User:Plambertiana/Myco-heterotrophy

Myco-heterotrophy
Myco-heterotrophy (from Greek μύκης mykes, "fungus", ἕτερος heteros, "another", "different" and τροφή trophe, "nutrition") is a relationship between certain kinds of plants and fungi, in which the plant gets all or part of its carbon from fungi rather than from photosynthesis. The term was coined by Jonathan Leake in 1994. A myco-heterotroph is the plant partner in this relationship and the relationship is sometimes referred to as mycotrophy, though this term is also used for plants that engage in mutualistic mycorrhizal relationships. The carbon obtained by myco-heterotrophs via fungal symbionts comes from either autotrophic plants with a shared mycorrhizal network or from an association with saprotrophic fungi. Myco-heterotrophy is considered to be a continuum from partial myco-heterotrophy (or mixotrophy), where plants obtain carbon from fungi during certain parts of their life cycle or under stressful growing conditions, to full myco-heterotrophy, where plants lack the ability to photosynthesize and obtain all their carbon from fungi. There are approximately 23,000 land plants that rely on myco-heterotrophy at some point in their life cycle.

Partial vs. Full Myco-heterotrophy
Approximately 10% of plants have a myco-heterotrophic stage during their growth. Full (or obligate) myco-heterotrophy exists when a non-photosynthetic plant (a plant largely lacking in chlorophyll or otherwise lacking a functional photosystem) gets all of its carbon from the fungi that it exploits. Partial (or facultative) myco-heterotrophy exists when a plant is capable of photosynthesis, but gets supplementary carbon from fungi. There are also plants, such as some orchid species, that are non-photosynthetic and obligately myco-heterotrophic for part of their life cycle, and photosynthetic and facultatively myco-heterotrophic or non-myco-heterotrophic for the rest of their life cycle. Some ferns and clubmosses also have myco-heterotrophic gametophyte stages. 'Initial' myco-heterotrophy, where plants use fungal carbon during germination and early seedling development, is especially common in orchid species. It remains unclear whether initial myco-heterotrophs become autotrophic after the emergence of their first leaf or if they are partially myco-heterotrophic for a longer period of time. However, not all non-photosynthetic or "achlorophyllous" plants are myco-heterotrophic with some non-photosynthetic plants directly parasitizing the vascular tissue of other plants.

Evolution of Myco-heterotrophy
Fossil evidence on myco-heterotrophy is sparse, with only one fossil series that has been linked to an extant myco-heterotroph lineage (Triuridaceae). However, phylogenetic evidence suggests there were at least 50 independent origins of myco-heterotrophy in distinct clades of land plants with at least 43 independent origins of full myco-heterotrophy in monocots and at least 7 origins of myco-heterotrophy outside of monocots. Myco-heterotrophy has evolved once in almost all major lineages of land plants with exceptions including hornworts and mosses. Available evidence indicates that myco-heterotrophic plants evolved from autotrophic ancestors with mutualistic mycorrhizal relationships and that the shift from autotrophy to full myco-heterotrophy evolved gradually through partially myco-heterotrophic ancestors, rather than a direct shift from autotrophy to myco-heterotrophy. Because mycorrhizal autotrophy is the evolutionary starting point for myco-heterotrophy, it is thought that this relationship represents an evolutionary breakdown of the plant-fungus symbiosis, where the relationship between plants and mycorrhiza shifted from mutualistic to exploitative. Mycorrhizal symbioses that involved multiple plant partners are considered fundamental to the evolution of myco-heterotrophy because the mycorrhizal fungus needs an autotrophic plant partner to obtain carbon. Therefore, fully myco-heterotrophic plants and mycorrhizal symbionts cannot exist in a one to one interaction, with the exception of myco-heterotrophic orchid species that associate with saprotrophic fungi.

Evolutionary Drivers
'Initial' myco-heterotrophy is thought to be the first step in the evolutionary trajectory from autotrophy to full myco-heterotrophy. Initial myco-heterotrophy allows small seeds, or 'dust' seeds, which depend on fungal symbionts for successful establishment, to be produced in large numbers, reducing the cost to the plant for seed production. It is thought that trends of increased fungal host dependence and reduced seed size evolved reciprocally. Light availability is also considered to be an important driver in the evolution of myco-heterotrophy, with reliance on fungal carbon increasing as light availability decreases. Stable isotope studies on plants in the Orchidaceae and Ericaceae families show that the degree of mycoheterotrophy is largely driven by light availability, but is not always explained by irradiance alone.

Fungal Specificity
Many myco-heterotrophs show high specificity towards their arbuscular mycorrhiza, ectomycorrhiza, and saprotrophic fungal symbionts, a phenomena that is observed among both non-angiosperm and angiosperm myco-heterotrophs. Research has shown that in the absence of their specific fungal symbiont myco-heterotrophic plants may exhibit diminished seedling growth. The evolutionary trajectory toward high fungal specificity is thought to be driven by two pathways: 1.) selection by the plant for the fungal community that best meets nutritional demands and 2.) denied access by most fungal partners due to the presumed parasitic nature of myco-heterotrophic plants. However, there are examples of full myco-heterotrophs that do not show high specificity toward their fungal symbionts (ex. Pyrola aphylla and Aphyllorchis species ). In orchids, associations with saprotrophic fungal symbionts is thought to be the ancestral state, but many fully myco-heterotrophic orchids form associations with ectomycorrhizal fungi. For initial myco-heterotrophs, seed germination can occur in the presence of both host and non-host fungi, as well as in the the absence of fungi altogether , but further growth and development depends on myco-heterotrophy and association with a specific fungal symbiont. The true host fungi of initial myco-heterotrophs are considered to be the fungi that support the plants from seedling development to the growth of the first leaf.

General Species Diversity
Many land plants including bryophytes, lycophytes, ferns, gymnosperms, monocots, and dicots use myco-heterotrophy at some point in their life cycle. Full myco-heterotrophy occurs in more than 400 plants species comprising 87 genera and 11 families. The family Orchidaceae contains the most fully myco-heterotrophic species (at least 210 species) and an estimated 20,000 species within the Orchidaceae family use initial myco-heterotrophy. Additionally, there are also numerous chlorophyll-containing orchids which depend on partial myco-heterotrophy during their adult stage. Partial and full myco-heterotrophic plant species have also evolved within Aneuraceae, Burmanniaceae, Corsiaceae, Ericaceae, Gentianaceae, Iridaceae, Petrosaviaceae, Podocarpaceae, Polygalaceae, and Triuridaceae.

Physiological Function
The physiological function of myco-heterotrophic plants was poorly understood until the application of isotope tracer studies and stable isotope analyses. It was in 1960 that a field-based experiment demonstrated that labeled carbon (14C glucose) and phosphorous (32P phosphate) in spruce and pine trees was transferred to nearby achlorophyllous Monotropa hypopitys plants but not to the other nearby understory plant species. Since then, numerous studies have also used stable isotope analysis of carbon and nitrogen to investigate myco-heterotrophy, finding that myco-heterotrophic plants are more enriched in 13C than nearby autotrophic plants. This enrichment of 13C is consistent with fungal assimilation and transport of organic carbon which typically results in preferential loss of 12C, indicating the use of fungi as a carbon source. This trend has been found numerous times in myco-heterotrophs that associate with ectomycorrhizal fungi as well as arbuscular mycorrhizal fungi. Nitrogen enrichment has also been observed in myco-heterotrophs, but this attribute is not ubiquitous. Stable isotope analyses can also provide a tool for estimating the proportion of carbon myco-heterotrophs obtain from fungi.

Metabolite Transfer
The mechanisms surrounding the transfer of nutrients and carbon from fungi to myco-heterotrophs are still being studied, but it has been argued that they are driven by source-sink dynamics where the plant creates a concentration gradient to produce a sink effect on the plant-fungus network. The strength of the sink may vary with life stage, seasonality, or environmental variability. The specific metabolites involved in fungus-to-plant metabolite fluxes have not yet been identified, but studies have identified key differences between the pathways of assimilation and metabolite transfer in Glomeralean arbuscular mycorrhiza and ectomycorrhizal basidiomycetes  which may influence the mechanism by which myco-heterotrophs are able to exploit these fungi. With respect to nitrogen transport, a genetic study on the symbiosis between mycorrhizal orchid host Tulasnella calospora and orchid species Serapias vomeracea identified genes coding for functional ammonium transporters as well as amino acid transporters. This allows the fungus to exploit both inorganic and organic nitrogen sources which may contribute to the particularly high concentrations of nitrogen found in the tissues of many orchid species. Additionally, upregulation of genes coding for membrane transporters suggests that transport of nitrogen is an active process. While active transport at the fungus-plant interface is thought to be the primary method by which myco-heterotrophs obtain fungal carbon, microscopy analysis of myco-heterotrophs have also shown that these plants digest fungal hyphae, which also contributes to carbon gain. Stable isotope cellular imaging has reveled that orchids receive carbon and nitrogen from fungi both through active transport from live pelotons, coils of fungal hyphae that develop inside the cells of the primary cortex, and from degenerating, senescent pelotons, suggesting that both transport across the mycorrhizal interface and lysis of fungal pelotons may play an important role in nutrient exchange in myco-heterotrophs.

Form
Unlike autotrophic plants where growth is typically limited by water and nutrient availability, myco-heterotrophs are carbon limited and have growth forms that maximize carbon reserves and minimize carbon loss. They are generally smaller than their most closely related autotrophic and partially myco-heterotrophic species. The leaves of fully myco-heterotrophic plants have become reduced to achlorophyllous scales because the leaves no longer serve a purpose for carbon gain. Additionally, the leaves of full myco-heterotrophs typically lack stomata, but some species do have vestigial stomata on their leaves and shoots. Fully myco-heterotrophic plants have slender stems and their shoots lack secondary thickening. Both xylem and phloem are present in very small amounts in these plants. The belowground organs of myco-heterotrophs are an example of convergent evolution from organs with absorptive functions towards organs with storage function. The roots of myco-heterotrophic plants typically lack root hairs and have a wider root cortex for carbohydrate and nutrient storage. Further, the wider root cortex and clumped nature of roots and rhizomes promotes mycorrhizal infection. Finally, most myco-heterotrophs have small, "dust-like" seeds with minimal carbohydrate reserves, reduced endosperms, and a lack of embryo differentiation at maturity.

Response of myco-heterotrophic plants to disturbance and drought
Myco-heterotrophs occur in landscapes that experience natural disturbances (ex. wildfire), but little evidence exists on how myco-heterotrophs respond to both natural and manmade disturbances. While limited research exists on the topic, myco-heterotrophic plants may be affected by anthropogenic disturbances such as forest management and climate change.

Anthropogenic Disturbance
In forests of the pacific northwest, research has suggested that both clear cutting and fire in forests can result in the extirpation of myco-heterotroph species. Research across Canadian boreal forests has found that myco-heterotroph presence was reduced or eliminated by clear cutting and did not recover within the 12 year post-logging study period. As a result, myco-heterotrophs have been considered sensitive species with respect to silviculture and may be negatively affected by silvicultural practices if habitat retention of old-growth forest attributes are not considered. Further, initial research on thinning and prescribed burning treatments in Sierra Nevada mixed-conifer forests found that these treatments reduced and eliminated the abundance of Corallhorhiza maculata and Pterospora andromedea, respectively. Research has also indicated that changes in soil nutrition can also affect myco-heterotroph abundance. A study conducted on lowland tropical forest in Panama found that the abundance of Voyria tenella and V.corymbosa significantly declined when soil phosphorous levels exceeded a threshold of 2 mg P kg−1. The reduction in the abundance of these two myco-heterotrophic species corresponded with decreasing abundance of soil arbuscular mycorrhizal fungi and a decreasing abundance of autotrophic plant roots.

Climate and Drought
Limited research exists on how myco-heterotrophic plants will respond to climate change and how climate affects their abundance and reproduction. Research in southeastern Arizona on Corallorhiza striata, a fully myco-heterotrophic orchid, found that the abundance of aboveground stems and flowering stems decreased during a seven year drought period, but increased when precipitation returned to average levels. The decrease in stem abundance during drought years corresponded with decreases in ectomycorrhizal abundance. Research on Corallorhiza odontorhiza also found that precipitation had a positive effect on rhizome abundance in this species. Current research suggests that flowering in some myco-heterotrophic species is at least partially dependent of climate, and association with drought-tolerant fungal hosts may promote the stability of these plants under climate change. However, fungal host variation is strongly linked to genetic variation within myco-heterotrophs, and therefore forming an association with a drought tolerant host may not be controlled by climate but by genetics.