Mixotrophic orchids do not use photosynthates for perennial underground organs

Lallemand, Félix; Figura, Tomáš; Damesin, Claire; Fresneau, Chantal; Griveau, Chantal; Fontaine, Ninon; Zeller, Bernhard; Selosse, Marc‐André

doi:10.1111/nph.15443

Cited by 24 publications

(21 citation statements)

References 38 publications

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“…Once mycorrhizal fungi have been detected and identified, the next step would be to assess their function in autotrophic, partially and fully mycoheterotrophic plants. Recent studies have shown that, in partially mycoheterotrophic orchids, carbon derived from mycorrhizal fungi mostly supports young spring shoots and below‐ground organs, whereas carbon originating from photosynthesis contributes most to sexual reproduction (Gonneau et al, ; Lallemand et al, ; Suetsugu, Ohta, & Tayasu, ). These results may explain why albino plants fail to produce similar levels of seeds than green plants, but show the same survival rates (Lallemand et al, ; Roy et al, ).…”

Section: Discussionmentioning

confidence: 99%

“…Recent studies have shown that, in partially mycoheterotrophic orchids, carbon derived from mycorrhizal fungi mostly supports young spring shoots and below‐ground organs, whereas carbon originating from photosynthesis contributes most to sexual reproduction (Gonneau et al, ; Lallemand et al, ; Suetsugu, Ohta, & Tayasu, ). These results may explain why albino plants fail to produce similar levels of seeds than green plants, but show the same survival rates (Lallemand et al, ; Roy et al, ). Using fungicides, Bellino et al () were able to eliminate the mycorrhizal fungi associating with the partially mycoheterotrophic orchid Limodorum abortivum without impairing fruit production, supporting the idea that carbon derived from fungi contributes little to sexual reproduction.…”

Section: Discussionmentioning

confidence: 99%

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Mycorrhizal symbioses and the evolution of trophic modes in plants

Jacquemyn

Merckx

2019

Journal of Ecology

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Since the early colonization of land, plants depend, to various extents, on mycorrhizal fungi to meet their nutrient demands. In most mycorrhizal symbioses, plants provide sugars derived from photosynthesis to the fungi, whereas the fungi provide essential minerals to the plant. However, in some plants, the flow of carbon has reversed and the fungi provide carbon to the plants. These plants are called mycoheterotrophs. However, it remains unclear how and under which circumstances trophic modes change and whether transitions in trophic modes are associated with changes in mycorrhizal communities. Here, we review the available literature on mycorrhizal associations and trophic modes in plants. We first outline how trophic modes can be determined and how they differ across plants. We then investigate the evolutionary context under which mycoheterotrophy originated. We also examine the mycorrhizal communities associating with autotrophic, partially mycoheterotrophic and fully mycoheterotrophic plants within different plant families and investigate whether commonalities can be observed. Our overview shows that mycoheterotrophy has originated more than 40 times through evolutionary time and can be found in a wide range of plant groups, including liverworts, lycophytes, ferns, monocots and dicots. Partial mycoheterotrophy appears to be much more common than previously anticipated and represents an almost continuous gradient between autotrophy and full mycoheterotrophy. Comparison of the mycorrhizal communities associating with autotrophic, partial and full mycoheterotrophic plants indicates that, although they share some commonalities, shifts from autotrophy to full mycoheterotrophy are accompanied by either losses or shifts in mycorrhizal partners, suggesting that full or partial loss of photosynthesis selects for different mycorrhizal communities. Synthesis. Partial mycoheterotrophy appears to be much more common than previously thought and represents an almost continuous gradient from autotrophy to full mycoheterotrophy. Evolution to full mycoheterotrophy is challenging as it requires specific adaptations and often a switch to other mycorrhizal partners. More detailed analyses of the functionality of different mycorrhizal systems co‐occurring in the roots of a single plant and the costs of mycorrhizal switching are needed to understand the precise mechanisms leading to full mycoheterotrophy.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Mycorrhizal symbioses and the evolution of trophic modes in plants

Jacquemyn

Merckx

2019

Journal of Ecology

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“…Mycoheterotrophic resources are mostly used for underground roots and rhizomes (Gonneau et al 2014): see Fig. 5 therein), as well as for elaboration of starch reserves (Lallemand et al 2019a). This explains why achlorophyllous variants produce fewer seeds (Roy et al 2013), but have good rhizome survival (Shefferson et al 2016).…”

Section: Introductionmentioning

confidence: 99%

“…grown in pots, such as E. helleborine, although every time we accessed these products (n = 2) they turned out to belong to E. palustris, a related but autotrophic species (Lallemand et al 2018). The Epipactis helleborine orchid species usually harbors a dominance of ectomycorrhizal fungi in its roots (Bidartondo et al 2004;Ogura-Tsujita and Yukawa 2008;Těšitelová et al 2012;Jacquemyn et al 2016;Jacquemyn and Merckx 2019) and, from many isotopic data, largely relies on mycoheterotrophy for its rhizome survival and growth of young shoots (Gebauer and Meyer 2003;Gonneau et al 2014;Schiebold et al 2017;Lallemand et al 2019a); Xing et al 2019), so that successful transplantation and pot culture appear unexpected.…”

Section: Introductionmentioning

confidence: 99%

Three-year pot culture of Epipactis helleborine reveals autotrophic survival, without mycorrhizal networks, in a mixotrophic species

et al. 2020

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Some mixotrophic plants from temperate forests use the mycorrhizal fungi colonizing their roots as a carbon source to supplement their photosynthesis. These fungi are also mycorrhizal on surrounding trees, from which they transfer carbon to mixotrophic plants. These plants are thus reputed difficult to transplant, even when their protection requires it. Here, we take profit of a successful ex situ pot cultivation over 1 to 3 years of the mixotrophic orchid Epipacis helleborine to investigate its mycorrhizal and nutrition status. Firstly, compared with surrounding autotrophic plants, it did not display the higher N content and higher isotopic (13 C and 15 N) abundance that normally feature mixotrophic orchids because they incorporate N-, 13 C-, and 15 N-rich fungal biomass. Second, fungal barcoding by next-generation sequencing revealed that the proportion of ectomycorrhizal fungi (expressed as percentage of the total number of either reads or operational taxonomic units) was unusually low compared with E. helleborine growing in situ: instead, we found a high percentage of rhizoctonias, the usual mycorrhizal partners of autotrophic orchids. Altogether, this supports autotrophic survival. Added to the recently published evidence that plastid genomes of mixotrophic orchids have intact photosynthetic genes, this suggests that at least some of them have abilities for autotrophy. This adds to the ecological plasticity of mixotrophic plants, and may allow some reversion to autotrophy in their evolution.

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“…Mixotrophic orchids, meeting their C demand via mycorrhizal fungi even when they are photosynthetic at the adult stage, may be the evolutionary intermediates between achlorophyllous and autotrophic orchids [15,31]. This partial myco-heterotrophy may enable orchids to adapt to the shaded environment of forests and the conditions when the photosynthetic abilities are reduced [35,36].…”

Section: Nutrient Exchange Between Orchids and Mycorrhizal Fungimentioning

confidence: 99%

New Insights into the Symbiotic Relationship between Orchids and Fungi

Yeh¹,

Chung

Liang

et al. 2019

Applied Sciences

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Mycorrhizas play an important role in plant growth and development. In mycorrhizal symbioses, fungi supply soil mineral nutrients, such as nitrogen and phosphorus, to their host plants in exchange for carbon resources. Plants gain as much as 80% of mineral nutrient requirements from mycorrhizal fungi, which form associations with the roots of over 90% of all plant species. Orchid seeds lack endosperms and contain very limited storage reserves. Therefore, the symbiosis with mycorrhizal fungi that form endomycorrhizas is essential for orchid seed germination and protocorm development under natural conditions. The rapid advancement of next-generation sequencing contributes to identifying the orchid and fungal genes involved in the orchid mycorrhizal symbiosis and unraveling the molecular mechanisms regulating the symbiosis. We aim to update and summarize the current understanding of the mechanisms on orchid-fungus symbiosis, and the main focus will be on the nutrient exchange between orchids and their fungal partners. Appl. Sci. 2019, 9, 585 2 of 14 sheath, which functions as a plant-fungus interface, surrounding the epidermal and outer cortical cells. The interface is used for the bidirectional nutrient transfer between a plant and its fungal partner [7]. (2) Endomycorrhiza: the fungi possess specific types of hyphae such as arbuscules and coils to penetrate and grow inside of the root cells of host plants [3]. Endomycorrhizas can be further classified as ectendomycorrhizas, ericoid, arbutoid, monotropoid, orchid and arbuscular mycorrhizas based on the specificity of plant families and the type of internal hyphae [3,8]. Ectomycorrhizas are also alternatively represented as arbuscular mycorrhizas because the class is the most prevalent type of mycorrhizae, as shown in approximately 71% of all vascular plant species [1,9].The Orchidaceae is the largest family of flowering plants including over 700 genera and about 30,000-35,000 species and still hundreds of new species displaying variable floral features, lifestyles, habitat distributions and trophic patterns are being discovered and developed every year [10,11]. Mycorrhizas in orchid species are highly important throughout their whole life including germination and further development. In this article, we provide a brief review of the roles of mycorrhizas in orchid growth and development and the current understanding of the mechanisms in nutrient exchange between orchids and their fungal partners.

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Mixotrophic orchids do not use photosynthates for perennial underground organs

Cited by 24 publications

References 38 publications

Mycorrhizal symbioses and the evolution of trophic modes in plants

Mycorrhizal symbioses and the evolution of trophic modes in plants

Three-year pot culture of Epipactis helleborine reveals autotrophic survival, without mycorrhizal networks, in a mixotrophic species

New Insights into the Symbiotic Relationship between Orchids and Fungi

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