Mycoheterotrophy evolved from mixotrophic ancestors: evidence in Cymbidium (Orchidaceae)

Motomura, Hiroyuki; Selosse, Marc‐André; Martos, Florent; Kagawa, Akira; Yukawa, Tomohisa

doi:10.1093/aob/mcq156

Cited by 96 publications

(83 citation statements)

References 34 publications

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“…The mycoheterotrophic Aphyllorchis montana and A. caudata from Thailand grow in tropical dipterocarpacean forests, and are associated with diverse ECM fungi including Sebacinales (Roy et al 2009). Ogura-Tsujita and Yukawa (in Motomura et al 2010) found a shift to exclusively ECM mycobionts, including sebacinoids, in apochlorotic, mycoheterotrophic Cymbidium species in Japan. A general conclusion was that mycoheterotrophy evolved from mixotrophic ancestors and not directly from autotrophic ones in these orchids.…”

Section: Mycoheterotrophic and Mixotrophic Orchidsmentioning

confidence: 98%

Enigmatic Sebacinales

Oberwinkler¹,

Riess²,

Bauer³

et al. 2013

Mycol Progress

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A historical retrospect and a taxonomic update will deal with Sebacina s.l. and s.str., Craterocolla, Efibulobasidium, Serendipita, Trem ell odendron, Trem ell oscypha, Tremellostereum, and Piriformospora, the Sebacinaceae, and the Sebacinales. Phylogenetic hypotheses for the order and subordinal taxa are discussed, including environmental sequence taxa. The cryptic biodiversity in Sebacinales is extensive but mostly unresolved with respect to the species involved.

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Section: Mycoheterotrophic and Mixotrophic Orchidsmentioning

confidence: 98%

Enigmatic Sebacinales

Oberwinkler¹,

Riess²,

Bauer³

et al. 2013

Mycol Progress

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“…Thus, part of their biomass is derived from mycorrhizal fungi, in a nutrition called partial mycoheterotrophy or mixotrophy (MX; see Selosse and Roy 2009 for review). MX species also occur out of Neottieae, and interestingly, MH species are often phylogenetically nested within them, e.g., in the orchid genera Platanthera (Yagame et al 2012) and Cymbidium orchids (Motomura et al 2010), and in Ericaceae (Tedersoo et al 2007). Thus, MX nutrition is often considered as a predisposition to MH evolution , and albinos furnish relevant candidates for a further step during transition to full heterotrophy.…”

Section: Introductionmentioning

confidence: 99%

Why do mixotrophic plants stay green? A comparison between green and achlorophyllous orchid individuals in situ

Roy

Gonneau

Rocheteau

et al. 2013

Ecological Monographs

123

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Abstract. Some forest plants adapt to shade by mixotrophy, i.e., they obtain carbon both from photosynthesis and from their root mycorrhizal fungi. Fully achlorophyllous species using exclusively fungal carbon (the so-called mycoheterotrophic plants) have repeatedly evolved from such mixotrophic ancestors. However, adaptations for this evolutionary transition, and the reasons why it has happened a limited number of times, remain unknown. We investigated this using achlorophyllous variants (i.e., albinos) spontaneously occurring in Cephalanthera damasonium, a mixotrophic orchid. In two populations, we compared albinos with co-occurring green individuals in situ. We investigated vegetative traits, namely, shoot phenology, dormancy, CO 2 and H 2 O leaf exchange, mycorrhizal colonization, degree of mycoheterotrophy (using 13 C abundance as a proxy), and susceptibility to pathogens and herbivores. We monitored seed production (in natural or experimental crosses) and seed germination. Albinos displayed (1) more frequent shoot drying at fruiting, possibly due to stomatal dysfunctions, (2) lower basal metabolism, (3) increased sensitivity to pathogens and herbivores, (4) higher dormancy and maladapted sprouting, and, probably due to the previous differences, (5) fewer seeds, with lower germination capacity. Over the growing season, green shoots shifted from using fungal carbon to an increasingly efficient photosynthesis at time of fruiting, when fungal colonization reached its minimum. Conversely, the lack of photosynthesis in fruiting albinos may contribute to carbon limitation, and to the abovementioned trends. With a 10 3 3 fitness reduction, albinos failed a successful transition to mycoheterotrophy because some traits inherited from their green ancestors are maladaptive. Conversely, mycoheterotrophy requires at least degeneration of leaves and stomata, optimization of the temporal pattern of fungal colonization and shoot sprouting, and new defenses against pathogens and herbivores. Transition to mycoheterotrophy likely requires progressive, joint evolution of these traits, while a sudden loss of photosynthesis leads to unfit plants. We provide explanations for the evolutionary stability of mixotrophic nutrition and for the rarity of emergence of carbon sinks in mycorrhizal networks. More broadly, this may explain what prevents the emergence of fully heterotrophic taxa in the numerous other mixotrophic plant or algal lineages recently described.

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“…of the tribe Neottieae (Bidartondo et al, 2004;Julou et al, 2005), and in Cymbidium spp. of the tribe Cymbidieae (Motomura et al, 2010). In mycoheterotrophic and mixotrophic orchids, ectomycorrhiza (ECM)-forming fungi, such as Sebacinales, Russulaceae and Thelephoraceae, are most often identified as mycobionts, suggesting that the photosynthates of nearby trees likely represent the final carbon sources.…”

Section: Introductionmentioning

confidence: 99%

Mixotrophy of Platanthera minor, an orchid associated with ectomycorrhiza‐forming Ceratobasidiaceae fungi

et al. 2011

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C, d15 N. Summary• We investigated the fungal symbionts and carbon nutrition of a Japanese forest photosynthetic orchid, Platanthera minor, whose ecology suggests a mixotrophic syndrome, that is, a mycorrhizal association with ectomycorrhiza (ECM)-forming fungi and partial exploitation of fungal carbon.• We performed molecular identification of symbionts by PCR amplifications of the fungal ribosomal DNA on hyphal coils extracted from P. minor roots. We tested for a 13 C and 15 N enrichment characteristic of mixotrophic plants. We also tested the ectomycorrhizal abilities of orchid symbionts using a new protocol of direct inoculation of hyphal coils onto roots of Pinus densiflora seedlings.• In phylogenetic analyses, most isolated fungi were close to ECM-forming Ceratobasidiaceae clades previously detected from a few fully heterotrophic orchids or environmental ectomycorrhiza surveys. The direct inoculation of fungal coils of these fungi resulted in ectomycorrhiza formation on P. densiflora seedlings. Stable isotope analyses indicated mixotrophic nutrition of P. minor, with fungal carbon contributing from 50% to 65%.• This is the first evidence of photosynthetic orchids associated with ectomycorrhizal Ceratobasidiaceae taxa, confirming the evolution of mixotrophy in the Orchideae orchid tribe, and of ectomycorrhizal abilities in the Ceratobasidiaceae. Our new ectomycorrhiza formation technique may enhance the study of unculturable orchid mycorrhizal fungi.

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Mycoheterotrophy evolved from mixotrophic ancestors: evidence in Cymbidium (Orchidaceae)

Cited by 96 publications

References 34 publications

Enigmatic Sebacinales

Enigmatic Sebacinales

Why do mixotrophic plants stay green? A comparison between green and achlorophyllous orchid individuals in situ

Mixotrophy of Platanthera minor, an orchid associated with ectomycorrhiza‐forming Ceratobasidiaceae fungi

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