Anatomy and ultrastructure of epidermal cells in the haustorium of a parasitic flowering plant,Cuscuta japonica, during attachment to the host

Changes of epidermal cells in the haustorium of the parasiticCuscuta japonica during its attachment to the host plantimpatiens balsamina were studied with light and electron microscopy. In the transverse sections of dodder stems not in contact with the host, epidermal cells had rounded outlines. However, when haustorial initials developed in the cortex of the parasite stem at the contact site, the epidermal cells had more dense cytoplasm and conspicuous nuclei than before, and their outline was flat in the longitudinal section. As meristem cells developed from those initials, the epidermal cells became more elongated. When the haustorium was fully matured, the apical tips of the elongated epidermal cells at the contact site branched like toes, producing numerous projections via cell wall invaginations. This event caused spaces to form between the projections; coincidently, the surface area of the apical ends of the epidermal cells increased. The dense cytoplasm at those projections contained prominent nuclei and abundant other organelles, suggesting a active metabolism. Osmiophilic particles, releasing into the cell walls from the cytoplasm, were though to be associated with the loosening and elongating of the epidermal cell walls. Dense and homogeneous materials were secreted within the spaces between the projections. These materials could play an important role in cementing the haustorium onto the surface of the host organ.     

Systematics and plastid genome evolution of the cryptically photosynthetic parasitic plant genus Cuscuta (Convolvulaceae)

Background  

The genus Cuscuta L. (Convolvulaceae), commonly known as dodders, are epiphytic vines that invade the stems of their host with haustorial feeding structures at the points of contact. Although they lack expanded leaves, some species are noticeably chlorophyllous, especially as seedlings and in maturing fruits. Some species are reported as crop pests of worldwide distribution, whereas others are extremely rare and have local distributions and apparent niche specificity. A strong phylogenetic framework for this large genus is essential to understand the interesting ecological, morphological and molecular phenomena that occur within these parasites in an evolutionary context.     

A species-specific recognition system directs haustorium development in the parasitic plant Triphysaria (Scrophulariaceae)

Parasitic plants use host molecules to trigger developmental programs essential for parasitism. One such program governs the initiation, development, and function of haustoria, parasite-specific organs responsible for attachment and invasion of host tissues. Haustoria development can be initiated by several different molecules produced by appropriate host species. We are interested in understanding how these signals are interpreted by two related facultative parasites, Triphysaria eriantha (Benth.) Chuang and Heckard, and T. versicolor Fischer and C. Meyer, to distinguish their own roots from those of potential hosts. We used an in vitro bioassay to determine what proportion of different Triphysaria populations formed haustoria in the presence and absence of closely related and unrelated host species. We found that the proportion of plants with haustoria was the same whether the plants were grown in isolation or with a conspecific host. In contrast, a significantly higher proportion of plants made haustoria when the host was a congeneric Triphysaria. Plants with haustoria neither enhanced nor inhibited other plants' propensity to form haustoria. Together these results indicate that qualitative differences exist in haustorium-inducing factors exuded by closely related species. The highest proportion of Triphysaria had haustoria when grown with Arabidopsis thaliana (L.) Heynh. Even in this case, however, some Triphysaria failed to develop haustoria. Interestingly, the percentage of haustoria that had vessel elements was higher when connections were made with Arabidopsis than with another Triphysaria. These results demonstrate that host recognition can be manifested at multiple points in haustorium development. Received: 18 December 1996 / Accepted: 14 February 1997     

Heritable variation in quinone-induced haustorium development in the parasitic plant Triphysaria

We are using the facultative hemiparasite, Triphysaria, as a model for studying host-parasite signaling in the Scrophulariaceae. Parasitic members of this family form subterranean connections, or haustoria, on neighboring host roots to access host water and nutrients. These parasitic organs develop in response to haustorial-inducing factors contained in host root exudates. A well-characterized inducing factor, 2, 6-dimethoxy-p-benzoquinone (DMBQ), can be used to trigger in vitro haustorium formation in the roots of Triphysaria. We have assayed three species, Triphysaria eriantha (Benth.) Chuang and Heckard, Triphysaria pusilla (Benth.) Chuang and Heckard, and Triphysaria versicolor Fischer and C. Meyer, for haustorium development in response to DMBQ. There were significant differences between the species in their ability to recognize and respond to this quinone. Ninety percent of T. versicolor individuals responded, whereas only 40% of T. pusilla and less than 10% of T. eriantha formed haustoria. Within field collections of self-pollinating T. pusilla, differential responsiveness to DMBQ was seen in distinct maternal families. Assaying haustorium development in subsequent generations of self-pollinated T. pusilla showed that DMBQ responsiveness was heritable. Reciprocal crosses between T. eriantha and T. versicolor demonstrated that DMBQ responsiveness was influenced by maternal factors. These results demonstrate heritable, natural variation in the recognition of a haustorial-inducing factor by a parasitic member of the Scrophulariaceae.     

Tocochromanol content and composition in different species of the parasitic flowering plant genus Cuscuta

The holoparasitic plant genus Cuscuta is comprised of species with various degrees of plastid functionality and significant differences in photosynthetic capacity, ranging from moderate to no photosynthetic carbon fixation. In the present study, several Cuscuta species were analyzed with respect to the overall contents of tocochromanols and plastoquinone and the levels of the individual tocochromanols. No correlations among photosynthetic capacity, the amount of carotenoids, of plastoquinone and of tocochromanols were observed. On the contrary, wide variation in the composition of the tocochromanol fraction was observed among different species, as well as in stems of the same species in response to starvation conditions. The implications of these findings are discussed.     

Caught in action: fine-scale plastome evolution in the parasitic plants of Cuscuta section Ceratophorae (Convolvulaceae)

Plant Molecular Biology - The mitochondrial metallochaperone COX19 influences iron and copper responses highlighting a role of mitochondria in modulating metal homeostasis in Arabidopsis. The...     

The parasitic mechanism of the holostemparasitic plant Cuscuta

Cuscuta is a stem holoparasitic plant without leaves or roots, which develops a haustorium and sucks nutrients from host plants. The genus Cuscuta comprises about 200 species, many of which can cause severe problems for certain crops. The parasitic process in Cuscuta begins in finding and attaching to a host plant and then developing a haustorium. The process does not always require any chemical signal, but does require a light signal. Finding a host involves detecting the lower red light:far-red light ratio near a potential host plant by phytochrome. A contact signal is also necessary for haustorium induction. Apparently, cytokinin increase is downstream of the light and contact signal and is critical for haustorium induction. This pathway, however, appears to be slightly different from a standard pathway. The direct connection between Cuscuta and its host involves both the xylem and phloem, and mRNA and proteins can translocate. Several features indicate that Cuscuta is a useful model plant for parasite plant research as well as plant–plant interaction research. These include the simple anatomical structure and seedling development, no chemical requirement for haustorium induction, and the wide range of host plants.     

The structure and development of the haustorium in parasitic Scrophulariaceae*

The structure and development of roots and haustoria in 37 species of parasitic Scrophulariaceae was studied using light microscopy. The mature haustorium consists of two regions: the swollen “body” and the parent root, which resembles non-haustorial roots in structure. The body arises from the parent root and is composed of an epidermis, cortex, central region of xylem (the vascular core), a region of parenchyma (the central parenchymatous core), and the portion of the haustorium contained in the host tissue (the endophyte). The xylem of the vascular core is composed predominately of vessel elements. The central parenchymatous core is composed of parenchyma and col-lenchyma. Vessels extend from the vascular core through the central parenchymatous core to the endophyte. The endophyte is composed of parenchyma cells and vessel elements. No phloem is present in the body of the haustorium. Early stages in the development of the haustorium are exogenous. Initial periclinal divisions in the epidermis or outer cortex are followed by hypertrophy of cortical parenchyma. These events are followed by development of the vascular core from the pericycle, attachment of haustorium to the host by a specialized layer of cementing cells or root hairs, and penetration of the host by dissolution of host cells.     

Molecular, functional and ultrastructural characterisation of plastids from six species of the parasitic flowering plant genus Cuscuta

 Hydroponically cultivated barley plants were exposed to nitrogen (N)-deficiency followed by N-resupply. Metabolic and genetic regulation of fructan accumulation in the leaves were investigated. Fructan accumulated in barley leaves under N-deficiency was mobilized during N-resupply. The enhanced total activity of fructan-synthesizing enzymes, sucrose:sucrose 1-fructosyltransferase (EC 2.4.1.99) and sucrose:fructan 6-fructosyltransferase (6-SFT; EC 2.4.1.10) caused by N-deficiency decreased with the mobilization of fructan during N-resupply. The activity of the barley fructan-degrading enzyme, fructan exohydrolyase (EC 3.2.1.80) was less affected by the N status. The low level of foliar soluble acid invertase activity under N-deficiency conditions was maintained during the commencement of N-resupply but increased subsequently. Further analyses by sodium dodecyl sulfate-polyacrylamide gel electrophoresis, western blot and northern blot demonstrated that the fructan accumulation and the total activity of fructan-synthesizing enzymes correlated with the 6-SFT mRNA level. We suggest that the changes in fructan levels under N stress are intimately connected with the regulation of fructan synthetic rate which is mostly controlled by 6-SFT. Received: 25 October 1999 / Accepted: 15 February 2000     

Testing the phylogenetic position of a parasitic plant (Cuscuta, Convolvulaceae, asteridae): Bayesian inference and the parametric bootstrap on data drawn from three genomes

Previous findings on structural rearrangements in the chloroplast genome of Cuscuta (dodder), the only parasitic genus in the morning-glory family, Convolvulaceae, were attributed to its parasitic life style, but without proper comparison to related nonparasitic members of the family. Before molecular evolutionary questions regarding genome evolution can be answered, the phylogenetic problems within the family need to be resolved. However, the phylogenetic position of parasitic angiosperms and their precise relationship to nonparasitic relatives are difficult to infer. Problems are encountered with both morphological and molecular evidence. Molecular data have been used in numerous studies to elucidate relationships of parasitic taxa, despite accelerated rates of sequence evolution. To address the question of the position of the genus Cuscuta within Convolvulaceae, we generated a new molecular data set consisting of mitochondrial (atpA) and nuclear (RPB2) genes, and analyzed these data together with an existing chloroplast data matrix (rbcL, atpB, trnL-F, and psbE-J), to which an additional chloroplast gene (rpl2) was added. This data set was analyzed with an array of phylogenetic methods, including Bayesian analysis, maximum likelihood, and maximum parsimony. Further exploration of data was done by using methods of phylogeny hypothesis testing. At least two nonparasitic lineages are shown to diverge within the Convolvulaceae before Cuscuta. However, the exact sister group of Cuscuta could not be ascertained, even though many alternatives were rejected with confidence. Caution is therefore warranted when interpreting the causes of molecular evolution in Cuscuta. Detailed comparisons with nonparasitic Convolvulaceae are necessary before firm conclusions can be reached regarding the effects of the parasitic mode of life on patterns of molecular evolution in Cuscuta.     

A new western Mediterranean species of Cuscuta (Convolvulaceae) confirms the presence of holocentric chromosomes in subgenus Cuscuta

Cuscuta nivea , a new western Mediterranean species of Cuscuta L. subgenus Cuscuta (Convolvulaceae) is described and illustrated for plants traditionally included in C. planiflora Ten. and sometimes recognized as C. planiflora var. algeriana Yunck., or the illegitimate C. cuspidata Pomel. The morphological, cytological and ecological features that allow it to be distinguished from the morphologically most similar plants, described as C. planiflora var. papillosa Engelm., are exposed. The chromosome numbers 2 n = 18 and 2 n = 20 are found for the new species and 2 n = 34 for the papillate forms of C. planiflora Ten. The presence of holocentric chromosomes is recorded, which confirms this type of chromosome as a synapomorphy for Cuscuta subgenus Cuscuta .     

Pollen evolution and its taxonomic significance in Cuscuta (dodders, Convolvulaceae)

The pollen morphology of 148 taxa (135 species and 13 varieties) of the parasitic plant genus Cuscuta (dodders, Convolvulaceae) was examined using scanning electron microscopy. Six quantitative characters were coded using the gap-weighting method and optimized onto a consensus tree constructed from three large-scale molecular phylogenies of the genus based on nuclear internal transcribed spacer (ITS) and plastid trn-LF sequences. The results indicate that 3-zonocolpate pollen is ancestral, while grains with more colpi (up to eight) have evolved only in two major lineages of Cuscuta (subg. Monogynella and clade O of subg. Grammica). Complex morphological intergradations occur between species when their tectum is described using the traditional qualitative types—imperforate, perforate, and microreticulate. This continuous variation is better expressed quantitatively as “percent perforation,” namely the proportion of perforated area (puncta or lumina) from the total tectum surface. Tectum imperforatum is likely the ancestral condition, while pollen grains with increasingly larger perforation areas have evolved multiple times. The reticulated tectum, unknown in other Convolvulaceae, has evolved in Cuscuta only in two lineages (subg. Monogynella, and clade O of subg. Grammica). Overall, the morphology of pollen supports Cuscuta as a sister to either the “bifid-style” Convolvulaceae clade (Dicranostyloideae) or to one of the members of this clade. Pollen characters alone are insufficient to reconstruct phylogenetic relationships; however, palynological information is useful for the species-level taxonomy of Cuscuta.     

Relatedness affects competitive performance of a parasitic plant (Cuscuta europaea) in multiple infections

Theoretical models predict that parasite relatedness affects the outcome of competition between parasites, and the evolution of parasite virulence. We examined whether parasite relatedness affects competition between parasitic plants (Cuscuta europaea) that share common host plants (Urtica dioica). We infected hosts with two parasitic plants that were either half-siblings or nonrelated. Relative size asymmetry between the competing parasites was significantly higher in the nonrelated infections compared to infections with siblings. This higher asymmetry was caused by the fact that the performance of some parasite genotypes decreased and that of others increased when grown in multiple infections with nonrelated parasites. This result agrees with the predictions of theories on the evolution of parasite virulence: to enhance parasite transmission, selection may favour reduced competition with genetically related parasites in hosts infected by several genotypes. However, in contrast to the most common predictions, nonrelated infections were not more virulent than the sibling infections.     

Epidermal cell-patterning genes of the stem parasitic plant Cuscuta campestris are involved in the development of holdfasts

Cuscuta campestris, a stem parasitic plant, commences its parasitic behavior by forming a specialized disk-like adhesive structure called a holdfast, which facilitates tight adhesion to the stem surface of the host plant. The morphology of epidermal cells in the holdfast is similar to that of the leaf trichome and root hairs of dicotyledonous plants. However, the regulatory network underlying the development of the holdfast has not been elucidated to date. In this study, we assessed the roles of epidermal cell-patterning genes in the development of a holdfast. Epidermal cell-patterning genes of C. campestris, including CcWER, CcGL3, CcTTG1, CcGL2, and CcJKD, were expressed slightly before the initiation of the outgrowth of stem epidermal cells. CcJKD-silencing repressed CcJKD, CcWER, CcGL3, CcTTG1, CcGL2; therefore, CcJKD is an upstream regulator of other epidermal cell-patterning genes. Unlike other genes, CcCPC was not upregulated after attachment to the host, and was not repressed by CcJKD-silencing. Protein interaction assays demonstrated that CcJKD interacted with CcTTG1 and CcCPC. Furthermore, CcJKD-silencing repressed the outgrowth of holdfast epidermal cells. Therefore, C. campestris invokes epidermal cell-patterning genes for the outgrowth of holdfast epidermal cells, and their regulatory mechanism is different from those for leaf trichome or root hairs.     

Defense response of resistant host Impatiens balsamina to the parasitic angiosperm Cuscuta japonica

The response of the stem of a resistant host (Impatiens baslamina) to infection by the parasitic flowering plant Cuscuta japonica was studied with light and electron microscopy. The intra- and interfascicular cambial cells in the host stem first reacted to the penetrating upper haustorium by dividing, and the differentiation of the host xylem (vascular) tissues proceeded toward interfascicular areas from vascular bundles. When the host vascular tissue was invaded by the endophyte (haustorial portion in the host stem), the host xylem was displaced, and host vessels became occluded with parenchyma cells, resulting in tyloses. As the parasitism progressed, areas of the host stem penetrated by the endophyte became swollen via secondary growth and cell division in the parenchymatous cortex, pith, and interfascicular areas. During this intrusion by the endophyte, darkly stained necrotic reactions were detected at the interface between the host tissue and the invading endophyte. The results suggested that in the host tissues penetrated by the parasite, the formation of secondary tissue and swellings caused by active cell division of ground tissue and host vessel occlusion by tyloses constitute the host structural defense against the parasite.     

Taxonomic status of Cuscuta nevadensis and C. veatchii (Convolvulaceae) in North America

The taxonomy ofCuscuta nevadensis andC. veatchii is investigated.Cuscuta nevadensis is more closely related toC. veatchii andC. denticulata than toC. salina, and the former two taxa are accepted as species. A summary of relevant taxonomic and biological information is provided, including synonymy, distribution and ecology, keys, and a comparison of the morphology of flowers and seeds are examined. The morphological basis of vivipary inC. nevadensis is discussed. The status ofCuscuta vivipara, an invalid name in recent use, is clarified.     

寄生被子植物吸器的研究

从吸器的发生、结构、功能、寄生的生理机制等方面概述了寄生被子植物吸器的研究进展。