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A revision of the family Thismiaceae (Dioscoreales) in Cambodia, Laos and Vietnam
Abstract
We present the first taxonomic account of the family Thismiaceae in the countries of Eastern Indochina. A single genus of Thismiaceae, Thismia, with eight species is known to inhabit this region. Six species, including four national endemics, are found in Vietnam, whereas Cambodia and Laos each has a single and endemic species of Thismia. We report new records of a number of species, which allowed us to establish for the first time their distribution areas. We show geographical distribution of all species of Thismia in Cambodia, Laos and Vietnam on a map. We recognise Hon Ba Nature Reserve and Chu Yang Sin National Park as hotspots of known Thismia diversity in Eastern Indochina. We confirm the presence of T. javanica in Vietnam, earlier known as a doubtful report, by specimen investigation. We significantly amend morphological descriptions of several Vietnamese species. We highlight a number of characters with remarkable intraspecific variation, along with the most important structural differences between morphologically similar species. We discuss remaining taxonomic problems of Indochinese Thismia, and present an identification key to species of Thismiaceae in Cambodia, Laos and Vietnam.
... Due to their very small size and the shortly time span of the above-ground parts, species in the genus are easily overlooked and are thus still poorly known. To date, eight species have been recorded from Indochina (Cambodia, Laos, and Vietnam) (Nuraliev et al., 2020). In Laos, only one species, T. nigricoronata Kumar & S.W.Gale, is known from the limestone forests of Vangvieng District in Vientiane Province (Kumar et al., 2017), and other species are probably still waiting to be found in the country. ...
... After a review of the relevant Thismia literature, especially on related species (e.g. Larsen, 1987;Chantanaorrapint, 2008;Kumar et al., 2017;Siti-Munirah & Dome, 2019;Nuraliev et al., 2020;Siti-Munirah, 2023;Siti-Munirah & Dome, 2023), one species was identified as T. angustimitra Chantanaorr. which was previously described from Thailand, based on the dark grey or brownish flowers, the absence of filiform appendages on the inner tepals, and the presence of golden-brownish hairs at the annulus mouth. ...
... Here, we report them as new findings for Laos, together with a key to the three Lao species of Thismia. (Larsen, 1987;Chantanaorrapint, 2008;Siti-Munirah & Dome, 2019;Nuraliev et al., 2020;Siti-Munirah, 2023). (Chantanaorrapint & Sridith, 2015). ...
Two species of the genus Thismia (Thismiaceae), T. angustimitra and T. javanica, from Nam Kading National Protected Area, central Laos, are recorded for Lao flora for the first time. The number of species of Thismia in Laos is raised to three, and a key to species of Thismia in Laos is provided.
... Additionally, measurements were taken from spirit material. The specimen features were compared in detail with the original drawings and descriptions of morphologically similar species of Thismia provided by Jonker (1938), Larsen and Averyanov (2007), Mar and Saunders (2015), Chantanaorrapint (2018), Tanaka et al. (2018), Suetsugu et al. (2018), Siti-Munirah and Dome (2019) and Nuraliev et al. (2020). Description. ...
... In a molecular phylogenetic Table 1. Morphological comparison of T. kenyirensis with similar species T. arachnites (Chantanaorrapint 2018), T. bokorensis (Suetsugu et al. 2018), T. breviappendiculata (Tanaka et al. 2018), T. brunonis (Jonker 1938), T. gardneriana (Jonker 1938;Bandara et al. 2020), T. hongkongensis (Mar et al. 2015), T. javanica (Siti-Munirah and Dome 2019;Nuraliev et al. 2020) and T. tentaculata (Larsen and Averyanov 2007;Nuraliev et al. 2020). ...
... In a molecular phylogenetic Table 1. Morphological comparison of T. kenyirensis with similar species T. arachnites (Chantanaorrapint 2018), T. bokorensis (Suetsugu et al. 2018), T. breviappendiculata (Tanaka et al. 2018), T. brunonis (Jonker 1938), T. gardneriana (Jonker 1938;Bandara et al. 2020), T. hongkongensis (Mar et al. 2015), T. javanica (Siti-Munirah and Dome 2019;Nuraliev et al. 2020) and T. tentaculata (Larsen and Averyanov 2007;Nuraliev et al. 2020). ...
Citation: Siti-Munirah MY, Dome N (2023) Thismia kenyirensis (Thismiaceae), a new species from Taman Negeri Kenyir, Terengganu, Peninsular Malaysia. PhytoKeys 221: 61-72. https://doi. Abstract A new mycoheterotrophic species, Thismia kenyirensis Siti-Munirah & Dome from Peninsular Malaysia, is described and illustrated. Thismia kenyirensis differs from other previously described species in the following characteristics: the flower tube is completely orange, with alternating darker and paler-coloured longitudinal lines on the outer and inner surfaces, the outer tepals are ovate (petaloid), the inner tepals are narrowly lanceolate, each ending with a long appendage. According to the IUCN Red List categories and criteria, T. kenyirensis is provisionally classified as Least Concern.
... are poorly represented in botanical collections, many of them are known only from a type specimen and only a few are observed in more than three locations (e.g. Sujanapal et al., 2017;Nuraliev et al., 2020). Additionally, only some of the known species are available as liquid collections apart from herbarium vouchers, which are not suitable for comprehensive morphological investigations. ...
... We use our data to elucidate the morphological nature of several floral parts in this genus. Organography of the species under study has previously been described in detail (Jonker, 1938(Jonker, , 1948Larsen, 1987;Larsen & Averyanov, 2007;Nuraliev et al., 2014Nuraliev et al., , 2020. The most evident structural differences between the species examined concern the perianth morphology. ...
... As a result, the placentas become column-like with an ovuliferous surface embracing the column at the inner and lateral sides. Thus, as the flower reaches a diameter of c. 1 mm (compared with that of c. 6-8 mm in a mature flower: Nuraliev et al., 2014Nuraliev et al., , 2020, its entire gross structure is almost completely formed. ...
Thismia is characterized by an exceptionally complicated floral morphology that is currently not understood properly. In the taxonomic literature, descriptive rather than morphological terms are often applied to parts of the flower in Thismia, relating to the general appearance of the floral organs instead of their precise homologies. Precise understanding of the floral structure is complicated by the rarity of Thismia spp. and the paucity of appropriate material. Here we provide a comprehensive study of reproductive organs of three Thismia spp. (T. annamensis, T. javanica and T. mucronata) including the first investigation of inflorescence architecture and early floral development in Thismiaceae. We found a hitherto unknown diversity of the reproductive shoots in the genus, manifested in the number of floral prophylls (two or three, in contrast to a single prophyll in the vast majority of monocots) and in the branching plane resulting in two distinct inflorescence types, a drepanium and a bostryx. We report the non-acropetal sequence of initiation of floral whorls (with stamens being the last elements to initiate), never previously described in monocots, and the gynoecium composed of completely plicate carpels, also a rare feature for monocots. Floral vasculature is relatively uniform in Thismia, but significant interspecific differences are found in tepal innervation, including the number of tepal traces; some of these differences are not immediately related to the external tepal morphology. We argue that the annulus, which acts as a roof of the hypanthium, possesses an androecium nature and represents congenitally fused bases of stamen filaments. We describe the stamens as laminar structures, which are also shortly tubular in the distal part of the supraconnective with the adaxial tubular side forming a skirt-like appendage. Finally, the placentas, which are column-like when mature, are initially parietal, becoming secondarily similar to free-central placentas through schizogenous separation from the ovary wall.
... In identification of the studied specimens, we followed Nuraliev et al. (2020), who based on floral structural traits such as number of teeth on stamen apex for species delimitation. Nuraliev et al. (2020) pointed the uncertainty of taxonomic assignment of the specimens from Hon Ba Nature Reserve (Vietnam): both T. javanica (Truong Ba Vuong et al. ...
... In identification of the studied specimens, we followed Nuraliev et al. (2020), who based on floral structural traits such as number of teeth on stamen apex for species delimitation. Nuraliev et al. (2020) pointed the uncertainty of taxonomic assignment of the specimens from Hon Ba Nature Reserve (Vietnam): both T. javanica (Truong Ba Vuong et al. BV426) and T. tentaculata (including Truong Ba Vuong BV175b) found in this area are remarkably similar to each other in flower shape and colour, and at the same time differ in flower shape and colour from other known specimens of these species. ...
The mycoheterotrophic genus Thismia shows a great number of structural and ecological traits which are rare or unique for angiosperms. Pollen morphology of this genus is still poorly known. Pollen of Thismia was reported to be porate with one to several pores. Position of the pores is unknown, and therefore, the pollen type has not been established to date. Information on sporoderm structure in the genus is scarce, as high-quality images of pollen grains are available for several species only. In our comprehensive investigation of pollen morphology of Thismia, we involved nine Asian species of the genus and employed an integrative approach, which included data from light microscopy, scanning electron microscopy and transmission electron microscopy. All studied species were shown to possess monoporate pollen of asymmetric-elliptic planoconvex shape. Using TEM investigation of immature anthers, we demonstrated that pollen grains are organized in tetragonal tetrads, and the pore occupies an equatorial position. We argue that Asian species of Thismia along with Burmannia from the same order Dioscoreales are the only known lineages of seed plants with a single equatorial aperture. The sporoderm surface is psilate or perforate with perforations of various size and density in the studied species. We discuss the interspecific variation of sporoderm morphology in the light of the phylogenetic relationships between Asian species of Thismia. We demonstrate that the pollen morphology of Thismia fails to conform to the idea of entomophily, which is believed to prevail in this genus. Finally, we describe an unexpected striking difference in sporoderm structure between the specimens belonging to T. javanica species group.
... Flowers usually coloured with white combined with dark to blackish blue/brown/green, with orange stamen appendages and sometimes certain other flower parts. Hypanthium inner surface without transverse bars, sometimes foveolate (described as "fenestrated" by Nuraliev et al. 2020Nuraliev et al. , 2021 or irregularly reticulate. Annulus usually dome-shaped to erect, fleshy. ...
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.
... Indeed, Taubert (1895) described Glaziocharis as being "reminiscent of the Malayan genus Geomitra due to the hat-shaped inner petals" and did not indicate any of its distinctive features. Consequently, this publication does not provide a valid genus description, and was erroneously cited by Nuraliev et al. (2020) as the protologue of 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 reshaping 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.
... Thismia Griffith (1844: 221) is a genus of mycoheterotrophic, achlorophyllous, herbaceous plants, comprising about 91 species with distribution from tropical and subtropical Asia, temperate Australia to New Zealand, Central USA, Central America (Costa Rica, Panama) to tropical South America (POWO 2022). Species diversity of Thismia worldwide is highest in Southeast Asia (Nuraliev et al. 2020a, Shepeleva et al. 2020, where numerous new species have been described in recent years (Chantanaorrapint & Suddee 2018, Siti-Munirah & Nikong 2019, Xu et al. 2020, Dančák et al. 2020a, Chantanaorrapint & Tosak. 2021, Siti-Munirah et al. 2021a, 2021b. ...
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.
... captivate by their amazing diversity in flower shape and colour (e.g. Nuraliev et al. 2020). These highly diverse floral traits have been used for tribal or generic systematics initiated by Schlechter (1921, as a generic subdivision of the tribe Thismieae), advanced by Jonker (1938) and more recently reviewed in Kumar et al. (2017). ...
Achlorophyllous, mycoheterotrophic plants often have an elaborate mycorrhizal colonization pattern, allowing a sustained benefit from external fungal root penetrations. The present study reveals the root anatomy and mycorrhizal pattern of eight mycoheterotrophic Thismia spp. (Thismiaceae), all of which show separate tissue compartments segregating different hyphal shapes of the mycorrhizal colonization, as there are intact straight, coiled and peculiarly knotted hyphae as well as degenerated clumps of hyphal material. Those tissue compartments in Thismia roots potentially comprise exo-, meso-and endoepidermae, and exo-, meso-and endocortices, although not all species develop all these root layers. Differences in details among species according to anatomy (number of root layers, cell sizes and shapes) and colonization pattern (hyphal shapes within cells) are striking and can be discussed as an evolutionary series towards increasing mycorrhizal complexity which roughly parallels the recently established phylogeny of Thismia. We suggest functional explanations for why the distinct elements of the associations can contribute to the mycorrhizal advantage for the plants and, thus, we emphasize the relevance of structural traits for mycorrhizae.
... The increasing availability of complete plastomes of Dioscoreales and especially Burmanniaceae (Ma et al., 2018;Li et al., 2019) also gives an opportunity to use larger datasets comprising the entire plastomes to reconstruct the relationships within this order and, in particular, to elucidate the phylogenetic vicinity of Thismiaceae (though this requires caution about long branch attraction -see Lam et al., 2018;Schelkunov et al., 2019). Thismia is a highly underexplored genus; more than 30 species of this genus were described after 2015 (e.g., Hroneš et al., 2018;Da Silva et al., 2020;Dančák et al., 2020b;Xu et al., 2020) and species complexes with uncertain boundaries between taxa become evident with discovery of new populations (Dančák et al., 2020b;Nuraliev et al., 2020). The majority of species of Thismia were described based exclusively on morphology, and the position of many of them in Thismia phylogeny remains unclear (Shepeleva et al., 2020). ...
Heterotrophic plants provide intriguing examples of reductive evolution. This is especially evident in the reduction of their plastid genomes, which can potentially proceed toward complete genome loss. Several milestones at the beginning of this path of degradation have been described; however, little is known about the latest stages of plastome reduction. Here we analyze a diversity of plastid genomes in a set of closely related non-photosynthetic plants. We demonstrate how a gradual loss of genes shapes the miniaturized plastomes of these plants. The subject of our study, the genus Thismia, represents the mycoheterotrophic monocot family Thismiaceae, a group that may have experienced a very ancient (60–80 mya) transition to heterotrophy. In all 18 species examined, the plastome is reduced to 14–18 kb and is highly AT-biased. The most complete observed gene set includes accD, seven ribosomal protein genes, three rRNA, and two tRNA genes. Different clades of Thismia have undergone further gene loss (complete absence or pseudogenization) compared to this set: in particular, we report two independent losses of rps2 and rps18.
Thismia papillata, a new species of Thismiaceae, is described and illustrated. The species was discovered in 2023 in Thanh Hoa Province, northern Vietnam. The new species is readily distinguishable from most of its congeners by the presence of appendages of outer and inner tepals, inner tepals fused into a mitre, absence of a wing-like appendage of supraconnective and absence of interstaminal glands. Thismia papillata is similar to T. abei, T. taiwanensis and T. tuberculata, differing mainly in prominently papillate outer hypanthium surface, appendages of the outer tepals up to 15 mm long, appendages of the inner tepals up to 9 mm long, and column-like placentas. Gaps in understanding of interactions between the inner tepals in Thismia are highlighted that are related to the postgenital tepal fusion and tepal aestivation. Similar uncertainties in determination of fusion between the stamens are also uncovered.
Thismia Griff. (Thismiaceae) is a holo-mycoheterotrophic genus with more than 100 species. In this study, phylogenetic analyses supported that T. malipoensis from Yunnan is a new species in T. sect. Glaziocharis. Morphologically, this new species can be distinguished from its phylogenetic sister species T. abei by having the annulus of the flower expanded and modified into a cucullate (hood-like) structure with zygomorphic symmetry with one opening on one side. Biogeographical inference showed that SW China to Indo-Burma and the Sunda Shelf region was suggested as the ancestral distribution region of Thismia s.s., then eastward to SE China and Japan, and southward to New Guinea to Australia, respectively. The Chinese species should have originated from at least two different ancestral sources, and geographical isolation caused the divergence between T. malipoensis and T. abei at 17.47 Mya.
The paper summarizes results of investigations of non-green plants carried out in the Russian-Vietnamese Tropical Center during the years 2009–2018. The checklist is provided which includes 29 species in seven families. Among them, holoparasites are represented only by the family Balanophoraceae (4 spp.), while the mycoheterotrophs comprise Ericaceae (1 sp.), Petrosaviaceae (1 sp.), Orchidaceae (16 spp.), Burmanniaceae (1 sp.), Thismiaceae (3 spp.) and Triuridaceae (4 spp.). Four species new to science and several new species records for Vietnam were published during this study. The highest diversity of non-photosynthetic plants was found in Central Highlands and especially in Thach Nham protected forest and Chu Yang Sin National Park. The obtained specimens are currently employed in morphological, phylogenetic and genomic studies of several groups of heterotrophic plants.
Background and aims:
Mycorrhizal associations in mycoheterotrophic plants are generally more specialized than in autotrophs. Mycoheterotrophs typically bear small, inconspicuous flowers that often self-pollinate to maximize seed set, although some have structurally complex flowers indicative of xenogamy. A trade-off has previously been proposed between specialization in these above- and below-ground symbioses, although empirical data are lacking.
Methods:
We used next-generation DNA sequencing to compare the mycorrhizal communities from the roots of a mycoheterotrophic species, Thismia tentaculata (Thismiaceae), and its neighbouring autotrophs. We furthermore conducted detailed assessments of floral phenology and pollination ecology, and performed artificial pollination experiments to determine the breeding system.
Key results:
Thismia tentaculata maintains a symbiotic association with a single arbuscular mycorrhizal Rhizophagus species. The flowers are pollinated by a single species of fungus gnats (Corynoptera, Sciaridae), which are attracted by the yellow pigments and are temporarily restrained within the perianth chamber before departing via apertures between the anthers. The plants are self-compatible but predominantly xenogamous.
Conclusions:
Our findings demonstrate that T. tentaculata maintains highly specialized associations with pollinators and mycorrhizal fungi, both of which are widely distributed. We suggest that specialization in multiple symbiotic interactions is possible in mycoheterotrophs if redundant selective pressures are not exerted to further restrict an already constrained suite of life-history traits.
Thismia kelabitiana, a new unique species from the Sarawak state of Malaysia in the island of Borneo is described and illustrated. This new species is not similar to any species of Thismia described so far especially by having a unique form of mitre and outer perianth lobes deeply divided into 8–10 acute lobes and forming striking fringe around perianth tube opening. The species appears to be critically endangered due to ongoing logging activities in the region. It may potentially become a surrogate species for lower montane forests of the region and thus help protect them against further destruction.
Oxygyne Schltr. (Thismiaceae) is a rare and little-known genus of achlorophyllous mycoheterotrophic perennial herbs with one of the most remarkable distributions of all angiosperm plant genera globally, being disjunct between Japan and West–Central Africa. Each species is known only from a single location, and in most cases from a single specimen. This monographic study names, describes and maps two new species, Oxygyne duncanii Cheek from cloud forest in SW Region Cameroon and O. frankei Cheek from gallery forest in the Central African Republic , representing the first new Oxygyne species described from Africa in 112 years, and raising the number of described Oxygyne species from four to six. Oxygyne duncanii is remarkable for sharing more morphological characters with two of the three Japanese species ( O. hyodoi C.Abe & Akasawa, O. shinzatoi (H. Ohashi) Tsukaya) than with the geographically much closer type species of the genus, O. triandra from Mt Cameroon. Based mainly on herbarium specimens and field observations made in Cameroon and Japan during a series of botanical surveys, we provide descriptions, synonymy, mapping and extinction risk assessments for each species of Oxygyne , together with keys to the genera of Thismiaceae and the species of Oxygyne . The subterranean structures of African Oxygyne are described for the first time, and found to be consistent with those of the Japanese species. We review and reject an earlier proposal that the Japanese species should be segregated from the African species as a separate genus, Saionia Hatus. The only character that separates the two disjunct species groups is now flower colour: blue or partly-blue in the Japanese species compared with orange-brown in the African species. Studies of the pollination biology and mycorrhizal partners of Oxygyne are still lacking. Two of the six species, O. triandra Schltr. and O. hyodoi , appear to be extinct, and the remaining four are assessed as Critically Endangered using the IUCN 2012 criteria. To avoid further extinction, an urgent requirement is for conservation management of the surviving species in the wild. Since few achlorophyllous mycoheterotrophs have been successfully cultivated from seed to maturity, ex situ conservation will not be viable for these species and protection in the wild is the only viable option. While natural habitat survives, further botanical surveys could yet reveal additional new species between Central Africa and Japan.
Premise of the Study
Phylogenomic studies employing large numbers of genes, including those based on plastid genomes (plastomes), are becoming common. Nonphotosynthetic plants such as mycoheterotrophs (which rely on root‐associated fungi for essential nutrients, including carbon) tend to have highly elevated rates of plastome evolution, substantial genome reduction, or both. Mycoheterotroph plastomes therefore provide excellent test cases for investigating how extreme conditions impact phylogenomic inference.
Methods
We used parsimony and likelihood analysis of protein‐coding gene sets from published and newly completed plastomes to infer the phylogenetic placement of taxa from the 10 angiosperm families in which mycoheterotrophy evolved.
Key Results
Despite multiple very long branches that reflect elevated substitution rates, and frequently patchy gene recovery due to genome reduction, inferred phylogenetic placements of most mycoheterotrophic lineages in DNA‐based likelihood analyses are both well supported and congruent with other studies. Amino‐acid‐based likelihood placements are broadly consistent with DNA‐based inferences, but extremely rate‐elevated taxa can have unexpected placements—albeit with weak support. In contrast, parsimony analysis is strongly misled by long‐branch attraction among many distantly related mycoheterotrophic monocots.
Conclusions
Mycoheterotrophic plastomes provide challenging cases for phylogenomic inference, as substitutional rates can be elevated and genome reduction can lead to sparse gene recovery. Nonetheless, diverse likelihood frameworks provide generally well‐supported and mutually concordant phylogenetic placements of mycoheterotrophs, consistent with recent phylogenetic studies and angiosperm‐wide classifications. Previous predictions of parallel photosynthesis loss within families are supported for Burmanniaceae, Ericaceae, Gentianaceae, and Orchidaceae. Burmanniaceae and Thismiaceae should not be combined as a single family in Dioscoreales.
The genus Thismia Griffith (1844: 221) of the tribe Thismieae, Burmanniaceae sensu APG IV (2016) or Thismiaceae of other authors, represents one of the most species-rich mycoheterotrophic genera and consists of more than 60 species (Jonker 1948, Merckx 2008). Considering that the majority of these species were collected only once (Jonker 1948), and that many new species have recently been discovered, especially from various Southeast Asian countries (e.g., Tsukaya & Okada 2012, Dančák et al. 2013, Nuraliev et al. 2014, 2015, Truong et al. 2014, Chantanaorrapint & Sridith 2015, Li & Bi 2013, Hroneš et al. 2015, Tsukaya et al. 2017, Suetsugu et al. 2017), many more undescribed species are probably still hidden in the tropical rain forests of Southeast Asia.
Thismia nigricoronata is described as a new species in family Burmanniaceae. Both morphological and phylogenetic analyses indicate that this new Lao endemic is allied to T. taiwanensis in section Glaziocharis, and it can be differentiated on the basis of its longer vestigial stem leaves, reflexed free outer perianth lobes and ornamented, vibrantly coloured outer surface of the perianth tube. The infrageneric taxonomy of Thismia is reviewed, the genera Geomitra and Scaphiophora are officially reduced to sectional status in Thismia, and all species are enumerated in systematic order. A key to all currently accepted subgenera, sections and subsections is presented to facilitate further examination of their phylogenetic integrity in light of apparent conflict between the traditional morphology-based system and the emerging DNA-based classification.
Aim
Achlorophyllous mycoheterotrophic plants and mycorrhizal fungi often have highly specific interactions that potentially limit the plants’ distribution and diversification potential. However, specificity in biotic interactions may differ considerably over a species’ distribution range and therefore interactions need to be studied over their entire range to assess their evolution in space and time. The present study investigates the biogeographical history of the interaction between five closely related mycoheterotrophic Thismia species and arbuscular mycorrhizal fungi over the distribution range of the plant species.
Location
Temperate south‐east Australia and New Zealand.
Methods
Phylogenetic relationships of Thismia (nr ITS and mt cob ) and their arbuscular mycorrhizal fungi (partial nr SSU ) were reconstructed based on data from 65 plant specimens. The diversification times in Thismia were estimated with a Bayesian relaxed clock approach using a Dioscoreales framework (nr SSU , mt atp1 , mt matR , mt nad1 b‐c ). Ancestral geographical ranges were reconstructed using a maximum likelihood approach. The same approach was used to reconstruct ancestral mycorrhizal associations.
Results
Our analysis shows that Thismia plants have highly specific, phylogenetically conserved and evolutionarily persistent interactions with Rhizophagus fungi. Nevertheless, Thismia was able to diversify and radiate recently due to the wide geographical distribution of the host fungi. In addition, we find that although the mycorrhizal interactions of this clade of mycoheterotrophs are strictly bound to a fungal lineage, host switches remain possible.
Main conclusions
In this clade of closely related mycoheterotrophs, dependency on highly specific fungal interactions is the result of phylogenetic niche conservatism, acting over at least 12 million years. Nevertheless, plants that are dependent on highly specific fungal interactions have ample opportunities to disperse and radiate over the geographical range of their hosts. Our study highlights the need to link the ecology and evolution of species interactions over broad geographical and evolutionary scales for understanding mycorrhizal interactions.
In general, plants and arbuscular mycorrhizal (AM) fungi exchange photosynthetically fixed carbon for soil nutrients, but occasionally nonphotosynthetic plants obtain carbon from AM fungi. The interactions of these mycoheterotrophic plants with AM fungi are suggested to be more specialized than those of green plants, although direct comparisons are lacking.
We investigated the mycorrhizal interactions of both green and mycoheterotrophic plants. We used next‐generation DNA sequencing to compare the AM communities from roots of five closely related mycoheterotrophic species of Thismia (Thismiaceae), roots of surrounding green plants, and soil, sampled over the entire temperate distribution of Thismia in Australia and New Zealand.
We observed that the fungal communities of mycoheterotrophic and green plants are phylogenetically more similar within than between these groups of plants, suggesting a specific association pattern according to plant trophic mode. Moreover, mycoheterotrophic plants follow a more restricted association with their fungal partners in terms of phylogenetic diversity when compared with green plants, targeting more clustered lineages of fungi, independent of geographic origin.
Our findings demonstrate that these mycoheterotrophic plants target more narrow lineages of fungi than green plants, despite the larger fungal pool available in the soil, and thus they are more specialized towards mycorrhizal fungi than autotrophic plants.
Premise of the study:
Few-gene studies with broad taxon sampling have provided major insights into phylogeny and underpin plant classification. However, they have typically excluded heterotrophic plants because of loss, pseudogenization, or rapid evolution of plastid genes. Here we performed a phylogenetic survey of three commonly retained plastid genes to assess their utility in placing mycoheterotrophs.
Methods:
We surveyed accD, clpP, and matK for 34 taxa from seven monocot families that include full mycoheterotrophs and a broad sampling of photosynthetic taxa. After screening for weak contaminants, we conducted phylogenetic analyses and characterized among-lineage rate variation.
Key results:
Likelihood analyses strongly supported local placements of fully mycoheterotrophic taxa for Corsiaceae, Iridaceae, Orchidaceae, and Petrosaviaceae, in positions consistent with other studies. Depression of likelihood bootstrap support values near mycoheterotrophic clades was alleviated when each mycoheterotrophic family was considered separately. Triuridaceae (Sciaphila) monophyly was recovered in a partitioned likelihood analysis, and the family then placed as sister to Cyclanthaceae-Pandanaceae. Burmanniaceae placed in Dioscoreales with weak to strong support depending on analysis details, and we inferred a plastid-based phylogeny for the family. Thismiaceae species may retain a plastid genome, based on accD retention. The inferred position of Thismiaceae is unstable, but was close to Taccaceae (Dioscoreales) in some analyses.
Conclusions:
Long branches/elevated substitution rates, missing genes, and occasional contaminants are challenges for plastid-based phylogenetic inference with full mycoheterotrophs. However, most mycoheterotrophs can be readily integrated into the broad picture of plant phylogeny using several plastid genes and broad taxonomic sampling.
This paper provides an up-to-date linear sequence of monocot families and genera (excluding Orchidaceae and Poaceae) based on current phylogenetic evidence. The sequence is provided in a numbered list of each of the 1225 genera in 75 monocot families, together with a complementary alphabetical list. The sequence represents a standardized tool for the organisation of monocot herbarium collections.
A new species, Thismia
hongkongensis S.S.Mar & R.M.K.Saunders, is described from Hong Kong. It is most closely related to Thismia
brunonis Griff. from Myanmar, but differs in the number of flowers per inflorescence, the colour of the perianth tube, the length of the filaments, and the shape of the stigma lobes. We also provide inferences on the pollination ecology and seed dispersal of the new species, based on field observations and interpretations of morphology. The flowers are visited by fungus gnats (Myctophilidae or Sciaridae) and scuttle flies (Phoridae), which are likely to enter the perianth tube via the annulus below the filiform tepal appendages, and exit via small apertures between the filaments of the pendent stamens. The flowers are inferred to be protandrous, and flies visiting late-anthetic (pistillate-phase) flowers are possibly trapped within the flower, increasing chances of pollen deposition on the receptive stigma. The seeds are likely to be dispersed by rain splash.
Recent phylogenetic analyses of monocotyledons have indicated that the largely heteromycotrophic families Burmanniaceae and Thismiaceae belong in Dioscoreales, with Dioscoreaceae, Taccaceae and three other hermaphrodite genera Stenomeris, Avetra and Trichopus. Historically this relationship was supported by floral morphological characters, but over the past century these characters have largely been disregarded. In light of the results of recent phylogenetic analyses, the development of floral characters in this group is re-examined by comparative studies of SEM specimens from juvenile to mature stages. Similar structures, such as reflexed stamens with a prolonged connective, umbrella-like stigmas and an urceolate floral chamber occur commonly within this group, and may provide phylogenetically informative characters. Ontogenetic data are critical in identifying possible homologies between floral structures, which may also be closely associated with pollination syndromes.
Tiputinia foetida is described here as a new genus of flowering plants in the Thismiaceae. A single individual of this achlorophyllous mycoheterotroph was found flowering in leaf litter at the Tiputini Biodiversity Station in Amazonian Ecuador. This new taxon is placed in Thismiaceae based on its pyramidal stigma, lack of septal nectaries, and other floral and vegetative features consistent with the other four genera known in the family. It differs from Thismia, the only other genus of the family present in the Neotropics, by its placentae parietally attached to the apex of the ovary; its identical, strap-shaped tepals that are blunt-tipped and horizontally spreading; and its stamens with highly ornamented filaments that are basally broad and erect, then curve inwards to partially obstruct the mouth of the floral tube. Some of these same characters, however, occur in African genera of Thismiaceae such as Afrothismia, Haplothismia, and Oxygyne. The closest relative of Tiputinia may actually be Oxygyne, which differs in having three (vs. six) stamens and less ornamented filaments. At anthesis, the flower of Tiputinia emits a foetid odor that attracts carrion flies and other insects that could function as pollinators. We hypothesize that Tiputinia evolved its scent and unusual floral morphology as a deceit pollination mechanism to attract flies or other pollinators down into the floral tube, where they would first contact the stigma, lay eggs on the inner, horizontal ridges of the tube, and finally contact the latrorse anthers as the insects emerge from the flower. Since foetid odors are capable of attracting pollinators from long distances in other carrion insect-pollinated plants, this pollination system may be particularly effective in rare, ephemeral, and otherwise inconspicuous forest herbs such as Thismiaceae.
Populations of Thismia tentaculata (Burmanniaceae tribe Thismieae) are described and illustrated from
Tai Mo Shan in Hong Kong, southern China. This represents the first report of the genus and tribe from continental
China.
The majority of achlorophyllous mycoheterotrophic plant species associate with arbuscular mycorrhizal fungi (AMF). Previous studies have shown that some species are highly specialized towards narrow lineages of AMF and have suggested that only particular lineages of these fungi are targeted by mycoheterotrophic plants. To test this hypothesis, we analyzed all available partial SSU sequences of AMF associated with mycoheterotrophic plants including data from 13 additional specimens from French Guiana, Gabon and Australia. Sequences were assigned to 'virtual taxa' (VT) according to the MaarjAM database. We found that 20% of all known Glomeromycota VT are involved in mycoheterotrophic interactions and the majority of associations involve Glomeraceae (Glomus Group A) fungi. While some mycoheterotrophic plant species have been found growing with only a single VT, many species are able to associate with a wide range of AMF. We calculated significant phylogenetic clustering of Glomeromycota VT involved in mycoheterotrophic interactions, suggesting that associations between mycoheterotrophic plants and AMF are influenced by the phylogenetic relationships of the fungi. Our results demonstrate that many lineages of AMF are prone to exploitation by mycoheterotrophic plants. However, mycoheterotrophs from different plant lineages and different geographical regions tend to be dependent on lineages of AMF that are phylogenetically related.
The mycoheterotrophic Burmanniaceae are one of the three families currently recognized in the order Dioscoreales. Phylogenetic inference using nucleotide sequences of the nuclear 18S rDNA region and the mitochondrial nad1 b-c intron revealed two well-supported, major lineages within the family, corresponding to the two tribes recognized in the family: Burmannieae and Thismieae. All data supported a strong relationship between Thismieae and Tacca (Dioscoreaceae) making both Burmanniaceae and Dioscoreaceae polyphyletic. The three largest Burmanniaceae genera, Burmannia, Gymnosiphon, and Thismia, are paraphyletic. The splitting of Burmanniaceae into Burmannieae and Thismieae indicates two independent origins of mycoheterotrophy and correlated loss of chlorophyll in Dioscoreales. In the genus Burmannia, in which many species still contain chlorophyll, the achlorophyllous species are nested in between the autotrophic species, suggesting many independent changes from autotrophy to heterotrophy or vice versa. A Bayesian relative rates test on the 18S rDNA data showed considerable variation in substitution rates among Burmanniaceae. The substitution rates in all Thismieae and many Burmannieae are significantly faster than in Dioscoreaceae, but there seems to be no correlation between rate increases and the loss of photosynthesis.
Due to morphological reduction and absence of amplifiable plastid genes, the identification of photosynthetic relatives of heterotrophic plants is problematic. Although nuclear and mitochondrial gene sequences may offer a welcome alternative source of phylogenetic markers, the presence of rate heterogeneity in these genes may introduce bias/systematic error in phylogenetic analyses. We examine the phylogenetic position of Thismiaceae based on nuclear 18S rDNA and mitochondrial atpA DNA sequence data, as well as using parsimony, likelihood and Bayesian inference methods. Significant differences in evolutionary rates of these genes between closely related taxa lead to conflicting results: while parsimony analyses of 18S rDNA and combined data strongly support the monophyly of Thismiaceae, Bayesian inference, with and without a relaxed molecular clock, as well as the Swofford-Olsen-Waddell-Hillis (SOWH) test confidently reject this hypothesis. We show that rate heterogeneity in our data leads to long-branch attraction artifacts in parsimony analysis. However, using model-based inference methods the question of whether Thismiaceae are monophyletic remains elusive. On the one hand maximum likelihood nonparametric bootstrapping and parametric hypothesis tests fail to support a paraphyletic Thismiaceae, on the other hand Bayesian inference methods (both without and with a relaxed clock) significantly reject a monophyletic Thismiaceae. These results show that an adequate sampling, the use of rate homogeneous data, and the application of different inference methods are important factors for developing phylogenetic hypotheses of myco-heterotrophic plants
The ancient arbuscular mycorrhizal association between the vast majority of plants and the fungal phylum Glomeromycota is a dominant nutritional mutualism worldwide. In the mycorrhizal mutualism, plants exchange photosynthesized carbohydrates for mineral nutrients acquired by fungi from the soil. This widespread cooperative arrangement is broken by 'cheater' plant species that lack the ability to photosynthesize and thus become dependent upon three-partite linkages (cheater-fungus-photosynthetic plant). Using the first fine-level coevolutionary analysis of mycorrhizas, we show that extreme fidelity towards fungi has led cheater plants to lengthy evolutionary codiversification. Remarkably, the plants' evolutionary history closely mirrors that of their considerably older mycorrhizal fungi. This demonstrates that one of the most diffuse mutualistic networks is vulnerable to the emergence, persistence and speciation of highly specific cheaters.
Thismia 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. sensu APG 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.
We present novelties in Thismiaceae for the south of the Brazilian Amazon, resulting from botanical expeditions in the north of the Mato Grosso State. The occurrence of four species is recorded: Thismia hyalina; T. melanomitra; T. singeri and a species new to science: T. ribeiroi. These are the first records of the family Thismiaceae, as well as of the genus Thismia and these species for the Mato Grosso State. Thismia melanomitra is a new species for the flora of Brazil and T. singeri is the second record of the species for Brazil. In this study, we also describe and illustrate the new species Thismia ribeiroi.
Thismia arachnites Ridl., previously known only from Perak, Malaysia, is newly reported in tropical lowland forest in south-eastern and peninsular Thailand. A detailed description and photographs are provided. In addition, a lectotype is also designated here.
Two new species of the genus Thismia Griff. (Thismiaceae), T. annamensis (Sect. Euthismia Schlechter, Subsect. Odoardoa Schlechter) and T. tentaculata (Sect. Euthismia Schlechter, Subsect. Brunonithismia Jonk.) are described and illustrated. Both were discovered recently in lowland areas of central Vietnam and represent important additions to the flora of this country.
Thismia mucronata, a new species of Thismiaceae, is described and illustrated. The species was discovered in 2013 during a botanical survey of a forest in the vicinity of Bao Loc town (Lam Dong province, Southern Vietnam). Thismia mucronata is characterised by vermiform roots and mitriform inner tepals. It differs from related species mainly by the short and appressed to each other appendages of inner tepals, which together resemble a short mucro, the narrow mitre without foveae, the almost horizontal annulus and the absence of interstaminal glands. A key to Vietnamese species of Thismia is provided.
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