Non-photosynthetic Plants Research Articles

Dual roles of terrestrial isopods in seed predation and seed dispersal in Phacellanthus tubiflorus (Orobancheaceae)

AbstractTerrestrial isopods are known to play significant roles in litter decomposition and seed predation. The present study examines the function of terrestrial isopods, particularly Armadillidium vulgare and Armadillidium nasatum, in the seed dispersal of a nonphotosynthetic plant, Phacellanthus tubiflorus. These isopods were observed ingesting seeds in the natural habitat of P. tubiflorus in Hyogo Prefecture, Japan. Contrary to the prevailing belief that invertebrates do not serve as effective internal seed dispersers, our analysis demonstrated that some seeds ingested by A. vulgare and A. nasatum were excreted whole, with viability rates comparable to those of seeds directly sourced from fruits. This indicates that these isopods could act not only as seed predators but also as seed dispersers. The research highlights the importance of further exploration into the ecological contributions of isopods and other invertebrates as seed dispersers.

Rediscovery of the presumably extinct fairy lantern Thismia kobensis (Thismiaceae) in Hyogo Prefecture, Japan, with discussions on its taxonomy, evolutionary history, and conservation

Thismia (commonly known as fairy lanterns) is a genus of strange-looking, elusive, and non-photosynthetic plants. Thismia kobensis was first discovered in Kobe City, Hyogo Prefecture, Japan in 1992, but it was believed to be extinct, given that its type locality was destroyed during the construction of an industrial complex. Here, we have reported the rediscovery of T. kobensis in Sanda City, Hyogo Prefecture, which is located approximately 30 km from the type locality. The new locality of T. kobensis is the northernmost distributional limit of Asian Thismiaceae species. As the original description of the species was based on a single museum specimen that lacked two of the three inner perianth lobes, we have provided an amended description of T. kobensis, highlighting its differences from the morphologically similar species T. huangii. Specifically, our morphological re-examination has revealed that T. kobensis is distinguishable from T. huangii by its short but expanded annulus and many short hairs on each stigma lobe. We have also demonstrated that the genetic distance between these taxa is comparable to that between other closely related species pairs. Finally, we have provided brief notes on the taxonomy, biogeography, evolutionary history, and conservation of T. kobensis and its closely related species, including an enigmatic species T. americana.

Phylotranscriptomic Analyses of Mycoheterotrophic Monocots Show a Continuum of Convergent Evolutionary Changes in Expressed Nuclear Genes From Three Independent Nonphotosynthetic Lineages.

Mycoheterotrophy is an alternative nutritional strategy whereby plants obtain sugars and other nutrients from soil fungi. Mycoheterotrophy and associated loss of photosynthesis have evolved repeatedly in plants, particularly in monocots. Although reductive evolution of plastomes in mycoheterotrophs is well documented, the dynamics of nuclear genome evolution remains largely unknown. Transcriptome datasets were generated from four mycoheterotrophs in three families (Orchidaceae, Burmanniaceae, Triuridaceae) and related green plants and used for phylogenomic analyses to resolve relationships among the mycoheterotrophs, their relatives, and representatives across the monocots. Phylogenetic trees based on 602 genes were mostly congruent with plastome phylogenies, except for an Asparagales + Liliales clade inferred in the nuclear trees. Reduction and loss of chlorophyll synthesis and photosynthetic gene expression and relaxation of purifying selection on retained genes were progressive, with greater loss in older nonphotosynthetic lineages. One hundred seventy-four of 1375 plant benchmark universally conserved orthologous genes were undetected in any mycoheterotroph transcriptome or the genome of the mycoheterotrophic orchid Gastrodia but were expressed in green relatives, providing evidence for massively convergent gene loss in nonphotosynthetic lineages. We designate this set of deleted or undetected genes Missing in Mycoheterotrophs (MIM). MIM genes encode not only mainly photosynthetic or plastid membrane proteins but also a diverse set of plastid processes, genes of unknown function, mitochondrial, and cellular processes. Transcription of a photosystem II gene (psb29) in all lineages implies a nonphotosynthetic function for this and other genes retained in mycoheterotrophs. Nonphotosynthetic plants enable novel insights into gene function as well as gene expression shifts, gene loss, and convergence in nuclear genomes.

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.

Respiratory energy demands and scope for demand expansion and destruction.

Nonphotosynthetic plant metabolic processes are powered by respiratory energy, a limited resource that metabolic engineers—like plants themselves—must manage prudently.

The plastomes of Hyalomonas oviformis and Hyalogonium fusiforme evolved dissimilar architectures after the loss of photosynthesis.

The loss of photosynthesis in land plants and algae is typically associated with parasitism but can also occur in free‐living species, including chlamydomonadalean green algae. The plastid genomes (ptDNAs) of colorless chlamydomonadaleans are surprisingly diverse in architecture, including highly expanded forms ( Polytoma uvella and Leontynka pallida) as well as outright genome loss (Polytomella species). Here, we explore the ptDNAs of Hyalomonas (Hm.) oviformis (SAG 62‐27; formerly known as Polytoma oviforme) and Hyalogonium (Hg.) fusiforme (SAG 62‐1c), each representing independent losses of photosynthesis within the Chlamydophyceae. The Hm. oviformis ptDNA is moderately sized (132 kb) with a reduced gene complement (but still encoding the ATPase subunits) and is in fact smaller than that of its photosynthetic relative Hyalomonas chlamydogama SAG 11‐48b (198.3 kb). The Hg. fusiforme plastome, however, is the largest yet observed in nonphotosynthetic plants or algae (~463 kb) and has a coding repertoire that is almost identical to that of its photosynthetic relatives in the genus Chlorogonium. Furthermore, the ptDNA of Hg. fusiforme shows no clear evidence of pseudogenization, which is consistent with our analyses showing that Hg. fusiforme is the nonphotosynthetic lineage of most recent origin among known colorless Chlamydophyceae. Together, these new ptDNAs clearly show that, in contrast to parasitic algae, plastid genome compaction is not an obligatory route following the loss of photosynthesis in free‐living algae, and that certain chlamydomonadalean algae have a remarkable propensity for genomic expansion, which can persist regardless of the trophic strategy.

Genomic comparison of non-photosynthetic plants from the family Balanophoraceae with their photosynthetic relatives.

The plant family Balanophoraceae consists entirely of species that have lost the ability to photosynthesize. Instead, they obtain nutrients by parasitizing other plants. Recent studies have revealed that plastid genomes of Balanophoraceae exhibit a number of interesting features, one of the most prominent of those being a highly elevated AT content of nearly 90%. Additionally, the nucleotide substitution rate in the plastid genomes of Balanophoraceae is an order of magnitude greater than that of their photosynthetic relatives without signs of relaxed selection. Currently, there are no definitive explanations for these features. Given these unusual features, we hypothesised that the nuclear genomes of Balanophoraceae may also provide valuable information in regard to understanding the evolution of non-photosynthetic plants. To gain insight into these genomes, in the present study we analysed the transcriptomes of two Balanophoraceae species (Rhopalocnemis phalloides and Balanophora fungosa) and compared them to the transcriptomes of their close photosynthetic relatives (Daenikera sp., Dendropemon caribaeus, and Malania oleifera). Our analysis revealed that the AT content of the nuclear genes of Balanophoraceae did not markedly differ from that of the photosynthetic relatives. The nucleotide substitution rate in the genes of Balanophoraceae is, for an unknown reason, several-fold larger than in the genes of photosynthetic Santalales; however, the negative selection in Balanophoraceae is likely stronger. We observed an extensive loss of photosynthesis-related genes in the Balanophoraceae family members. Additionally, we did not observe transcripts of several genes whose products function in plastid genome repair. This implies their loss or very low expression, which may explain the increased nucleotide substitution rate and AT content of the plastid genomes.

Comparative Analysis of Plastid Genomes in the Non-photosynthetic Genus Thismia Reveals Ongoing Gene Set Reduction.

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.

A specialized avian seed dispersal system in a dry-fruited nonphotosynthetic plant, Balanophora yakushimensis.

The family Balanophoraceae are among the most unusual of plants because they have aberrant vegetative bodies, highly reduced flowers, and small and reduced embryos (Hansen 1972, Gonzalez et al. 2019). Because the plants lack chlorophyll and are incapable of photosynthesis, they draw nutrition from other organisms. Indeed, like the well-known parasitic plant, Rafflesia, members of the Balanophoraceae acquire both water and nutrients from host plants. They are, therefore, highly specialized root parasites.

Oxidative Stress and Marine Carotenoids: Application by Using Nanoformulations.

Carotenoids are natural fat-soluble pigments synthesized by plants, algae, fungi and microorganisms. They are responsible for the coloration of different photosynthetic organisms. Although they play a role in photosynthesis, they are also present in non-photosynthetic plant tissues, fungi, and bacteria. These metabolites have mainly been used in food, cosmetics, and the pharmaceutical industry. In addition to their utilization as pigmentation, they have significant therapeutically applications, such as improving immune system and preventing neurodegenerative diseases. Primarily, they have attracted attention due to their antioxidant activity. Several statistical investigations indicated an association between the use of carotenoids in diets and a decreased incidence of cancer types, suggesting the antioxidant properties of these compounds as an important factor in the scope of the studies against oxidative stress. Unusual marine environments are associated with a great chemical diversity, resulting in novel bioactive molecules. Thus, marine organisms may represent an important source of novel biologically active substances for the development of therapeutics. Marine carotenoids (astaxanthin, fucoxanthin, β-carotene, lutein but also the rare siphonaxanthin, sioxanthin, and myxol) have recently shown antioxidant properties in reducing oxidative stress markers. Numerous of bioactive compounds such as marine carotenoids have low stability, are poorly absorbed, and own very limited bioavailability. The new technique is nanoencapsulation, which can be used to preserve marine carotenoids and their original properties during processing, storage, improve their physiochemical properties and increase their health-promoting effects. This review aims to describe the role of marine carotenoids, their potential applications and different types of advanced nanoformulations preventing and treating oxidative stress related disorders.

Use of radiocarbon for assessing the mycorrhizal status of mycoheterotrophic plants

ABSTRACT Mycoheterotrophic plants are non-photosynthetic plants that obtain nutrients from fungi. Even though most of these plants are associated with the mycorrhizal partners of surrounding photosynthetic plants, recent studies have suggested that some mycoheterotrophic orchids indirectly obtain carbon from decaying organic matter through associations with saprotrophic fungi. However, such suggestions have been based primarily on indirect evidence, such as the 13C and 15N abundances of fungi and plants. It was recently reported that some mycoheterotrophs yield elevated Δ 14C values, owing to the indirect acquisition of 14C-enriched bomb carbon from dead wood. The approach was based on the anthropogenic change of Δ 14C values; atmospheric CO2 were globally elevated by nuclear weapons testing in the 1950s and early 1960s, but have steadily declined since its peak after the atmospheric nuclear test ban treaty of 1963. The study has provided novel evidence that mycoheterotrophic plants can exploit both mycorrhizal and saprotrophic fungi. We suggest that the radiocarbon analysis is also useful for investigating the nutritional modes of mixotrophic plants as well as for investigating whether the recruitment of wood-decaying fungi into novel mycorrhizal partnerships preceded the evolution of full mycoheterotrophy.

Mitochondrial genome of the nonphotosynthetic mycoheterotrophic plant Hypopitys monotropa, its structure, gene expression and RNA editing.

Heterotrophic plants—plants that have lost the ability to photosynthesize—are characterized by a number of changes at all levels of organization. Heterotrophic plants are divided into two large categories—parasitic and mycoheterotrophic (MHT). The question of to what extent such changes are similar in these two categories is still open. The plastid genomes of nonphotosynthetic plants are well characterized, and they exhibit similar patterns of reduction in the two groups. In contrast, little is known about the mitochondrial genomes of MHT plants. We report the structure of the mitochondrial genome of Hypopitys monotropa, a MHT member of Ericaceae, and the expression of its genes. In contrast to its highly reduced plastid genome, the mitochondrial genome of H. monotropa is larger than that of its photosynthetic relative Vaccinium macrocarpon, and its complete size is ~810 Kb. We observed an unusually long repeat-rich structure of the genome that suggests the existence of linear fragments. Despite this unique feature, the gene content of the H. monotropa mitogenome is typical of flowering plants. No acceleration of substitution rates is observed in mitochondrial genes, in contrast to previous observations in parasitic non-photosynthetic plants. Transcriptome sequencing revealed the trans-splicing of several genes and RNA editing in 33 of 38 genes. Notably, we did not find any traces of horizontal gene transfer from fungi, in contrast to plant parasites, which extensively integrate genetic material from their hosts.

Root-Associated Fungal Communities in Two Populations of the Fully Mycoheterotrophic Plant Arachnitis uniflora Phil. (Corsiaceae) in Southern Chile.

The microbiological interactions of the roots of non-photosynthetic plants in South America have been scarcely explored. This study analyzes culturable fungal diversity associated with the mycoheterotrophic plant Arachnitis uniflora Phil. (Corsiaceae) in southern Chile, growing in two different understoreys of native (Nothofagus-dominated) and mixed forest (native, Cupressus sempervirens, and Pinus radiata). Rhizospheric and endophytic fungi were isolated, cultured, and purified to identify microorganisms associated with A. uniflora roots. We showed the different fungi associated with the plant, and that these distributions are influenced by the sampling site. We isolated 410 fungal strains (144 endophytic and 266 from the rhizosphere). We identified 13 operative taxonomical units from plants sampled in the mixed forest, while 15 were from the native forest. Rhizospheric microorganisms were mainly related to Penicillium spp., whereas some pathogenic and saprophytic strains were more frequent inside the roots. Our results have also shown that the fungal strains are weak for phosphate solubilization, but other pathways such as organic acid exudation and indole acetic acid production can be considered as major mechanisms to stimulate plant growth. Our results point to new fungal associates of A. uniflora plants reported in Andean ecosystems, identifying new beneficial endophytic fungi associated with roots of this fully mycoheterotrophic plant.

Antiproliferative and antiviral activity of methanolic extracts from Sardinian Maltese Mushroom (Cynomorium coccineum L.)

Cynomorium coccineum is a non-photosynthetic plant that grows in Mediterranean countries and that is amply used in the traditional medicine. The aim of this study was to extend previous studies on the chemical and biological properties of C. coccineum, evaluating the potential antiviral and antiproliferative activity of the methanolic extract. The MTT assay was used for the in vitro cytotoxic studies against human cancer-derived cell lines, while both MTT and plaque reduction (PRT) methods were used to evaluate the potential inhibitory effect of the extract against a panel of mammal viruses. The results obtained showed no selective activity against any DNA and RNA virus but revealed an interesting antiproliferative activity against human leukaemia-derived cell lines.

Oxygyne: An extraordinarily elusive flower

<i>Oxygyne</i>: An extraordinarily elusive flower

Evolution: A Plant Plastid Genome that Has Forsaken Guanine and Cytosine

The plastid genomes of the non-photosynthetic plants Balanophora reflexa and B.laxiflora are among the most GC-biased genomes observed to date. A new study shows that ∼80% of the plastid-derived proteome is represented by only six amino acids, and several genes are in excess of 95% AT.

Novel genetic code and record-setting AT-richness in the highly reduced plastid genome of the holoparasitic plant Balanophora

Plastid genomes (plastomes) vary enormously in size and gene content among the many lineages of nonphotosynthetic plants, but key lineages remain unexplored. We therefore investigated plastome sequence and expression in the holoparasitic and morphologically bizarre Balanophoraceae. The two Balanophora plastomes examined are remarkable, exhibiting features rarely if ever seen before in plastomes or in any other genomes. At 15.5 kb in size and with only 19 genes, they are among the most reduced plastomes known. They have no tRNA genes for protein synthesis, a trait found in only three other plastid lineages, and thus Balanophora plastids must import all tRNAs needed for translation. Balanophora plastomes are exceptionally compact, with numerous overlapping genes, highly reduced spacers, loss of all cis-spliced introns, and shrunken protein genes. With A+T contents of 87.8% and 88.4%, the Balanophora genomes are the most AT-rich genomes known save for a single mitochondrial genome that is merely bloated with AT-rich spacer DNA. Most plastid protein genes in Balanophora consist of ≥90% AT, with several between 95% and 98% AT, resulting in the most biased codon usage in any genome described to date. A potential consequence of its radical compositional evolution is the novel genetic code used by Balanophora plastids, in which TAG has been reassigned from stop to tryptophan. Despite its many exceptional properties, the Balanophora plastome must be functional because all examined genes are transcribed, its only intron is correctly trans-spliced, and its protein genes, although highly divergent, are evolving under various degrees of selective constraint.

Comparative analysis of nucleus-encoded plastid-targeting proteins in Rafflesia cantleyi against photosynthetic and non-photosynthetic representatives reveals orthologous systems with potentially divergent functions

Parasitic plants are known to discard photosynthesis thus leading to the deletion or loss of the plastid genes. Despite plastid genome reduction in non-photosynthetic plants, some nucleus-encoded proteins are transported back to the plastid to carry out specific functions. In this work, we study such proteins in Rafflesia cantleyi, a member of the holoparasitic genus well-known for producing the largest single flower in the world. Our analyses of three transcriptome datasets, two holoparasites (R. cantleyi and Phelipanche aegyptiaca) and one photosynthetic plant (Arabidopsis thaliana), suggest that holoparasites, such as R. cantleyi, retain some common plastid associated processes such as biosynthesis of amino acids and lipids, but are missing photosynthesis components that can be extensions of these pathways. The reconstruction of two selected biosynthetic pathways involving plastids correlates the trend of plastid retention to pathway complexity - transcriptome evidence for R. cantleyi suggests alternate mechanisms in regulating the plastidial heme and terpenoid backbone biosynthesis pathways. The evolution to holoparasitism from autotrophy trends towards devolving the plastid genes to the nuclear genome despite the functional sites remaining in the plastid, or maintaining non-photosynthetic processes in the plastid, before the eventual loss of the plastid and any site dependent functions.

RNA-seq highlights parallel and contrasting patterns in the evolution of the nuclear genome of fully mycoheterotrophic plants

BackgroundWhile photosynthesis is the most notable trait of plants, several lineages of plants (so-called full heterotrophs) have adapted to obtain organic compounds from other sources. The switch to heterotrophy leads to profound changes at the morphological, physiological and genomic levels.ResultsHere, we characterize the transcriptomes of three species representing two lineages of mycoheterotrophic plants: orchids (Epipogium aphyllum and Epipogium roseum) and Ericaceae (Hypopitys monotropa). Comparative analysis is used to highlight the parallelism between distantly related fully heterotrophic plants.In both lineages, we observed genome-wide elimination of nuclear genes that encode proteins related to photosynthesis, while systems associated with protein import to plastids as well as plastid transcription and translation remain active. Genes encoding components of plastid ribosomes that have been lost from the plastid genomes have not been transferred to the nuclear genomes; instead, some of the encoded proteins have been substituted by homologs. The nuclear genes of both Epipogium species accumulated nucleotide substitutions twice as rapidly as their photosynthetic relatives; in contrast, no increase in the substitution rate was observed in H. monotropa.ConclusionsFull heterotrophy leads to profound changes in nuclear gene content. The observed increase in the rate of nucleotide substitutions is lineage specific, rather than a universal phenomenon among non-photosynthetic plants.

Sequencing and assembly of transcriptome in non-photosynthetic plant Lathraea squamaria and its dynamics during the light and dark period of the day

Sequencing and assembly of transcriptome in non-photosynthetic plant Lathraea squamaria and its dynamics during the light and dark period of the day