Abstract:As hypothesized, it is suggested that the observed gradient in 15 N enrichment of Epipactis species is strongly driven by 15 N abundance of their mycorrhizal fungi; i.e. ɛ 15 N in Epipactis spp. associated with rhizoctonias < ɛ 15 N in Epipactis spp. with ectomycorrhizal basidiomycetes < ɛ 15 N in Epipactis spp. with ectomycorrhizal ascomycetes and basidiomycetes < ɛ 15 N in Epipactis spp. with ectomycorrhizal ascomycetes.
“…The two investigated species display different nutritional modes: E. helleborine is a partially heterotrophic (mixotrophic) orchid species (Bidartondo et al, ; Schiebold, Bidartondo, Karasch, Gravendeel, & Gebauer, ) that obtains a part of its carbon from its own photosynthesis and the other part from its mycorrhizal fungi. In this species, the fungus may provide 20%–100% of its carbon to the plant, depending on the time in the growth season (Gonneau et al, ).…”
Aim
Interactions with mycorrhizal fungi are increasingly recognized as an important factor underlying the distribution and abundance of orchid species. However, the geographical distribution of orchid mycorrhizal fungi (OMF) and how their communities vary over large geographical areas are less well understood. Because climatic and environmental similarity may decrease with geographical distance or because some OMF have limited dispersal capabilities, similarities in orchid mycorrhizal communities can be expected to decrease with increasing distances separating orchid populations. However, up till now empirical evidence is largely lacking.
Location
Eurasia.
Taxa
Gymnadenia conopsea (L.) R. Brown and Epipactis helleborine (L.) Crantz.
Methods
High‐throughput sequencing was used to perform a cross‐continental comparison of OMF that associate with two widespread Eurasian terrestrial orchids, Epipactis helleborine and Gymnadenia conopsea. Both phylogenetic and nonphylogenetic measures of community dissimilarity and their components were calculated and related to geographical distances using Mantel tests.
Results
Our results showed that in both orchid species similarity in mycorrhizal communities decreased significantly with geographical distance. Decomposing the contribution of spatial turnover and nestedness to overall dissimilarity showed that the observed dissimilarity was mainly the result of species replacement between regions, and not of species loss. Similarly, a strong relationship was observed between phylogenetic community dissimilarity and geographical distance. Decomposing PCD values into a nonphylogenetic and phylogenetic component showed that orchid populations located closely next to each other were likely to contain the same operational taxonomic units (OTUs), but that the non‐shared taxa came from different phylogenetic clades. Species indicator analyses showed that the majority of OMF OTUs were restricted to particular geographical areas. However, some OTUs occurred in both continents, indicating that some fungi have very wide distributions.
Main conclusions
Overall, these results demonstrate that orchid mycorrhizal communities differ substantially across large geographical areas, but that the distribution of orchids is not necessarily restricted by the distribution of particular OMF. Hence, widespread orchid species can be considered mycorrhizal generalists that are flexible in the OMF with which they associate across large geographical areas.
“…The two investigated species display different nutritional modes: E. helleborine is a partially heterotrophic (mixotrophic) orchid species (Bidartondo et al, ; Schiebold, Bidartondo, Karasch, Gravendeel, & Gebauer, ) that obtains a part of its carbon from its own photosynthesis and the other part from its mycorrhizal fungi. In this species, the fungus may provide 20%–100% of its carbon to the plant, depending on the time in the growth season (Gonneau et al, ).…”
Aim
Interactions with mycorrhizal fungi are increasingly recognized as an important factor underlying the distribution and abundance of orchid species. However, the geographical distribution of orchid mycorrhizal fungi (OMF) and how their communities vary over large geographical areas are less well understood. Because climatic and environmental similarity may decrease with geographical distance or because some OMF have limited dispersal capabilities, similarities in orchid mycorrhizal communities can be expected to decrease with increasing distances separating orchid populations. However, up till now empirical evidence is largely lacking.
Location
Eurasia.
Taxa
Gymnadenia conopsea (L.) R. Brown and Epipactis helleborine (L.) Crantz.
Methods
High‐throughput sequencing was used to perform a cross‐continental comparison of OMF that associate with two widespread Eurasian terrestrial orchids, Epipactis helleborine and Gymnadenia conopsea. Both phylogenetic and nonphylogenetic measures of community dissimilarity and their components were calculated and related to geographical distances using Mantel tests.
Results
Our results showed that in both orchid species similarity in mycorrhizal communities decreased significantly with geographical distance. Decomposing the contribution of spatial turnover and nestedness to overall dissimilarity showed that the observed dissimilarity was mainly the result of species replacement between regions, and not of species loss. Similarly, a strong relationship was observed between phylogenetic community dissimilarity and geographical distance. Decomposing PCD values into a nonphylogenetic and phylogenetic component showed that orchid populations located closely next to each other were likely to contain the same operational taxonomic units (OTUs), but that the non‐shared taxa came from different phylogenetic clades. Species indicator analyses showed that the majority of OMF OTUs were restricted to particular geographical areas. However, some OTUs occurred in both continents, indicating that some fungi have very wide distributions.
Main conclusions
Overall, these results demonstrate that orchid mycorrhizal communities differ substantially across large geographical areas, but that the distribution of orchids is not necessarily restricted by the distribution of particular OMF. Hence, widespread orchid species can be considered mycorrhizal generalists that are flexible in the OMF with which they associate across large geographical areas.
“…Recent analyses have revealed that partial mycoheterotrophy may be more widespread than previously assumed, as plants that were initially assumed to be autotrophic based on their 13 C signature appeared to be significantly enriched in isotopes other than 13 C (Gebauer et al, ). Using normalized enrichment factors, Schiebold, Bidartondo, Karasch, Gravendeel, and Gebauer (), for example, showed that in a large number of terrestrial orchids of the genus Epipactis , normalized enrichment factors for 15 N showed a continuous gradient from low values (<5) in so‐called ‘rhizoctonia’ orchids ( Epipactis palustris and E. gigantea ) (Figure ) to high values for species that are assumed to form orchid mycorrhizas exclusively with ectomycorrhizal ascomycetes ( E. neglecta , E. muelleri , E. leptochila and E. distans ). Similarly, normalized enrichment factors for 13 C continuously increased from zero to five (Figure ).…”
Section: Trophic Modes: a Continuum From Autotrophy To Mycoheterotrophy?mentioning
confidence: 99%
“…The green box represents the mean enrichment factors (± 1 SD ) for autotrophic reference plants that were sampled together with the Epipactis species. The red box represents mean enrichment factors (± 1 SD ) of all partially mycoheterotrophic orchid species that associate with ectomycorrhizal fungi that were reviewed by Hynson, Madsen, et al () before the publication of Schiebold et al (). (Figure reproduced from Schiebold et al, , with permission)…”
Section: Trophic Modes: a Continuum From Autotrophy To Mycoheterotrophy?mentioning
Since the early colonization of land, plants depend, to various extents, on mycorrhizal fungi to meet their nutrient demands. In most mycorrhizal symbioses, plants provide sugars derived from photosynthesis to the fungi, whereas the fungi provide essential minerals to the plant. However, in some plants, the flow of carbon has reversed and the fungi provide carbon to the plants. These plants are called mycoheterotrophs. However, it remains unclear how and under which circumstances trophic modes change and whether transitions in trophic modes are associated with changes in mycorrhizal communities.
Here, we review the available literature on mycorrhizal associations and trophic modes in plants. We first outline how trophic modes can be determined and how they differ across plants. We then investigate the evolutionary context under which mycoheterotrophy originated. We also examine the mycorrhizal communities associating with autotrophic, partially mycoheterotrophic and fully mycoheterotrophic plants within different plant families and investigate whether commonalities can be observed.
Our overview shows that mycoheterotrophy has originated more than 40 times through evolutionary time and can be found in a wide range of plant groups, including liverworts, lycophytes, ferns, monocots and dicots. Partial mycoheterotrophy appears to be much more common than previously anticipated and represents an almost continuous gradient between autotrophy and full mycoheterotrophy.
Comparison of the mycorrhizal communities associating with autotrophic, partial and full mycoheterotrophic plants indicates that, although they share some commonalities, shifts from autotrophy to full mycoheterotrophy are accompanied by either losses or shifts in mycorrhizal partners, suggesting that full or partial loss of photosynthesis selects for different mycorrhizal communities.
Synthesis. Partial mycoheterotrophy appears to be much more common than previously thought and represents an almost continuous gradient from autotrophy to full mycoheterotrophy. Evolution to full mycoheterotrophy is challenging as it requires specific adaptations and often a switch to other mycorrhizal partners. More detailed analyses of the functionality of different mycorrhizal systems co‐occurring in the roots of a single plant and the costs of mycorrhizal switching are needed to understand the precise mechanisms leading to full mycoheterotrophy.
“…The G. repens tendency to enrichment in δ 15 N compared to EcM plants is very important for this element is currently presumed to be very important in the displaying of partial heterotrophy (Schiebold et al 2017).…”
mentioning
confidence: 99%
“…The mechanism of 15 N increase in IMHOs is still unclear too (Hynson et al 2013), but for the mixotrophic genus Epipactis 15 N enrichment in plant is strongly driven by 15 N abundance of their mycobionts (Schiebold et al 2017). δ 15 N values for G. repens were rather variable, but their similarity to those for litter saprotrophic fungi was detected (Table 4).…”
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