The Mycorrhizae: A plant-fungus relation that has existed for more than 400 million years;Las micorrizas: Una relación planta-hongo que dura más de 400 millones de años

Anales del Jardin Botanico de Madrid

Volumn 66, Issue SUPPL. 1, 2009, Pages 133-144

  Honrubia, Mario ^a  

^a UNIVERSITY OF MURCIA   (Spain)

Author keywords

Evolution; Mycorrhizae; Origin; Symbiosis

Indexed keywords

ARBUSCULAR; ASCOMYCOTA; BASIDIOMYCOTA; FUNGI; GLOMEROMYCOTA; MONOTROPA; ORCHIDACEAE;

EID: 78649867432     PISSN: 02111322     EISSN: 19883196     Source Type: Journal    
DOI: 10.3989/ajbm.2226     Document Type: Article

References (89)

1. Arditti, J. 1977. Orchid Biology: Reviews and Perspectives I. Cornell University Press, London. Pp 25-46.
2. Barea, J.M. & Honrubia, M. 2004. La micorrización dirigida de la planta forestal. In: Vallejo, R. & al. (ed.), Avances en el estudio de la gestión del monte mediterráneo. CEAM. 84-921259-3-4. Pp: 215-260.
3. Berbee, M.L. & Taylor, J.W. 1993. Dating the radiations of the true fungi. Canadian Journal of Botany 71: 1114-1127.
4. Berbee, M.L. & Taylor, J.W., 2001. Fungal molecular evolution: genes trees and geologic time. In: McLaughin/McLaughin/Lemke (eds.), The Mycota VII Part B. Systematics and Evolution. Springer-Verlag Berlin Heiidelberg. Pp. 229-245.
5. Berbee, M.L. & Taylor, J.W., 2007. Rhynia Chert: a window into a lost world of complex plant-fungus interactions. New Phytologist 174: 475-479.
6. Bidartondo, M.J. & Bruns, T. 2005. On the origins of extreme mycorrhizal specificity in the Monotropoideae (Ericaceae): performance trade-offs during seed germination and seedling development. Molecular Ecology 14: 1549-1560.
7. Bonfante, P & Genre, A. 2008. Plants and arbuscular mycorrhizal fungi: an evolutionary-developmental perspective. Trends in Plant Science 13: 492-498.
8. Brundrett, MC. 2002. Coevolution of roots and mycorrhizas of land plants. New Phytologist 154: 275-304.
9. Brundrett, MC. 2004. Diversity and classification of mycorrhizal associations. Biological Reviews 79: 473-495.
10. Brundrett MC. 2008. Mycorrhizal Associations: The Web Resource. Date accessed. "mycorrhizas.info".
11. Bruns, T. & Shefferson, R.P.. 2004. Evolutionary studies of mycorrhizal fungi: milestones and future directions. Canadian Journal of Botany 82: 1122-1132.
12. Cairney, J.W. 2000. Evolution of mycorrhiza systems. Naturwissenschaften 87: 467-475.
13. Cairney, J.W.G. & Ashford, A.E. 2002. Biology of mycorrhizal associations of epicrids (Ericaceae). New Phytologist 154: 305-326.
14. Carrión, JS. 2003. Evolución vegetal. DM. ISBN 84-8425-335-X. 497 pp.
15. Cazares, E. & Smith, J.E. 1996. Ocurrence of arbuscular mycorrhizae in Pseudotsuga menziesii and Tsuga heterophylla seedlings grown in Oregon Coastal range soils. Mycorrhiza 6: 65-67.
16. Comandini, O; Contu, M. & Rinaldi, A.C. 2006. A overview of Cistus ectomycorrhizal fungi. Mycorrhiza 16: 381-395.
17. Díaz, G., Barrantes, O., Honrubia, M. & Gracia, C. 1996. Effect of ozone and sulphur dioxide on mycorrhizae of: Pinus halepensis Miller. Ann. Sci. For. 53: 849-856.
18. Ding, T-Y. 1995. Origin, divergence and geographical distribution of Salicaceae. Acta Botanica Yunnanica 17: 277-290.
19. Dreyer, B., Morte, A., López, J.A. & Honrubia, M. (en preparación). Comparative root morphology and anatomy of four palm species and their relation with the mycorrhizal susceptibility and morphology.
20. Duckett, J.G. & Ligrone, R. 2005. A comparative cytological analysis of fungal endophytes in the sporophyte rhizomes and vascularized gametophytes of Tmesipteris and Psilotum. Canadian Journal of Botany 83: 1443-1456.
21. Duckett, JG., Carafa, A & Ligrone, R. 2006. A highly differentiated glomeromycotean association with the mucilage-secreting, primitive abtipodean liverwort Treubia (Treubiaceae): clues to the origin of mycorrhizas. American Journal of Botany 93: 797-813.
22. Ellul, P., Boscaiu, M., Vicente, O., Moreno, V. & Rosselló, J.A. 2002. Intra-and Interspecific Variation in DNA Content in Cistus (Cistaceae). Annals of Botany 90: 345-351.
23. Fassi, B. 1957. Ectomycorhizie chez le Gnetum africanum Welw. due a Scleroderma sp., Bulletin de la Société Française de Mycologie 73: 280-285.
24. Frank B. 1885. Über die auf Wurzeisymbiosen beruhende Ernährung gewisser Bäume durch unterirdische Pilze. Ber Deutsch Bot Ges 3: 128-145.
25. Gargas, A. DePriest, PT., Grube, M. & Theler, A. 1995. Multiple origins of lichen symbioses in fungi suggested by SSU rDNA phylogeny. Science 268: 1492-1495.
26. Genre, A., Chabaud, M., Timmers, T., Bonfante, P. & Barker, DG. 2005. Arbuscular mycorrhizal fungi elicit a novel intracellular apparatus in Medicago truncatula root epidermal cells before infection. Plant Cell 17: 3489-3499.
27. Genre, A., Chabaud, M., Faccio, A., Barker, DG. & Bonfante, P. 2008. 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 20: 1407-1420.
28. Giovannetti, G. & Fontana, A. 1982. Mycorrhizal synthesis between Cistaceae and Tuberaceae. New Phytol. 92: 533-537
29. Gutiérrez, A., Morte, A. & Honrubia, M. 2003. Morphological characterization of the mycorrhizae formed by Helianthemum almeriense Pau with Terfezia claveryi Chatin and Picoa lefebvrei (Pat.) Maire. Mycorrhiza 13: 299-307.
30. Guzmán, B. & Vargas, P. 2005. Systematics, character evolution, and biogeography of Cistus L. (Cistaceae) based on ITS, trnLtrnF, and matK sequences. Molecular Phylogenetics and Evolution 37: 644-660.
31. Heckman, D.S., Geiser, D.M., Eidell, B.R., Stauffer, R.L., Kardos, N.L. & Hedges, S.B. 2001. Molecular evidence for the early colonization of land by fungi and plants. Science 293: 1129-1133.
32. Hibbett, D.S. Gilbert, L.B. & Donoghe, M.J. 2000. Evolutionary instability of ectomycorrhizal symbioses in basidiomycetes. Nature 407: 506-508.
33. Honrubia, M. & Díaz, G. 1996. Effect of simulated acid rain on mycorrhizae of Aleppo pine (Pinus halepensis Miller). Ann. Sci. For. 53: 947-954.
34. Honrubia, M., Torres, P., Díaz, G., Barreno, E., Morte, A., Sánchez, F., Pérez, P. & Sánchez-Saorín, J.A. 1997. Efectos de las micorrizas en la restauración de las zonas afectadas por incendios forestales en la Comunidad Valenciana. 345-393 pp. In La Restaura-ción de la Cubierta Vegetal en la Comunidad Valenciana. Ed. Centro de Estudios Ambientales del Mediterráneo CEAM. Generalitat Valenciana. Conselleria deAgricultura y Medio Ambiente. ISBN 84-921259-0-X.
35. Honrubia, M., Morte, A. & Díaz, G. 2002. Dinamismo del componente fúngico micorrícico y su incidencia en la regeneración del bosque mediterráneo. In: Charco, J. (coord.), La regeneración natural del bosque mediterráneo en la península Ibérica: evaluación de problemas y propuesta de soluciones. ARBA-MMA (eds.), ISBN 84-922095-5-0. Pp: 87-113.
36. Honrubia, M., Morte, A. & Gutiérrez, A. 2007. Las Terfezias. Un cultivo para el desarrollo rural en regiones áridas y semi-áridas. In: Reyna, S. (coord.), Truficultura, Fundamentos y Técnicas, Capítulo 10. Pp. 365-397. Ediciones Mundi-Prensa, Madrid.
37. Ji, Q., Li, H., Bowe, M., Liu, Y. & Taylor, D.W. 2004. Early Cretaceous Archaefructus eoflora sp. nov. with Bisexual Flowers from Beipiao, Western Liaoning, China. Acta Geologica Sinica 78: 883-896.
38. Kiers, E.T. & Van der Heijden, M.G. 2006. Mutualistic stability in the arbuscular mycorrhizal symbiosis: exploring hypothesis of the evolutionary cooperation. Ecology 87: 1627-1636.
39. Koch, M.A. & Mummenhof, K. 2006. Editorial: Evolution and phylogeny of the Brassicaceae. Pl. Syst. Evol. 259: 81-83.
40. Konzalova, M., 1967. Paleontologicke zprava klokalite. Archiv Geoindustria, Geofond, Prague.
41. Kottke, I & Nebel, M. 2005. The evolution of mycorrhiza-like associations in liverworts: an update. New Phytologist 167: 330-334.
42. Krings M., Taylor. T.N., Hass, H., Kerp., H., Dotzler, N & Hermsen, E.J. 2007. Fungal endophytes in a 400-million-year-old land plants: infection pathways, spatial distribution, and host responses. New Phytologist 174: 648-657.
43. LePage, B.A., Currah, RS., Stockey, RA & Rothwell, GW. 1997. Fossil ectomycorrhizae from the Middle Eocene. American Journal of Botany 84: 410-410.
44. Lewis, D.H. 1987. Evolutionary aspects of mutualistic associations between fungi and photosynthetic organisms. In: Rayner, A.D.M., Brasier, C.M. & Moore, D. (eds.), Evolutionary biology of the fungi. Cambridge University Press, Cambridge. Pp. 161-178.
45. Li, JQ., 1996. The origin and distribution of the family Fagaceae. Acta Phytotaxonomica Sinica 34: 376-396.
46. Ligrone, R., Carafa, A., Lumini, E., Bianciotto, V., Bonfante P. & Duckett, J.G. 2007. Glomeromycotean associations in liverworts: a molecular, cellular, and taxonomic analysis. American Journal of Botany 94: 1756-1777.
47. Mabberley, DJ. 1997. The plant-book. A portable dictionary of the vascular plants. Cambridge: Cambridge University Press.
48. Malloch, D.W., Pirozynski, K.A. & Raven, P.H. 1980. Ecological and evolutionary significance of mycorrhizal symbioses in vascular plants (A Review). Proceedings of the National Academy of Sciences USA 77: 2113-2118.
49. Massicotte, H.B., Melville, L.H., Molina, R., Peterson, R.L. 1993. Structure and histochemistry of mycorrhizar synthesized between Arbutus menziessi (Ericaceae) and two basidiomycetes, Pisolithus tinctorius (Pisolithaceae) and Piloderma bicolor (Corticiaceae). Mycorrhiza 3: 1-11.
50. McGee, P.A., Bullock, S. & Summerell, B.A. 1999. Structure of mycorrhizae of Wollemi Pine (Wollemia nobilis) and related Araucariaceae. Australian Journal of Botany 47: 85-95.
51. Morte, A., Honrubia, M. & Gutiérrez, A. 2008. Biotechnology and Cultivation of Desert Truffles. In: A. Varma (ed.). Mycorrhiza. Biology, Genetics, Novel Endophytes and Biotechnology. 3rd edition, Chapter 38. Springer-Verlag. Heidelberg, New York. Pp. 467-483.
52. Moyersoen B. 2006. Pakaraimaea dipterocarpacea is ectomycorrhizal, indicating an ancient Gondwanaland origin for the ectomycorrhizal habit in Dipterocarpaceae. New Phytologist 172: 753-762.
53. Nan, L. 1995. Studies on the geographic distribution, origin and dispersal of the family Pinaceae Lindl. Acta Phytotaxonomica Sinica 32: 105-130.
54. Navarro, A., Sánchez-Blanco, M.J., Morte, A., Bañon, S. (En prensa). The influence of mycorrhizal infection on water and nutritional status of Arbutus unedo L. treated and not treated with paclobutrazol. Environmental and Experimental Botany.
55. Nebel, M., Kreier, HP., Preußing, M., Weiß, M. & Kottke, I. 2004. Symbiotic fungal associations of liverworts are the possible ancestors of mycorrhizae. In: Agerer, R., Piepenbring, M. & Blanz, P. (eds.), Frontiers in Basidiomycote Mycology. Eching, Germany: IHW-Verlag. Pp. 339-360.
56. Onguene, N.A. & Kuyper, T.W. 2001. Mycorrhizal associations in the rain forest of South Cameroon. Forest Ecology Management 140: 277-287.
57. Pérez-Moreno, J. & Read, D. J. 2004. Los hongos ectomicorrícicos, lazos vivientes que conectan y nutren a los árboles en la naturaleza. Interciencia 29: 239-247.
58. Phipps, C.J. & Taylor, T.N. 1997. Mixed arbuscular mycorrhizae from the Triassic of Antarctica. Mycologia 88: 707-714.
59. Pirozynski, K.A. 1980. Interactions between fungi and plants through the ages. Canadian Journal of Botany 59: 1824-1827.
60. Pirozynski, K.A. & Malloch, D.W. 1975. The origin of land plnats: a matter of mycotrophism. Biosystems 6: 153-164.
61. Pressel, S., Ligrone, R., Duckett, J.G. & Davis, E.C. 2008. A novel ascomycetous endophytic association in the rhizoids of the leaf liverwot family Schistochilaceas (Jungermanniidae, Hepaticopsida). American Journal of Botany 95: 531-541.
62. Read, D.J., Duckett, J.G., Francis, R., Ligrone, R. & Russell, A. 2000. Symbiotic fungal association in "lower"plants. Phil. Trans. R. Soc. Lond. B. 355: 815-831.
63. Redecker, D. 2002. Molecular identification and phylogeny of arbuscular mycorrhizal fungi. Plant and Soil 244: 67-73.
64. Redecker, D., Kodner, R. & Graham, L.E. 2000. Glomean Fungi from the Ordovician. Science 289 (5486): 1920-1921.
65. Remy, W., Taylor, T.N., Hass, H. & Kerp, H. 1994. Four hundredmillion-year-old vesicular arbuscular mycorrhizae. Proc. Nat. Acad. Sci. (USA) 91: 11841-11843.
66. Russell, J. & Bulman, S. 2005. The liverwort Marchantia foliacea forms a specialized symbiosis with arbuscular mycorrhizal fungi in the genus Glomus. New Phytologist 165: 567-579.
67. Schmidt, A.R., Dörfelt, H. & Perrichot, V. 2007. Carnivorous fungi from Cretaceous Amber. Science 318: 1743.
68. Schüßler, A. 2000. Glomus claroideum forms an arbuscular mycorrhiza-like symbiosis with the hornwort Anthoceros punctatus. Mycorrhiza 10: 15-21.
69. Schüßler, A., Schwarzott, D. & Walker, C. 2001. A new fungal phylum, the Glomeromycota: phylogeny and evolution. Mycol. Res. 105: 1413-1421.
70. Selosse, MA. 2005. Are liverworts imitating mycorrhizas? New Phytologist 165: 345-349.
71. Selosse, M.A. & Le Tacon, F. 1998. The land flora: a phototrophfungus partnership. Tree 13: 15-20.
72. Selosse, M.A., Setaro, S., Glatard, F., Richard, F., Urcelay, C. & Weiß, M. 2007. Sebacinales are common mycorrhizal associates of Ericaceae. New Phytologist 174: 864-878.
73. Simon, L., Bousquet, J., Levesque, R.C. & Lalonde, M. 1993. Origin and diversification of endomycorrhizal fungi and coincidence with vascular land plants. Nature 363: 67-69.
74. Smith, S. & Read, D. 2008. Mycorrhizal Symbiosis. 3er Ed. Academic Press. ISBN 9780123705266. 800 pp.
75. St. John,TV. 1980. A survey of mycorrhizal infection in a Amazonian rain forest. Acta amazonica 10: 527-533.
76. Sun, G., Ji, Q., Dilcher, D.L., Zheng, S., Nixon, K.C. & Wang, X. 2002. Archaefructaceae, a New Basal Angiosperm Family. Science 296: 899-904.
77. Sung, G.H., Poinar, G.O. & Spatafora, J.W. 2008. The oldest fossil evidence of animal parasitism by fungi supports a Cretaceous diversification of fungal-arthropod symbioses. Molecular phylogenetics and evolution 49: 495-502.
78. Taylor, T.N., Remy, W., Hass, H. & Kerp, H. 1995. Fossil arbuscular mycorrhizae from the Early Devonian. Mycologia 87: 560-573.
79. Taylor, T.N., Klavins S.D., Krings, M., Taylor, E.I., Kerp, H. & Hass, H. 2004. Fungi from the Rhynia chert: a view from the dark side. Transactions of the Royal Society of Edimburgh-Earth Sciences 94: 457-473.
80. Torres, P. & Honrubia, M. 1997. Changes and effects of a natural fire on ectomycorrhizal inoculum potential of soil in a Pinus halepensis forest. For. Ecol. Manag. 96: 189-196
81. Vajda, V. & McLoughlin, S. 2004 Fungal Proliferation at the Cretaceous-Tertiary Boundary. Science 303: 1489
82. Vajda, V., Raine, J.I. & Hollis, C.J. 2001. Indication of global deforestation at the Cretaceous-Tertiary Boundary by New Zealand fern spike. Science 294: 1700-1702.
83. Vrälstad, T., Schumacher, T. & Taylor, A.F.S., 2002. Mycorrhizal synthesis between fungal strains of the Hymenoscyphus aggregate and potential ectomycorrhizal and ericoid hosts. New Phytologist 153: 143-152.
84. Wang, B. & Qiu, Y.L. 2006. Phylogenetic distribution and evolution of mycorrhizas in land plants. Mycorrhiza 16: 299-363.
85. Willis, K.J. & McElwain, J.C. 2002. The evolution of plants. Oxford Univ. Press.
86. Wing, S.L. & Boucher, L.D. 1998. Ecological aspects of the Cretaceous flowering plant radiation. Annual Review of Earth and Planetery Science 26: 379-421.
87. Yuan, X., Xiao, S. & Taylor, T.N. 2005. Lichen-like symbiosis 600 Million year ago. Science 308: 1017-1020.
88. Zhang, Y. & Guo, LD. 2007. Arbuscular mycorrhizal structure and fungi associated with mosses. Mycorrhiza. 17: 319-325.
89. Zhu, GL. 1995. Origin, differentiation and geographical distribution of Chenopodiaceae. Acta Phytotaxonomica Sinica 34: 486-504.