The worldwide holoparasitic Apodanthaceae confidently placed in the Cucurbitales by nuclear and mitochondrial gene trees

Filipowicz, Natalia; Renner, Susanne S.

doi:10.1186/1471-2148-10-219

Cited by 41 publications

(32 citation statements)

References 47 publications

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“…The position of parasitic clades within angiosperm phylogeny has been controversial, and even the higher-level relationships are debated [63-65]. As a consequence, there have been many changes to higher-level taxonomy.…”

Section: Methodsmentioning

confidence: 99%

Parasitic plants have increased rates of molecular evolution across all three genomes

2013

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BackgroundTheoretical models and experimental evidence suggest that rates of molecular evolution could be raised in parasitic organisms compared to non-parasitic taxa. Parasitic plants provide an ideal test for these predictions, as there are at least a dozen independent origins of the parasitic lifestyle in angiosperms. Studies of a number of parasitic plant lineages have suggested faster rates of molecular evolution, but the results of some studies have been mixed. Comparative analysis of all parasitic plant lineages, including sequences from all three genomes, is needed to examine the generality of the relationship between rates of molecular evolution and parasitism in plants.ResultsWe analysed DNA sequence data from the mitochondrial, nuclear and chloroplast genomes for 12 independent evolutionary origins of parasitism in angiosperms. We demonstrated that parasitic lineages have a faster rate of molecular evolution than their non-parasitic relatives in sequences for all three genomes, for both synonymous and nonsynonymous substitutions.ConclusionsOur results prove that raised rates of molecular evolution are a general feature of parasitic plants, not confined to a few taxa or specific genes. We discuss possible causes for this relationship, including increased positive selection associated with host-parasite arms races, relaxed selection, reduced population size or repeated bottlenecks, increased mutation rates, and indirect causal links with generation time and body size. We find no evidence that faster rates are due to smaller effective populations sizes or changes in selection pressure. Instead, our results suggest that parasitic plants have a higher mutation rate than their close non-parasitic relatives. This may be due to a direct connection, where some aspect of the parasitic lifestyle drives the evolution of raised mutation rates. Alternatively, this pattern may be driven by an indirect connection between rates and parasitism: for example, parasitic plants tend to be smaller than their non-parasitic relatives, which may result in more cell generations per year, thus a higher rate of mutations arising from DNA copy errors per unit time. Demonstration that adoption of a parasitic lifestyle influences the rate of genomic evolution is relevant to attempts to infer molecular phylogenies of parasitic plants and to estimate their evolutionary divergence times using sequence data.

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Section: Methodsmentioning

confidence: 99%

Parasitic plants have increased rates of molecular evolution across all three genomes

2013

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“…The use of combined datasets that include questionable sequences can affect phylogenetic tree construction (Saarela et al, ; Stefanović et al, ; Filipowicz & Renner, ). For example, Tinomiscium (Menispermaceae) was considered a member of the expanded Tinosporeae based on the combined rbcL and atpB data, but it was regarded as the earliest‐diverging genus in the family based on the combined rbcL , atpB , and ndhF data (Hoot et al, ).…”

mentioning

confidence: 99%

Revisiting the phylogeny of Ranunculeae: Implications for divergence time estimation and historical biogeography

Wang

Xiao

et al. 2014

J of Sytematics Evolution

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Previous studies based on different molecular datasets have generated conflicting topologies for Ranunculeae. Here, we revisit the phylogeny of Ranunculeae by analyzing the individual matK/trnK, psbJ-petA, and internal transcribed spacer (ITS) data, the combined matK/trnK, psbJ-petA, and ITS dataset, and the combined rbcL, trnL-F, matK/trnK, psbJ-petA, and ITS dataset. Based on the tree-based comparisons, BLAST searches against NCBI of the sequences, and close examination of the alignment, we found that 10 psbJ-petA sequences previously used were questionable (erroneous or problematic) and responsible for previous conflicting topologies. After omitting these questionable sequences, we provide a new phylogeny for Ranunculeae, in which Beckwithia-Cyrtorhyncha, Kumlienia, and Peltocalathos were replaced. These new replacements are supported by corresponding morphological characters. Moreover, three previously proposed intercontinental disjunct distributions within Ranunculus were also refuted. In our framework, our divergence time and biogeographic analyses indicate that divergence time estimates and the ancestral areas reconstructed for 10 of the 15 nodes in the genus-level phylogeny were influenced by elimination of the questionable sequences. The most recent common ancestor of Ranunculeae was inferred to be present in Europe and North America during the late Eocene. Clades I and II began to diversify in Europe and North America, respectively, and subsequently migrated to other continents. This study shows that it is necessary to analyze individual chloroplast DNA region datasets separately to detect questionable sequences early in the study. The combined dataset including the questionable sequences resulted in an erroneous phylogenetic tree, and the use of this tree subsequently affected age estimates and biogeographic analyses.

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“…Members of the Cucurbitales show considerable variation (Matthews et al ., 2001; Matthews & Endress, 2004), particularly among Anisophylleaceae, which is sister to the remaining ‘core’ families (Begoniaceae, Coriariaceae, Corynocarpaceae, Cucurbitaceae, Datiscaceae, Tetramelaceae), and the holoparasitic family Apodanthaceae recently confirmed to be included in the order (Filipowicz & Renner, 2010; Schaefer & Renner, 2011). They all appear to share the synapomorphies of two whorls of similar perianth parts with valvate aestivation, similar surface texture of the petals, raised stomata and perforation plates with no or minimal borders (Stevens, 2001 onwards).…”

Section: Introductionmentioning

confidence: 99%

Fossil floral and fruit evidence for the evolution of unusual developmental characters in Fagales

Taylor

Tiffney

2012

Botanical Journal of the Linnean Society

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Flowers of many living Fagales exhibit unusual developmental characteristics. At anthesis, ovulate flowers have carpels bearing immature orthotropous ovules. After pollination, the ovules increase in size and become anatropous and the ovary enlarges. Simultaneously, the pollen tubes extend from the stigma to the ovules with several phases of growth and quiescence. Finally, after the first fertilization, the remaining ovules abort, resulting in a single‐seeded fruit. Three‐dimensionally preserved potentially fagaceous mesofossil flowers from the Campanian of Massachusetts, USA, provide evidence on the evolution of these characters. The fossils share putative synapomorphies with the Fagales (six tepals, mostly inferior, three‐carpellate ovary with each locule initially containing two pendant ovules, punctate‐rugulate, tricolporate pollen and fruit with a single seed). However, the fossil is bisexual and has nectaries, characters shared with the sister order Cucurbitales, and both lack the fagalean immature orthotropous developmental stage. The fossil shares synapomorphies of an inferior ovary and a single‐seeded indehiscent fruit with both living orders and appears to be transitional. Comparison of ontogenetic changes between the fossil and related fagalean taxa suggests independent stepwise changes in development in which some characters of the modern clades were in place at ∼ 75 Myr and others evolved more recently. © 2012 The Linnean Society of London, Botanical Journal of the Linnean Society, 2012, 168, 353–376.

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The worldwide holoparasitic Apodanthaceae confidently placed in the Cucurbitales by nuclear and mitochondrial gene trees

Cited by 41 publications

References 47 publications

Parasitic plants have increased rates of molecular evolution across all three genomes

Parasitic plants have increased rates of molecular evolution across all three genomes

Revisiting the phylogeny of Ranunculeae: Implications for divergence time estimation and historical biogeography

Fossil floral and fruit evidence for the evolution of unusual developmental characters in Fagales

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