Parasitic plant, from inside out: endophytic development in Lathrophytum peckoltii (Balanophoraceae) in host liana roots from tribe Paullineae (Sapindaceae).

BACKGROUND AND AIMS: Balanophoraceae is one of the most bizarre and biologically interesting plant clades. It groups species with peculiar features that offers an opportunity for investigating several aspects of parasite plant development and morphogenesis. We analysed the development and the mature vegetative body of Lathrophytum peckoltii Eichler, focusing on the formation of the host-parasite interface. Additionally, we analysed how this parasitic interaction causes modifications to the anatomy of Paullinia uloptera Radlk and Serjania clematidifolia Cambess host roots. METHODS: Vegetative bodies of the parasite at different developmental stages were collected while infesting the roots of Sapindaceae vines. Non-parasitized host roots were also collected for comparison. Light, epifluorescence, confocal and scanning electron microscopy were used for the analysis. KEY RESULTS: The initial cells of the vegetative axis divide repeatedly, originating a parenchymatous matrix, which occupies the space from the cortex to the vascular cylinder of the host's root. In the peripheral layers of the matrix, located near the xylem of the host's roots, a few cells initiate the process of wall lignification, originating the parasitic bundle. The vascular cambium of the host's root changes the division plane and becomes composed of fusiform initials, forming the vascular bundle. The vegetative axis presents a dermal tissue similar to a phellem, a parenchymatous matrix and a vascular system with different origins. CONCLUSION: The parasite reproduces by endophytic development, in a manner similar to that observed for endoparasites. The strategy of late cell differentiation could aid the parasite in avoiding early detection and triggering of defence responses by the host. This development causes changes to the host root cambial activity, leading to the establishment of direct, vessel to vessel connection between host and parasite. We associate these changes with the cambium modularity and an influx of parasite-derived hormones into the host cambium.

Living with a giant, flowering parasite: metabolic differences between Tetrastigma loheri Gagnep. (Vitaceae) shoots uninfected and infected with Rafflesia (Rafflesiaceae) and potential applications for propagation.

MAIN CONCLUSION: Metabolites in Rafflesia-infected and non-infected Tetrastigma were compared which may have applications in Rafflesia propagation. Benzylisoquinoline alkaloids, here reported for the first time in Vitaceae, were abundant in non-infected shoots and may be a form of defense. In Rafflesia-infected shoots, oxylipins, which mediate immune response, were elevated. Endemic to the forests of Southeast Asia, Rafflesia (Rafflesiaceae) is a genus of holoparasitic plants producing the largest flowers in the world, yet completely dependent on its host, the tropical grape vine, Tetrastigma. Rafflesia species are threatened with extinction, making them an iconic symbol of plant conservation. Thus far, propagation has proved challenging, greatly decreasing efficacy of conservation efforts. This study compared the metabolites in the shoots of Rafflesia-infected and non-infected Tetrastigma loheri to examine how Rafflesia infection affects host metabolomics and elucidate the Rafflesia infection process. Results from LC-MS-based untargeted metabolomics analysis showed benzylisoquinoline alkaloids were naturally more abundant in non-infected shoots and are here reported for the first time in the genus Tetrastigma, and in the grape family, Vitaceae. These metabolites have been implicated in plant defense mechanisms and may prevent a Rafflesia infection. In Rafflesia-infected shoots, oxygenated fatty acids, or oxylipins, and a flavonoid, previously shown involved in plant immune response, were significantly elevated. This study provides a preliminary assessment of metabolites that differ between Rafflesia-infected and non-infected Tetrastigma hosts and may have applications in Rafflesia propagation to meet conservation goals.

Horizontal gene transfers dominate the functional mitochondrial gene space of a holoparasitic plant.

Although horizontal gene transfer (HGT) is common in angiosperm mitochondrial DNAs (mtDNAs), few cases of functional foreign genes have been identified. The one outstanding candidate for large-scale functional HGT is the holoparasite Lophophytum mirabile, whose mtDNA has lost most native genes but contains intact foreign homologs acquired from legume host plants. To investigate the extent to which this situation results from functional replacement of native by foreign genes, functional mitochondrial gene transfer to the nucleus, and/or loss of mitochondrial biochemical function in the context of extreme parasitism, we examined the Lophophytum mitochondrial and nuclear transcriptomes by deep paired-end RNA sequencing. Most foreign mitochondrial genes in Lophophytum are highly transcribed, accurately spliced, and efficiently RNA edited. By contrast, we found no evidence for functional gene transfer to the nucleus or loss of mitochondrial functions in Lophophytum. Many functional replacements occurred via the physical replacement of native genes by foreign genes. Some of these events probably occurred as the final act of HGT itself. Lophophytum mtDNA has experienced an unprecedented level of functional replacement of native genes by foreign copies. This raises important questions concerning population-genetic and molecular regimes that underlie such a high level of foreign gene takeover.

Striking developmental convergence in angiosperm endoparasites.

PREMISE: A subset of parasitic plants bear extremely reduced features and grow nearly entirely within their hosts. Until recently, most of these endoparasites were thought to represent a single clade united by their reduced morphology. Current phylogenetic understanding contradicts this assumption and indicates these plants represent distantly related clades, thus offering an opportunity to examine convergence among plants with this life history. METHODS: We sampled species from Apodanthaceae, Cytinaceae, Mitrastemonaceae, and Rafflesiaceae spanning a range of developmental stages. To provide a broader comparative framework, Santalaceae mistletoes with a similar lifestyle were also analyzed. Microtomography and microscopy were used to analyze growth patterns and the ontogeny of host-parasite vascular connections. RESULTS: Apodanthaceae, Cytinaceae, Mitrastemonaceae, and Rafflesiaceae species demonstrated a common development characterized by late cell differentiation. These species were also observed to form direct connections to host vessels and to cause severe alterations of host xylem development. Apodanthaceae and Rafflesiaceae species were additionally observed to form sieve elements, which connect with the host phloem. Endophytic Santalaceae species demonstrated a dramatically different developmental pattern, featuring early cell differentiation and tissue organization, and little effect on host anatomy and cambial activity. CONCLUSIONS: Our results illuminate two distinct developmental trajectories in endoparasites. One involves the retention of embryonic characteristics and late connection with host vessels, as demonstrated in species of Apodanthaceae, Cytinaceae, Mitrastemonaceae, and Rafflesiaceae. The second involves tissue specialization and early connection with host xylem, as exemplified by Santalaceae species. These differences are hypothesized to be related to the absence/presence of photosynthesis in these plants.

Multichromosomal structure and foreign tracts in the Ombrophytum subterraneum (Balanophoraceae) mitochondrial genome.

Horizontal gene transfer (HGT) is frequent in parasitic plant mitochondria as a result of vascular connections established in host-parasite relationships. Recent studies of the holoparasitic plant Lophophytum mirabile (Balanophoraceae) revealed the unprecedented acquisition of a large amount of mitochondrial sequences from its legume host. We focused on a close relative, the generalist holoparasite Ombrophytum subterraneum, to examine the incidence of HGT events in the mitochondrial genome (mtDNA). The mtDNA of O. subterraneum assembles into 54 circular chromosomes, only 34 of which contain the 51 full-length coding regions. Numerous foreign tracts (totaling almost 100 kb, ~ 14% of the mtDNA), including 12 intact genes, were acquired by HGT from the Asteraceae hosts. Nine chromosomes concentrate most of those regions and eight are almost entirely foreign. Native homologs of each foreign gene coexist in the mtDNA and are potentially functional. A large proportion of shorter regions were related to the Fabaceae (a total of ~ 110 kb, 15.4%), some of which were shared with L. mirabile. We also found evidence of foreign sequences donated by angiosperm lineages not reported as hosts (Apocynaceae, Euphorbiaceae, Lamiaceae, and Malvales). We propose an evolutionary hypothesis that involves ancient transfers from legume hosts in the common ancestor of Ombrophytum and Lophophytum followed by more recent transfer events in L. mirabile. Besides, the O. subterraneum mtDNA was also subjected to additional HGT events from diverse angiosperm lineages, including large and recent transfers from the Asteraceae, and also from Lamiaceae.

Rafflesia patma Blume flower organs: histology of the epidermis and vascular structures, and a search for stomata.

MAIN CONCLUSION: A histological study of Rafflesia patma revealed the simplicity of a flower's vascular tissue and epidermal features of flower organs, including their structures and pigmentation. Rafflesia is an endophytic holoparasitic plant that infects Tetrastigma. In a previous study, we characterized the shape of the strands of an endophyte (Rafflesia patma Blume) and hypothesized their distribution. In this study, we deepened our analysis by assessing parts of flower tissue sampled during anthesis, performed surface casting of the abaxial and adaxial sides of the perigone lobe to profile their surface features, and histologically characterized the perigone lobe, perigone tube, and central column base, including the anther and cupula region. The objective of these observations was to compare tissues from different organs and the distribution of cells staining positive for tannin, suberin, and lignin. Observable features in this study were vascular and epidermal tissue. We also observed reduced vascular tissue with xylem and vascular parenchyma in multiple organs. The adaxial epidermis found in the perigone lobes and tube had papillate cells, and their function might be to assist with the emission of odor through chemical evaporation. The abaxial epidermis, also found in perigone lobes and tube, had flattened cells. These, combined with the nearby flattened parenchyma cells, especially in the outermost, early perigone lobe, might provide a tougher (stiffer) outer protective barrier for the flower. The accumulation of tannin in perigone lobes might offer protection to the flower from herbivores prior to anthesis. Although a previous observation indicated the possibility of stomata on the surface of Rafflesia flowers, no stomata were found in this study.

The impact of a native hemiparasite on a major invasive shrub is affected by host size at time of infection.

Many studies have investigated the effect of parasitic plants on their hosts; however, few have examined how parasite impact is affected by host size. In a glasshouse experiment, we investigated the impact of the Australian native hemiparasitic vine, Cassytha pubescens, on a major invasive shrub, Ulex europaeus, of different sizes. Infected plants had significantly lower total, shoot, and root biomass, but the parasite's impact was more severe on small than on large hosts. When infected, small but not large hosts had significantly lower nodule biomass. Irrespective of size, infection significantly decreased the host shoot/root ratio, pre-dawn and midday quantum yields, maximum electron transport rates, and carbon isotope composition, and the host nodule biomass per gram of root biomass significantly increased in response to infection. Infection did not affect host foliar nitrogen concentration or midday shoot water potential. Parasite biomass was significantly lower on small relative to large hosts, but was similar when expressed on a per gram of host total biomass basis. Parasite stem nitrogen, phosphorus, and potassium concentrations were significantly greater when C. pubescens was growing on small than on large hosts. Our results clearly show that C. pubescens strongly decreases performance of this major invasive shrub, especially when hosts are small. This suggests that C. pubescens could be used most effectively as a native biocontrol when deployed on smaller hosts.

Unique bacterial assembly, composition, and interactions in a parasitic plant and its host.

How plant-associated microbiota are shaped by, and potentially contribute to, the unique ecology and heterotrophic life history of parasitic plants is relatively unknown. Here, we investigate the leaf and root bacterial communities of the root holoparasite Orobanche hederae and its host Hedera spp. from natural populations. Root bacteria inhabiting Orobanche were less diverse, had fewer co-associations, and displayed increased compositional similarity to leaf bacteria relative to Hedera. Overall, Orobanche bacteria exhibited significant congruency with Hedera root bacteria across sites, but not the surrounding soil. Infection had localized and systemic effects on Hedera bacteria, which included effects on the abundance of individual taxa and root network properties. Collectively, our results indicate that the parasitic plant microbiome is derived but distinct from the host plant microbiota, exhibits increased homogenization between shoot and root tissues, and displays far fewer co-associations among individual bacterial members. Host plant infection is accompanied by modest changes of associated microbiota at both local and systemic scales compared with uninfected individuals. Our results are a first step towards extending the growing insight into the assembly and function of the plant microbiome to include the ecologically unique but often overlooked guild of heterotrophic plants.

Genome-scale transfer of mitochondrial DNA from legume hosts to the holoparasite Lophophytum mirabile (Balanophoraceae).

Angiosperm mitochondrial horizontal gene transfer (HGT) has been widely reported during the past decades. With a few exceptions, foreign sequences are mitochondrial genes or intronic regions from other plants, indicating that HGT has played a major role in shaping mitochondrial genome evolution. Host-parasite relationships are a valuable system to study this phenomenon due to the high frequency of HGT. In particular, the interaction between mimosoid legumes and holoparasites of the genus Lophophytum represents an outstanding opportunity to discern HGT events. The mitochondrial genome of the holoparasite L. mirabile has remarkable properties, the most extraordinary of which is the presence of 34 out of 43 mitochondrial protein genes acquired from its legume host, with the stunning replacement of up to 26 native homologs. However, the origin of the intergenic sequences that represent the majority (>90%) of the L. mirabile mtDNA remains largely unknown. The lack of mitochondrial sequences available from the donor angiosperm lineage (mimosoid legumes) precluded a large-scale evolutionary study. We sequenced and assembled the mitochondrial genome of the mimosoid Acacia ligulata and performed genome wide comparisons with L. mirabile. The A. ligulata mitochondrial genome is almost 700 kb in size, encoding 60 genes. About 60% of the L. mirabile mtDNA had greatest affinity to members of the family Fabaceae (∼49% to mimosoids in particular) with an average sequence identity of ∼96%, including genes but mostly intergenic regions. These findings strengthen the mitochondrial fusion compatibility model for angiosperm mitochondrion-to-mitochondrion HGT.

Cytinus hypocistis (L.) L. subsp. macranthus Wettst.: Nutritional Characterization.

The habit of eating wild plants in Europe is often associated with times of famine; an example of such is the nectar of Cytinus hypocistis (L.) L., a parasitic plant. To the authors' best knowledge, there are no studies on its nutritional and chemical composition; thus, the whole C. hypocistis (L.) L. subsp. macranthus Wettst. plant (CH) and its nectar (NCH) were nutritionally and chemically characterized. The proximate composition of CH and NCH were very similar in terms of energy, ash, and carbohydrate content. Protein and fat were approximately 2-fold higher in NCH, and crude fiber was 4.6-fold higher in CH compared to NCH. Fructose, glucose, sucrose, and trehalose were the free sugars present in both samples. Oxalic, malic, and citric acids were the identified organic acids in both samples, with citric acid as the most abundant molecule. For both samples, polyunsaturated and saturated fatty acids (PUFA and SFA, respectively) predominate over monounsaturated fatty acids (MUFA) due to the significant contribution of linoleic and palmitic acids, respectively. However, unsaturated fatty acids (UFA) prevail over SFA in CH and NCH. Therefore, CH proved to be an excellent source of nutritional compounds, which supports its use during past periods of scarcity.

Unparalleled replacement of native mitochondrial genes by foreign homologs in a holoparasitic plant.

Horizontal gene transfer (HGT) among flowering plant mitochondria occurs frequently and, in most cases, leads to nonfunctional transgenes in the recipient genome. Parasitic plants are particularly prone to this phenomenon, but their mitochondrial genomes (mtDNA) have been largely unexplored. We undertook a large-scale mitochondrial genomic study of the holoparasitic plant Lophophytum mirabile (Balanophoraceae). Comprehensive phylogenetic analyses were performed to address the frequency, origin, and impact of HGT. The sequencing of the complete mtDNA of L. mirabile revealed the unprecedented acquisition of host-derived mitochondrial genes, representing 80% of the protein-coding gene content. All but two of these foreign genes replaced the native homologs and are probably functional in energy metabolism. The genome consists of 54 circular-mapping chromosomes, 25 of which carry no intact genes. The likely functional replacement of up to 26 genes in L. mirabile represents a stunning example of the potential effect of rampant HGT on plant mitochondria. The use of host-derived genes may have a positive effect on the host-parasite relationship, but could also be the result of nonadaptive forces.

Rafflesia spp.: propagation and conservation.

MAIN CONCLUSION: The propagation of Rafflesia spp. is considered to be important for future development of ornamental and other applications. Thus far, the only successful propagation technique has been grafting. This mini-review succinctly emphasizes what is known about Rafflesia species. Members of the genus Rafflesia (Rafflesiaceae), which are holoparasitic plants known to grow on a host vine, Tetrastigma sp., are widely spread from the Malayan Peninsula to various islands throughout Indonesia. The plant's geographical distribution as well as many other aspects pertaining to the basic biology of this genus have still not been studied. The young flower buds and flowers of wild Rafflesia hasseltii Suringar, Rafflesia keithii Meijer and Rafflesia cantleyi Solms-Laubach are used in local (Malaysia and Indonesia) traditional ethnomedicine as wound-healing agents, but currently no formal published research exists to validate this property. To maintain a balance between its ethnomedicinal and ornamental use, and conservation, Rafflesia spp. must be artificially cultivated to prevent overexploitation. A successful method of vegetative propagation is by host grafting using Rafflesia-impregnated Tetrastigma onto the stem of a normal Tetrastigma plant. Due to difficulties with culture contamination in vitro, callus induction was only accomplished in 2010 for the first time when picloram and 2,4-D were added to a basal Murashige and Skoog medium, and the tissue culture of holoparasitic plants continues to be extremely difficult. Seeds harvested from fertile fruit may serve as a possible method to propagate Rafflesia spp. This paper provides a brief synthesis on what is known about research related to Rafflesia spp. The objective is to further stimulate researchers to examine, through rigorous scientific discovery, the mechanisms underlying the ethnomedicinal properties, the flowering mechanisms, and suitable in vitro regeneration protocols that would allow for the fortification of germplasm conservation.

Cryptic host-specific diversity among western hemisphere broomrapes (Orobanche s.l., Orobanchaceae).

BACKGROUND AND AIMS: The broomrapes, Orobanche sensu lato (Orobanchaceae), are common root parasites found across Eurasia, Africa and the Americas. All species native to the western hemisphere, recognized as Orobanche sections Gymnocaulis and Nothaphyllon, form a clade that has a centre of diversity in western North America, but also includes four disjunct species in central and southern South America. The wide ecological distribution coupled with moderate taxonomic diversity make this clade a valuable model system for studying the role, if any, of host-switching in driving the diversification of plant parasites. METHODS: Two spacer regions of ribosomal nuclear DNA (ITS + ETS), three plastid regions and one low-copy nuclear gene were sampled from 163 exemplars of Orobanche from across the native geographic range in order to infer a detailed phylogeny. Together with comprehensive data on the parasites' native host ranges, associations between phylogenetic lineages and host specificity are tested. KEY RESULTS: Within the two currently recognized species of O. sect. Gymnocaulis, seven strongly supported clades were found. While commonly sympatric, members of these clades each had unique host associations. Strong support for cryptic host-specific diversity was also found in sect. Nothaphyllon, while other taxonomic species were well supported. We also find strong evidence for multiple amphitropical dispersals from central North America into South America. CONCLUSIONS: Host-switching is an important driver of diversification in western hemisphere broomrapes, where host specificity has been grossly underestimated. More broadly, host specificity and host-switching probably play fundamental roles in the speciation of parasitic plants.

Possible loss of the chloroplast genome in the parasitic flowering plant Rafflesia lagascae (Rafflesiaceae).

Rafflesia is a genus of holoparasitic plants endemic to Southeast Asia that has lost the ability to undertake photosynthesis. With short-read sequencing technology, we assembled a draft sequence of the mitochondrial genome of Rafflesia lagascae Blanco, a species endemic to the Philippine island of Luzon, with ∼350× sequencing depth coverage. Using multiple approaches, however, we were only able to identify small fragments of plastid sequences at low coverage depth (<2×) and could not recover any substantial portion of a chloroplast genome. The gene fragments we identified included photosynthesis and energy production genes (atp, ndh, pet, psa, psb, rbcL), ribosomal RNA genes (rrn16, rrn23), ribosomal protein genes (rps7, rps11, rps16), transfer RNA genes, as well as matK, accD, ycf2, and multiple nongenic regions from the inverted repeats. None of the identified plastid gene sequences had intact reading frames. Phylogenetic analysis suggests that ∼33% of these remnant plastid genes may have been horizontally transferred from the host plant genus Tetrastigma with the rest having ambiguous phylogenetic positions (<50% bootstrap support), except for psaB that was strongly allied with the plastid homolog in Nicotiana. Our inability to identify substantial plastid genome sequences from R. lagascae using multiple approaches--despite success in identifying and developing a draft assembly of the much larger mitochondrial genome--suggests that the parasitic plant genus Rafflesia may be the first plant group for which there is no recognizable plastid genome, or if present is found in cryptic form at very low levels.

Hydathode trichomes actively secreting water from leaves play a key role in the physiology and evolution of root-parasitic rhinanthoid Orobanchaceae.

BACKGROUND AND AIMS: Root hemiparasites from the rhinanthoid clade of Orobanchaceae possess metabolically active glandular trichomes that have been suggested to function as hydathode trichomes actively secreting water, a process that may facilitate resource acquisition from the host plant's root xylem. However, no direct evidence relating the trichomes to water secretion exists, and carbon budgets associated with this energy-demanding process have not been determined. METHODS: Macro- and microscopic observations of the leaves of hemiparasitic Rhinanthus alectorolophus were conducted and night-time gas exchange was measured. Correlations were examined among the intensity of guttation, respiration and transpiration, and analysis of these correlations allowed the carbon budget of the trichome activity to be quantified. We examined the intensity of guttation, respiration and transpiration, correlations among which indicate active water secretion. KEY RESULTS: Guttation was observed on the leaves of 50 % of the young, non-flowering plants that were examined, and microscopic observations revealed water secretion from the glandular trichomes present on the abaxial leaf side. Night-time rates of respiration and transpiration and the presence of guttation drops were positively correlated, which is a clear indicator of hydathode trichome activity. Subsequent physiological measurements on older, flowering plants indicated neither intense guttation nor the presence of correlations, which suggests that the peak activity of hydathodes is in the juvenile stage. CONCLUSIONS: This study provides the first unequivocal evidence for the physiological role of the hydathode trichomes in active water secretion in the rhinanthoid Orobanchaceae. Depending on the concentration of organic elements calculated to be in the host xylem sap, the direct effect of water secretion on carbon balance ranges from close to neutral to positive. However, it is likely to be positive in the xylem-only feeding holoparasites of the genus Lathraea, which is closely related to Rhinanthus. Thus, water secretion by the hydathodes might be viewed as a physiological pre-adaptation in the evolution of holoparasitism in the rhinanthoid lineage of Orobanchaceae.

Ethnomedicinal uses, phytochemistry, and pharmacology of the genus Sarcophyte: a review.

Although medicinal plants have been used by ethnic communities since ancient times to prevent and treat various diseases, only a few have been scientifically documented. Therefore, due to their rare availability and lack of comprehensive scientific information, we reviewed the ethnomedicinal uses, phytochemistry, and pharmacological activities of plants within the genus Sarcophyte. To do this, we used specific search terms and phrases to retrieve relevant information from online sources published in English from 2000 to July 2023. The results showed that there are only two plants in the genus Sarcophyte (Sarcophyte sanguinea Sparrm. and Sarcophyte piriei Hutch.), which are traditionally used to treat a wide range of diseases, especially cancer, and skin, gastrointestinal, and urinogenital tract ailments in humans, and to cure animals in ethnoveterinary practices. It was noted that 13 secondary metabolites have been isolated from the two plants, the most prominent of which are flavonoids (diinsininol, diinsinin, and naringenin). The antioxidant activity of S. piriei is reported based on the scavenging of 2,2-diphenyl-1-picrylhydrazyl (DPPH) (IC50: 4.26 ± 0.22 µg/mL) and 2 -2'-Azino-di-[3-ethylbenzthiazoline sulfonate (ABTS) radicals (IC50: 4.62 ± 0.14 µg/mL), chelating iron (IC50: 1.82 ± 0.01 µg/mL, 3.50 ± 0.09 µg/mL), and nitric oxide (IC50: 9.97 ± 0.88 µg/mL, 9.09 ± 0.11 µg/mL). The methanolic stem extracts of S. piriei possess antimicrobial activity against Staphylococcus aureus, Escherichia coli, Klebsiella pneumoniae, Vibrio fluvialis, and Enterococcus avium, with minimum inhibitory concentration (MIC) values ranging from 0.16 to 0.625 mg/mL, and a minimum bactericidal concentration (MBC) of 1.25 to 5 mg/mL. Cytotoxic effects of the extracts from the two plant species were also demonstrated. Sarcophyte piriei possesses therapeutic potential as evidenced by the inhibitory effects of the aqueous rhizome extract on edema (1,000 mg/kg) and prostaglandin synthesis (IC50 = 0.2 mg/mL). In addition, diinsininol and diinsinin were isolated from S. sanguinea inhibited prostaglandin synthesis (IC50: 9.20 µM, 13.14 µM) and platelet-activating factor-induced exocytosis. Therefore, based on this review, further scientific research is needed to demystify the links between traditional medicinal uses, various secondary metabolites, and the pharmacology of the two plants.

Structural Plastome Evolution in Holoparasitic Hydnoraceae with Special Focus on Inverted and Direct Repeats.

Plastome condensation during adaptation to a heterotrophic lifestyle is generally well understood and lineage-independent models have been derived. However, understanding the evolutionary trajectories of comparatively old heterotrophic lineages that are on the cusp of a minimal plastome, is essential to complement and expand current knowledge. We study Hydnoraceae, one of the oldest and least investigated parasitic angiosperm lineages. Plastome comparative genomics, using seven out of eight known species of the genus Hydnora and three species of Prosopanche, reveal a high degree of structural similarity and shared gene content; contrasted by striking dissimilarities with respect to repeat content [inverted and direct repeats (DRs)]. We identified varying inverted repeat contents and positions, likely resulting from multiple, independent evolutionary events, and a DR gain in Prosopanche. Considering different evolutionary trajectories and based on a fully resolved and supported species-level phylogenetic hypothesis, we describe three possible, distinct models to explain the Hydnoraceae plastome states. For comparative purposes, we also report the first plastid genomes for the closely related autotrophic genera Lactoris (Lactoridaceae) and Thottea (Aristolochiaceae).

Cuscuta species: Model organisms for haustorium development in stem holoparasitic plants.

Parasitic plants are notorious for causing serious agricultural losses in many countries. Specialized intrusive organs, haustoria, confer on parasitic plants the ability to acquire water and nutrients from their host plants. Investigating the mechanism involved in haustorium development not only reveals the fascinating mystery of how autotrophic plants evolved parasitism but also provides the foundation for developing more effective methods to control the agricultural damage caused by parasitic plants. Cuscuta species, also known as dodders, are one of the most well-known and widely spread stem holoparasitic plants. Although progress has been made recently in understanding the evolution and development of haustoria in root parasitic plants, more and more studies indicate that the behaviors between root and stem haustorium formation are distinct, and the mechanisms involved in the formation of these organs remain largely unknown. Unlike most endoparasites and root holoparasitic plants, which have high host-specificity and self- or kin-recognition to avoid forming haustoria on themselves or closely related species, auto-parasitism and hyper-parasitism are commonly observed among Cuscuta species. In this review, we summarize the current understanding of haustorium development in dodders and the unique characteristics of their parasitizing behaviors. We also outline the advantages of using Cuscuta species as model organisms for haustorium development in stem holoparasitic plants, the current unknown mysteries and limitations in the Cuscuta system, and potential future research directions to overcome these challenges.

Trophic Transfer without Biomagnification of Cadmium in a Soybean-Dodder Parasitic System.

Cadmium (Cd) is among the most available and most toxic heavy metals taken up by plants from soil. Compared to the classic plant-animal food chains, the host-parasitic plant food chains have, thus far, been largely overlooked in the studies of Cd trophic transfer. To investigate the pattern of Cd transfer during the infection of parasitic plants on Cd-contaminated hosts, we conducted a controlled experiment that grew soybeans parasitized by Chinese dodders (Cuscuta chinensis) in soil with different levels of Cd treatment, and examined the concentration, accumulation, allocation and transfer coefficients of Cd within this parasitic system. Results showed that among all components, dodders accounted for more than 40% biomass of the whole system but had the lowest Cd concentration and accumulated the least amount of Cd. The transfer coefficient of Cd between soybean stems and dodders was much lower than 1, and was also significantly lower than that between soybean stems and soybean leaves. All these features were continuously strengthened with the increase of Cd treatment levels. The results suggested no evidence of Cd biomagnification in dodders parasitizing Cd-contaminated hosts, and implied that the Cd transfer from hosts to dodders may be a selective process.

How do holoparasitic plants exploit vitamin K1?

Phylloquinone (vitamin K1) is a thylakoid-embedded electron carrier essential for photosynthesis. Paradoxically, we found that phylloquinone biosynthesis is retained in the nonphotosynthetic holoparasite Phelipanche aegyptiaca (Egyptian broomrape). The phylloquinone pathway genes are preferentially expressed during development of the invasive organ, the haustorium, and exhibit strong coexpression with redox-active proteins known to be involved in parasitism. Unlike in photoautotrophic taxa, the late pathway genes of the holoparasite lack the chloroplast-targeting sequence and their proteins are targeted to the plasma membrane instead. Plasma membrane phylloquinone may enable Phelipanche to sense changes in the redox environment during host interactions. The N-truncated isoforms are conserved in several other Orobanchaceae root holoparasites, and interestingly, in a number of closely related photoautotrophic species as well. This suggests an ancient origin of distinct phylloquinone pathways predating the evolution of parasitic plants in the Orobanchaceae. These findings represent exciting opportunities to probe plasma membrane phylloquinone function and diversification in parasitic and nonparasitic plant responses to external redox chemistry in the rhizosphere.