Orchid mycorrhiza: implications of a mycophagous life style

Abstract

Orchid mycorrhiza probably affects about 25 000 plant species and thus roughly one tenth of all higher plants.Histologically, this symbiosis resembles other kinds of endomycorrhiza, the fungal hyphae growing within living plant cells. Considerable evidence, however, suggests that it is not a two-way exchange relationship and thus not potentially mutualistic, such as the wide-spread endomycorrhiza between plants and Glomalean fungi, known as arbuscular mycorrhiza. During the achlorophyllous seedling stage orchids are obligately dependent on the fungi; some species remain so through life, while others establish photosynthesis but to varying degrees remain facultatively dependent of / responsive to fungal infection as adults. None of the fungi involved are so far known to depend on the symbiosis with orchids. Transfer of organic carbon compounds from hyphae to the orchid has been demonstrated repeatedly, but it is not clear to what extent this takes place during a biotrophic phase while the intracellular hyphae remain intact, or during the subsequent extensive degradation of the hyphal coils. The advantage of viewing orchid mycorrhiza basically as a unilateral mycophagous relationship, in spite of hypothetical beneficial spin-offs to the mycobiont, is that it provides a conceptual framework similar to that of other parasitic or fungivore relationships; mechanisms known in such relationships could be searched for in future studies of the orchidÁfungus symbiosis. These could include mechanisms for recognition, attraction and selection of fungi, physiological regulation of internal hyphal growth, breakdown, and material transfer, nutritional consequences of the plant's preference(s) and trophic changes, fungal avoidance mechanisms, and consequences at population and ecosystem levels. A whole range of possible life strategies becomes apparent that could support divergent evolution and lead to the proliferation of species that has indeed occurred in the orchid family. We outline some of the possible physiological mechanisms and ecological implications of this approach.

Characterization of seed germination and protocorm development of Cyrtopodium glutiniferum (Orchidaceae) promoted by mycorrhizal fungi Epulorhiza spp.

“…The fact that fungal colonization is absent from aerial parts of plants further explains the restriction of fungal colonization to basal cells, and demonstrates that even in early development stages orchids exert control over their symbiotic fungi. However, physiological factors that control this pattern of colonization remain poorly understood (Rasmussen & Rasmussen 2009 Data subjected to analysis of variance and the Duncan mean test at 5% significance level, obtained after an arcsine square root-transformation of the proportions. The means followed by the same lowercase letters in the line and by the same uppercase letters in the column are statistically equal among each other.…”

“…The embryo develops and forms the protocorm, an achlorophyllous and heterotrophic stage of the orchid life cycle (Rasmussen & Rasmussen 2009;Dearnaley et al 2012). Mycorrhizal colonization and fungi consumption persist in orchid roots into adulthood, when the interaction serves an important role in orchid nutrition (Dearnaley 2007;Rasmussen & Rasmussen 2009).…”

“…The embryo develops and forms the protocorm, an achlorophyllous and heterotrophic stage of the orchid life cycle (Rasmussen & Rasmussen 2009;Dearnaley et al 2012). Mycorrhizal colonization and fungi consumption persist in orchid roots into adulthood, when the interaction serves an important role in orchid nutrition (Dearnaley 2007;Rasmussen & Rasmussen 2009). Inoculation with mycorrhizal fungi has been applied to in vitro symbiotic seed germination and orchid cultivation (Pereira et al 2011;Guimarães et al 2013), with promising applications in the propagation of ornamental (Pereira et al 2003a;2005a), endangered (Zettler & McInnis 1992;Zettler et al 2007), and medicinal orchids (Chang & Chou 2001;Tan et al 2014).…”

Gene expression in mycorrhizal orchid protocorms suggests a friendly plant–fungus relationship

“…After washing in the same buffer, the samples were post-fixed in 1 % (w/v) osmium tetroxide in water for 1 h, washed three times with water, and dehydrated in an ethanol series [30,50,70,90, and 100 % (v/v); 15 min each step] at room temperature. Samples were infiltrated in 2:1 (v/v) ethanol/LR White (Polysciences, Warrington, PA, USA) for 1 h, 1:2 (v/v) ethanol/LR White resin for 2 h, 100 % LR White overnight at 4 °C, and embedded in LR White resin, according to Balestrini et al (1996).…”

The epiphytic orchids Ionopsis utricularioides and Psygmorchis pusilla associate with different Ceratobasidium lineages at Valle del Cauca, Colombia

“…The dependence on OM fungi may be conserved throughout the life-cycle of some orchids, while others may receive carbon by either CO 2 fixation or mycorrhizal transfer after establishing photosynthesis (Rasmussen & Rasmussen 2009). Thus, the availability of suitable mycorrhizal fungi able to germinate or to symbiotically associate with adult orchids is probably a key factor constraining the distribution of orchid species (Otero et al 2007).…”