Evolution of mycoheterotrophy in Polygalaceae: The case of <i>Epirixanthes</i>

Mennes, Constantijn B.; Moerland, Michelangelo Sergio; Rath, Magnus; Smets, Erik; Merckx, Vincent

doi:10.3732/ajb.1400549

Cited by 11 publications

(16 citation statements)

References 51 publications

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“…Within the genus Burmannia , the fully mycoheterotrophic species are all associated with Glomeraceae fungi, which are a subset of the fungal associates of the autotroph Burmannia capitata (Merckx et al, ; Suetsugu et al, ; Ogura‐Tsujita et al, ; Figure b). A similar pattern is observed for Petrosavia – Japonolirion (Petrosaviaceae; Yamato et al, ) and Epirixanthes – Salomonia (Polygalaceae; Mennes et al, ), which suggests that the shift from autotrophy to full mycoheterotrophy in arbuscular mycorrhizal lineages occurs in parallel with an increased specificity towards fungi which were already present in the mycorrhizal communities of the autotrophic ancestor.…”

Section: Mycorrhizal Fungi Associated With Shifts In Trophic Modessupporting

confidence: 60%

“…Mycorrhizal associates of Burmannia coelestis, a species capable of partial mycoheterotrophy (Bolin et al, ), have not been characterized yet. Other lineages, such as Petrosaviaceae and Polygalaceae, show a similar trend (Mennes et al, ; Yamato et al, ). (c) Initial mycoheterotrophy likely evolved in the common ancestor of Orchidaceae, in parallel with a shift from arbuscular mycorrhizas to orchid mycorrhizas (Yukawa et al, ).…”

Section: Multiple Origins Of Full Mycoheterotrophymentioning

confidence: 66%

“…While some lineages of fully mycoheterotrophic species are evolutionary ‘isolated’ and diverged from their most closely related photosynthetic relatives many million years ago (e.g. Voyria; Merckx, Kissling, et al, , Corsiaceae; Mennes, Moerland, Rath, Smets, & Merckx, ), several fully mycoheterotrophic species have close photosynthetic relatives, which are confirmed as, or candidates for, partial mycoheterotrophs (e.g. Motomura et al, ).…”

Section: Multiple Origins Of Full Mycoheterotrophymentioning

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: Mycorrhizal Fungi Associated With Shifts In Trophic Modessupporting

confidence: 60%

Section: Multiple Origins Of Full Mycoheterotrophymentioning

confidence: 66%

Section: Multiple Origins Of Full Mycoheterotrophymentioning

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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“…For this purpose, we considered the 15 independent shifts towards mycoheterotrophy represented by our data (Supporting Information Table S1). Based on recent phylogenetic insights, we considered four independent shifts in Gentianaceae represented by the genera Voyria , Voyriella , Exacum and Exochaenium (Merckx et al, ), two shifts in Ericaceae including Monotropoideae and Pyrola (Freudenstein, Broe, & Feldenkris, ), and a single shift in Polygalaceae: Epirixanthes (Mennes, Lam, et al, ), Liliales: Corsiaceae (Mennes, Moerland, Rath, Smets, & Merckx, ), Petrosaviaceae: Petrosavia (Cameron, Chase, & Rudall, ), Triuridaceae (Mennes, Smets, Moses, & Merckx, ) and Iridaceae: Geosiris (Goldblatt et al, ). In Dioscoreales, we recognized three shifts: Afrothismia , Thismiaceae s.s. and Burmanniaceae (Merckx et al, ).…”

Section: Methodsmentioning

confidence: 99%

Global distribution patterns of mycoheterotrophy

Gomes

Bodegom

Merckx

et al. 2019

Global Ecol Biogeogr

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Aim Mycoheterotrophy is a mode of life where plants cheat the mycorrhizal symbiosis, receiving carbon via their fungal partners. Despite being widespread, mycoheterotrophic plants are locally rare, hampering the understanding of their global environmental drivers. Here, we explore global environmental preferences of mycoheterotrophy, and investigate environmental drivers of differential habitat preferences of mycoheterotrophic plants associated with arbuscular (AM) and ectomycorrhizal (EM) fungi. Location Global. Time period Current. Major taxa studied Mycoheterotrophic flowering plants. Methods We compiled the largest global dataset of epiparasitic mycoheterotrophic plant species occurrences and examined which environmental factors, including soil type, climate, vegetation type and distribution patterns of mycorrhizal autotrophic plants, relate to occurrence patterns of mycoheterotrophic plant species associated with AM and EM fungi. Results Mycoheterotrophic plant species avoid cold and highly seasonal climates and show a strong preference for forests. AM‐associated mycoheterotrophs are predominantly found in broadleaved tropical evergreen forests whereas EM‐associated mycoheterotrophs occur in temperate regions, mostly in broadleaved deciduous and evergreen needleleaved forests. The abundance of AM and EM autotrophic plants was a weaker predictor for mycoheterotrophs occurrences than forest type. Temperature and precipitation variables – but not edaphic factors – were the best predictors explaining the distribution patterns of mycoheterotrophs after accounting for the effects of forest type. For individual lineages, major differences in environmental preferences (often related to edaphic factors) occurred that were significantly associated with plant evolutionary relationships, indicating that these cheater plants have limited adaptive capabilities. Main conclusions The strong global geographical segregation of AM and EM mycoheterotrophs does not reflect the abundance of their potential autotrophic hosts, but seems to be driven by differential climate and habitat preferences. Our results highlight the non‐trivial nature of mycorrhizal interactions, and indicate that identity of the partners is not enough to understand the underlying mechanisms promoting plant–fungal interactions in mycoheterotrophic plants.

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“…It is sister to the autotrophic genus Salomonia Lour. with which it shares several synapomorphies such as spike-like terminal inflorescence and three antesepalous stamen primordia (Van der Meijden, 1988;Mennes et al, 2015). Members of the genus are generally tiny plants with reduced bract-like leaves and dense spike-like inflorescences (Van der Meijden, 1988).…”

Section: Introductionmentioning

confidence: 99%

Novitates Bruneienses, 9. A synopsis of Epirixanthes (Polygalaceae) in Brunei Darussalam and notes on species elsewhere

Dančák¹,

Sukri²,

Metali³

et al. 2017

GBS

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ABSTRACT. The genus Epirixanthes Blume is revised for Brunei Darussalam. Four species are recognised for the country: Epirixanthes cylindrica Blume, E. elongata Blume, E. kinabaluensis T.Wendt and E. papuana J.J.Sm., with the two latter species being newly recorded for the Brunei flora. A single collection from Brunei that was formerly identified as Epirixanthes pallida T.Wendt is now confirmed as E. papuana. A revised key for the genus is included.

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Evolution of mycoheterotrophy in Polygalaceae: The case of Epirixanthes

Cited by 11 publications

References 51 publications

Mycorrhizal symbioses and the evolution of trophic modes in plants

Mycorrhizal symbioses and the evolution of trophic modes in plants

Global distribution patterns of mycoheterotrophy

Novitates Bruneienses, 9. A synopsis of Epirixanthes (Polygalaceae) in Brunei Darussalam and notes on species elsewhere

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