Abstracts Dealing with Parasitic Angiosperms
Botany 2006
Chico, CA USA, July 28 to August 2, 2006

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Abstracts of Oral Presentations and Posters Arranged Taxonomically

Parasitic Plants in General (1)

Shyu, Shin-Yi, Hu, Jer-Ming. Studies of plastid 16S rDNA suggest that the evolutionary rates vary among nonphotosynthetic plants. Nonphotosynthetic plants usually retain a reduced plastid genome, although most of the photosynthesis-related genes are lost or become pseudogenes. In order to elucidate the plastid genome evolution in non-photosynthetic plants, we examined plastid-derived 16S rDNAs of nine nonphotosynthetic plants, including some with partial photosynthetic ability. The 16S rDNA sequences from all examined taxa were included in a phylogenetic analysis with other land plants and green algae to show their relationships. To evaluate rate heterogeneity among various 16S rDNA sequences, a relative rate tests was conducted. Compared with other angiosperms, the 16S rDNA sequences show an increasing substitution rates in four nonphotosynthetic species: Balanophora laxiflora, Mitrastemon kanehirai, Cheilotheca humilis and Cheilotheca macrocarpa. However the other five species, Aeginetia indica, Cassytha filiformi, Cuscuta australis, Galeola lindleyana, and Orobanche coerulescens, exhibited only slightly higher rates relative to most angiosperms. Some of the high sequence divergences are accompanied by an increase in A+T content of the sequences, especially in M. kanehirai, which has the highest rate among the examined taxa. In species with higher evolutionary rates of 16S rDNAs, B. laxiflora, M. kanehirai are holoparasites and C. humilis, C. macrocarpa are mycoheterotrophs. Theses plants have completely lost their photosynthetic ability. However, among the other five species examined, C. filiformi is a hemiparasitic plant and can photosynthesize itself; G. lindleyana and young stage of C. australis are slight green and maybe retain some photosynthetic ability. Although A. indica and O. coerulescens are holoparasitc plants, Orobanchaceae parasites lost their photosynthetic ability recently, and may not have enough time to accumulate variations.
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Hydnoraceae (2)

Bolin, Jay F., Tennakoon, Kushan U., Musselman, Lytton John, Maass, Erika. Germination and seedling development of the highly modified root holoparasite Hydnora triceps.  Hydnora (Hydnoraceae) is a small genus of root holoparasites native to Africa, the southern Arabian Peninsula and Madagascar. The most unusual of the group, the furtive H. triceps, resides and flowers completely underground and exclusively parasitizes Euphorbia dregeana. We present the results of the first successful seed germination for the genus. The permeable seeds of H. triceps required host root exudates of E. dregeana to germinate and did not respond to root exudates from other Euphorbia spp. or control treatments. Anatomical studies (light microscopy and SEM) revealed that seeds of H. triceps have spherical undeveloped embryos in the center of a large endosperm. Germination occurred when a cylindrical mass of tissues originated from the embryo and emerged through the testa to a length of 2-3 mm. ‘Germ tube’ rather than radicle or hypocotyl was used to describe the cylindrical protrusion due to the lack of well defined vascular tissue. This study also addresses inconsistent terminology/interpretations encountered in the literature for seedlings of highly modified holoparasites.
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Bolin, Jay F., Musselman, Lytton John, Maass, Erika. The generalist pollination syndrome of the root holoparasite Hydnora africana and a test of a selective insect trapping mechanism.  Hydnora africana (Hydnoraceae) is a root holoparasite of southern Africa that parasitizes a variety of shrubby Euphorbia spp. The trimerous flowers of H. africana are comprised of an androecial and gynoecial chamber. Flowers are putatively protogynous (carpellate for 3 days) and produce a fetid odor from osmophores recessed on their interior tepal surfaces. Within the flowers of H. africana we observed 18 insect species and several other non-insect floral visitors at two sites in southern Namibia. The hide beetle Dermestes maculatus accounted for 65% of the floral visitors observed. Glabrous and waxy inner surface of the androecial chamber was selective; it prevented the escape of small beetles but was not a barrier to ants, grasshoppers, roaches, or large beetles. A beetle addition experiment (n = 8) using D. maculatus was used to evaluate the trapping mechanism of H. africana. Beetles began to escape the day pollen was shed due to changes in the androecial wall. Beetle escape was 31.1 (± 19.2), 42.2 (± 17.1), and 55.5 (± 16.7) % for 1-3 days after pollen shed, respectively. Pollen was still viable 72 hours after shedding. This suggests that the trapped beetles can be effective pollinators after escape.
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Loranthaceae (2)

Amico, Guillermo C., Nickrent, Daniel. Phylogeography of the mistletoe Tristerix corymbosus (Loranthaceae) inferred from chloroplast DNA sequences. The mistletoe Tristerix corymbosus is distributed from 30º S in Chile to 42º S in Chile and Argentina. Throughout this range this species is present in two habitats, the temperate forest and the more recent Chilean matorral which formed ca. 5 mybp. We examined chloroplast sequence variation among populations covering the entire range of the species. Given the recency of the matorral habitat, we postulate that mistletoe populations found here have derived from forest populations. To test this hypothesis we conducted molecular analyses of two non-coding chloroplast regions: the atpB–rbcL spacer and the trnT-L-F region. A network was constructed with statistical parsimony and phylogenetic relationships between haplotypes were assessed using parsimony, likelihood and Bayesian analyses. The trnT-L-F region is less informative than the atpB-rbcL spacer; hence only one individual per populations was sequenced from it. Sequences for the atpB-rbcL spacer were obtained from 108 individual in 26 populations. The network structure for both chloroplast regions was congruent. For the atpB–rbcL spacer, eight haplotypes were identified that did not correspond simply to matorral and forest types, but were placed in three clades (here designated A, B, C). Only three populations had more than one haplotype. Several phenomena at different geological times may have influenced the present spatial pattern and genetic differentiation of T. corymbosus populations. The uplift of the Andes had a great impact, first dividing a widespread ancestral haplotype (clade A). After glaciations, one of the clade B haplotypes may have dispersed south from refugia in central Chile. Although the original hypothesis was confirmed, the northernmost matorral populations of clade C were most similar to the forest populations (not the geographically closer southern ones), thus indicating the presence of a northern refugium. These localities have already been inferred to be refugia for other plants and animals.
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Wilson, C., Calvin, C. Origin of Aerial Parasitism in the Loranthaceae. The large mistletoe family, Loranthaceae, contains 75 genera and approximately 1000 species. The family originated in the Southern Hemisphere and dispersed, apparently early, between fragments of Gondwana. It is now widely distributed on land surfaces of the former supercontinent. The Loranthaceae has three terrestrial, root-parasitic genera—a habit considered ancestral—and 72 genera of aerial, branch parasites. For almost two centuries, the origin of the mistletoe habit has been of interest to biologists. Two main evolutionary pathways have been proposed to explain the transition from terrestrial to aerial parasitism in the family. One theorizes the presence of an intermediate climbing ancestor in the path to the aerial habit. The other proposes a direct transfer from terrestrial to epiphytic growth following the germination of seeds on tree branches. We present molecular and morphological evidence that aerial parasitism has originated multiple times in the family, and that the origin of aerial parasitism in one Old World clade resulted from the direct transfer from terrestrial to epiphytic growth following the germination of seeds on tree branches. Our results argue against the currently preferred hypothesis that aerial Santalales necessarily evolved from climbing ancestors.
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Misodendraceae (2)

Vidal-Russell, Romina, Nickrent, Daniel. A Molecular Phylogeny of the Feathery Mistletoe Misodendrum (Misodendraceae). Misodendrum comprises eight species of aerial hemiparasite shrubs endemic to temperate forests of Chile and Argentina from 33º S to 55º S. All parasitize Nothofagus, however, host ranges vary among the species. Misodendrum can be distinguished from all other mistletoes by the presence of achenes with feathery staminodes that are wind dispersed. Previous classifications (Orfila 1978, Rossow 1982) included two subgenera, Misodendrum (two sections) and Angelopogon (three sections). Our project tested this classification using molecular markers: nuclear ITS rDNA and two chloroplast genes (trnL-F and matK). All species except the rare M. macrolepis were sampled. Maximum parsimony, likelihood and Bayesian analyses were performed for individual and combined partitions. Other molecular work in our lab has shown that Misodendraceae is sister to Loranthaceae, thus this taxon was used as an outgroup. Results from analyses of the separate partitions were generally congruent, differing only in the position of M. linearifolium and M. quadriflorum; however, the 3-gene tree gave higher support for M. quadriflorum as sister to all other species. Misodendrum brachystachyum and M. oblongifolium form a well supported clade that is sister to one composed of M. punctulatum, M. gayanum and M. angulatum. This clade is sister to M. linearifolium. These phylogenetic relationships generally agree with previous classifications. Subgenus Misodendrum, characterized by warty stems and two stamens, here resolves as a polytomy: M. punctulatum, M. gayanum and M. angulatum (and likely M. macrolepis). Subgenus Angelopogon, characterized by the plesiomorphies three stamens and foliacious bracts, is paraphyletic given our rooting. Misodendrum brachystachyum and M. oblongifolium (section Archiphyllum) differ morphologically only by the length of their fruiting staminodes. M. oblongifolium is restricted to northern Patagonia where it parasitizes trees at higher elevations than the widespread M. brachystachyum. Our data suggest that M. oblongifolium could be considered a variety of M. brachystachyum.
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Vidal-Russell, Romina, Nickrent, Daniel. Misodendraceae: the first aerial parasites of Santalales. Molecular phylogenetic investigations have provided information on the relationships among the families of Santalales. The order contains five monophyletic families (Loranthaceae, Misodendraceae, Schoepfiaceae, Opiliaceae and Viscaceae) and two polyphyletic families (“Olacaceae” and “Santalaceae”). Olacaceae s. lat. is polyphyletic partly because Schoepfia is more closely related to Misodendrum and Loranthaceae than to Olacaceae s. str. Although Olacaceae s. str. is sister to the remaining members of the order, relationships among the remaining families are not well resolved. Past molecular studies suggest five independent origins of aerial parasitism, however, which group first evolved this habit was not clear. To resolve relationships among the non-Olacaceous families, we generated sequences from five genes: nuclear SSU and LSU rDNA, and chloroplast rbcL, matK, and trnL-F. Sequences from 25 taxa representing all families in the order were used (including four Olacaceae as the outgroups). Separate and combined data partitions were analyzed with maximum parsimony and Bayesian inference. All partitions were generally congruent, thus the total evidence tree will be described. Two major clades were resolved: 1) Opiliaceae, Santalaceae and Viscaceae which was sister to 2) Loranthaceae, Misodendraceae and Schoepfiaceae. The latter family, sister to Misodendraceae, contained Quinchamalium and Arjona, previously considered members of Santalaceae. The common ancestor of Misodendrum and Schoepfiaceae was a root parasite, thus aerial parasitism arose subsequent to the divergence of Misodendrum which only parasitizes Nothofagus. From a time calibrated Santalales tree, we estimate that this divergence occurred ca. 75 mybp which preceeds the evolution of aerial parasitism in Loranthaceae (ca. 40 mybp) and is not incompatible with the fossil history of Nothofagus.  Misodendrum has no tendency towards root parasitism and is highly adapted to the aerial parasitic habit. Its wind-dispersed seeds likely represent the earliest adaptation to stem parasitism, i.e. earlier than Loranthaceae with bird dispersed seeds.
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Lennoaceae (1)

Zhang, Yan, McNeal, Joel R., Smith, Alan R., Kuehl, Jennifer V., Boore, Jeffrey L., dePamphilis, Claude W. Striking convergence of plastid genomes in independent nonphotosynthetic lineages.  Parasitic plants are valuable models for studying gene and genome evolution in the absence of photosynthesis. Under relaxed functional constraints, the plastid genomes of some parasitic plant have experienced great reductions in gene content and accelerated rates of evolution for the remaining genes. For example, the fully sequenced plastid genome of Epifagus virginiana (Orobanchaceae) displays extreme genome reduction; it lacks functional copies of all photosynthetic and ndh genes, all four RNA polymerase genes, almost half of the tRNAs, and one third of the ribosomal protein genes. Accelerated evolution is observed in Epifagus, a result of both relaxed selection and an increase in the neutral rate of base substitution. To understand whether genome evolution is similar in independent lineages of nonphotosynthetic plants, the plastid genome of the holoparasite Pholisma arenarium (Lennoaceae/Boraginaceae) was cloned into fosmid vectors, sequenced, and analyzed. The plastid genome of Pholisma shows a pattern of gene loss that is strikingly similar to that observed in Epifagus. All of the photosynthetic genes (with the notable exception of rbcL) and ndh genes are lost, as are the RNA polymerase genes and some components of the translation apparatus. The gene losses in Pholisma are a perfect subset of those observed in Epifagus, and the remaining genes are also evolving at an accelerated rate. The results indicate parallel and convergent evolution of the two independent lineages of nonphotosynthetic plants and also suggest that photosynthesis has been lost more recently in the lineage including Pholisma.
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Convolvulaceae (Cuscuta) (2)

McNeal, Joel R., Kuehl, Jennifer V., Boore, Jeffrey L., dePamphilis, Claude W. Evolution of matK, a conserved plastid intron maturase, in the parasitic plant genus Cuscuta. Plastid genome content and arrangement are highly conserved across most land plants and their closest relatives in the algal order Charales. Almost all plastid introns appeared prior to the divergence of these two lineages; one such intron within the transfer RNA trnK-UUU contains a large open reading frame that encodes a presumed intron maturase, matK. Although this gene is found in all published land plant and Charophyte plastid genomes, including that of the nonphotosynthetic angiosperm Epifagus virginiana (Orobanchaceae), its exact function is still not fully known. The parasitic angiosperm genus Cuscuta (Convolvulaceae) is highly heterogeneous in plastid intron content and serves as a good candidate for studying the intron-splicing function and specificity of matK. We examined intron evolution and distribution in Cuscuta along with corresponding evolutionary changes in matK. Loss of many group II introns from the plastid genome results in substantial change in selective pressure within the hypothetical RNA-binding region (domain X) of matK in both Cuscuta and Epifagus. The intron-splicing function of matK is likely limited to group IIA introns in Cuscuta, corroborating previous circumstantial evidence from cereal crops.
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Stefanovic, Sasa, Kuzmina, Maria, Costea, Mihai. Delimitation and relationships of major lineages within Cuscuta subgenus Grammica (dodders; Convolvulaceae).  Subgenera Monogyna, Cuscuta, and Grammica are recognized traditionally within the parasitic genus Cuscuta based primarily on the morphology of styles and stigmas. The largest and most diverse group, subgenus Grammica, comprises some 120-130 species (approximately _ of the species-richness within the genus) and is distributed primarily throughout the New World, with Mexico and South America as its centers of diversity. While this group is well characterized morphologically by two styles with globular stigmas, neither its monophyly nor the relationships within Grammica were subjected to a broad and explicit phylogenetic study. In order to circumscribe the subgenus and assess the relationships among its major lineages, we conducted the first phylogenetic study of Grammica using plastid and nuclear sequence data (trnLF and ITS) from a wide taxonomic sampling covering its morphological, physiological, and geographical diversity. The results indicate the presence of 15 well-supported clades. Some of those clades correspond to a large degree to earlier taxonomic treatments (e.g., subsections sensu Yuncker), but majority of the groups are identified in this study for the first time. The backbone relationship among these clades, however, remains unresolved in many cases. Morphological, taxonomical, and biogeographical implications of these results are discussed. Also, a minimum of three potential cases of species of hybrid origin were confirmed or newly documented from strongly conflicting nuclear and plastid gene trees.
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Orobanchaceae (4)

Morawetz, Jeffery J., Wolfe, Andrea D. Phylogenetic analyses of the primarily hemiparasitic Alectra (Orobanchaceae): a preliminary study. Alectra Benth. (Orobanchaceae) is a genus of mostly hemiparasitic herbaceous plants, and is comprised of approximately 30 species distributed primarily throughout southern and eastern Africa as well as Madagascar. Three species are of particular interest due to their geographical distributions, A. sessiliflora, A. aspera, and A. stricta. Alectra sessiliflora is a widespread and polymorphic species present throughout sub-Saharan Africa into India and China. Additionally, A. aspera and A. stricta occur in tropical South America, but the relationship of these species to each other and the rest of the genus is currently unclear. Two types of parasitism exist within flowering plants (hemi- and holo-parasitism) and within Alectra both types are known. A preliminary phylogeny of Alectra is presented here based on combined ITS, trnT-F and rpl16 sequence data. This phylogeny provides an opportunity to begin answering several questions about the evolutionary history of the genus; particularly, the number of times that holoparasitism has arisen and the biogeographic patterns of diversification of Alectra both within the Old World and the events leading to its arrival in the New World. The implications of the placement of the closely related holoparasitic genus Aeginetia are also examined.
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Morawetz, Jeffery J., Wolfe, Andrea D. Phenetic analyses of morphological traits in the Alectra sessiliflora complex (Orobanchaceae). Alectra (Orobanchaceae) is a genus of primarily hemiparasitic herbs. Alectra sessiliflora var. sessiliflora, var. senegalensis, and var. monticola form a morphologically cohesive group with overlapping distributions throughout sub-Saharan Africa, and are characterized by sessile yellow flowers and a branching habit. Traditional characters used to distinguish these varieties were stamen filament pubescence and calyx pubescence. These characters are variable and overlapping, thus preventing confident determination of specimens. This difficulty suggested that the taxonomic delimitations are problematic, and required further investigation. A phenetic study was undertaken to determine if this complex is best treated as a single large polymorphic taxon or as a series of similar yet discrete taxa. Twenty-four morphological traits were examined on 134 operational taxonomic units (OTUs) and the data were analyzed using UPGMA and PCoA. Discrete clusters were not identified by the analyses. These results suggest that A. sessiliflora should be recognized as a single species without infraspecific divisions. The implications of this study will be addressed in a monograph of Alectra currently in preparation.
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McNeal, Joel R., Bennett, Jonathan R., Wolfe, Andrea D., Mathews, Sarah. Five-gene phylogeny of Orobanchaceae (Broomrape Family). The family Orobanchaceae is nearly cosmopolitan in distribution and contains the most agriculturally damaging parasitic weeds in the world. We have gathered DNA sequence data from more than 50 genera and 170 species of Orobanchaceae using both nuclear (ribosomal internal transcribed spacer, phytochrome A, and phytochrome B) and plastid (ribosomal protein subunit 2 and maturase K) loci in order to ascertain phylogenetic relationships within the family. We have greatly augmented taxon sampling for genes previously used for Orobanchaceae phylogenetics, and novel phyB data corroborates published phylogenies from the other individual loci. The combined five-gene dataset represents the highest degree of taxonomic sampling within this economically important family to date and provides greater phylogenetic resolution than the single-gene phylogenies.
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Tsai, Yi-Hsin Erica, Manos, Paul S. Do hosts and their obligate parasites co-migrate? Inferences from post-glacial phylogeographies of beech (Fagus grandifolia) and beech-drop (Epifagus virginiana). Describing how the migration patterns of parasites are constrained by their hosts is a first step in understanding the cohesiveness of communities during migration. This study compares the post-glacial migration of the parasitic plant, Epifagus virginiana (beechdrop; Orobanchaceae), with the migration history of its host tree, Fagus grandifolia (American beech; Fagaceae). The host's post-glacial history is well known with past molecular work describing its range expansion and paleo-pollen data reflecting population density changes over time. This history is used to frame questions regarding the migration of the obligate, host-specific parasite, E. virginiana; for instance, was E. virginiana present at the migration front of F. grandifolia with its range expansion mimicking its host's, or was the parasite's spread limited by host density with its migration matching the host's population density changes? To discern among these scenarios we present the molecular phylogeography of E. virginiana based on chloroplast DNA sequences. We identify the parasite's glacial refugia, migration corridors, and overall population structure and compare these with the host’s history. The results show that the range expansion of E. virginiana is largely coincident with the density changes of its host, though in some instances E. virginiana was present in the low density host populations at the migration front. The dependence of parasite establishment on host density results in a lag time between expansion into an area by the host and colonization by the parasite. How the host's distribution and density dictates the parasite's movements has implications for the migration capacity of E. virginiana and how quickly it can respond to climate change. Also, this study provides significant data on herbaceous plant migration that is currently missing and can answer broader questions about the cohesiveness of communities during migration.
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SIUC / College of Science / Parasitic Plant Connection
URL: http://www.parasiticplants.siu.edu/meetings/Bot2006ParAbstracts.html
Last updated: 25-Sept-06 / dln