Mycobiont diversity and first evidence of mixotrophy associated with Psathyrellaceae fungi in the chlorophyllous orchid Cremastra variabilis

Yagame, Takahiro; Lallemand, Félix; Selosse, Marc‐André; Funabiki, Eriko; Yukawa, Tomohisa

doi:10.1007/s10265-021-01337-w

Cited by 7 publications

(12 citation statements)

References 67 publications

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“…(Psathyrellaceae) in rhizomes, which were closely related to those isolated of mature C. appendiculata in Japan for a symbiotic seed experiment ( Yagame et al 2013 ), and rhizoctonia (Ceratobasidiaceae and Serendipitaceae) in the seedling roots. Analogously to mature C. appendiculata from different populations ( Yagame et al 2021 ), we can confirm a link between subterranean root system morphology and the type of fungal partners in seedlings.…”

Section: Discussionsupporting

confidence: 70%

“…However, our results contrast to findings on C. appendiculata var. variabilis individuals from Japan, which showed the same subterranean morphology and type of mycobiont but have been proposed as ‘cryptic’ mycoheterotrophic ( sensu Hynson et al 2013 ) due to enrichment in 15 N relative to autotrophic reference plants ( Yagame et al 2021 ). Yet, mature C. appendiculata can be partially mycoheterotrophic when having already accomplished the switch from rhizoctonia fungal partners to saprotrophic non-rhizoctonia Psathyrellaceae fungi and forming coralloid rhizomes ( Suetsugu et al 2021a ; Yagame et al 2021 ), traits similar to fully mycoheterotrophic C. aphylla ( Yagame et al 2018 ; Suetsugu et al 2021a ).…”

Section: Discussionmentioning

confidence: 98%

“…seem to be substantial mycobionts involved in the mycoheterotrophic nutrition mode within the Cremastra genus. They are fungal hosts of fully mycoheterotrophic orchid C. aphylla ( Yagame et al 2018 ) and partially mycoheterotrophic mature C. appendiculata ( Suetsugu et al 2021a ; Yagame et al 2021 ). Identifying wood-/litter-decaying Coprinellus fungi as dominant mycobionts in C. appendiculata protocorm–rhizomes directly from an in situ experimental set-up is new to science but in accordance with earlier findings from symbiotic laboratory cultivation ( Yagame et al 2013 ).…”

Section: Discussionmentioning

confidence: 99%

“…variabilis individuals sampled in a cool-temperate forest in Japan were recognized to obtain approximately 83.4 ± 0.9 % of their total C demand from wood-decaying Psathyrellaceae ( Psathyrella or Coprinellus ) ( Suetsugu et al 2021a ). Though confirming partial mycoheterotrophy for several individuals with Psathyrellaceae as fungal partners, Yagame et al (2021) identified rhizoctonia (Tulasnellaceae, Ceratobasidiaceae, Serendipitaceae) as the main mycobionts of C. appendiculata var. variabilis .…”

Section: Introductionmentioning

confidence: 87%

“…Strikingly, Psathyrellaceae fungi were exclusively detected in mature C. appendiculata var. variabilis individuals with coralloid rhizomes ( Suetsugu et al 2021a ; Yagame et al 2021 ), a morphological root structure typical for mycoheterotrophic plants ( Burgeff 1932 ; Leake 1994 ), while rhizoctonia were mainly found in individuals without coralloid rhizomes ( Yagame et al 2021 ). Therefore, Yagame et al (2021) suggested an environmentally driven link between fungal partners and subterranean morphology.…”

Section: Introductionmentioning

confidence: 99%

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Fungal association and root morphology shift stepwise during ontogenesis of orchidCremastra appendiculatatowards autotrophic nutrition

2022

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Background and Aims The chlorophyllous, terrestrial orchid Cremastra appendiculata from East Asia is unique concerning its fungal mycorrhiza partners. The initially mycoheterotrophic protocorms exploit rather specialised non-rhizoctonia saprotrophic Psathyrellaceae. Adult individuals of this orchid species are either linked to Psathyrellaceae being partially mycoheterotrophic or form mycorrhiza with fungi of the ubiquitous saprotrophic rhizoctonia group. This study provides new insights on nutrition mode, subterranean morphology, and fungal partners across different life-stages of C. appendiculata. Methods We compared different development stages of C. appendiculata to surrounding autotrophic reference plants based on multi-element natural abundance stable isotope analyses (δ 13C, δ 15N, δ 2H, δ 18O) and total N concentrations. Site- and sampling-time-independent enrichment factors of stable isotopes were used to reveal trophic strategies. We determined mycorrhizal fungi of C. appendiculata protocorm, seedling, and adult samples using high-throughput DNA sequencing. Key Results We identified saprotrophic non-rhizoctonia Psathyrellaceae as dominant mycorrhizal fungi in protocorm and seedling rhizomes. In contrast, the roots of seedlings and mature C. appendiculata were mainly colonised with fungi belonging to the polyphyletic assembly of rhizoctonia (Ceratobasidium, Thanatephorus and Serendipitaceae). Mature C. appendiculata did not differ in isotopic signature from autotrophic reference plants suggesting a fully autotrophic nutrition mode. Characteristic of orchid specimens entirely relying on fungal nutrition, C. appendiculata protocorms were enriched in 15N, 13C and 2H compared to reference plants. Seedlings showed an intermediate isotopic signature, underpinning the differences in the fungal community depending on their subterranean morphology. Conclusions In contrast to the suggestion that C. appendiculata is a partially mycoheterotrophic orchid species, we provide novel evidence that mature C. appendiculata with rhizoctonia mycobionts can be entirely autotrophic. Besides an environmentally driven variability among populations, we suggest high within-individual flexibility in nutrition and mycobionts of C. appendiculata, which is subject to the ontogenetic development stage.

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Section: Discussionsupporting

confidence: 70%