Anatomical relations among endophytic holoparasitic angiosperms, autotrophic host plants and mycorrhizal fungi: A novel tripartite interaction

American Journal of Botany

Volumn 97, Issue 5, 2010, Pages 730-737

  de Vega, Clara ^a   Arista, Montserrat ^b   Ortiz, Pedro L ^b   Talavera, Salvador ^b  

^a DEPARTMENT OF CONSERVATION BIOLOGY   (Spain)

^b UNIVERSITY OF SEVILLE   (Spain)

Author keywords

Cistaceae; Cistus; Cytinaceae; Cytinus hypocistis; Halimium; Host parasite interactions; Mutualism; Mycoheterotrophic plant; Mycorrhizal fungi; Parasitic plant; Tripartite interaction

Indexed keywords

ANATOMY; ANGIOSPERM; ANTAGONISM; AUTOTROPHY; DICOTYLEDON; ENDOPHYTE; FUNGUS; HOST PLANT; HOST-PARASITE INTERACTION; MUTUALISM; MYCORRHIZA; PARASITIC PLANT; SHRUB; TERRESTRIAL ECOSYSTEM;

CISTACEAE; CISTUS; CYTINACEAE; CYTINUS HYPOCISTIS; FUNGI; HALIMIUM; MAGNOLIOPHYTA;

EID: 77952387369     PISSN: 00029122     EISSN: None     Source Type: Journal    
DOI: 10.3732/ajb.0900147     Document Type: Article

References (63)

1. Águeda, B., J. Parladé, A. M. de Miguel, and F. Martínez-Peña. 2006. Characterization and identification of field ectomycorrhizae of Boletus edulis and Cistus ladanifer. Mycologia 98: 23-30.
2. Bardgett, R. D., D. A. Wardle, and G. W. Yeates. 1998. Linking above-ground and below-ground interactions: How plant responses to foliar herbivory influence soil organisms. Soil Biology & Biochemistry 30: 1867-1878.
3. Baskin, C. C., and J. M. Baskin. 1998. Seeds: Ecology, biogeography, and evolution of dormancy and germination. Academic Press, San Diego, USA.
4. Bennett, A. E., and J. D. Bever. 2007. Mycorrhizal species differentially alter plant growth and response to herbivory. Ecology 88: 210-218.
5. Berliner, R., B. Jacoby, and E. Zamski. 1986. Absence of Cistus incanus from basaltic soils in Israel: Effect of mycorrhizae. Ecology 67: 1283-1288.
6. Bhandari, N. N., and R. G. Mukerji. 1993. The haustorium. Research Studies Press, New York, New York, USA.
7. Bidartondo, M. I.2005. The evolutionary ecology of my co-heterotrophy. New Phytologist 167: 335-352.
8. Boursnell, J. G. 1950. The symbiotic seed-borne fungus in the Cistaceae. I. Distribution and function of the fungus in the seedling and the tissues of the mature plants. Annals of Botany 14: 217-243.
9. Bouwmeester, H. J., C. Roux, J. A. Lopez-Raez, and G. Bécard. 2007. Rhizosphere communication of plants, parasitic plants and AM fungi. Trends in Plant Science 12: 224-230.
10. Brundrett, M. C. 2009. Mycorrhizal associations and other means of nutrition of vascular plants: Understanding the global diversity of host plants by resolving conflicting information and developing reliable means of diagnosis. Plant and Soil 320: 37-77.
11. Bruns, T. D., and D. J. Read. 2000. In vitro germination of nonphotosynthetic, myco-heterotrophic plants stimulated by fungi isolated from the adult plants. New Phytologist 148: 335-342.
12. Cahill, J. F., E. Elle, G. R. Smith, and B. H. Shore. 2008. Disruption of a belowground mutualism alters interactions between plants and their floral visitors. Ecology 89: 1791-1801.
13. Çakan, H. C., and Ç. Karataş. 2006. Interactions between mycorrhizal colonization and plant life forms along the successional gradient of coastal sand dunes in the eastern Mediterranean, Turkey. Ecological Research 21: 301-310.
14. Comandini, O., M. Contu, and A. C. Rinaldi. 2006. An overview of Cistus ectomycorrhizal fungi. Mycorrhiza 16: 381-395.
15. Davies, D. M., and J. D. Graves. 1998. Interactions between arbuscular mycorrhizal fungi and the hemiparasitic angiosperm Rhinanthus minor during co-infection of a host. New Phytologist 139: 555-563.
16. de la Peña, E., S. R. Echevarría, W. H. van der Putten, H. Freitas, and M. Moens. 2006. Mechanism of control of root-feeding nematodes by mycorrhizal fungi in the dune grass Ammophila arenaria. New Phytologist 169: 829-840.
17. de Vega, C. 2007. Reproductive biology of Cytinus hypocistis (L.) L.: Host parasite interactions. Ph.D. dissertation, University of Seville, Seville, Spain.
18. de Vega, C., M. Arista, P. L. Ortiz, C. M. Herrera, and S. Talavera. 2009. Theant-pollinationsystemofCytinus hypocistis (Cytinaceae), a Mediterranean root holoparasite. Annals of Botany 103: 1065-1075.
19. de Vega, C., R. Berjano, M. Arista, P. L. Ortiz, S. Talavera, and T. F. Stuessy. 2008. Genetic races associated with the genera and sections of host species in the holoparasitic plant Cytinus (Cytinaceae) in the Western Mediterranean basin. New Phytologist 178: 875-887.
20. de Vega, C., P. L. Ortiz, M. Arista, and S. Talavera. 2007. The endophytic system of Mediterranean Cytinus (Cytinaceae) developing on five host Cistaceae species. Annals of Botany 100: 1209-1217.
21. Dickie, I. A., R. C. Guza, S. E. Krazewski, and P. B. Reich. 2004. Shared ectomycorrhizal fungi between a herbaceous perennial (H elianthemum bicknellii) and oak (Quercus) seedlings. New Phytologist 164: 375-382.
22. Duke, S. E., R. B. Jackson, and M. M. Caldwell. 1994. Local reduction of mycorrhizal arbuscule frequency in enriched soil microsites. Canadian Journal of Botany 72: 998-1001.
23. Ewald, P. W. 1995. The evolution of virulence: A unifying link between parasitology and ecology. Journal of Parasitology 81: 659-669.
24. Feild, T. S., and T. J. Brodribb. 2005. A unique mode of parasitism in the conifer coral tree Parasitaxus ustus (Podocarpaceae). Plant, Cell & Environment 28: 1316-1325.
25. Ferrandis, P., J. M. Herranz, and J. Martínez-Sánchez. 1999. Effect of fire on hard-coated Cistaceae seed banks and its influence on techniques for quantifying seed banks. Plant Ecology 144: 103-114.
26. Gange, A. C., and A. K. Smith. 2005. Arbuscular mycorrhizal fungi influence visitation rates of pollinating insects. Ecological Entomology 30: 600-606.
27. Gaur, A., and A. Varma. 2007. Research methods in arbuscular mycorrhizal fungi. In A. Varma and R. Oelmüller [eds.], Techniques in soil microbiology, 377-396. Springer, Berlin, Germany.
28. Gehring, C., and A. Bennett. 2009. Mycorrhizal fungal-plant-insect interactions: The importance of a community approach. Environmental Entomology 38: 93-102.
29. Gehring, C., and T. G. Whitham. 1992. Reduced mycorrhizae on Juniperus monosperma with mistletoe: The influence of environmental stress and tree gender on a plant parasite and a plant fungal mutualism. Oecologia 89: 298-303.
30. Giovannetti, M., and B. Mosse. 1980. An evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots. New Phytologist 84: 489-500.
31. Greuter, W., H. M. Burdet, and G. Long. 1989. Med-Checklist, vol. 4. Editions des Conservatoire et Jardin Botaniques de la Ville de Genève, Geneva, Switzerland.
32. Gutiérrez, A., A. Morte, and M. Honrubia. 2003. Morphological characterization of the mycorrhiza formed by Helianthemum almeriense Pau with Terfezia claveryi Chatin and Picoa lefebvrei (Pat.) Maire. Mycorrhyza 13: 299-307.
33. Gworgwor, N. A., and H. C. Weber. 2003. Arbuscular mycorrhizal fungi parasite host interaction for the control of Striga hermonthica (Del.) Benth. in sorghum [Sorghum bicolor (L.) Moench]. Mycorrhiza 13: 277-281.
34. Harley, J. L., and S. E. Smith. 1983. Mycorrhizal symbiosis. Academic Press, New York, New York, USA.
35. Herrera, C. M., M. Medrano, P. J. Rey, A. M. Sánchez-Lafuente, M. B. García, J. Guitián, and A. J. Manzaneda. 2002. Interaction of pollinators and herbivores on plant fitness suggests a pathway for correlated evolution of mutualismand antagonism-related traits. Proceedings of the National Academy of Sciences, USA 99: 16823-16828.
36. Junqueira, C. U. 1990. O uso de cortes finos de tecidos na medicina e biologia. Meios and M étodos 66: 167-171.
37. Khalid, A. N., and S. H. Iqbal. 1996. Mycotrophy in a vascular stem parasite Cuscuta reflexa. Mycorrhiza 6: 69-71.
38. Kuijt, J. 1969. The biology of parasitic flowering plants. University of California Press, Davis, California, USA.
39. Kuijt, J. 1977. Haustoria of phanerogamic parasites. Annual Review of Phytopathology 15: 91-118.
40. Leake, J. R. 1994. The biology of myco-heterotrophic ('saprophytic') plants. New Phytologist 127: 171-216.
41. Lendzemo, V. W., T. W. Kuyper, M. J. Kropff, and A. van Ast. 2005. Field inoculation with arbuscular mycorrhizal fungi reduces Striga hermonthica performance on cereal crops and has the potential to contribute to integrated Striga management. Field Crops Research 91: 51-61.
42. Lesica, P., and R. K. Antibus. 1986. Mycorrhizae of alpine fell field communities on soils derived from crystalline and calcareous parent materials. Canadian Journal of Botany 64: 1691-1697.
43. Li, A.-R., and K.-Y. Guan. 2007. Mycorrhizal and dark septate endophytic fungi of Pedicularis species from northwest of Yunnan Province, China. Mycorrhiza 17: 103-109.
44. Li, A.-R., and K.-Y. Guan. 2008. Arbuscular mycorrhizal fungi may serve as another nutrient strategy for some hemiparasitic species of Pedicularis (Orobanchaceae). Mycorrhiza 18: 429-436.
45. Mabberley, D. 1997. The plant book, 2nd ed. Cambridge University Press, Cambridge, UK.
46. Molina, R., H. Massicotte, and J. M. Trappe. 1992. Specificity phenomena in mycorrhizal symbiosis: Community-ecological consequences and practical implications. In M. F. Allen [ed.], Mycorrhizal functioning: An integrated plant fungal process, 357-423. Chapman & Hall, London, UK.
47. Musselman, L. J., and M. C. Press. 1995. Introduction to parasitic plants. In M. C. Press and J. D. Graves [eds.], Parasitic plants, 1-11. Chapman and Hall, London, UK.
48. Nickrent, D. L. 2002. Plantas par á sitas en el mundo. In J. A. López-Sáez, P. Catalán, and L. Sáez [eds.], Plantas parásitas de la Península Ibéricae Islas Baleares, 7-28. Mundi-Prensa Libros, Madrid, Spain.
49. Pate, J. S., J. Kuo, and N. J. Davidson. 1990. Morphology and anatomy of the haustorium of the root hemiparasite Olax phyllanthi (Olacaceae) with special reference to the haustorial interface. Annals of Botany 65: 425-436.
50. Pennings, S. C., and R. M. Callaway. 2002. Parasitic plants: Parallels and contrasts with herbivores. Oecologia 131: 479-489.
51. Salonen, V., M. Vestberg, and M. Vauhkonen. 2001. The effect of host mycorrhizal status on host plant parasitic plant interactions. Mycorrhiza 11: 95-100.
52. Sanders, I. R., R. T. Koide, and D. L. Shumway. 1993. Mycorrhizal stimulation of plant parasitism. Canadian Journal of Botany 71: 1143-1146.
53. Smith, S. E., and D. J. Read. 2008. Mycorrhizal symbiosis, 3rd ed. Academic Press, London, UK.
54. StatSoft. 2001. STATISTICA (data analysis software), version 6. StatSoft, Tulsa, Oklahoma, USA. Website http://www.statsoft.com.
55. Stein, C., C. Cornelia Rissmann, S. Hempel, C. Renker, F. Buscot, D. Prati, and H. Auge. 2009. Interactive effects of mycorrhizae and a root hemiparasite on plant community productivity and diversity. Oecologia 159: 191-205.
56. Thalouarn, P., L. Rey, and S. Renaudin. 1986. Carbon nutrition in a Rafflesiaceae holoparasitic Cytinus hypocistis L. fixed on, or experimentally isolated from the host Cistus monspeliensis. Journal of Plant Physiology 123: 271-281.
57. Thompson, J. N., and C. C. Fernández. 2006. Temporal dynamics of antagonism and mutualism in a geographically variable plant -insect interaction. Ecology 87: 103-112.
58. Torres, P., A. Roldán, A. R. Lansac, and A. Martin. 1995. Ectomycorrhizal formation between Cistus ladanifer and Laccaria laccata. Nova Hedwigia 60: 311-315.
59. Trabaud, L. 1995. Modalités de germination des cistes et des pins méditerran é es et colonisation des sites perturbés. Revue d'Ecologie: La Terre et la Vie 50: 3-14.
60. Trappe, J. M. 1987. Phylogenetic and ecologic aspects of mycotrophy in the angiosperms from an evolutionary viewpoint. In G. R. Safir [ed.], Ecophysiology of VA mycorrhizal plants, 5-25. CRC Press, Boca Raton, Florida, USA.
61. van der Heijden, M. G. A., J. N. Klironomos, M. Ursic, P. Moutoglis, R. Streitwolf-Engel, T. Boller, A. Wiemken, and I. R. Sanders. 1998. Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396: 69-72.
62. Wenkart, S., N. Roth-Bejerano, D. Mills, and V. Kagan-Zur. 2001. Mycorrhizal association between Tuber melanosporum mycelia and transformed roots of Cistus incanus. Plant Cell Reports 20: 369-373.
63. Woltz, P., R. A. Stockey, M. Gondran, and J. F. Cherrier. 1994. Interspecific parasitism in the Gymnosperms: Unpublished data on two endemic New Caledonian Podocarpaceae using scanning electron microscopy. Acta Botanica Gallica 141: 731-746.