Evidence for mycorrhizal cheating in Apostasia nipponica, an early‐diverging member of the Orchidaceae

Abstract

Most land plants, from liverworts to angiosperms, form mutualistic mycorrhizal symbioses with fungal partners. However, several plants known as mycoheterotrophs exploit fungal partners by reversing the polarity of carbon movement, which usually moves from plant to fungus. We investigated the physiological ecology of a photosynthetic orchid, Apostasia nipponica, which belongs to the first branching group within the Orchidaceae, to improve our understanding of mycoheterotrophic evolution in orchids. The fungal symbionts and nutrition modes of A. nipponica were investigated using molecular barcoding and carbon-13 (13 C) and nitrogen-15 (15 N) measurements, respectively. Community profiling based on a metabarcoding technique revealed that A. nipponica associates with specific Ceratobasidium spp. within ectomycorrhizas-forming clades, whereas isotope analysis revealed that A. nipponica was similar to fully mycoheterotrophic orchids in its 13 C signature and was even more enriched in 15 N than most of the fully mycoheterotrophic orchids that exploit ectomycorrhizal fungi. Our molecular and mass-spectrometric approaches demonstrated, for the first time, that a member of the Apostasioideae, the earliest-diverging lineage of the Orchidaceae, gains carbon through both photosynthesis and fungal cheating (i.e. partial mycoheterotrophy) during the adult stage.

Symbiont switching and trophic mode shifts in Orchidaceae

“…Similarly, a dual symbiotic association was also recently inferred as a prerequisite for shifts between major mycorrhizas among land plants (Werner et al, 2018). These studies collaboratively support the overall hypothesis that the evolution of symbiotic shifts follows a stepwise process, in which fungal partners in a later stage of a mycorrhizal association have been latently present in the fungal community of the ancestor (Selosse et al, 2010;van der Heijden et al, 2015;Jacquemyn & Merckx, 2019;Suetsugu & Matsubayashi, 2021).…”

“…The occurrence of mycoheterotrophy in orchids exhibits phylogenetic conservatism and is mainly confined to nine tribes in the subfamilies Vanilloideae, Orchidoideae, and Epidendroideae (Figs S5, S6). In addition, a recent study has shown that in the early divergent subfamily Apostasioideae a photosynthetic orchid species is potentially mycoheterotrophic due to its enriched 13 C and 15 N signatures (Suetsugu & Matsubayashi, 2021). As the 13 C and 15 N signatures of only few species have been investigated, and because these isotopes cannot detect low degrees of PMH in orchids, especially for those associated with rhizoctonias (Gebauer et al, 2016; Schiebold et al, 2018; Schweiger et al, 2019), the number of shifts to mycoheterotrophy may have been underestimated here.…”

Subterranean morphology modulates the degree of mycoheterotrophy in a green orchid Calypso bulbosa exploiting wood‐decaying fungi

“…We performed bioinformatic analysis using Claident v0.2.2019.05.10 (Tanabe & Toju, 2013), as described in Suetsugu and Matsubayashi (2021). In brief, the forward and reverse primer positions and sequencing reads with low quality scores (i.e.…”

“…Therefore, measurements of stable C and N isotopes can be used to estimate the degree of mycoheterotrophy (Gebauer & Meyer, 2003; Hynson et al., 2013). The proportion of fungal‐derived C has been reported to vary considerably, from as little as a few percent to as much as 90% (Bidartondo et al., 2004; Gebauer & Meyer, 2003; Julou et al., 2005; Suetsugu & Matsubayashi, 2021; Zimmer et al., 2008). In particular, leafless orchids with chlorophyllous stems obtain most of their C from their fungal partners (Suetsugu et al., 2018; Zimmer et al., 2008).…”

Integrative Study Supports the Role of Trehalose in Carbon Transfer From Fungi to Mycotrophic Orchid

“…Orchids can obtain several elements from mycorrhizal fungi, as demonstrated for carbon ( Gebauer and Meyer, 2003 ; Trudell et al, 2003 ; Suetsugu and Matsubayashi, 2021 ), nitrogen ( Gebauer and Meyer, 2003 ; Schiebold et al, 2017 ; Suetsugu and Matsubayashi, 2021 ; Valadares et al, 2021 ), phosphorus ( Alexander et al, 1984 ), hydrogen ( Schiebold et al, 2017 ; Schweiger et al, 2018 ), and oxygen ( Yoder et al, 2000 ). Most of these elements can be transferred also in other types of mycorrhizal association.…”