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Oriented cell division shapes carnivorous pitcher leaves of Sarracenia purpurea.

ABSTRACT: Complex morphology is an evolutionary outcome of phenotypic diversification. In some carnivorous plants, the ancestral planar leaf has been modified to form a pitcher shape. However, how leaf development was altered during evolution remains unknown. Here we show that the pitcher leaves of Sarracenia purpurea develop through cell division patterns of adaxial tissues that are distinct from those in bifacial and peltate leaves, subsequent to standard expression of adaxial and abaxial marker genes. Differences in the orientation of cell divisions in the adaxial domain cause bifacial growth in the distal region and adaxial ridge protrusion in the middle region. These different growth patterns establish pitcher morphology. A computer simulation suggests that the cell division plane is critical for the pitcher morphogenesis. Our results imply that tissue-specific changes in the orientation of cell division underlie the development of a morphologically complex leaf.

SUBMITTER: Fukushima K

PROVIDER: S-EPMC4382701 | biostudies-literature | 2015

REPOSITORIES: biostudies-literature

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Oriented cell division shapes carnivorous pitcher leaves of Sarracenia purpurea.

Fukushima Kenji K Fujita Hironori H Yamaguchi Takahiro T Kawaguchi Masayoshi M Tsukaya Hirokazu H Hasebe Mitsuyasu M

Nature communications 20150316

Complex morphology is an evolutionary outcome of phenotypic diversification. In some carnivorous plants, the ancestral planar leaf has been modified to form a pitcher shape. However, how leaf development was altered during evolution remains unknown. Here we show that the pitcher leaves of Sarracenia purpurea develop through cell division patterns of adaxial tissues that are distinct from those in bifacial and peltate leaves, subsequent to standard expression of adaxial and abaxial marker genes. ...[more]

PMID: 25774486

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Project description:The carnivorous pitcher plant Sarracenia purpurea exhibits many ethnobotanical uses, including the treatments of type 2 diabetes and tuberculosis-like symptoms. In this study, we prepared different extracts from the leaves (pitchers), stems, and roots of S. purpurea and investigated their antioxidant and anticancer properties. To evaluate the extraction efficiency, we individually used different solvents, namely methanol, ethanol, acetone, and distilled water, for S. purpurea extract preparations. The root extract of S. purpurea, obtained by 100% acetone (S. purpurea-root-acetone), had the highest anticancer activities, antioxidation capacity (the DPPH activity with IC50 of 89.3 ± 2.2 μg/mL), antibacterial activities, total phenolic content (33.4 ± 0.7 mg GAE/g), and total flavonoid content (107.9 ± 2.2 mg QUE/g). The most abundant compounds in S. purpurea-root-acetone were identified using gas chromatography-mass spectrometry; 7,8-Dihydro-α-ionone was the major compound present in S. purpurea-root-acetone. In addition, the co-cytotoxicity of S. purpurea-root-acetone (combined with the clinical anticancer drug 5-fluorouracil (5-FU) on the survival, apoptosis, proliferation, and migration of the 4T1 mammary carcinoma) was examined. The combination of 5-FU with S. purpurea-root-acetone could be highly efficient for anti-4T1 cells. We also found that S. purpurea-root-acetone could inhibit the enzymatic activity of human dihydroorotase (huDHOase), an attractive target for potential anticancer chemotherapy. The sic most abundant compounds in S. purpurea-root-acetone were tested using an in silico analysis via MOE-Dock software for their binding affinities. The top-ranked docking conformations were observed for 7,8-dihydro-α-ionone and stigmast-5-en-3-ol, suggesting the inhibition potential against huDHOase. Overall, the collective data in this study may indicate the pharmacological potentials of S. purpurea-root-acetone for possible medical applications.

Project description:BackgroundThe pitcher plant Sarracenia purpurea supplements nutrient acquisition through carnivory, capturing insect prey which are digested by a food web community of eukaryotes and bacteria. While the food web invertebrates are well studied, and some recent studies have characterized bacteria, detailed genetic analysis of eukaryotic diversity is lacking. This study aimed to compare eukaryotic and bacterial composition and diversity of pitcher communities within and between populations of host plants in nearby but distinct wetland habitats, and to characterize microbial functions across populations and in comparison with another freshwater community.MethodsPitcher fluid was sampled from the two wetlands, Cedarburg and Sapa Bogs, community DNA was extracted, and 16S and 18S rRNA amplicons were sequenced and data processed for community-level comparisons.Results and conclusionsBacterial diversity in the small pitcher volume rivaled that of larger aquatic communities. Between pitcher plant populations, several bacterial families (Kiloniellaceae, Acetobacteraceae, Xanthobacteraceae, Sanguibacteraceae, Oligoflexaceae, Nitrosomonadaceae, Chromatiaceae, Saprospiraceae) were significantly higher in one population. However, although predicted pitcher bacterial functions were distinct from other freshwater communities, especially for some amino acid metabolism, functions were similar across all the pitchers in the two populations. This suggests some functional redundancy among bacterial taxa, and that functions converge to achieve similar food web processes. The sequencing identified a previously under-appreciated high diversity of ciliates, Acari mites, fungi and flagellates in pitcher communities; the most abundant sequences from eukaryotic taxa were Oligohymenophorea ciliates, millipedes and Ichthyosporea flagellates. Two thirds of taxa were identified as food web inhabitants and less than one third as prey organisms. Although eukaryotic composition was not significantly different between populations, there were different species of core taxonomic groups present in different pitchers-these differences may be driven by wetland habitats providing different populations to colonize new pitchers. Eukaryotic composition was more variable than bacterial composition, and there was a poor relationship between bacterial and eukaryotic composition within individual pitchers, suggesting that colonization by eukaryotes may be more stochastic than for bacteria, and bacterial recruitment to pitchers may involve factors other than prey capture and colonization by eukaryotic food web inhabitants.

Project description:The interconnected and overlapping habitats present in natural ecosystems remain a challenge in determining the forces driving microbial community composition. The cuplike leaf structures of some carnivorous plants, including those of the family Sarraceniaceae, are self-contained ecological habitats that represent systems for exploring such microbial ecology questions. We investigated whether Sarracenia minor and Sarracenia flava cultivate distinct bacterial communities when sampled at the same geographic location and time. This sampling strategy eliminates many abiotic environmental variables present in other studies that compare samples harvested over time, and it could reveal biotic factors driving the selection of microbes. DNA extracted from the decomposing detritus trapped in each Sarracenia leaf pitcher was profiled using 16S rRNA amplicon sequencing. We identified a surprising amount of bacterial diversity within each pitcher, but we also discovered bacteria whose abundance was specifically enriched in one of the two Sarracenia species. These differences in bacterial community representation suggest some biotic influence of the Sarracenia plant on the bacterial composition of their pitchers. Overall, our results suggest that bacterial selection due to factors other than geographic location, weather, or prey availability is occurring within the pitchers of these two closely related plant species. This indicates that specific characteristics of S. minor and S. flava may play a role in fostering distinct bacterial communities. These confined, naturally occurring microbial ecosystems within Sarracenia pitchers may provide model systems to answer important questions about the drivers of microbial community composition, succession, and response to environmental perturbations. IMPORTANCE This study uses amplicon sequencing to compare the bacterial communities of environmental samples from the detritus of the leaf cavities of Sarracenia minor and Sarracenia flava pitcher plants. We sampled the detritus at the same time and in the same geographic location, eliminating many environmental variables present in other comparative studies. This study revealed that different species of Sarracenia contain distinct bacterial members within their pitchers, suggesting that these communities are not randomly established based on environmental factors and the prey pool but are potentially enriched for by the plants' chemical or physical environment. This study of these naturally occurring, confined microbial ecosystems will help further establish carnivorous pitcher plants as a model system for answering important questions about the development and succession of microbial communities.

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Oriented cell division shapes carnivorous pitcher leaves of Sarracenia purpurea.

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Oriented cell division shapes carnivorous pitcher leaves of Sarracenia purpurea.

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