Further evidence of Ceratobasidium D.P. Rogers (Basidiomycota) serving as the ubiquitous fungal associate of Platanthera leucophaea (Orchidaceae) in the North American tallgrass prairie

Abstract

Background: In the United States and Canada, ca. one-half of native orchid species are now threatened with extinction. A number of these species are restricted to tallgrass prairies of central North America, such as the Eastern Prairie Fringed Orchid, Platanthera leucophaea (Nutt.) Lindl.-a U.S. Federally threatened species. Results:We provide new records of fungi recovered from roots of P. leucophaea and five other orchid species inhabiting prairie sites in Illinois and neighboring states during a 10-year period (2008)(2009)(2010)(2011)(2012)(2013)(2014)(2015)(2016)(2017). A total of 39 fungal endophytes were isolated from Cypripedium candidum (1), Platanthera lacera (1), P. leucophaea (32), P. peramoena (3), Spiranthes lacera (1), and S. magnicamporum (1), 31 (79%) of which were assignable to Ceratobasidium and the remainder to Tulasnella. These fungi were acquired from 16 different sites, 13 of which are new records including two new state records (Iowa, Wisconsin). Molecular analysis revealed that some Ceratobasidium strains were virtually identical despite being geographically isolated by > 300 km. Conclusions:This study, encompassing a decade of work, confirms that Platanthera leucophaea is a mycorrhizal specialist with heavy reliance on Ceratobasidium with the tallgrass prairie ecosystem of North America. Our isolation of Ceratobasidium from P. leucophaea spanning additional sites suggests that the association is widespread. Such information should provide conservationists and land managers with more confidence in developing protocols that facilitate the long-term conservation of this prairie orchid.

Progress and Prospects of Mycorrhizal Fungal Diversity in Orchids

“…The OM specificity may be affected by environmental factors, climate changes, extreme host selections, evolutionary history, accompanying plant species, biocompatibility, biogeographic range, and density of OMF in the soil or, for epiphytes, Frontiers in Plant Science | www.frontiersin.org phorophytes (Jacquemyn et al, 2011b(Jacquemyn et al, , 2017aMcCormick et al, 2012McCormick et al, , 2018Pandey et al, 2013;Waud et al, 2016a;Shefferson et al, 2019;Xing et al, 2019), thus showing strong and complex variations. For example, Neottia and Caladenia prefer symbiosis with sebacinales fungi (Těšitelová et al, 2015;Phillips et al, 2016;Reiter et al, 2020); the rare terrestrial orchid Caladenia huegelii specifically associates with Serendipita (= Sebacina) vermifera (Swarts et al, 2010); Cypripedium, Ophrys, and Chiloglottis prefer Tulasnellaceae (Shefferson et al, 2005(Shefferson et al, , 2019Roche et al, 2010;Schatz et al, 2010); Dendrobium nobile and Liparis japonica have high specificity for Tulasnellaceae (Ding et al, 2014;Xing et al, 2017); Pterostylis nutans and Sarcochilus weinthalii are only symbiotic with Ceratobasidium fungi (Irwin et al, 2007;Graham and Dearnaley, 2012); Platanthera leucophaea tends to be associated with Ceratobasidium fungi over a 10-year period (Thixton et al, 2020); Corallorhiza trifida shows high specificity for Thelephoraceae in different countries and varied habitats (McKendrick et al, 2000;Zimmer et al, 2008). Jacquemyn et al (2010) asserted the possibility of promoting widespread associations between orchids and available OMF in an environment devoid of water and nutrients.…”

“…Mycorrhizal specificity does not limit the distribution range or rarity of at least some orchids (Shefferson et al, 2007;Phillips et al, 2011Phillips et al, , 2016Bailarote et al, 2012;Pandey et al, 2013;Waud et al, 2017), since specificity for a widespread fungus is not limitative. Indeed, OMF associated with orchids exhibiting high mycorrhizal specificity tend to have a wide distribution (Jacquemyn et al, 2011b;Swift et al, 2019;Thixton et al, 2020). Even OMF promoting the germination of narrowly distributed orchids may display a wider distribution (Oktalira et al, 2019).…”

How Mycorrhizal Associations Influence Orchid Distribution and Population Dynamics

“…Serendipitaceae are also widely distributed, shared by orchids and their accompanying plants in several habitats, or serving as a beneficial growth-promoting fungus for a wide range of agricultural crops (e.g., Davis et al, 2015;Jacquemyn et al, 2015a;Fritsche et al, 2020;Reiter et al, 2020). While Platanthera leucophaea, which is protected by the United States federal government, is highly dependent on Ceratobasidium in the tallgrass prairie ecosystems of North America, Ceratobasidium species has also been isolated from various orchid species found in other locations (Thixton et al, 2020). Similarly, two rare Orchis sister species have high specificity for the dominant fungal symbiont Tulasnella helicospora, even though this fungus is found across the world (Calevo et al, 2020).…”

Environmental and Management Effects on Demographic Processes in the U.S. Threatened Platanthera leucophaea (Nutt.) Lindl. (Orchidaceae)

“…following burning. The association of Ceratobasidium fungi with P. leucophaea in prairie habitats may correspond to the fire dependency of this habitat, how fire cycles soil nutrients, and subsequent effects on both Ceratobasidium and P. leucophaea [ 45 ]. Likewise, the closely related species, P. praeclara , also associates primarily with Ceratobasidium fungi in fire-dependent prairie habitat [ 75 ].…”

“…Protocorms ( Figure 4 ) remain underground for 1–3 years as obligate mycotrophs until they initiate a solitary strap leaf early in the growing season ( Figure 4 ). The mature root system consists of a starch-filled elongated tuber positioned beneath 3–10 narrow, brittle lateral roots that harbor mycorrhizal fungi, mostly free-living saprophytes in the genus Ceratobasidium (Basidiomycota, Cantharellales) [ 45 , 46 , 47 ]. The persistence of Ceratobasidium in roots, even after leaves are formed, suggests that P. leucophaea augments photosynthesis with mycotrophy throughout its life.…”