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• W3010845174 abstract "Most land plants, from liverworts to angiosperms, form mutualistic arbuscular mycorrhizal (AM) symbioses with Glomeromycotina (Smith & Read, 2008). Plants gain essential mineral nutrients from their mycorrhizal partners in exchange for photosynthesis-derived carbon (Smith & Read, 2008). Nonetheless, mutualisms, including mycorrhizal ones, allow exploitation by a third lineage (cheating strategies; Bronstein, 2001; West et al., 2007). Mycorrhizas represent a diffuse symbiosis, wherein a single plant simultaneously associates with multiple fungi and each fungus concurrently associates with multiple plants (Simard et al., 2012). It has been suggested that when several partners interact, natural selection favors the less-mutualistic partners that obtain more benefits while paying fewer costs, leading to the potential disruption of cost–benefit balances (Bronstein, 2001; Walder & van der Heijden, 2015). Theoretical models predict that the evolutionary stability of mutualism is greatly enhanced when participants employ mechanisms to prevent excessive exploitation by the other (Bronstein, 2001; West et al., 2007). The reciprocally regulated exchange of resources has thus been considered the main factor stabilizing mutualism and the evolutionary maintenance of AM symbiosis (Kiers et al., 2011; Walder & van der Heijden, 2015). Despite this, numerous examples exist of nonphotosynthetic mycorrhizal plants targeting AM fungi without suffering sanction (Merckx & Freudenstein, 2010; Selosse & Rousset, 2011). Several green plants obtain carbon through both photosynthesis and mycorrhizal fungi; this dual nutritional strategy is called mixotrophy (Selosse & Roy, 2009). Mixotrophic plants can be divided into two types: those that employ mycoheterotrophy in the early stages and later develop full autotrophy (initial mycoheterotrophy) and those that, although being photosynthetic, maintain a partially mycoheterotrophic nutrition throughout their life cycle (partial mycoheterotrophy; Merckx, 2013; Gomes et al., 2017). Since some species with initial mycoheterotrophy can stay partially mycoheterotrophic at adult stage, several studies suggest that the evolution of initial mycoheterotrophy is the first step in the evolutionary path toward partial and full mycoheterotrophy (Selosse & Roy, 2009; Hynson et al., 2013; Jacquemyn & Merckx, 2019). Initial mycoheterotrophy associated with AM fungi is not limited to angiosperms, with most members of Lycopodiaceae, some Schizaeaceae, one Gleicheniaceae, and all Ophioglossaceae and Psilotaceae (adding up to > 1000 species) having subterranean, mycoheterotrophic gametophytes (Winther & Friedman, 2007, 2008, 2009). These lineages could have yielded undocumented partial mycoheterotrophy (Selosse & Roy, 2009; Hynson et al., 2013). Here, we focused on the adder's tongue fern Ophioglossum, which produces subterranean, mycoheterotrophic gametophytes. Intriguingly, the sterile leaf is lacking at the sporophytic stage in some species such as Ophioglossum kawamurae (Fig. 1 (inset) and Supporting Information Fig. S1; Tagawa, 1939). The photosynthetic ability of fertile leaves is substantially lower than that of sterile leaves in many ferns (Britton & Watkins, 2016); hence, O. kawamurae could be mixotrophic at the adult sporophytic stage, thereby compensating for its reduced photosynthetic ability. The abundance of natural stable isotopes facilitates the assessment of the degree of mycoheterotrophy in orchidaceous and ericaceous species (Gebauer & Meyer, 2003) since their main symbionts are enriched in carbon-13 (13C) and nitrogen-15 (15N) abundance; this is reflected in the isotopic signatures of mycoheterotrophic plants (Gebauer & Meyer, 2003). However, 13C and 15N abundance is of limited use as an assessment tool for plants associated with AM fungi (Selosse et al., 2017), since these fungi have isotopic signatures similar to those of their surrounding autotrophic plants (Courty et al., 2011). However, 13C abundance is still a powerful tool to detect mixotrophy associated with AM fungi in plant communities harboring C4 plants because C4 plants have significantly higher δ13C values than C3 plants (O'Leary, 1988) and the δ13C values of AM fungi mirror those of the surrounding plants acting as carbon donors (Courty et al., 2011). Therefore, significant 13C enrichment would be a strong indicator of carbon transfer from the C4 plants to the candidate taxa through a common AM network in mixed habitats containing both C3 and C4 plants (Bolin et al., 2017). Here, we investigated whether adult O. kawamurae plants obtain carbon through a common AM mycorrhizal network. The field studies were conducted at two sites in Kushima City, Miyazaki Prefecture, Japan, on 20 May 2017, and Hikawa Town, Kumamoto Prefecture, Japan, on 22 May 2017, Japan. The Miyazaki site was dominated by Imperata cylindrica (Poaceae, C4 plant), Zoysia pacifica (Poaceae, C4 plant), Gamochaeta coarctata (Asteraceae, C3 plant), Sisyrinchium rosulatum (Iridaceae, C3 plant), and Vulpia myuros (Poaceae, C3 plant), while the Kumamoto site was dominated by Zoysia matrella (Poaceae, C4 plant) and G. coarctata (C3 plant). These C4 grasses accounted for > 50% of the total vegetation cover. After sample collection, we investigated the existence of a common network of AM fungi in the mycorrhizal partners of O. kawamurae and the neighboring C3 and C4 plants, through molecular identification of mycorrhizal fungi (see Methods S1). We also determined whether O. kawamurae plants had significantly higher δ13C values than the surrounding C3 plants and other Ophioglossum species growing in habitats containing both C3 and C4 plants (see Methods S1). Molecular identification of mycorrhizal fungi detected 68 AM operational taxonomic units (OTUs; 320 836 reads). Ophioglossum kawamurae, O. parvum, G. coarctata, and Z. matrella (Poaceae), respectively, presented 35, 46, 64 and 50 AM OTUs (Fig. 1). In addition, each plant species shared > 20 AM OTUs with other plant species, whereas no or very few AM symbionts were unique to each plant species (Fig. 1). The numbers of AM symbionts shared were 27 between O. kawamurae and O. parvum, 32 between O. kawamurae and G. coarctata, and 25 between O. kawamurae and Z. matrella (Fig. 1; Tables S1). This indicated that some AM fungi associated with O. kawamurae and O. thermale were also associated with the adjacent C3 and C4 plants, so that Ophioglossum species and surrounding C3 and C4 plants were linked by a common mycorrhizal network. As Glomeromycotina are completely reliant on their plant partners for organic carbon to complete their life cycle (Smith & Read, 2008), the link between these fungi and O. kawamurae provides a potential mechanism for mixotrophy in O. kawamurae. Although Ophioglossum spp. are C3 plants (Field et al., 2015b), the δ13C values of O. kawamurae (−26.8 ± 1.1‰; mean ± SD) were significantly higher than those of the C3 autotrophic reference plants (−29.9 ± 0.2‰, P < 0.001), O. parvum (−27.8 ± 1.0‰, P = 0.03) and O. thermale (−28.0 ± 0.8‰, P = 0.01, Table S2) at the Miyazaki site. Similarly, the δ13C values were significantly higher in O. kawamurae (−26.7 ± 1.2‰) than in both the C3 autotrophs G. coarctata (−30.2 ± 0.3‰, P < 0.001) and O. parvum (−29.5 ± 1.2‰, P < 0.001) at the Kumamoto site (Fig. 2; Table S3). These 13C abundance data suggest carbon transfer from C4 plants through a common AM network. At the Miyazaki site, the δ13C values for O. parvum and O. thermale, each of which bears one expanded photosynthetic leaf, were also significantly higher than those of the two co-occurring C3 plants (P < 0.001). Therefore, Ophioglossum species with developed photosynthetic leaves might also be facultatively mixotrophic. Alternatively, differences in stomatal aperture control and carbon allocation to belowground parts may influence δ13C values, given the marked evolutionary divergence between ferns and reference plants (Field et al., 2015b; Porter et al., 2017). However, this is unlikely at least for O. kawamurae, because we found that the δ13C values of O. kawamurae were significantly higher, even compared to those of the other sympatric Ophioglossum species with a developed photosynthetic leaf in both Miyazaki and Kumamoto, and the δ13C values of O. thermale in Kumamoto were not significantly different from those of the C3 reference plant G. coarctata. Therefore, we consider mixotrophy to be the most likely explanation for the 13C enrichment observed in O. kawamurae, because it has higher δ13C values than the phylogenetically close species that should be physiologically similar. In fact, some orchids and pyroloids with rudimentary leaves are more dependent on a mycoheterotrophic mode of nutrition than closely related mixotrophic species with developed leaves (Shutoh et al., 2016; Suetsugu et al., 2018). However, it is impossible to completely exclude the confounding phylogenetic effects. Samples of O. kawamurae from C3-only vegetation would allow the exclusion of any idiosyncratic 13C abundance in Ophioglossum species. Unfortunately, O. kawamurae is very rare, with only three extant populations, whose dominant surrounding plants are C4. Labeling experiments will be needed to conclusively confirm partial mycoheterotrophy in O. kawamurae. The exploitation of fungi has evolved independently many times in angiosperms (Merckx & Freudenstein, 2010), most notably in the Orchidaceae, which contains > 200 examples of fully mycoheterotrophic species (Merckx & Freudenstein, 2010; Merckx, 2013). A distinct feature of this family is the production of numerous minute seeds that initially depend on fungal associations (Leake et al., 2008). Their initial mycoheterotrophic nature arguably makes them particularly predisposed to the evolution of life-long (partial or full) mycoheterotrophy. Similar transitions to life-long mycoheterotrophy have been documented in other plant taxa, including the Ericaceae and Burmanniaceae, which also produce dust seeds and exhibit initial mycoheterotrophy (Hynson et al., 2009; Hashimoto et al., 2012; Bolin et al., 2017). The genus Ophioglossum is also known to produce millions of minute spores that develop into subterranean, mycoheterotrophic gametophytes. Its life history could be considered analogous to that of the orchids and pyroloids that produce dust seeds (Leake et al., 2008). Therefore, convergent evolutionary pathways have probably led to life-long partial and full mycoheterotrophy in both a fern and multiple lineages of angiosperms. Interestingly, fully achlorophyllous leaf-bearing variants of some ferns and lycophytes that exhibit (at least) initial mycoheterotrophy can survive (Bruce & Beitel, 1979; Johnson-Groh & Lee, 2002). Normal green variants of such species might also obtain significant amounts of carbon from their mycorrhizal fungi, as described for albino variants occurring in mixotrophic orchids (Julou et al., 2005; Suetsugu et al., 2017). Therefore, mixotrophy in ferns and lycophytes may be more common than hitherto believed. Typically, both plant and AM fungal partners regulate resource delivery to favor beneficial symbionts, leading to a strictly reciprocal resource exchange (Kiers et al., 2011). Although plants that have evolved an initially mycoheterotrophic and later autotrophic life history, including many ferns and lycophytes, seem to disrupt this model of evolutionary stability, AM symbiosis could be maintained on a ‘take now, pay later’ basis in these plants (Leake et al., 2008; Field et al., 2015a,b). However, such delays very likely provide a window for exploitation by species that can acquire the resource without reward. This is because it would be much more difficult for such AM fungal partners to identify beneficial symbionts, due to the long time lags in reward provision. Our study suggests that life-long fungal exploitation has in fact evolved in a fern lineage initially exhibiting mycoheterotrophy followed by autotrophy later in the life history, allowing the plants to exploit the AM fungus without being sanctioned. However, because most species exhibiting initial mycoheterotrophy do not appear to prolong their fungal dependence throughout life history (Leake et al., 2008; Field et al., 2015a,b), carbon gain through photosynthesis is likely to be a more effective strategy under most circumstances. Further study is therefore required to understand the evolutionary stability of the ‘take now, pay later’ mutualist strategy, and the factors that can lead to its corruption in favor of life-long mycoheterotrophy. Th authors thank Drs Jakub Těšitel, Marc-André Selosse and two anonymous reviewers for their constructive comments on earlier versions of the manuscript. The authors thank Nobuyuki Inoue, Tadashi Minamitani, Masato Watanabe, and Masayuki Takamiya for help with the field study. This work was financially supported by JSPS Kakenhi, grant nos. 17H05016 (KS) and 16H02524 (IT). The present study was also supported by a Joint Usage/Research Grant from the Center for Ecological Research, Kyoto University. KS planned and designed the research, collected the materials, conducted the laboratory experiments, carried out analyses, and wrote the initial draft. ST, AST, TFH and HT conducted the laboratory experiments, carried out analyses, and revised the manuscript. IT supervised the isotopic experiments and revised the manuscript. The sequence data were deposited in the Sequence Read Archive of the DNA Data Bank of Japan (accession no. DRA009261). In addition, further information can be found online in the Supporting Information section at the end of the article. Fig. S1 Mature Ophioglossum plants in their natural habitats. Methods S1 Methods used to conduct stable isotope analysis and molecular identification of mycorrhizal fungi. Table S1 The number of sequences of mycorrhizal fungi that were unique to Ophioglossum kawamurae, O. parvum, Gamochaeta coarctata and Zoysia matrella, or shared among O. kawamurae, O. parvum, G. coarctata, and Z. matrella. Table S2 Values of δ13C in each individual of Ophioglossum kawamurae, O. parvum, O. thermale and surrounding autotrophic plant species obtained from Miyazaki. Table S3 Values of δ13C in each individual of Ophioglossum kawamurae, O. parvum and surrounding autotrophic plant species obtained from Kumamoto. Please note: Wiley Blackwell are not responsible for the content or functionality of any Supporting Information supplied by the authors. Any queries (other than missing material) should be directed to the New Phytologist Central Office. Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article." @default.
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• W3010845174 title "Isotopic and molecular data support mixotrophy in <i>Ophioglossum</i> at the sporophytic stage" @default.
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