Mycoheterotrophic Genus Research Articles

A new section in Asian Thismia (Thismiaceae), T. sect. Mirabiles, and its checklist

The paper continues a series of contributions aimed to develop a phylogenetically sound sectional subdivision of the mycoheterotrophic genus Thismia. Here, a formal taxonomic status is provided for a remarkable monophyletic Asian group of species that is also well-defined morphologically within the genus. It is demonstrated that no supraspecific taxon name of any rank is available for this group. Hence, a new section, Thismia sect. Mirabiles, is established. Inconsistencies are highlighted in the earlier treatments where the species placed here in Thismia sect. Mirabiles were assigned to Thismia sect. Sarcosiphon. Indeed, in all such treatments, either the taxon monophyly or the nomenclatural applicability of the latter sectional name is violated. A checklist of the newly described section is provided along with an identification key to its species. The section is currently known to comprise eight species mainly distributed in mainland Southeast Asia and including a species endemic to the Andaman and Nicobar Islands.

A checklist of Thismia section Labiothismia (Thismiaceae), reinstated to include Asian species earlier placed in the neotropical T. sect. Glaziocharis

The paper contributes to a construction of a comprehensive sectional subdivision of the mycoheterotrophic genus Thismia through elucidating nomenclaturally correct application of the existing names and re-shaping the earlier proposed species groups in line with the ideas on phylogenetic relationships. The name Thismia sect. Glaziocharis widely used for a section accommodating certain Asian and Australian species is here demonstrated to be typified by the neotropical Thismia caudata (≡ Glaziocharis macahensis). This finding in conjunction with the phylogenetic views means that Thismia sect. Glaziocharis is to be applied to a neotropical group of the genus. Moreover, Thismia sect. Glaziocharis is the correct name for Thismia sect. Pyramidalis, since they are based on the same type species and the former name has a nomenclatural priority over the latter. The Asian species commonly placed into Thismia sect. Glaziocharis belong to a monophyletic group that has a single available name at the sectional rank, i.e. Thismia sect. Labiothismia. Thismia sect. Labiothismia is therefore formally reinstated, and a checklist of this section in the new circumscription is provided. The section is currently known to comprise 14 species, including a single North American species of Thismia, and the rest being distributed from India and Japan to Sumatra. Finally, a lectotype is designated for T. huangii.

Plastome analysis elucidates the phylogenetic placement of the mycoheterotrophic genus Yoania (Orchidaceae) and its plastomic degeneration during the evolution of mycoheterotrophy

Abstract Subtribe Calypsoinae (Epidendroideae, Orchidaceae) comprises several fully mycoheterotrophic species. Phylogenetic analysis indicates that full mycoheterotrophy has evolved independently at least four times within this group, including the Yoania clade. The taxonomic classification of Yoania species has been challenging. Therefore, to understand the plastomic degeneration during the evolution of mycoheterotrophy and to uncover the phylogenetic relationship within Yoania, we conducted a phylogenetic analysis using eight specimens representing all six recognized Yoania taxa from the complete plastome and partial ribosomal DNA (rDNA) operon sequence (ETS–18S–ITS1–5.8S–ITS2–26S). Among the Calypsoinae taxa examined, Yoania possessed the shortest plastome, ranging from 43 998 to 44 940 bp. Comparative analysis of the plastomes revealed a relatively conserved gene structure, content, and order, with species-level sequence variation (in the form of indels) primarily observed in the intergenic spacer regions. Plastomic gene-block inversions were observed between Yoania and Danxiaorchis singchiana, but not between Yoania and other related genera. Phylogenetic analyses based on the plastome and rDNA data strongly supported the monophyletic placement of Yoania within Calypsoinae, and indicated substantial molecular divergence between Yoania and other Calypsoinae taxa. Yoania can thus be considered genetically isolated from the other Calypsoinae taxa.

Relictithismia kimotsukiensis, a new genus and species of Thismiaceae from southern Japan with discussions on its phylogenetic relationship.

The family Thismiaceae, known as "fairy lanterns" for their urn- or bell-shaped flowers with basally fused tepals, consists of non-photosynthetic flowering monocots mainly in tropical regions, extending into subtropical and temperate areas. Here, we propose a new mycoheterotrophic genus, Relictithismia Suetsugu & Tagane (Thismiaceae), with its monotypic species Relictithismia kimotsukiensis Suetsugu, Yas.Nakam. & Tagane from Kimotsuki Mountains in the Osumi Peninsula, Kagoshima Prefecture, Kyushu Island, southern Japan. Relictithismia resembles Haplothismia Airy Shaw in having a cluster of tuberous roots, a feature previously observed only in this genus within the family Thismiaceae. However, it differs in having solitary flowers (vs. 2-6-flowered pseudo-raceme in Haplothismia), anther thecae largely separated (vs. connate), and the presence of an annulus (vs. absent). Additionally, Relictithismia differs from the geographically overlapping genus Thismia Griff. in its stamen structure and the position of the annulus. In Relictithismia, the stamens lack connectives, and its free filaments arise from the annulus located inside the perianth mouth, while in Thismia, the stamens typically have connate connectives, forming a staminal tube pendulous from the annulus located at the mouth of the floral tube. Our morphological and phylogenetic data indicated that R. kimotsukiensis holds an early-diverging position within the family, situated outside the Old World Thismia clade. This paper offers an extensive description and color photographs of R. kimotsukiensis, complemented by notes on its phylogenetic relationship and evolutionary history.

Thismia andicola sp. nov. (Thismiaceae): a new species from the northern Andes in Colombia

Knowledge on the mycoheterotrophic genus Thismia (Thismiaceae) in the neotropics is scarce, where the majority of species are known from Brazil, with 13 currently accepted species, of which seven are endemics. All the 15 known species of the genus in the Americas, except T. americana, inhabit forests below 1300 m a.s.l. Two species of Thismia are known from Colombia, T. panamensis from the Chocó biogeographical region and T. glaziovii from the Amazonian region. Here we describe a third Colombian species, T. andicola sp. nov. distinguished by having outer surface of the floral tube light blue and densely punctate with sky-blue metallic dots, inner tepals 4.6–5 mm long and stigma obovoid, covered adaxially by regularly distributed simple uniseriate multicellular trichomes. It is collected in the buffer zone of the Tamá National Park, Norte de Santander and is the first species of Thismia recorded from the Andes, and the first American species found above 2000 m a.s.l. We provide a description, drawings, photographs, distribution map, and the provisional conservation status of the new species. A key to species of Thismia sect. Ophiomeris species is also included.

Monotropastrum kirishimense (Ericaceae), a new mycoheterotrophic plant from Japan based on multifaceted evidence

Due to their reduced morphology, non-photosynthetic plants have been one of the most challenging groups to delimit to species level. The mycoheterotrophic genus Monotropastrum, with the monotypic species M. humile, has been a particularly taxonomically challenging group, owing to its highly reduced vegetative and root morphology. Using integrative species delimitation, we have focused on Japanese Monotropastrum, with a special focus on an unknown taxon with rosy pink petals and sepals. We investigated its flowering phenology, morphology, molecular identity, and associated fungi. Detailed morphological investigation has indicated that it can be distinguished from M. humile by its rosy pink tepals and sepals that are generally more numerous, elliptic, and constantly appressed to the petals throughout its flowering period, and by its obscure root balls that are unified with the surrounding soil, with root tips that hardly protrude. Based on genome-wide single-nucleotide polymorphisms, molecular data has provided clear genetic differentiation between this unknown taxon and M. humile. Monotropastrum humile and this taxon are associated with different Russula lineages, even when they are sympatric. Based on this multifaceted evidence, we describe this unknown taxon as the new species M. kirishimense. Assortative mating resulting from phenological differences has likely contributed to the persistent sympatry between these two species, with distinct mycorrhizal specificity.

Phylogenomics, plastome degradation and mycoheterotrophy evolution of Neottieae (Orchidaceae), with emphasis on the systematic position and Loess Plateau-Changbai Mountains disjunction of Diplandrorchis

BackgroundMycoheterotrophy is a unique survival strategy adapted to dense forests and has attracted biologists’ attention for centuries. However, its evolutionary origin and related plastome degradation are poorly understood. The tribe Neottieae contains various nutrition types, i.e., autotrophy, mixotrophy, and mycoheterotrophy. Here, we present a comprehensive phylogenetic analysis of the tribe based on plastome and nuclear ITS data. We inferred the evolutionary shift of nutrition types, constructed the patterns of plastome degradation, and estimated divergence times and ancestral ranges. We also used an integration of molecular dating and ecological niche modeling methods to investigate the disjunction between the Loess Plateau and Changbai Mountains in Diplandrorchis, a mycoheterotrophic genus endemic to China that was included in a molecular phylogenetic study for the first time.ResultsDiplandrorchis was imbedded within Neottia and formed a clade with four mycoheterotrophic species. Autotrophy is the ancestral state in Neottieae, mixotrophy independently originated at least five times, and three shifts from mixotrophy to mycoheterotrophy independently occurred. The five mixotrophic lineages possess all plastid genes or lost partial/all ndh genes, whereas each of the three mycoheterotroph lineages has a highly reduced plastome: one lost part of its ndh genes and a few photosynthesis-related genes, and the other two lost almost all ndh, photosynthesis-related, rpo, and atp genes. These three mycoheterotrophic lineages originated at about 26.40 Ma, 25.84 Ma, and 9.22 Ma, respectively. Diplandrorchis had presumably a wide range in the Pliocene and migrated southward in the Pleistocene.ConclusionsThe Pleistocene climatic fluctuations and the resultant migration resulted in the Loess Plateau-Changbai Mountains disjunction of Diplandrorchis. In the evolution of mycoheterotrophic lineages, the loss of plastid-encoded genes and plastome degradation are staged and irreversible, constraining mycoheterotrophs to inhabit understories with low light levels. Accordingly, the rise of local forests might have promoted the origin of conditions in which mycoheterotrophy is advantageous.

Thismialimkokthayi (Thismiaceae): A new mycoheterotrophic species from Genting Highlands in Pahang, Malaysia.

Thismialimkokthayi, a distinct mitriform species of the mycoheterotrophic genus Thismia, is described and illustrated. It was found at a locality in the upland areas of Genting Highlands, Pahang, Malaysia. This new species is morphologically similar to members of Thismiasect.Geomitra, but differs in several characteristics, including the colour of the floral tube, the inner surface of the floral tube with longitudinal ribs and absent transverse bars, a stamen apex with a central lobe (prolongation of the rib) and two lateral lobes (the tips of each are recurved) and a black-purplish stigma. Thismialimkokthayi is provisionally classified as Critically Endangered according to the IUCN Red List Categories and Criteria.

Unravelling the species diversity, phylogeny and biogeography of the mycoheterotrophic Voyrieae (Gentianaceae) and the description of a new species

AbstractBecause different tropical forest regions possess their own species diversity and communities, it is crucial to investigate the diversification history of their biota to understand how biodiversity was assembled. However, this requires reliable species concepts and robust, well‐sampled phylogenies. Here we focus on the fully mycoheterotrophic genus Voyria (Gentianaceae) and its diversification history in the Neotropics. We use a likelihood‐based approach to test species boundaries in Voyria with a population‐level ITS dataset and we build an extensive multigene species‐level phylogenetic framework for Voyria, which we use to infer the biogeographic evolution of the genus. We find strong support for the established morphology‐based species delimitation in this genus but we also discover a new species, which we describe here. Ancestral area reconstructions place the origin of the Voyrieae in the Guianas. Frequent exchange with other forest regions is inferred to have started from the Oligocene and continued toward the present. In these exchanges, the Guianas appeared to have acted as the most important source, while other regions mainly functioned as sinks. We conclude that well‐sampled phylogenies of fully mycoheterotrophic plants, which are ecologically restricted to rainforest habitats, can be instrumental to test hypotheses on rainforest biome evolution.

Thismia minutissima (Thismiaceae), a remarkable new mycoheterotrophic species from Sarawak, Borneo

Thismia minutissima, a distinctive minute species of the mycoheterotrophic genus Thismia is described and illustrated. It was found in several localities in mountain areas of Sarawak, Malaysia. The new species is superficially similar to members of Thismia sect. Rodwaya from Australia and New Zealand but differs by several distinctive morphological traits, including a fishtail-like lateral connective appendage and a perfect mitre. Its ecology, distribution and taxonomic status, as well as phylogenetic placement, are discussed.

Plastid Genome Evolution in the Subtribe Calypsoinae (Epidendroideae, Orchidaceae)

Calypsoinae is a small subtribe in Orchidaceae (Epidendroideae) characterized by diverse trophic strategies and morphological characters. Calypsoinae includes 13 genera, four of which are leafless and mycoheterotrophic. Mycoheterotrophic species in the leafless genus Corallorhiza are well suited to studies of plastome evolution. However, the lack of plastome sequences for other genera in Calypsoinae limits the scope of comparative and phylogenetic analyses, in particular our understanding of plastome evolution. To understand plastid genome evolution in Calypsoinae, we newly sequenced the plastomes of 12 species in the subtribe, including representatives of three mycoheterotrophic genera as well as five autotrophic genera. We detected two parallel photosynthetic losses in Corallorhiza. Evolutionary analyses indicated that the transition to obligate mycoheterotrophy leads to the relaxation of selection in a highly gene-specific pattern.

Morpho-anatomical differences among mycoheterotrophic Afrothismia spp. (Thismiaceae) indicate an evolutionary progression towards improved mycorrhizal benefit

Achlorophyllous, mycoheterotrophic plants depend on their mycorrhizal fungi for 100% of their carbon supply. Hence, there is strong evolutionary pressure towards a well-organized functioning of the association from the plant’s perspective. Members of the mycoheterotrophic genus Afrothismia have evolved elaborate fungal colonization patterns allowing a sustained benefit from external fungal penetration events. On the basis of anatomical details of the root-shoot systems of A. korupensis and A. hydra, we elucidate an evolutionary progression between the comparatively simple mycorrhizal pattern in A. gesnerioides and the so far most complex mycorrhiza in A. saingei. We detected two major advancements: (1) two species, A. korupensis and A. saingei, use the fungus itself as energy storage, replacing starch depositions used by A. gesnerioides and A. hydra, and (2) the morphological complexity of hyphal forms in plant tissue compartments increases from A. gesnerioides to A. saingei. We discuss the omitting of starch metabolism as well as the morpho-anatomical differences as an evolutionary fine-tuning of the compartmented mycorrhizal organization in Afrothismia. Our results support the idea of a taxonomic distinction between Afrothismia and other Thismiaceae.

Phylogenetics of the mycoheterotrophic genusThismia(Thismiaceae: Dioscoreales) with a focus on the Old World taxa: delineation of novel natural groups and insights into the evolution of morphological traits

AbstractThismia is a genus of > 80 mycoheterotrophic species characterized by a peculiar appearance and complex floral morphology. A significant proportion of the species and morphological diversity of Thismia has only been uncovered in the past two decades, and new discoveries continue to be made. Given that many new data have recently become available, and the most comprehensive taxonomic revision of the genus from 1938 addresses less than half of the currently known species, previous hypotheses for species relationships and infrageneric taxonomic classification in Thismia was in need of review. Extensive molecular phylogenetic studies of Thismia at the genus level have never been presented. We investigate the phylogenetic relationships of 41 species (and one variety) of Thismia from the Old World. Our study comprises 68 specimens (for 28 of which the data were newly generated), including outgroup taxa broadly representing Thismiaceae (= Burmanniaceae p.p. sensuAPG IV, 2016), and is based on two nuclear and one mitochondrial marker. We use maximum likelihood and Bayesian inference to infer relationships among the taxa. We also constructed a morphological dataset of 12 mostly floral characters, comparing these characters to hypotheses based on molecular evidence to identify putative synapomorphies for major clades and to discuss hypotheses regarding the evolution of structural traits in the genus. Our analyses indicate that the majority of currently accepted infrageneric taxa of Thismia are polyphyletic. We find support for the monophyly of the Old World group, in which we recognize five well-supported lineages (clades); the only New World species studied appears to be related to the Neotropical genus Tiputinia. Ancestral state reconstructions demonstrate that the evolution of most morphological characters was homoplastic, but we identify characters that provide each of the five clades of Old World Thismia with a unique morphological description. The geographical distribution of the species under study is also shown to be consistent with the major clades. Our investigation provides a phylogenetic basis for the development of a novel sectional classification of Thismia reflecting morphological and geographical traits.

Gastrodia amamiana (Orchidaceae; Epidendroideae; Gastrodieae), a new completely cleistogamous species from Japan

Gastrodia Brown (1810: 330; Gastrodieae, Epidendroideae) is a mycoheterotrophic leafless genus that is distributed throughout the temperate and tropical regions of Asia, Oceania, Madagascar and Africa (Cribb et al. 2010, Hsu & Kuo 2010, Suetsugu et al. 2018a) and characterized by fleshy tubers, united tepals and two mealy pollinia that lack caudicles (Cribb et al. 2010, Hsu & Kuo 2010, Suetsugu et al. 2018a,b). Several recent studies have re-examined the diversity of Gastrodia in many Asian countries (Hsu et al. 2012, 2016, Ong & O’Byrne 2012, Tan et al. 2012, Suetsugu 2013b, 2014, 2016, 2017, Huang et al. 2015, 2018, Tsukaya & Hidayat 2016, Metusala & Supriatna 2017, Pelser et al. 2016, Suetsugu et al. 2018a,b). As a result, the genus now comprises ca. 100 species, thereby making it the most diverse mycoheterotrophic genus (Hsu et al. 2016, Suetsugu 2017, Suetsugu et al. 2018a,b). However, it is likely that the distribution and diversity of Gastrodia species remain underestimated because plants are easily overlooked in the field due to their short flowering seasons and small size (Hsu et al. 2016, Suetsugu 2017, Suetsugu et al. 2018b).

Thismiadomei and T.terengganuensis (Thismiaceae), two new species, and T.javanica, a new record from Terengganu, Peninsular Malaysia.

Two new species of the mycoheterotrophic genus Thismia Griff. (Thismiaceae), Thismiadomei Siti-Munirah and T.terengganuensis Siti-Munirah from Peninsular Malaysia, are described and illustrated. Thismiadomei, characterized by its perianth lobes that are upright and curve inward, but are imperfectly connate, falls within sectionOdoardoa. Thismiaterengganuensis is characterized by its mitre with three appendages on its apex, so falls within sectionGeomitra. Both new species are unique and totally different from other described species, T.domei by the trichomes on its outer perianth tube surface and T.terengganuensis by its mitre with slender appendages. Thismiajavanica J.J.Sm, also from Terengganu, is a new record for Peninsular Malaysia.

Lecanorchis moritae (Orchidaceae, Vanilloideae), a new mycoheterotrophic species from Amami-Oshima Island, Japan, based on morphological and molecular data

A new species of the mycoheterotrophic genus Lecanorchis Blume (Orchidaceae), L. moritae, is described from Amami-Oshima Island, Japan. It is most similar to L. suginoana but differs in having a transversely elliptic (slightly contracted at base) midlobe (vs. semiorbicular, not contracted at base), more triangular with almost entire margins (vs. relatively rounded, denticulate margins) and reddish apices (vs. somewhat whitish apices) and a lip with white and purple hairs (vs. white and lemon yellow hairs) and sparse unicellular papillae scattered on the disc (vs. dense unicellular papillae). An illustration and nuclear ribosomal internal transcribed spacer (nrITS) sequence (i.e., DNA barcode) of the new species are also provided.

Gymnosiphon queenslandicus (Burmanniaceae), a new addition to the mycoheterotroph flora of tropical rainforest in Australia

The mycoheterotrophic genus Gymnosiphon Blume is recorded for Australia for the first time after the recent discovery of plants at Mossman Gorge, Queensland. On the basis of examination of living plants in the field as well as materials preserved in spirit, the Mossman Gorge Gymnosiphon taxon is a novelty closely related to Gymnosiphon affinis J.J.Sm., which is known only from New Guinea. The new species is here described as Gymnosiphon queenslandicus B.Gray & Y.W.Low based on floral characteristics important for species distinction in the genus.

Thismiasumatrana (Thismiaceae), a new species from West Sumatra, Indonesia, with discussions on the taxonomic identity of Thismiaclavigera.

A new species of the mycoheterotrophic genus Thismia Griff. (Thismiaceae), Thismiasumatrana Suetsugu & Tsukaya, from West Sumatra, Indonesia, is described, based on a rehydrated herbarium specimen from National Museum of Nature and Science, Japan. Thismiasumatrana is closely related to T.clavigera (Becc.) F.Muell. but is distinguished by a much larger flower.

Thismia aurantiaca sp. nov. (section Rodwaya, Thismiaceae): First record of the family from Andaman and Nicobar Islands, India with a new species

Thismia is a mycoheterotrophic genus in the family Thismiaceae. We report a new family record for Andaman and Nicobar Islands and a new species for India. A detailed description along with conservation assessment, colour photos, distribution map, and key to the species from India are provided.

Sciaphila lambirensis (Triuridaceae), a New Mycoheterotrophic Plant from Sarawak, Borneo, Malaysia

Borneo is known to harbor the greatest species diversity of the mycoheterotrophic genus Sciaphila (Triuridaceae) and is home to 11 species, including five endemics, another undescribed Sciaphila speci