Mycorrhizal Switching and the Role of Fungal Abundance in Seed Germination in a Fully Mycoheterotrophic Orchid, Gastrodia confusoides

Abstract

Mycorrhizal associations are essential for orchid germination and seedling establishment, and thus may constrain the distribution and abundance of orchids under natural conditions. Previous studies have shown that germination and seedling establishment in several orchids often decline with increasing distance from adult plants, resulting in non-random spatial patterns of seedling establishment. In contrast, individuals of the fully mycoheterotrophic orchid Gastrodia confusoides often tend to have random aboveground spatial patterns of distribution within bamboo forests. Since G. confusoides is parasitic on litter-decaying fungi, its random spatial patterns of distribution may be due to highly scattered patterns of litter-decaying fungi within bamboo forests. To test this hypothesis, we first identified the main mycorrhizal fungi associating with developing seeds and adult plants at a bamboo forest site in Taiwan using Miseq high-throughput DNA sequencing. Next, we combined seed germination experiments with quantitative PCR (qPCR) analyses to investigate to what extent the abundance of mycorrhizal fungi affected spatial patterns of seed germination. Our results show that seed germination and subsequent growth to an adult stage in G. confusoides required a distinct switch in mycorrhizal partners, in which protocorms associated with a single Mycena OTU, while adults mainly associated with an OTU from the genus Gymnopus. A strong, positive relationship was observed between germination and Mycena abundance in the litter, but not between germination and Gymnopus abundance. Fungal abundance was not significantly related to the distance from the adult plants, and consequently germination was also not significantly related to the distance from adult plants. Our results provide the first evidence that the abundance of litter-decaying fungi varies randomly within the bamboo forest and independently from G. confusoides adults.

<i>In-vitro</i> symbiotic germination of seeds of five mycoheterotrophic <i>Gastrodia</i> orchids with <i>Mycena</i> and <i>Marasmiaceae</i> fungi

“…In G. elata Blume, litter-decomposing fungi of the genus Mycena promote seed germination, whereas wood-decaying Armillaria species are associated with mature plants ( Xu & Guo, 2000 ). Such ontogenetic turnover in mycobiont associations was also observed in G. confusoides T.C.Hsu, S.W.Chung & C.M.Kuo ( Li, Boeraeve, Cho, Jacquemyn, & Lee, 2022 ). Information about the mycobionts involved in the early stages of development is needed for a comprehensive understanding of mycorrhizal symbiosis in Gastrodia and other orchid species.…”

Root-associated Fungi in Orchidaceae: Diversity, Phylogeny, Ecology, and Outstanding Questions

“…Litter decaying Mycena ( Mycenaceae ) and wood-decaying Armillaria ( Physalacriaceae ) are the dominant symbionts of the Gastrodia orchid species (Xu & Mu 1990; Xu & Guo 2000; Ogura-Tsujita et al 2009; Guo et al 2016). Litter-decaying Gymnopus (Omphalotaceae) has also recently been identified as common symbionts with adult individuals of G. confusoides within a bamboo forest (Li et al 2022). Species of the genus Gastrodia frequently change fungal partners between the seedling stage and the adult stage (Xu & Mu 1990; Li et al 2022).…”

“…Litter-decaying Gymnopus (Omphalotaceae) has also recently been identified as common symbionts with adult individuals of G. confusoides within a bamboo forest (Li et al 2022). Species of the genus Gastrodia frequently change fungal partners between the seedling stage and the adult stage (Xu & Mu 1990; Li et al 2022). Strains of Mycena and Armillaria have been successfully applied for symbiotic seed germination of fully mycoheterotrophic Gastrodia species (Xu & Guo 1989; Park & Lee 2013; Li et al 2020) and Cyrtosia septentrionalis (Umata et al 2013), as well as several autotrophic species, e.g.…”

Ectomycorrhizal Networks in the Anthropocene: From Natural Ecosystems to Urban Planning

“…In particular, the ability of CMNs to mediate the recruitment of late-stage tree seedlings under the canopies of pioneer species has been largely explored. Interplant nutrient transferring through ECM CMNs is now considered as one of the most fascinating mechanisms involved in shade tolerance of late-stage tree species, which establish during forest ontogeny ( Figure 1B ; Teste and Simard, 2008 ; Simard et al, 2012 ), and partially and fully heterotrophic plant lineages living in the undergrowth ( Figure 1B ; Li et al, 2021 ). However, we still know little about the ecological significance of these trophic interactions among neighboring trees at the forest ecosystem level.…”

“…In multi-layered forests, the co-occurrence of plants from various mycorrhizal guilds constitutes the support for the establishment of common mycorrhizal networks (CMNs) linking canopies to the undergrowth through belowground mycelia. While AM networks interconnect roots from similar or different AM species of trees to shrubs and herbaceous plants ( Wipf et al, 2019 ), fully autotrophs ECM trees exchange nutrients among each other ( Klein et al, 2016 ) and with mixotrophic and mycoheterotrophic orchids (e.g., Li et al, 2021 for orchids) and ericaceous forest plants ( Suetsugu et al, 2021 ).…”