Diversification of myco-heterotrophic angiosperms: evidence from Burmanniaceae.

Background - Myco-heterotrophy evolved independently several times during angiosperm evolution. Although many species of myco-heterotrophic plants are highly endemic and long-distance dispersal seems unlikely, some genera are widely dispersed and have pantropical distributions, often with large disjunctions. Traditionally this has been interpreted as evidence for an old age of these taxa. However, due to their scarcity and highly reduced plastid genomes our understanding about the evolutionary histories of the angiosperm myco-heterotrophic groups is poor. Results - We provide a hypothesis for the diversification of the myco-heterotrophic family Burmanniaceae. Phylogenetic inference, combined with biogeographical analyses, molecular divergence time estimates, and diversification analyses suggest that Burmanniaceae originated in West Gondwana and started to diversify during the Late Cretaceous. Diversification and migration of the species-rich pantropical genera Burmannia and Gymnosiphon display congruent patterns. Diversification began during the Eocene, when global temperatures peaked and tropical forests occurred at low latitudes. Simultaneous migration from the New to the Old World in Burmannia and Gymnosiphon occurred via boreotropical migration routes. Subsequent Oligocene cooling and breakup of boreotropical flora ended New-Old World migration and caused a gradual decrease in diversification rate in Burmanniaceae. Conclusion - Our results indicate that extant diversity and pantropical distribution of myco-heterotrophic Burmanniaceae is the result of diversification and boreotropical migration during the Eocene when tropical rain forest expanded dramaticall

Rate accelerations in nuclear 18S rDNA of mycoheterotrophic and parasitic angiosperms

Rate variation in genes from all three genomes has been observed frequently in plant lineages with a parasitic and mycoheterotrophic mode of life. While the loss of photosynthetic ability leads to a relaxation of evolutionary constraints in genes involved in the photosynthetic apparatus, it remains to be determined how prevalent increased substitution rates are in nuclear DNA of non-photosynthetic angiosperms. In this study we infer rates of molecular evolution of 18S rDNA of all parasitic and mycoheterotorphic plant families (except Lauraceae and Polygalaceae) using relative rate tests. In several holoparasitic and mycoheterotrophic plant lineages extremely high substitution rates are observed compared to other photosynthetic angiosperms. The position and frequency of these substitutions have been identified to understand the mutation dynamics of 18S rRNA in achlorophyllous plants. Despite the presence of significantly elevated substitution rates, very few mutations occur in major functional and structural regions of the small ribosomal molecule, providing evidence that the efficiency of the translational apparatus in non-photosynthetic plants has not been affected

Orbicules in angiosperms: Morphology, function, distribution, and relation with tapetum types

Orbicules, or Ubisch bodies, are sporopollenin particles lining the inner tangential and sometimes also the radial tapetal cell walls, They occur only in species with a secretory tapetum, The surface ornamentation of orbicules and pollen of the same species is often strikingly similar. Although orbicules were discovered more than a century ago, these structures remain enigmatic since their function is still obscure. Proposed hypotheses about their possible function are discussed. We also deal here with topics such as the possible allergenicity of orbicules and their representation in the fossil record. The use of orbicule characters for systematics is reviewed. The distribution of orbicules throughout the angiosperms, based on a literature review from the first report until today, is shown in a list with 314 species from 72 families. Those species found in the literature without orbicules are presented together with their tapetum type. We plotted this information on a dahlgrenogram to visualize the distribution of orbicules. Orbicules occur in all subclasses of the angiosperms, Their occurrence is not correlated with certain modes of pollination or habitats.status: publishe

Pollen development of Rondeletia odorata (Rubiaceae)

Pollen wall ontogeny of Rondeletia odorata was studied with transmission electron microscopy (TEM) and scanning electron microscopy (SEM) from tetrad stage until maturity. The ontogenetic sequence of wall development in Rondeletia follows, to some extent, the basic scheme in the angiosperms, i.e., development starts centripetally with the pro-columellae in a plasmalemma surface coating (primexine) at the early tetrad stage when the microspores are still enveloped by callose, until intine formation in young pollen grains. The main ontogenetical features of Rondeletia odorata pollen are (1) the very thin irregular foot layer, (2) development of a continuous layer of radially oriented membranous granular material under the thick endexine, (3) initiation of intine before first mitosis with characteristic radial plasmalemma invaginations, and (4) a strong stretching force upon engorgement just prior to dehiscence, which leads to reduction in thickness of all wall layers. The possible function of Golgi vesicles in the considerable increase in surface area of the plasmalemma at intine initiation is discussed. The endocingulum observed on acetolyzed and sectioned mature grains is explained ultrastructurally.status: publishe

Distribution of orbicules in Annonaceae mirrors evolutionary trend in angiosperms

Background and aims – Orbicules or Ubisch bodies have been recorded in many angiosperm families and although the first observations date back to 1865, their function in the anther remains enigmatic. In flowering plants a general evolutionary trend is observed from common occurrence of orbicules in early diverging lineages towards a more patchy distribution in derived clades of eudicots. Annonaceae was our family of choice for an in depth study of orbicule distribution in early diverging angiosperms since it met the following three criteria: (1) high tapetum diversity, (2) orbicule presence and absence recorded, and (3) recent phylogeny at genus level available. Key results – Our SEM data of eighteen species show that orbicules are more common in Annonaceae than previously perceived. The resulting orbicule distribution pattern on the family topology indicates a consistent absence of orbicules in the ‘long branch clade’ while orbicules are present in Anaxagorea, the ambavioids, and the ‘short branch clade’. Presence of orbicules is the ancestral condition in the family. Morphologically, Annonaceae orbicules are small (< 1 μm), spherical and smooth. Conclusions – The orbicule distribution pattern in Annonaceae reflects the general evolutionary trend in flowering plants. We hypothesize that orbicule presence can be considered as a powerful proxy for non- amoeboid tapetum characterization in Annonaceae.status: publishe

Distribution of orbicules in Annonaceae mirrors evolutionary trend in angiosperms

Background and aims – Orbicules or Ubisch bodies have been recorded in many angiosperm families and although the first observations date back to 1865, their function in the anther remains enigmatic. In flowering plants a general evolutionary trend is observed from common occurrence of orbicules in early diverging lineages towards a more patchy distribution in derived clades of eudicots. Annonaceae was our family of choice for an in depth study of orbicule distribution in early diverging angiosperms since it met the following three criteria: (1) high tapetum diversity, (2) orbicule presence and absence recorded, and (3) recent phylogeny at genus level available. Key results – Our SEM data of eighteen species show that orbicules are more common in Annonaceae than previously perceived. The resulting orbicule distribution pattern on the family topology indicates a consistent absence of orbicules in the 'long branch clade' while orbicules are present in Anaxagorea, the ambavioids, and the 'short branch clade'. Presence of orbicules is the ancestral condition in the family. Morphologically, Annonaceae orbicules are small (< 1 μm), spherical and smooth. Conclusions – The orbicule distribution pattern in Annonaceae reflects the general evolutionary trend in flowering plants. We hypothesize that orbicule presence can be considered as a powerful proxy for non-amoeboid tapetum characterization in Annonaceae

Systematic relevance of pollen and orbicule characters in the tribe Hillieae (Rubiaceae)

Pollen and orbicule morphology of 26 species in the tribe Hillieae is described based on observations by light, scanning and transmission electron microscopy. Pollen and orbicule characters are critically evaluated and discussed in the context of existing hypotheses of systematic relationships within the tribe. Pollen is 3-zonocolporate with a perforate, microreticulate, reticulate or eutectate sexine. In the two species of Blepharidium, however, the pollen has one, four or five apertures. These pollen morphological data were incorporated into an existing macromorphological matrix of the group and cladistically analysed. The resulting phylogenies indicate that it may be appropriate to reduce Cosmibuena to a subgenus of the genus Hillia, while Blepharidium should be removed from Hillieae because of the deviating pollen type that is unique to the Rubiaceae. All species investigated produce orbicules, which are mostly spherical and possess an electron-lucent core that is sometimes characteristically flattened. (C) 2004 The Linnean Society of London, Botanical Journal of the Linnean Society, 2004, 146, 303-321.status: publishe

Phylogenetic signal of orbicules at family level – Rubiaceae as case study

Orbicules are tiny a-cellular sporopollenin structures that occur in the anthers of many angiosperms together with the pollen grains. Although their occurrence is common, little is known about their function and systematic usefulness. With regard to orbicules, Rubiaceae (Gentianales) are the most intensively studied plant family and therefore an ideal case to present the evolution and phylogenetic signal of orbicule characters at family level. The occurrence and morphology of orbicules was investigated in 64 species of Rubiaceae using scanning electron microscopy. Five relevant orbicule features (presence/absence, abundance, size, shape, ornamentation) were optimized onto a custom-made phylogeny of the family. By optimizing the five orbicule characters some evolutionary trends can be observed. The previously suggested trend in angiosperms towards orbicule absence in more derived taxa is confirmed for Rubiaceae. Orbicules appear to have been independently lost at least nine times within the family, with two subsequent reversals. Small orbicules represent the plesiomorphic character state for the family. A trend from spherical towards irregular orbicules is observed, while ornamented orbicules occur only in derived lineages. Orbicule characters are constant at generic level and in most cases at tribal level, and therefore have potential for systematics. The presence of orbicules is correlated with the occurrence of a non-amoeboid tapetum.status: publishe

Bias and conflict in phylogenetic inference of myco-heterotrophic plants: a case study in Thismiaceae

Due to morphological reduction and absence of amplifiable plastid genes, the identification of photosynthetic relatives of heterotrophic plants is problematic. Although nuclear and mitochondrial gene sequences may offer a welcome alternative source of phylogenetic markers, the presence of rate heterogeneity in these genes may introduce bias/systematic error in phylogenetic analyses. We examine the phylogenetic position of Thismiaceae based on nuclear 18S rDNA and mitochondrial atpA DNA sequence data, as well as using parsimony, likelihood and Bayesian inference methods. Significant differences in evolutionary rates of these genes between closely related taxa lead to conflicting results: while parsimony analyses of 18S rDNA and combined data strongly support the monophyly of Thismiaceae, Bayesian inference, with and without a relaxed molecular clock, as well as the Swofford-Olsen-Waddell-Hillis (SOWH) test confidently reject this hypothesis. We show that rate heterogeneity in our data leads to long-branch attraction artifacts in parsimony analysis. However, using model-based inference methods the question of whether Thismiaceae are monophyletic remains elusive. On the one hand maximum likelihood nonparametric bootstrapping and parametric hypothesis tests fail to support a paraphyletic Thismiaceae, on the other hand Bayesian inference methods (both without and with a relaxed clock) significantly reject a monophyletic Thismiaceae. These results show that an adequate sampling, the use of rate homogeneous data, and the application of different inference methods are important factors for developing phylogenetic hypotheses of myco-heterotrophic plants. (C) The Willi Hennig Society 2009.status: publishe