Mycorrhizal communities of two closely related species, Pyrola subaphylla and P. japonica, with contrasting degrees of mycoheterotrophy in a sympatric habitat

Suetsugu, Kenji; Matsuoka, Shiro; Shutoh, Kohtaroh; Okada, Hidehito; Taketomi, Shintaro; Onimaru, Kaede; Tanabe, Akifumi S.; Yamanaka, Hiroki

doi:10.1007/s00572-020-01002-5

Cited by 10 publications

(8 citation statements)

References 60 publications

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“…They are wintergreen and form ectendomycorrhizas, generally occurring in coniferous and mixed deciduous forests in Japan. These species are partially mycoheterotrophic, primarily associating with ectomycorrhizal fungi in the genus Russula , although P. subaphylla appears more strongly restricted to this group (Matsuda et al., 2020; Suetsugu, Matsuoka, et al., 2021). In previous research on populations of both species (including our study populations), P. subaphylla demonstrated 13 C and 15 N enrichment comparable to levels expected of full mycoheterotrophs, while P. japonica exhibited 13 C enrichment significantly lower than that expected for full mycoheterotrophs, suggesting a stronger reliance on autotrophy in the latter (Shutoh et al., 2020; Shutoh, Kurosawa, & Kaneko, 2016).…”

Section: Methodsmentioning

confidence: 99%

“…Therefore, it is essential to investigate mycoheterotrophic evolution that occurred during actual speciation, in addition to studying non‐photosynthetic mutants, to gain a comprehensive understanding of this phenomenon. As far as we are aware, a microevolutionary study of closely related species differing in trophy has not been conducted due to the very limited number of sympatric, closely related taxa exhibiting contrasting levels of mycoheterotrophy (Suetsugu, Matsuoka, et al., 2021).…”

Section: Introductionmentioning

confidence: 99%

“…P. japonica and P. subaphylla are suitable taxa to investigate the changes associated with mycoheterotrophic evolution because they differ significantly in their levels of mycoheterotrophy and because recent systematic research suggests that they are sister species (e.g. Shutoh, Kaneko, et al., 2016; Suetsugu, Matsuoka, et al., 2021). Pyrola subaphylla , which often only produces rudimentary, scale‐like leaves, appears to be fully or almost fully mycoheterotrophic based on stable carbon and nitrogen isotope analyses (Shutoh et al., 2020; Shutoh, Kurosawa, & Kaneko, 2016).…”

Section: Introductionmentioning

confidence: 99%

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Life history costs drive the evolution of mycoheterotrophs: Increased sprouting and flowering in a strongly mycoheterotrophic Pyrola species

Shefferson,

Shutoh,

Suetsugu

2024

Journal of Ecology

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Land plants are typically photosynthetic, but some species have lost the ability to photosynthesize, instead relying on mycorrhizal fungi to obtain carbon. Increasing levels of partial mycoheterotrophy, in which seemingly autotrophic plants receive fungal carbon from their fungal partners, and reduced sprouting in concert with greater reproduction when sprouting, may be intermediate steps in the evolution of this trait. We studied the microevolutionary demography of Pyrola japonica and the closely related species P. subaphylla, which are currently considered sister species. While these species are both partially mycoheterotrophic, P. subaphylla is more strongly so, indicating that it may be closer to evolving full mycoheterotrophy. We tracked individuals in two nearby populations in Fukushima, Japan from 2015 to 2020. We analysed vital rates, population trends and long‐run population structure with historical function‐based matrix projection models. We assessed how shifts in P. subaphylla demography relate to fitness using a stochastic life table response experiment (SLTRE). P. subaphylla exhibited strong costs of growth to survival and of reproduction to sprouting, size and fecundity. It sprouted more than P. japonica but to smaller stages. P. subaphylla's flowering frequency was approximately four times that of P. japonica, but after flowering it was smaller and more likely to die. These life history costs appeared to drive differences in fitness, measured as stochastic population growth rate. Relative to P. japonica, shifts in fitness in P. subaphylla were due more to shifts in means than standard deviations of matrix elements. Shifts in growth transitions had the strongest negative impacts on fitness but also had the strongest positive impacts. Increased shifts to small non‐flowering stages were associated with increased fitness, while transitions involving dormancy were associated more strongly with drops in fitness. Synthesis. As far as we are aware, we found the first evidence that costs of growth and reproduction drive the evolution of increased sprouting and smaller size as a species becomes more intensely mycoheterotrophic. Surprisingly, vegetative dormancy did not evolve with mycoheterotrophy. We suggest further studies assessing whether these seemingly maladaptive trends result from genetic drift, genetic linkage or another mechanism.

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Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Life history costs drive the evolution of mycoheterotrophs: Increased sprouting and flowering in a strongly mycoheterotrophic Pyrola species

Shefferson,

Shutoh,

Suetsugu

2024

Journal of Ecology

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“…We used nine plant species: five AM-associated species (Magnolia obovata, Cerasus jamasakura, Viburnum dilatatum, Viburnum furcatum, and Aesculus turbinata) and four ECM-associated species (Pinus densiflora, Betula platyphylla, Quercus crispula, and Quercus serrata) [12][13][14][15][16]. The natural population densities of ECM-associated species are higher than those of AM-associated species (Table S1) [17].…”

Section: Experimental Speciesmentioning

confidence: 99%

Evolutionary relations between mycorrhizal symbiosis and plant–plant communication in trees

Yamawo

Hagiwara

Yoshida

et al. 2022

Preprint

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Ecological factors that drive the evolution of plant-plant communication via volatile organic compounds (VOCs) have not been elucidated. Here, we examined the relationship between type of mycorrhizal symbiosis (arbuscular mycorrhiza, AM; ectomycorrhizal mycorrhiza, ECM) and plant-plant communication within tree species. We hypothesized that ECM promotes plant-plant communication among conspecific individuals in trees, because it promotes their cooccurrence through positive plant-soil feedback. We tested communication using saplings of nine tree species with either AM or ECM, either exposed for 10 days to volatiles from an injured conspecific or not exposed. We evaluated the number of insect-damaged leaves and the area of leaf damage after 1 and 2 months in the field. Most exposed ECM-associated trees had less leaf damage than controls. However, AM-associated trees did not differ in leaf damage between treatments. We combined our results with those of previous studies and analysed the evolutionary relation between mycorrhizal type and the presence or absence of plant-plant communication within tree species. ECM symbiosis is associated with the evolution of plant-plant communication within species. These results suggest that the evolution of types of mycorrhizal symbiosis associates with the evolution of plant-plant communications within tree species.

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“…In multi-layered forests, the co-occurrence of plants from various mycorrhizal guilds constitutes the support for the establishment of common mycorrhizal networks (CMNs) linking canopies to the undergrowth through belowground mycelia. While AM networks interconnect roots from similar or different AM species of trees to shrubs and herbaceous plants ( Wipf et al, 2019 ), fully autotrophs ECM trees exchange nutrients among each other ( Klein et al, 2016 ) and with mixotrophic and mycoheterotrophic orchids (e.g., Li et al, 2021 for orchids) and ericaceous forest plants ( Suetsugu et al, 2021 ).…”

Section: Introductionmentioning

confidence: 99%

Ectomycorrhizal Networks in the Anthropocene: From Natural Ecosystems to Urban Planning

Authier

Violle²,

Richard³

2022

Front. Plant Sci.

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Trees acquire hydric and mineral soil resources through root mutualistic associations. In most boreal, temperate and Mediterranean forests, these functions are realized by a chimeric structure called ectomycorrhizae. Ectomycorrhizal (ECM) fungi are highly diversified and vary widely in their specificity toward plant hosts. Reciprocally, association patterns of ECM plants range from highly specialist to generalist. As a consequence, ECM symbiosis creates interaction networks, which also mediate plant–plant nutrient interactions among different individuals and drive plant community dynamics. Our knowledge of ECM networks essentially relies on a corpus acquired in temperate ecosystems, whereas the below-ground facets of both anthropogenic ECM forests and inter-tropical forests remain poorly investigated. Here, we successively (1) review the current knowledge of ECM networks, (2) examine the content of early literature produced in ECM cultivated forests, (3) analyze the recent progress that has been made in understanding the place of ECM networks in urban soils, and (4) provide directions for future research based on the identification of knowledge gaps. From the examined corpus of knowledge, we reach three main conclusions. First, the emergence of metabarcoding tools has propelled a resurgence of interest in applying network theory to ECM symbiosis. These methods revealed an unexpected interconnection between mutualistic plants with arbuscular mycorrhizal (AM) herbaceous plants, embedding ECM mycelia through root-endophytic interactions. This affinity of ECM fungi to bind VA and ECM plants, raises questions on the nature of the associated functions. Second, despite the central place of ECM trees in cultivated forests, little attention has been paid to these man-made landscapes and in-depth research on this topic is lacking. Third, we report a lag in applying the ECM network theory to urban soils, despite management initiatives striving to interconnect motile organisms through ecological corridors, and the highly challenging task of interconnecting fixed organisms in urban greenspaces is discussed. In particular, we observe a pauperized nature of resident ECM inoculum and a spatial conflict between belowground human pipelines and ECM networks. Finally, we identify the main directions of future research to make the needed link between the current picture of plant functioning and the understanding of belowground ECM networks.

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Mycorrhizal communities of two closely related species, Pyrola subaphylla and P. japonica, with contrasting degrees of mycoheterotrophy in a sympatric habitat

Cited by 10 publications

References 60 publications

Life history costs drive the evolution of mycoheterotrophs: Increased sprouting and flowering in a strongly mycoheterotrophic Pyrola species

Life history costs drive the evolution of mycoheterotrophs: Increased sprouting and flowering in a strongly mycoheterotrophic Pyrola species

Evolutionary relations between mycorrhizal symbiosis and plant–plant communication in trees

Ectomycorrhizal Networks in the Anthropocene: From Natural Ecosystems to Urban Planning

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