138.
38. Morgante M, Rafalski A, Biddle P, Tingey S, Olivieri AM. 1994. Genetic mapping and variability of seven soybean simple sequence repeat loci. Genome 37: 763-769.
39. Moser MM. 1997. Contribution to the knowledge of North American Suillus species (Basidiomycotina, Boletales). Mycotaxon 65: 391-402.
40. Mou P, Jones RH, Mitchell RJ, Zutter B. 1995. Spatial distribution of roots in Sweergum and Loblolly pine monocultures and relations with aboveground biomass and soil nutrients. Functional Ecology 9: 689-699.
41. Palmer MW. 1990. The estimation of species richness by extrapolation. Ecology 71: 1195-1198.
42. Parker PG, Snow AA, Schug MD, Booton GC, Fuerst PA. 1998. What molecules can tell us about populations: Choosing and using a molecular marker. Ecology 79: 361-382.
43. Parker MM, Van Lear DH. 1996. Soil heterogeneity and root distribution of mature Loblolly pine stands in Piedmont soils. Soil Science Society of America Journal 60: 1920-1925.
44. Pearson WR, Lipman DJ. 1988. Improved tools for biological sequence comparison. Proceedings of the National Academy of Sciences, USA 85: 2444-2448.
45. Perry DA, Choquette C. 1987. Allelopathic effects on mycorrhizae - influence on structure and dynamics of forest ecosystems. ACS Symposium Series 330: 185-194.
46. Read DJ, Perez-Moreno J. 2003. Mycorrhizas and nutrient cycling in ecosystems - a journey towards relevance? New Phytologist 157: 475-492.
47. Rosado SCS, Kropp BR, Piche Y. 1994a. Genetics of ectomycorrhizal symbiosis. 1. Host-plant variability and heritability of ectomycorrhizal and root traits. New Phytologist 126: 105-110.
48. Rosado SCS, Kropp BR, Piche Y. 1994b. Genetics of ectomycorrhizal symbiosis. 2. Fungal variability and heritability of ectomycorrhizal traits. New Phytologist 126: 111-117.
49. Rosling A, Landeweert R, Lindahl BD, Larsson KH, Kuyper TW, Taylor AFS, Finlay RD. 2003. Vertical distribution of ectomycorrhizal fungal taxa in a podzol soil profile. New Phytologist 159: 775-783.
50. Sen R. 1990. Isozymic identification of individual ectomycorrhizas synthesized between Scots pine (Pinus sylvestris L.) and isolates of 2 species of Suillus. New Phytologist 114: 617-626.
51. Shepherd M, Cross M, Maguire TL, Dieters MJ, Williams CG, Henry RJ. 2002. Transpecific microsatellites for hard pines. Theoretical and Applied Genetics 104: 819-827.
52. Smith JHG. 1964. Root spread can be estimated from crown width of Douglas fir, Lodgepole pine, and other British Columbia tree species. Forestry Chronicle 40: 456-473.
53. Smith SE, Read DJ. 1997. Mycorrhizal symbiosis. London, UK: Academic Press.
54. Smith AH, Thiers HD, Miller OK. 1965. The species of Suillus and Fuscoboletinus of the Priest River Experimental Forest and vicinity, Priest River, Idaho. Lloydia 28: 138.
55. Soranzo N, Provan J, Powell W. 1998. Characterisation of microsatellite loci in Pinus sylvestris L. Molecular Ecology 7: 1260-1261.
56. Tabbener HE, Cottrell JE. 2003. The use of PCR based DNA markers to study the paternity of poplar seedlings. Forest Ecology and Management 179: 363-376.
57. Tautz D, Renz M. 1984. Simple sequences are ubiquitous repetitive components of eukaryotic genomes. Nucleic Acids Research 12: 4127-4138.
58. Timonen S, Tammi H, Sen R. 1997a. Characterization of the host genotype and fungal diversity in Scots pine ectomycorrhiza from natural humus microcosms using isozyme and PCR-RFLP analyses. New Phytologist 135: 313-323.
59. Timonen S, Tammi H, Sen R. 1997b. Outcome of interactions between genets of two Suillus spp. & different Pinus sylvestris genotype combinations: identity and distribution of ectomycorrhizas and effects on early seedling growth in N-limited nursery soil. New Phytologist 137: 691-702.
60. Tofts RJ, Orton PD. 1998. The species accumulation curve for agarics and boleti from a Caledonian Pinewood. Mycologist 12: 98-102.
61. Tonkin CM, Malajczuk N, Mccomb JA. 1989. Ectomycorrhizal formation by micropropagated clones of Eucalyptus marginata inoculated with isolates of Pisolithus tinctorius. New Phytologist 111: 209-214.
62. Vandenkoornhuyse P, Ridgway KP, Watson IJ, Fitter AH, Young JPW. 2003. Co-existing grass species have distinctive arbuscular mycorrhizal communities. Molecular Ecology 12: 3085-3095.
63. Villarréal-Ruiz L, Anderson IC, Alexander IJ. 2004. The interaction between an isolate from the Hymenoscyphus ericae aggregate and roots of Pinus and Vaccinium. New Phytologist 164: 183-192.
64. Vrålstad T, Fossheim T, Schumacher T. 2000. Piceirhiza bicolorata - the ectomycorrhizal expression of the Hymenoscyphus ericae aggregate? New Phytologist 145: 549-563.
65. Vrålstad T, Schumacher T, Taylor AFS. 2002. Mycorrhizal synthesis between fungal strains of the Hymenoscyphus ericae aggregate and potential ectomycorrhizal and ericoid hosts. New Phytologist 153: 143-152.
66. Walker C, Biggin P, Jardine DC. 1986. Differences in mycorrhizal status among clones of Sitka spruce. Forest Ecology and Management 14: 275-283.
67. Wang XR, Szmidt AE. 2001. Molecular markers in population genetics of forest trees. Scandinavian Journal of Forest Research 16: 199-220.
68. White TJ, Bruns TD, Lee S, Taylor JW. 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfaud DH, Sninsky JJ, White TJ (eds) PCR protocols. a guide to methods and applications. San Diego, CA, USA: Academic Press, 315-322.
69. Williams CG, Zhou Y, Hall SE. 2001. A chromosomal region promoting outcrossing in a conifer. Genetics 159: 1283-1289.
70. Zhou ZH, Miwa M, Matsuda Y, Hogetsu T. 2001. Spatial distribution of the subterranean mycelia and ectomycorrhizae of Suillus grevillei genets. Journal of Plant Research 114: 179-185.