Figure 9 - uploaded by Luiza Teixeira-Costa
Content may be subject to copyright.
Likelihood ancestral state reconstruction of haustorium types within the Loranthaceae, plus outgroups. Phylogenetic reconstruction based on Bayesian inference, as originally recovered by Liu et al. (2018) using both nuclear and chloroplast genes. Posterior probability values are indicated in the original reference, all of them scored as 0.52 or higher.
Source publication
Parasitic plants have evolved independently at least 12 times among the angiosperms, adding up to ca. 1% of the diversity of this group. Mistletoes, shrubby to arboreal parasitic plants infesting the aboveground organs of their hosts, have evolved at least five times within the Santalales. Currently accounted to include 89 genera, representing near...
Contexts in source publication
Context 1
... aerial Loranthaceae, the largest and most diverse group among the five independent mistletoe evolutions, epicortical roots were reconstructed to be the ancestral haustorium type (Figure 9). When compared to the haustorial system of early diverging root-parasitic species within the family, both epicortical root-forming mistletoes and root parasites show similar general organization, with the formation of a network of multiple host-parasite connections. ...
Context 2
... as lateral flanges become embedded within the host wood, newly formed, and therefore certainly functional host xylem, is constantly abutted by parasitic cells, guaranteeing continuous sap flux towards the parasite (Menzies 1954). Likewise, considering the evolution of a single group of aerial parasites within Santaleae (Santalaceae), with Antidaphne being the earliest diverging genera (Der and Nickrent 2008;Vidal-Russell and Nickrent 2008;Nickrent et al. 2010;Liu et al. 2018;Nickrent, Anderson, and Kuijt 2019), epicortical roots were also reconstructed to be the ancestral haustorium type among aerial species of this clade (Figure 9). Lateral flanges formed by Antidaphne spp. ...
Context 3
... Phacellaria species are known to have a fragmented and dispersed endophytic tissue (Kuijt 1969;Heide-Jørgensen 2008;Kuijt and Hansen 2015), which indicates the formation of cortical strands similar to those observed in Arceuthobium spp. Species belonging to few Loranthaceae genera also develop bark strands (Figure 9). These genera are Oncocalyx spp., native to southeast Africa, extending to Arabia (Calvin and Wilson 1998;Kuijt and Hansen 2015); Helixanthera spp., native to central and southeast Africa andAsia (Calvin andWilson 1998, Kuijt andHansen 2015); Diplatia spp., native to Australia (Thoday 1963;Kuijt and Hansen 2015); Tristerix spp., native to the Andean region (Kuijt 1982;Mauseth, Montenegro, and Walckowiak 1984;Kuijt and Hansen 2015); and Ligaria spp., native to south and north Brazil, and western South America (Reiche 1907;Kuijt and Hansen 2015). ...
Similar publications
Mistletoe Dendrophthoe pentandra (L.)Miq is a parasitic plant commonly found parasitizing and infesting medicinal plants such as Cassia fistula L. This research aimed to investigate the infestation of D. pentandra on C. fistula on various trees canopy shading, infested host number and plant diversity. Study was conducted in Purwodadi Botanic Garden...
Citations
... The enrichment of gall-associated bacteria [22,26,41,72] in floral buds of both Rafflesia species, alongside elevated levels of adenine/cytokinin-a key phytohormone involved in gall formation-supports the 'gall hypothesis' for Rafflesia. While Teixeira-Costa et al. [75] highlighted mistletoes as unique among plant parasites for their ability to induce woody galls in hosts, our current findings suggest that members of the Rafflesiaceae may also be capable of forming gall-like structures. Notably, transcriptomic studies on Rafflesia and Sapria have revealed gene expression patterns akin to those observed in oak galls [38], suggesting that these parasitic plants exhibit transcriptomic features reminiscent of gall structures (M. ...
Rafflesia, known for producing the world’s largest flowers, is a holoparasite found only in Southeast Asia's rapidly diminishing tropical forests. Completely dependent on its Tetrastigma host plants, Rafflesia grows covertly within its host until flowering, but the ecological factors driving host susceptibility are unknown. With most Rafflesia species on the brink of extinction due to habitat loss, understanding the complex ecological interactions between Rafflesia and its host is crucial for conservation. In this study, we integrated metagenomic data with metabolomic profiles to identify potential functional relationships between microbial communities and specific metabolites, shedding light on their ecological roles in Rafflesia's life cycle. Key findings reveal that microbial taxa such as Microbacteriaceae and Nocardioidaceae correlate with elevated levels of polyphenols, particularly gallic acid derivatives, which may shape the chemical environment conducive to Rafflesia development. Complex-carbon-degrading bacteria thrive in the chemically distinct environment of Rafflesia buds, while an unknown group of Saccharimonadales was enriched in Tetrastigma host species. Docosenamide production in Rafflesia buds and their hosts may facilitate parasitic infection, while coumarin compounds in non-host Tetrastigma species may exert allelopathic effects. The enrichment of gallic acid derivatives, the phytohormone adenine, and gall-associated bacteria suggests that Rafflesia buds may function similarly to plant galls, manipulating host tissues to support their reproductive development. This study highlights the dynamic microbial shifts during Rafflesia’s development, emphasizing its symbiotic relationship with microbial communities and hosts. In identifying essential microbial and chemical conditions that could improve propagation techniques, this research has practical applications in ex situ conservation efforts, aiding in the rescue of the world’s largest flowers from the brink of extinction.
... The evolutionary history of haustorial type corresponds to changes to the Australian climate and biomes with ERs considered plesiomorphic in Loranthaceae based on structural (Hamilton and Barlow, 1963), phylogenetic , and character reconstruction (Teixeira-Costa et al., 2020) studies. Species with ERs are currently present in ancestral mesic biomes identified by Byrne et al. (2011) while derived, single-attachment haustoria in Australia, WR, CU, and BS, are considered convergent Teixeira-Costa, 2020) and are present in species from the arid interior of Australia. ...
... The evolutionary history of haustorial type corresponds to changes to the Australian climate and biomes with ERs considered plesiomorphic in Loranthaceae based on structural (Hamilton and Barlow, 1963), phylogenetic , and character reconstruction (Teixeira-Costa et al., 2020) studies. Species with ERs are currently present in ancestral mesic biomes identified by Byrne et al. (2011) while derived, single-attachment haustoria in Australia, WR, CU, and BS, are considered convergent Teixeira-Costa, 2020) and are present in species from the arid interior of Australia. This suggests the evolution of derived haustoria is associated with the historic shift in habitat type from a continent-wide mesic biome to a more complex mosaic of habitats that includes a large arid region in central Australia. ...
... This suggests the evolution of derived haustoria is associated with the historic shift in habitat type from a continent-wide mesic biome to a more complex mosaic of habitats that includes a large arid region in central Australia. Teixeira-Costa et al. (2020) noted based on results of Liu et al. (2018) that Loranthaceae genera with BSs, including those from Australia, diverged during periods marked by dry climates. The extent of haustorial diversity present prior to the development of modern Australian biomes is unknown, but any diversity present is likely to have contributed to the ability of mistletoes to persist and diversify during aridification. ...
Mistletoes are branch parasites of trees and shrubs, occur world-wide, and are considered keystone species in many forest communities. They have complex interactions with seed dis- persers, pollinators, and animals that use them for shelter, and contribute to community pro- ductivity and biotic diversity. Current understanding of mistletoe occurrence largely attributes host availability and preference to patterns of distribution. Using occurrence records, climate data, and climate modeling, we investigated current distributions and modeled contemporary and future distributions of Australian mistletoes in the Loranthaceae by haustorial type. Although Loranthaceae mistletoes are distributed throughout Australia, our results show distributional differences among haustorial types across biomes and identify their actual and predicted ecological niches based on temperature and precipitation. Epicortical roots, which are considered plesiomorphic in Australia, are mostly associated with mesic ancestral habitats while derived types are associated with drier habitats. Combining the results of all analyses we show that mistletoe distributional patterns, similar to distribution patterns in other angiosperms, are correlated with climate and are susceptible to climate change with expected loss of habitat, primarily in interior arid regions of Australia.
... Pouco depois do processo de germinação, estas parasitas dão início à formação do haustório, o qual se desenvolve em uma estrutura de madeira frequentemente volumosa. Conforme seu desenvolvimento progride, a maioria das espécies de ervas-de-passarinho forma pontos adicionais de conexão com o caule da hospedeira (Teixeira-Costa et al., 2020) ...
A madeira é um recurso natural extremamente versátil, utilizado pela humanidade para variados fins, desde geração de energia até fabricação de papel. Ao mesmo tempo, a madeira é uma parte fundamental do corpo das plantas que a produzem, desempenhando funções mecânicas, metabólicas e fisiológicas. Do ponto de vista botânico, a maderia corresponde a um tecido vegetal composto por diversos tipos de células, as quais podem ser formadas em diferentes proporções e organizadas em uma variedade de padrões. Tal diversidade estrutural tem relação direta com os usos adequados para cada tipo de madeira, bem como com as funções desempenhadas por essa estrutura no corpo de uma planta. Assim, estudos sobre desenvolvimento, estrutura anatômica, resposta ao meio ambiente e análise de propriedades fisicoquímicas das madeiras são de extrema importância. Este manual apresenta os procedimentos para coleta e armazenamento de amostras de madeira que se destinem coleções biológicas, num esforço para estimular o crescimento destas coleções, além de padronizar e elevar a qualidade das informações associadas às amostras. Além da coleta de madeira proveniente de árvores, este manual apresenta procedimentos e cuidados específicos para a coleta de de outros tipos de plantas que produzem madeira, como cipós lenhosos (lianas) e plantas parasitas. Dois capítulos deste guia dedicam-se às especificidades da coleta de material para análises de anéis de crescimento. Por fim, técnicas para coleta de madeiras antigas ou fósseis também são descritas em um capítulo específico.
... Despite their multiple evolutionary origins and huge diversity, certain parasitic plants have the potential to form specialized organ (haustoria), which penetrates host tissues and establishes a vascular connection between parasite and host (Teixeira-Costa et al. 2020; Pan et al. 2022). External features of haustoria of different parasitic plants may vary, but they are usually recognizable as swollen, knob-shaped, or clasping structures composed of different tissues and cell types, homologous to the root or subterranean plant structures, such as tubers and rhizomes or occur as numerous lateral organs on roots or shoots (Atsatt 1983;Joel 2013;Teixeira-Costa et al. 2020 (Haynes et al. 1996). Lauraceae is a family of about 50 genera and about 3000 species with mostly subtropical and tropical trees and shrubs except for the genus Cassytha which is most diverse in the American and Asian tropics, although many species occur in Australia and Madagascar (Harris 2004). ...
Climbers are essential part of our ecological systems and forests. They give us foods, medicines and other life stuffs. They are also important ornamental plants throughout the world and show unique horticultural uses. The most of species of the family Dioscoreaceae, Cucurbitaceae, Apocynaceae, Celastraceae, Convulvulaceae etc are climbers. Many of these species are used as foods and in folk medicinal practices, still they are unexplored. The book “Medicinal Climbers” is designed to bring attention towards the importance of climbers in our day-to-day life in general and particular as medicinal agents. The book will be very useful to students, researchers, local people and intellectuals. Although further studies and research are needed still, this book will certainly raise an interest on this hitherto little-known climbing plant.
... Parasitic seed plants are distinguished by their capacity to form specialized intrusive and absorptive organs called haustoria (Atsatt 1983). Despite their multiple evolutionary origins and huge diversity, certain parasitic plants have the potential to form specialized organ (haustoria), which penetrates host tissues and establishes a vascular connection between parasite and host (Teixeira-Costa et al. 2020;Pan et al. 2022). External features of haustoria of different parasitic plants may vary, but they are usually recognizable as swollen, knob-shaped, or clasping structures composed of different tissues and cell types, homologous to the root or subterranean plant structures, such as tubers and rhizomes or occur as numerous lateral organs on roots or shoots (Atsatt 1983;Joel 2013;Teixeira-Costa et al. 2020 (Haynes et al. 1996). ...
... Despite their multiple evolutionary origins and huge diversity, certain parasitic plants have the potential to form specialized organ (haustoria), which penetrates host tissues and establishes a vascular connection between parasite and host (Teixeira-Costa et al. 2020;Pan et al. 2022). External features of haustoria of different parasitic plants may vary, but they are usually recognizable as swollen, knob-shaped, or clasping structures composed of different tissues and cell types, homologous to the root or subterranean plant structures, such as tubers and rhizomes or occur as numerous lateral organs on roots or shoots (Atsatt 1983;Joel 2013;Teixeira-Costa et al. 2020 (Haynes et al. 1996). Lauraceae is a family of about 50 genera and about 3000 species with mostly subtropical and tropical trees and shrubs except for the genus Cassytha which is most diverse in the American and Asian tropics, although many species occur in Australia and Madagascar (Harris 2004). ...
Cassytha filiformis L. is a medicinal parasitic plant belonging to the family Lauraceae. This plant shows a wider distribution in India. The species is a vine resembling the common parasitic dodder, the Cuscuta spp. It grows irrespective of the choice of host plant species. The host may be herbs, shrubs, woody trees and sometimes shows attachment to itself (auto parasitism) as it does to its host. Cassytha filiformis is used in various formulations in Ayurveda and folk medicines to treat malaria, urinary problems, nephritis, headache, hepatitis, piles, sinusitis, etc. It is also a rich source of phytochemical constituents such as aporphine alkaloids, tannins, saponins, and leucanthocyanins, etc. with therapeutic potential against diverse health problems. Keeping the importance of this parasitic plant, authors discussed here the uses and its pathogenicity to the host plants.
... Host preferences in mistletoes are reputedly dynamic and attributed to several factors such as host morphology defining the compatibility with a mistletoe's haustorium, physiological fitness and nitrogen content determining the host's "quality," as well as host abundance and stability in an ecosystem crucial for the duration of mistletoe-host contact (Gairola et al., 2013;Norton & Carpenter, 1998;Polhill & Wiens, 1998;Teixeira-Costa et al., 2020). ...
Mistletoes, as perennial hemiparasitic angiosperms that parasitize woody plants, are an important component of the highly diverse, endemically rich and mosaic African flora, which is attributed to the Holarctic, Paleotropical, and Cape Floristic kingdoms. The richness of African mistletoes from the Loranthaceae and Viscaceae, along with many aspects of their biology and ecology, was covered in the comprehensive monograph of Polhill and Wiens (1998, Mistletoes of Africa , Royal Botanic Gardens). The present review is devoted to the taxonomic and functional diversity of symbionts associated with mistletoes in Africa and adjacent islands that contribute to the major biological functions of mistletoes, such as establishment and growth, nutrition and fitness, resistance to external stresses, as well as pollination and dispersal. These functions are favored by more or less distinct sets of associated bionts, including host plants, animal herbivores, frugivorous birds, nectar‐ and pollen‐feeding insects, and endophytic microorganisms. A separate section is devoted to mistletoe epiparasitism as a special case of host selection. All these organisms, which are components of the mistletoe‐associated community and multitrophic network, define the role of mistletoes as keystone species. Some aspects of the symbiont communities are compared here with patterns reported for mistletoes from other continents, particularly to identify potential relationships that remain to be explored for the African species. In addition, properties of endophytic mistletoe associates that contribute to the plant's communication with coexisting organisms are considered. We also highlight the important gaps of knowledge of the functioning of mistletoe‐associated communities in Africa and indicate some applied issues that need future attention.
Abstract in French is available with online material.
... In turn, epicortical roots occur in the mistletoe genera Bakerella, Helixanthera, Plicosepalus, Taxillus, and Vanwykia (Calvin & Wilson, 2006), whereas clasping unions characterize Actinanthella, Emelianthe, Englerina, Globimetula, Oedina, Oliverella, Oncella, Phragmanthera, Septulina, Spragueanella, and Oncocalyx section Oncocalyx (Calvin & Wilson, 1998. According to Teixeira- Costa et al. (2020), Helixanthera and all Viscaceae develop bark strands, similarly to some members of the genera Oncocalyx (sections Longicalyculati and Oncocalyx), Agelanthus (sections Erectilobi and Purpureiflori), Oedina, and Spragueanella (Calvin & Wilson, 1998;Kuijt & Hansen, 2015). In general, the external haustorium morphology may vary in the same mistletoe species depending on the host plant, whereas the developmental process is more conserved, allowing for a more precise differentiation of haustorium types (L. ...
... Host preferences in mistletoes are reputedly dynamic and attributed to several factors such as host morphology defining the compatibility with a mistletoe's haustorium, physiological fitness and nitrogen content determining the host's "quality," as well as host abundance and stability in an ecosystem crucial for the duration of mistletoe-host contact (Gairola et al., 2013;Norton & Carpenter, 1998;Polhill & Wiens, 1998;Teixeira-Costa et al., 2020). ...
... A similar pattern involving the formation of cortical strands soon after initial seed germination is also observed for closely related, nonendophytic mistletoe species (Calvin and Wilson, 1996;Wilson and Calvin, 2006;Mauseth and Rezaei, 2013;Kuijt, 2015). Indeed, analysis of haustorial development and evolution suggests that the endoparasitic lifestyle among mistletoes may have evolved in a similar way on three different occasions, always from ancestral species with a highly specialized system of cortical strands (Teixeira-Costa et al., 2020). ...
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.
... Polishing wood samples is perhaps one of the oldest, most common methods for analyzing their anatomical structure. Wood polishing has been used to facilitate the characterization of entire families of woody plants (Koek-Noorman and Westra, 2012), in wood and charcoal identification by both humans and semiautomated machine-based methods (Kisser, 1967;Lantican and Hughes, 1973;Mainieri et al., 1983;Gärtner and Nievergelt, 2010;Botosso, 2011;Hermanson and Wiedenhoeft, 2011;Ruffinatto et al., 2019;Ravindran et al., 2020), in dendrochronology (Brandes et al., 2011(Brandes et al., , 2018Alves et al., 2013;Gärtner et al., 2015;Locosselli et al., 2016;Arzac et al., 2018), and even to describe parasite-host interactions in the formation of wood galls Ceccantini, 2015, 2016;Teixeira-Costa et al., 2020). Despite the importance of this technique in the field, few works describe in detail how to successfully perform wood sanding (Gärtner and Schweingruber, 2013;Arzac et al., 2018). ...
Premise:
Polishing entire stem and root samples is an effective method for studying their anatomy; however, polishing fresh samples to preserve woods with soft tissues or barks is challenging given that soft tissues shrink when dried. We propose sanding fresh or liquid-preserved samples under water as an alternative, given that it preserves all tissues in an intact and clear state.
Methods and results:
By manually grinding the surface of the samples under water using three ascending grits of waterproof sandpapers, an excellent polished sanded surface is obtained. The wood swarf goes into the water without clogging the cell lumina, rendering the surfaces adequate for cell visualization and description. We show results in palms, liana stems, roots, and wood blocks.
Conclusions:
Using this simple, inexpensive, rapid technique, it is possible to polish either fresh, dry, or liquid-preserved woody plant samples, preserving the integrity of both the soft and hard tissues and allowing for detailed observations of the stems and roots.
... Likewise, the convergence between Cassytha (Fig. 4c) and Cuscuta (Fig. 4d) has long been observed, and it extends from their lianescent form and rudimentary roots, to the general aspect of their haustorium (Kuijt 1969;Heide-Jørgensen 2008). Among mistletoes, the remarkable diversity in haustorium morphology has been recently shown to have a common developmental trajectory, one that is also partially shared with Santalalean root hemiparasites (Teixeira-Costa et al. 2020). Striking developmental similarities have also been observed among endoparasitic species of the families Apodanthaceae, Cytinaceae, Mitrastemonaceae (Fig. 4e), and Rafflesiaceae (Fig. 4F) Fig. 4g) forms multiple haustoria, which emerge laterally along the root system, while Scybalium fungiforme (Balanophoraceae, Fig. 4h) forms a single haustorium, which emerges at a terminal position. ...
... Because haustorium development is a dynamic process that involves shifts in structure and functionality (Yoshida et al. 2016), tissues and cell types that are readily identified during one phase may not be distinguishable later in development. For instance, in Loranthaceae mistletoes such as Psittacanthus and Loranthus species, few sinkers can be observed at young stages of haustorium development, but become indistinguishable at a later, mature stage (Dzerefos and Witkowski 1997;Teixeira-Costa et al. 2020). ...
Parasitic flowering plants are characterized by the development of an organ known as haustorium, which has evolved in multiple independent angiosperms clades. The haustorium has also been deemed “the most plastic of organs” due to its ability to accommodate physiological and anatomical differences between the parasite itself and its host plants. This is achieved through the development of vascular connections, which involve the differentiation of various specialized cell types by the parasite. The development, structure, and evolution of the haustorium and the connections it fosters are reviewed here considering all 12 parasitic plant lineages. A multi-level comparison between “model” parasitic plants, such as Orobanchaceae and Cuscuta species, with members of often neglected groups, such as Lennoaceae, Mitrastemonaceae, and Santalales yields the idea of a shared general body plan of the mature haustorium. This proposed haustorium bauplan is composed of an upper part, including structures associated with mechanical attachment to the host body, and a lower part, including all parasitic tissues and cell types within the host body. The analysis of multi-level convergence is also applied here to the comparison between haustoria and other plant organs. Considering the structure, molecular development, and functionality of this organ under the framework of continuum and process plant morphology, I propose the interpretation of haustoria as morphological misfits.
