Biomechanical analysis of prey capture in the carnivorous Southern bladderwort (Utricularia australis).
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SUBMITTER: Poppinga S
PROVIDER: S-EPMC5431978 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:Background and aimsThe typical rootless linear shoots of aquatic carnivorous plants exhibit clear, steep polarity associated with very rapid apical shoot growth. The aim of this study was to determine how auxin and cytokinin contents are related to polarity and shoot growth in such plants.MethodsThe main auxin and cytokinin metabolites in separated shoot segments and turions of two carnivorous plants, Aldrovanda vesiculosa and Utricularia australis, were analysed using ultra-high-performance liquid chromatography coupled with triple quad mass spectrometry.Key resultsIn both species, only isoprenoid cytokinins were identified. Zeatin cytokinins predominated in the apical parts, with their concentrations decreasing basipetally, and the trans isomer predominated in A. vesiculosa whereas the cis form was more abundant in U australis. Isopentenyladenine-type cytokinins, in contrast, increased basipetally. Conjugated cytokinin metabolites, the O-glucosides, were present at high concentrations in A. vesiculosa but only in minute amounts in U. australis. N(9)-glucoside forms were detected only in U. australis, with isopentenyladenine-9-glucoside (iP9G) being most abundant. In addition to free indole-3-acetic acid (IAA), indole-3-acetamide (IAM), IAA-aspartate (IAAsp), IAA-glutamate (IAGlu) and IAA-glycine (IAGly) conjugates were identified.ConclusionsBoth species show common trends in auxin and cytokinin levels, the apical localization of the cytokinin biosynthesis and basipetal change in the ratio of active cytokinins to auxin, in favour of auxin. However, our detailed study of cytokinin metabolic profiles also revealed that both species developed different regulatory mechanisms of active cytokinin content; on the level of their degradation, in U. australis, or in the biosynthesis itself, in the case of A. vesiculosa Results indicate that the rapid turnover of these signalling molecules along the shoots is essential for maintaining the dynamic balance between the rapid polar growth and development of the apical parts and senescence of the older, basal parts of the shoots.
| S-EPMC4866309 | biostudies-literature
Project description:Utricularia multifida is carnivorous bladderwort from Western Australia and belongs to a phylogenetically early-diverging lineage of the genus. We present a prey spectrum analysis resulting from a snapshot sampling of 17 traps-the first of this species to our knowledge. The most abundant prey groups were Ostracoda, Copepoda, and Cladocera. The genus cf. Cypretta (Cyprididae, Ostracoda) was the predominant prey. However, a high variety of other prey organisms with different taxonomic backgrounds was also detected. Our results indicate that U. multifida may potentially be specialized in capturing substrate-bound prey. Future approaches should sample plants from different localities to allow for robust comparative analyses.
| S-EPMC8026053 | biostudies-literature
Project description:We investigated the predator-prey interactions between an Australian ecotype of the carnivorous waterwheel plant (Aldrovanda vesiculosa, Droseraceae) and its potential natural prey, the water flea Daphnia longicephala (Daphniidae), which also occurs in Australia. A. vesiculosa develops snap-traps, which close within ~10-100?ms after mechanical triggering by zooplankton prey. Prey capture attempts (PCAs) were recorded via high-speed cinematography in the laboratory. From 14 recorded PCAs, nine were successful for the plant (the prey was caught), and five were unsuccessful (prey could escape), resulting in a capture rate of ~64%. The prey animals' locomotion behaviour (antenna beat frequency and movement type) in trap vicinity or inside the open traps is very variable. Traps were mainly triggered with the second antennae. During trap closure, the animals moved only very little actively. A flight response in reaction to an initiated trap closure was not observed. However, several animals could escape, either by having a "lucky" starting position already outside the triggered trap, by freeing themselves after trap closure, or by being pressed out by the closing trap lobes. According to our observations in the successful PCAs, we hypothesize that the convex curvature of the two trap lobes (as seen from the outside) and the infolded trap rims are structural means supporting the capture and retention of prey. Our results are discussed in a broader biological context and promising aspects for future studies are proposed.
| S-EPMC6901478 | biostudies-literature
Project description:The genome of the bladderwort Utricularia gibba provides an unparalleled opportunity to uncover the adaptive landscape of an aquatic carnivorous plant with unique phenotypic features such as absence of roots, development of water-filled suction bladders, and a highly ramified branching pattern. Despite its tiny size, the U. gibba genome accommodates approximately as many genes as other plant genomes. To examine the relationship between the compactness of its genome and gene turnover, we compared the U. gibba genome with that of four other eudicot species, defining a total of 17,324 gene families (orthogroups). These families were further classified as either 1) lineage-specific expanded/contracted or 2) stable in size. The U. gibba-expanded families are generically related to three main phenotypic features: 1) trap physiology, 2) key plant morphogenetic/developmental pathways, and 3) response to environmental stimuli, including adaptations to life in aquatic environments. Further scans for signatures of protein functional specialization permitted identification of seven candidate genes with amino acid changes putatively fixed by positive Darwinian selection in the U. gibba lineage. The Arabidopsis orthologs of these genes (AXR, UMAMIT41, IGS, TAR2, SOL1, DEG9, and DEG10) are involved in diverse plant biological functions potentially relevant for U. gibba phenotypic diversification, including 1) auxin metabolism and signal transduction, 2) flowering induction and floral meristem transition, 3) root development, and 4) peptidases. Taken together, our results suggest numerous candidate genes and gene families as interesting targets for further experimental confirmation of their functional and adaptive roles in the U. gibba's unique lifestyle and highly specialized body plan.
| S-EPMC4350169 | biostudies-literature
Project description:Bladderworts (Utricularia, Lentibulariaceae, Lamiales) constitute the largest genus of carnivorous plants but only aquatic species (about one fifth of the genus) have so far been thoroughly studied as to their suction trap functioning. In this study, we comparatively investigated trap biomechanics in 19 Utricularia species to examine correlations between life-forms, trapping mechanisms, and functional-morphological traits. Our investigations show the existence of two functional trap principles (passive trap in U. multifida vs. active suction traps), and - in active suction traps - three main trapdoor movement types (with several subtypes). The trapdoor movement types and their corresponding functional-morphological features most presumably represent adaptations to the respective habitat. We furthermore give insights into fluid dynamics during suction in three representatives of the main types of trapdoor movement. The results on functional morphology and trapdoor movement were mapped onto a new phylogenetic reconstruction of the genus, derived from the rapidly evolving chloroplast regions trnK, rps16 and trnQ-rps16 and a sampling of 105 Utricularia species in total. We discuss potential scenarios of trap character evolution and species radiation, highlighting possible key innovations that enable such a unique carnivorous lifestyle in different habitats.
| S-EPMC5608911 | biostudies-literature
Project description:Background:The genus Utricularia belongs to Lentibulariaceae, the largest family of carnivorous plants, which includes terrestrial, epiphytic and aquatic species. The development of specialized structures that evolved for carnivory is a feature of this genus that has been of great interest to biologists since Darwin's early studies. Utricularia gibba is itself an aquatic plant with sophisticated bladder traps having one of the most complex suction mechanisms for trapping prey. However, the molecular characterization of the mechanisms that regulate trap development and the biophysical processes involved in prey trapping are still largely unknown due to the lack of a simple and reproducible gene transfer system. Results:Here, we report the establishment of a simple, fast and reproducible protocol for genetic transformation of U. gibba based on the T-DNA of Agrobacterium tumefaciens. An in vitro selection system using Phosphinotricin as a selective agent was established for U. gibba. Plant transformation was confirmed by histochemical GUS assays and PCR and qRT-PCR analyses. We report on the expression pattern of the 35S promoter and of the promoter of a trap-specific ribonuclease gene in transgenic U. gibba plants. Conclusions:The genetic transformation protocol reported here is an effective method for studying developmental biology and functional genomics of this genus of carnivorous plants and advances the utility of U. gibba as a model system to study developmental processes involved in trap formation.
| S-EPMC7149871 | biostudies-literature
Project description:Aquatic species of Utricularia are carnivorous plants living in environments poor in nutrients. Their trapping mechanism has fascinated generations of scientists and is still debated today. It was reported recently that Utricularia traps can fire spontaneously. We show here that these spontaneous firings follow an unexpected diversity of temporal patterns, from "metronomic" traps which fire at fixed time intervals to "random" patterns, displaying more scattered firing times. Some "bursting" traps even combine both aspects, with groups of fast regular firings separated by a variable amount of time. We propose a physical model to understand these very particular behaviors, showing that a trap of Utricularia accomplishes mechanical oscillations, based on continuous pumping and sudden opening of the trap door (buckling). We isolate the key parameters governing these oscillations and discuss the effect of their fluctuations.
| S-EPMC3103537 | biostudies-literature
Project description:BackgroundBiological controls with predators of larval mosquito vectors have historically focused almost exclusively on insectivorous animals, with few studies examining predatory plants as potential larvacidal agents. In this study, we experimentally evaluate a generalist plant predator of North America, Utricularia macrorhiza, the common bladderwort, and evaluate its larvacidal efficiency for the mosquito vectors Aedes aegypti and Aedes albopictus in no-choice, laboratory experiments. We sought to determine first, whether U. macrorhiza is a competent predator of container-breeding mosquitoes, and secondly, its predation efficiency for early and late instar larvae of each mosquito species.MethodsNewly hatched, first-instar Ae. albopictus and Ae. aegypti larvae were separately exposed in cohorts of 10 to field-collected U. macrorhiza cuttings. Data on development time and larval survival were collected on a daily basis to ascertain the effectiveness of U. macrorhiza as a larval predator. Survival models were used to assess differences in larval survival between cohorts that were exposed to U. macrorhiza and those that were not. A permutation analysis was used to investigate whether storing U. macrorhiza in laboratory conditions for extended periods of time (1 month vs 6 months) affected its predation efficiency.ResultsOur results indicated a 100% and 95% reduction of survival of Ae. aegypti and Ae. albopictus larvae, respectively, in the presence of U. macrorhiza relative to controls within five days, with peak larvacidal efficiency in plant cuttings from ponds collected in August. Utricularia macrorhiza cuttings, which were prey-deprived, and maintained in laboratory conditions for 6 months were more effective larval predators than cuttings, which were maintained prey-free for 1 month.ConclusionsDue to the combination of high predation efficiency and the unique biological feature of facultative predation, we suggest that U. macrorhiza warrants further development as a method for larval mosquito control.
| S-EPMC7175535 | biostudies-literature
Project description:BackgroundThe carnivorous plant Utricularia gibba (bladderwort) is remarkable in having a minute genome, which at ca. 80 megabases is approximately half that of Arabidopsis. Bladderworts show an incredible diversity of forms surrounding a defined theme: tiny, bladder-like suction traps on terrestrial, epiphytic, or aquatic plants with a diversity of unusual vegetative forms. Utricularia plants, which are rootless, are also anomalous in physiological features (respiration and carbon distribution), and highly enhanced molecular evolutionary rates in chloroplast, mitochondrial and nuclear ribosomal sequences. Despite great interest in the genus, no genomic resources exist for Utricularia, and the substitution rate increase has received limited study.ResultsHere we describe the sequencing and analysis of the Utricularia gibba transcriptome. Three different organs were surveyed, the traps, the vegetative shoot bodies, and the inflorescence stems. We also examined the bladderwort transcriptome under diverse stress conditions. We detail aspects of functional classification, tissue similarity, nitrogen and phosphorus metabolism, respiration, DNA repair, and detoxification of reactive oxygen species (ROS). Long contigs of plastid and mitochondrial genomes, as well as sequences for 100 individual nuclear genes, were compared with those of other plants to better establish information on molecular evolutionary rates.ConclusionThe Utricularia transcriptome provides a detailed genomic window into processes occurring in a carnivorous plant. It contains a deep representation of the complex metabolic pathways that characterize a putative minimal plant genome, permitting its use as a source of genomic information to explore the structural, functional, and evolutionary diversity of the genus. Vegetative shoots and traps are the most similar organs by functional classification of their transcriptome, the traps expressing hydrolytic enzymes for prey digestion that were previously thought to be encoded by bacteria. Supporting physiological data, global gene expression analysis shows that traps significantly over-express genes involved in respiration and that phosphate uptake might occur mainly in traps, whereas nitrogen uptake could in part take place in vegetative parts. Expression of DNA repair and ROS detoxification enzymes may be indicative of a response to increased respiration. Finally, evidence from the bladderwort transcriptome, direct measurement of ROS in situ, and cross-species comparisons of organellar genomes and multiple nuclear genes supports the hypothesis that increased nucleotide substitution rates throughout the plant may be due to the mutagenic action of amplified ROS production.
| S-EPMC3141634 | biostudies-literature
Project description:The carnivorous plants of the family Lentibulariaceae have attained recent attention not only because of their interesting lifestyle, but also because of their dynamic nuclear genome size. Lentibulariaceae genomes span an order of magnitude and include species with the smallest genomes in angiosperms, making them a powerful system to study the mechanisms of genome expansion and contraction. However, little is known about mitochondrial DNA (mtDNA) sequences of this family, and the evolutionary forces that shape this organellar genome. Here we report the sequencing and assembly of the complete mtDNA from the endemic terrestrial Brazilian species Utricularia reniformis. The 857,234bp master circle mitochondrial genome encodes 70 transcriptionaly active genes (42 protein-coding, 25 tRNAs and 3 rRNAs), covering up to 7% of the mtDNA. A ltrA-like protein related to splicing and mobility and a LAGLIDADG homing endonuclease have been identified in intronic regions, suggesting particular mechanisms of genome maintenance. RNA-seq analysis identified properties with putative diverse and important roles in genome regulation and evolution: 1) 672kbp (78%) of the mtDNA is covered by full-length reads; 2) most of the 243kbp intergenic regions exhibit transcripts; and 3) at least 69 novel RNA editing sites in the protein-coding genes. Additional genomic features are hypothetical ORFs (48%), chloroplast insertions, including truncated plastid genes that have been lost from the chloroplast DNA (5%), repeats (5%), relics of transposable elements mostly related to LTR retrotransposons (5%), and truncated mitovirus sequences (0.4%). Phylogenetic analysis based on 32 different Lamiales mitochondrial genomes corroborate that Lentibulariaceae is a monophyletic group. In summary, the U. reniformis mtDNA represents the eighth largest plant mtDNA described to date, shedding light on the genomic trends and evolutionary characteristics and phylogenetic history of the family Lentibulariaceae.
| S-EPMC5516982 | biostudies-literature