Mycobiology

The Korean Society of Mycology (한국균학회)
권호 표지
DOI QR코드

DOI QR Code

Diversity of Arbuscular Mycorrhizal Fungi and Their Roles in Ecosystems

  • Lee, Eun-Hwa (Department of Biology Education, Korea National University of Education) ;
  • Eo, Ju-Kyeong (Department of Biology Education, Korea National University of Education) ;
  • Ka, Kang-Hyeon (Division of Wood Chemistry and Microbiology, Korea Forest Research Institute) ;
  • Eom, Ahn-Heum (Department of Biology Education, Korea National University of Education)
  • Received : 2013.09.10
  • Accepted : 2013.09.11
  • Published : 2013.09.30
Download PDF
⟨ Previous Next ⟩

Abstract

Arbuscular mycorrhizal fungi (AMF) have mutualistic relationships with more than 80% of terrestrial plant species. This symbiotic relationship is ancient and would have had important roles in establishment of plants on land. Despite their abundance and wide range of relationship with plant species, AMF have shown low species diversity. However, molecular studies have suggested that diversity of these fungi may be much higher, and genetic variation of AMF is very high within a species and even within a single spore. Despite low diversity and lack of host specificity, various functions have been associated with plant growth responses to arbuscular mycorrhizal fungal colonization. In addition, different community composition of AMF affects plants differently, and plays a potential role in ecosystem variability and productivity. AMF have high functional diversity because different combinations of host plants and AMF have different effects on the various aspects of symbiosis. Consequently, recent studies have focused on the different functions of AMF according to their genetic resource and their roles in ecosystem functioning. This review summarizes taxonomic, genetic, and functional diversities of AMF and their roles in natural ecosystems.

Keywords

References

  1. Smith SE, Read D. Mycorrhizal symbiosis. 3rd ed. San Diego: Academic Press; 2008.
  2. Redecker D, Kodner R, Graham LE. Glomalean fungi from the Ordovician. Science 2000;289:1920-1. https://doi.org/10.1126/science.289.5486.1920
  3. Schu$\beta$ler A, Walker C. The Glomeromycota: a species list with new families and new genera. Edinburgh and Kew: The Royal Botanic Garden Kew, Botanische Staatssammlung Munich, and Oregon State University; 2010.
  4. Schu$\beta$ler A, Schwarzott D, Walker C. A new fungal phylum, the Glomeromycota: phylogeny and evolution. Mycol Res 2001;105:1413-21. https://doi.org/10.1017/S0953756201005196
  5. Kruger M, Krüger C, Walker C, Stockinger H, Schu$\beta$ler A. Phylogenetic reference data for systematics and phylotaxonomy of arbuscular mycorrhizal fungi from phylum to species level. New Phytol 2012;193:970-84. https://doi.org/10.1111/j.1469-8137.2011.03962.x
  6. Fitter AH. Darkness visible: reflections on underground ecology. J Ecol 2005;93:231-43. https://doi.org/10.1111/j.0022-0477.2005.00990.x
  7. Clapp JP, Rodriguez A, Dodd JC. Inter- and intra-isolate rRNA large subunit variation in Glomus coronatum spores. New Phytol 2001;149:539-54.
  8. Vandenkoornhuyse P, Leyval C. SSU rDNA sequencing and PCR-fingerprinting reveal genetic variation within Glomus mosseae. Mycologia 1998;90:791-7. https://doi.org/10.2307/3761320
  9. Angelard C, Colard A, Niculita-Hirzel H, Croll D, Sanders IR. Segregation in a mycorrhizal fungus alters rice growth and symbiosis-specific gene transcription. Curr Biol 2010;20: 1216-21. https://doi.org/10.1016/j.cub.2010.05.031
  10. Munkvold L, Kjoller R, Vestberg M, Rosendahl S, Jakobsen I. High functional diversity within species of arbuscular mycorrhizal fungi. New Phytol 2004;164:357-64. https://doi.org/10.1111/j.1469-8137.2004.01169.x
  11. Avio L, Pellegrino E, Bonari E, Giovannetti M. Functional diversity of arbuscular mycorrhizal fungal isolates in relation to extraradical mycelial networks. New Phytol 2006;172:347-57 https://doi.org/10.1111/j.1469-8137.2006.01839.x
  12. Croll D, Wille L, Gamper HA, Mathimaran N, Lammers PJ, Corradi N, Sanders IR. Genetic diversity and host plant preferences revealed by simple sequence repeat and mitochondrial markers in a population of the arbuscular mycorrhizal fungus Glomus intraradices. New Phytol 2008; 178:672-87. https://doi.org/10.1111/j.1469-8137.2008.02381.x
  13. Allen EB, Allen MF, Helm DJ, Trappe JM, Molina R, Rincon E. Patterns and regulation of mycorrhizal plant and fungal diversity. Plant Soil 1995;170:47-62. https://doi.org/10.1007/BF02183054
  14. Burleigh SH, Cavagnaro T, Jakobsen I. Functional diversity of arbuscular mycorrhizas extends to the expression of plant genes involved in P nutrition. J Exp Bot 2002;53:1593-601. https://doi.org/10.1093/jxb/erf013
  15. Smith SE, Smith FA, Jakobsen I. Functional diversity in arbuscular mycorrhizal (AM) symbioses: the contribution of the mycorrhizal P uptake pathway is not correlated with mycorrhizal reponses in grwoth and total P uptake. New Phytol 2004;162:511-24. https://doi.org/10.1111/j.1469-8137.2004.01039.x
  16. Redecker D. Molecular identification and phylogeny of arbuscular mycorrhizal fungi. Plant Soil 2002;244:67-73. https://doi.org/10.1023/A:1020283832275
  17. Law R. Evolution in a mutualistic environment. In: Boucher DH, editor. The biology of mutualism: ecology and evolution. London: Croons Helm; 1985. p. 145-70.
  18. Morton JB. Taxonomy of VA mycorrhizal fungi: classification, nomenclature, and identification. Mycotaxon 1988;32:267-324
  19. Morton JB, Benny GL. Revised classification of arbuscular mycorrhizal fungi (Zygomycetes): a new order, Glomales, two new suborders, Glomineae and Gigasporineae, and two new families, Acaulosporaceae and Gigasporaceae, with an emendation of Glomaceae. Mycotaxon 1990;37:471-91.
  20. Sanders IR, Alt M, Groppe K, Boller T, Wiemken A. Identification of ribosomal DNA polymorphisms among and within spores of the Glomales: application to studies on the genetic diversity of arbuscular mycorrhizal fungal communities. New Phytol 1995;130:419-27. https://doi.org/10.1111/j.1469-8137.1995.tb01836.x
  21. Lloyd-Macgilp SA, Chambers SM, Dodd JC, Fitter AH, Walker C, Young JPW. Diversity of the ribosomal internal transcribed spacers within and among isolates of Glomus mosseae and related mycorrhizal fungi. New Phytol 1996; 133:103-11. https://doi.org/10.1111/j.1469-8137.1996.tb04346.x
  22. Husband R, Herre EA, Turner SL, Gallery R, Young JP. Molecular diversity of arbuscular mycorrhizal fungi and patterns of host association over time and space in a tropical forest. Mol Ecol 2002;11:2669-78. https://doi.org/10.1046/j.1365-294X.2002.01647.x
  23. Msiska Z, Morton JB. Phylogenetic analysis of the Glomeromycota by partial $\beta$-tubulin gene sequences. Mycorrhiza 2009;19:247-54. https://doi.org/10.1007/s00572-008-0216-z
  24. Morton JB, Msiska Z. Phylogenies from genetic and morphological characters do not support a revision of Gigasporaceae (Glomeromycota) into four families and five genera. Mycorrhiza 2010;20:483-96. https://doi.org/10.1007/s00572-010-0303-9
  25. Helgason T, Fitter A, Young JP. Molecular diversity of arbuscular mycorrhizal fungi colonising Hyacinthoides nonscripta (bluebell) in a seminatural woodland. Mol Ecol 1999; 8:659-66. https://doi.org/10.1046/j.1365-294x.1999.00604.x
  26. Lee J, Lee S, Young JP. Improved PCR primers for the detection and identification of arbuscular mycorrhizal fungi. FEMS Microbiol Ecol 2008;65:339-49. https://doi.org/10.1111/j.1574-6941.2008.00531.x
  27. Wubet T, Weiss M, Kottke I, Teketay D, Oberwinkler F. Phylogenetic analysis of nuclear small subunit rDNA sequences suggests that the endangered African Pencil Cedar, Juniperus procera, is associated with distinct members of Glomeraceae. Mycol Res 2006;110(Pt 9):1059-69. https://doi.org/10.1016/j.mycres.2006.04.005
  28. Gollotte A, Van Tuinen D, Atkinson D. Diversity of arbuscular mycorrhizal fungi colonising roots of the grass species Agrostis capillaris and Lolium perenne in a field experiment. Mycorrhiza 2004;14:111-7. https://doi.org/10.1007/s00572-003-0244-7
  29. Pivato B, Mazurier S, Lemanceau P, Siblot S, Berta G, Mougel C, Van Tuinen D. Medicago species affect the community composition of arbuscular mycorrhizal fungi associated with roots. New Phytol 2007;176:197-210. https://doi.org/10.1111/j.1469-8137.2007.02151.x
  30. Rosendahl S, McGee P, Morton JB. Lack of global population genetic differentiation in the arbuscular mycorrhizal fungus Glomus mosseae suggests a recent range expansion which may have coincided with the spread of agriculture. Mol Ecol 2009;18:4316-29. https://doi.org/10.1111/j.1365-294X.2009.04359.x
  31. van der Heijden MG, Klironomos JN, Ursic M, Moutoglis P, Streitwolf-Engel R, Boller T, Wiemken A, Sanders IR. Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 1998;396:69-72 https://doi.org/10.1038/23932
  32. Kuhn G, Hijri M, Sanders IR. Evidence for the evolution of multiple genomes in arbuscular mycorrhizal fungi. Nature 2001;414:745-8. https://doi.org/10.1038/414745a
  33. Hijri M, Sanders IR. Low gene copy number shows that arbuscular mycorrhizal fungi inherit genetically different nuclei. Nature 2005;433:160-3. https://doi.org/10.1038/nature03069
  34. Colard A, Angelard C, Sanders IR. Genetic exchange in an arbuscular mycorrhizal fungus results in increased rice growth and altered mycorrhiza-specific gene transcription. Appl Environ Microbiol 2011;77:6510-5. https://doi.org/10.1128/AEM.05696-11
  35. Koch AM, Croll D, Sanders IR. Genetic variability in a population of arbuscular mycorrhizal fungi causes variation in plant growth. Ecol Lett 2006;9:103-10. https://doi.org/10.1111/j.1461-0248.2005.00853.x
  36. Johnson NC, Graham JH, Smith FA. Functioning of mycorrhizal associations along the mutualism-parasitism continuum. New Phytol 1997;135:575-85. https://doi.org/10.1046/j.1469-8137.1997.00729.x
  37. van der Heijden MG, Boller T, Wiemken A, Sanders IR. Different arbuscular mycorrhizal fungal species are potential determinants of plant community structure. Ecology 1998; 79:2082-91. https://doi.org/10.1890/0012-9658(1998)079[2082:DAMFSA]2.0.CO;2
  38. Tinker PB, Durall DM, Jones MD. Carbon use efficiency in mycorrhizas theory and sample calculations. New Phytol 1994;128:115-22. https://doi.org/10.1111/j.1469-8137.1994.tb03994.x
  39. Sanders FE, Tinker PB, Black RL, Palmerley SM. The development of endomycorrhizal root systems: I. Spread of infection and growth-promoting effects with four species of vesicular-arbuscular endophyte. New Phytol 1977;78:257-68. https://doi.org/10.1111/j.1469-8137.1977.tb04829.x
  40. Abbott LK, Robson AD. Formation of external hyphae in soil by four species of vesicular-arbuscular mycorrhizal fungi. New Phytol 1985;99:245-55. https://doi.org/10.1111/j.1469-8137.1985.tb03653.x
  41. Giovannetti M, Fortuna P, Citernesi AS, Morini S, Nuti MP. The occurrence of anastomosis formation and nuclear exchange in intact arbuscular mycorrhizal networks. New Phytol 2001; 151:717-24. https://doi.org/10.1046/j.0028-646x.2001.00216.x
  42. Maldonado-Mendoza IE, Dewbre GR, Harrison MJ. A phosphate transporter gene from the extra-radical mycelium of an arbuscular mycorrhizal fungus Glomus intraradices is regulated in response to phosphate in the environment. Mol Plant Microbe Interact 2001;14:1140-8. https://doi.org/10.1094/MPMI.2001.14.10.1140
  43. Govindarajulu M, Pfeffer PE, Jin H, Abubaker J, Douds DD, Allen JW, Bücking H, Lammers PJ, Shachar-Hill Y. Nitrogen transfer in the arbuscular mycorrhizal symbiosis. Nature 2005;435:819-23. https://doi.org/10.1038/nature03610
  44. Liu J, Blaylock LA, Endre G, Cho J, Town CD, VandenBosch KA, Harrison MJ. Transcript profiling coupled with spatial expression analyses reveals genes involved in distinct developmental stages of an arbuscular mycorrhizal symbiosis. Plant Cell 2003;15:2106-23. https://doi.org/10.1105/tpc.014183
  45. Hohnjec N, Vieweg MF, Puhler A, Becker A, Kuster H. Overlaps in the transcriptional profiles of Medicago truncatula roots inoculated with two different Glomus fungi provide insights into the genetic program activated during arbuscular mycorrhiza. Plant Physiol 2005;137:1283-301. https://doi.org/10.1104/pp.104.056572
  46. Genre A, Chabaud M, Faccio A, Barker DG, Bonfante P. Prepenetration apparatus assembly precedes and predicts the colonization patterns of arbuscular mycorrhizal fungi within the root cortex of both Medicago truncatula and Daucus carota. Plant Cell 2008;20:1407-20. https://doi.org/10.1105/tpc.108.059014
  47. Parniske M. Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nat Rev Microbiol 2008;6:763-75. https://doi.org/10.1038/nrmicro1987
  48. Read DJ. Mycorrhizas in ecosystems. Experientia 1991;47: 376-91. https://doi.org/10.1007/BF01972080
  49. Lambert DH, Baker DE, Cole H Jr. The role of mycorrhizae in the interactions of phosphorus with zinc, copper, and other elements. Soil Sci Soc Am J 1979;43:976-80. https://doi.org/10.2136/sssaj1979.03615995004300050033x
  50. Feng G, Zhang FS, Li XL, Tian CY, Tang C, Rengel Z. Improved tolerance of maize plants to salt stress by arbuscular mycorrhiza is related to higher accumulation of soluble sugars in roots. Mycorrhiza 2002;12:185-90. https://doi.org/10.1007/s00572-002-0170-0
  51. Augé RM. Water relations, drought and vesicular-arbuscular mycorrhizal symbiosis. Mycorrhiza 2001;11:3-42. https://doi.org/10.1007/s005720100097
  52. Linderman RG. Effects of mycorrhizas on plant tolerance to diseases. In: Koltai H, Kapulnik Y, editors. Arbuscular mycorrhizas: physiology and function. Dordrecht: Springer; 2000. p. 345-65.
  53. Leake J, Johnson D, Donnelly D, Muckle G, Boddy L, Read D. Networks of power and influence: the role of mycorrhizal mycelium in controlling plant communities and agroecosystem functioning. Can J Bot 2004;82:1016-45. https://doi.org/10.1139/b04-060