Myco-heterotrophy (fromGreekμύκηςmýkes'fungus',ἕτεροςhéteros'another','different' andτροφήtrophé'nutrition') is asymbiotic relationship between certain kinds ofplants andfungi, in which the plant gets all or part of its food fromparasitism upon fungi rather than fromphotosynthesis. Amyco-heterotroph is theparasitic plant partner in this relationship. Myco-heterotrophy is considered a kind ofcheating relationship and myco-heterotrophs are sometimes informally referred to as "mycorrhizal cheaters". This relationship is sometimes referred to asmycotrophy, though this term is also used for plants that engage inmutualisticmycorrhizal relationships.
Relationship between myco-heterotrophs and host fungi
Full (or obligate) myco-heterotrophy exists when a non-photosynthetic plant (a plant largely lacking inchlorophyll or otherwise lacking a functionalphotosystem) gets all of its food from the fungi that it parasitizes. Partial (or facultative) myco-heterotrophy exists when a plant is capable of photosynthesis, but parasitizes fungi as a supplementary food supply. There are also plants, such as someorchid species (e.g.,Neottia nidus-avis), that are non-photosynthetic and obligately myco-heterotrophic for part of theirlife cycle, and photosynthetic and facultatively myco-heterotrophic or non-myco-heterotrophic for the rest of their life cycle.[2] Not all non-photosynthetic or "achlorophyllous" plants are myco-heterotrophic – some non-photosynthetic plants likedodder directly parasitize thevascular tissue of other plants.[3] The partial or full loss of photosynthesis is reflected by extreme physical and functional reductions of plastid genomes in mycoheterophic plants,[4] an ongoing evolutionary process.[5]
In the past, non-photosynthetic plants were mistakenly thought to get food by breaking downorganic matter in a manner similar tosaprotrophic fungi. Such plants were therefore called "saprophytes". It is now known that these plants are not physiologically capable of directly breaking down organic matter and that in order to get food, non-photosynthetic plants must engage in parasitism, either through myco-heterotrophy or direct parasitism of other plants.[6][7]
The interface between the plant and fungal partners in this association is between the roots of the plant and the mycelium of the fungus. Myco-heterotrophy therefore closely resemblesmycorrhiza (and indeed is thought to have evolved from mycorrhiza),[6] except that in myco-heterotrophy, the flow of carbon is from the fungus to the plant, rather than vice versa.[8][9]
Most myco-heterotrophs can therefore be seen as ultimately beingepiparasites, since they take energy from fungi that in turn get their energy fromvascular plants.[6][7][10] Indeed, much myco-heterotrophy takes place in the context of commonmycorrhizal networks,[11] in which plants use mycorrhizal fungi to exchange carbon and nutrients with other plants.[7] In these systems, myco-heterotrophs play the role of "mycorrhizal cheaters", taking carbon from the common network, with no known reward.[6] A special form of mycoheterotrophic association, which appears to be a chimera between the haustorial parasitism of aparasitic plant and mycoheterotrophy, is observed inParasitaxus usta, the only mycoheterotrophicgymnosperm.[12]
In congruence with older reports, it has been recently shown that some myco-heterotrophic orchids can be supported by saprotrophic fungi, exploiting litter- or wood-decaying fungi.[13] In addition, several green plants (evolutionarily close to myco-heterotrophic species) have been shown to engage in partial myco-heterotrophy, that is, they are able to take carbon from mycorrhizal fungi, in addition to their photosynthetic intake.[14][15]
Species diversity of myco-heterotrophs and host fungi
Myco-heterotrophs are found among several plant groups, mainlyflowering plants. Allmonotropes and non-photosyntheticorchids are full myco-heterotrophs, as is the non-photosyntheticliverwortAneura mirabilis (previously considered a species ofCryptothallus).[16] Partial myco-heterotrophy is common in theGentian family, with a few genera such asVoyria being fully myco-heterotrophic; in photosynthetic orchids; and in a number of other plant groups. Someferns andclubmosses have myco-heterotrophicgametophyte stages.[2][7][17] The fungi that are parasitized by myco-heterotrophs are typically fungi with large energy reserves to draw on, usually mycorrhizal fungi, though there is some evidence that they may also parasitize parasitic fungi that form extensive mycelial networks, such asArmillaria.[7]Examples of fungi parasitized by myco-heterotrophic plants can be found among theectomycorrhizal,arbuscular mycorrhizal, andorchid mycorrhizal fungi.[18] The great diversity in unrelated plant families with myco-heterotrophic members, as well as the diversity of fungi targeted by myco-heterotrophs, suggests multipleparallel evolutions of myco-heterotrophs from mycorrhizal ancestors.[18]
^Yang, S; DH Pfister. (2006). "Monotropa uniflora plants of eastern Massachusetts form mycorrhizae with a diversity of russulacean fungi".Mycologia.98 (4):535–540.doi:10.3852/mycologia.98.4.535.PMID17139846.
^Dawson, JH; Musselman, LJ; Wolswinkel, P; Dörr, I (1994). "Biology and control ofCuscuta".Reviews of Weed Science.6:265–317.
^Wicke, S.; Naumann, J. (2018). "Molecular evolution of plastid genomes in parasitic flowering plants".Advances in Botanical Research.85 (1):315–347.doi:10.1016/bs.abr.2017.11.014.
^Gebauer, G; Meyer, M (2003). "15N and 13C natural abundance of autotrophic and myco-heterotrophic orchids provides insights into nitrogen and carbon gain from fungal association".New Phytologist.160 (1):209–223.doi:10.1046/j.1469-8137.2003.00872.x.PMID33873535.
^Selosse, M-A; Roy, M (2009). "Green plants eating fungi: facts and questions about mixotrophy".Trends in Plant Science.14 (2):64–70.doi:10.1016/j.tplants.2008.11.004.PMID19162524.
^Taylor DL, Bruns TD, Leake JR, Read DJ. 2002.Mycorrhizal specificity and function in myco-heterotrophic plants. In:Mycorrhizal Ecology (Sanders IR, van der Heijden M, eds.), Ecological Studies vol. 157, pp 375–414. Berlin: Springer-Verlag.ISBN3-540-00204-9. (NOTE: this PDF is from the page proofs, and is not identical to the published version)
