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1.
Ann Bot ; 2024 Jul 16.
Article in English | MEDLINE | ID: mdl-39012023

ABSTRACT

BACKGROUND: Species of the carnivorous family Lentibulariaceae exhibit the smallest genomes in flowering plants. We explored the hypothesis that their minute genomes result from the unique mitochondrial cytochrome c oxidase (COX) mutation. The mutation may boost mitochondrial efficiency, which is especially useful for suction-bladder traps of Utricularia, but also increase DNA-damaging reactive oxygen species, leading to genome shrinkage through deletion-biased DNA repair. We aimed to explore this mutation's impact on genome size, providing insights into genetic mutation roles in plant genome evolution under environmental pressures. METHODS: We compiled and measured genome and mean chromosome sizes for 127 and 67 species, respectively, representing all three genera (Genlisea, Pinguicula, and Utricularia) of Lentibulariaceae. We also isolated and analyzed COX sequences to detect the mutation. Through phylogenetic regressions and Ornstein-Uhlenbeck models of trait evolution, we assessed the impact of the COX mutation on the genome and chromosome sizes across the family. RESULTS: Our findings reveal significant correlations between the COX mutations and smaller genome and chromosome sizes. Specifically, species carrying the ancestral COX sequence exhibited larger genomes and chromosomes than those with the mutation. This evidence supports the notion that the COX mutation contributes to genome downsizing, with statistical analyses confirming a directional evolution towards smaller genomes in species harboring these mutations. CONCLUSIONS: Our study confirms that the COX mutation in Lentibulariaceae is associated with genome downsizing, likely driven by increased reactive oxygen species production and subsequent DNA damage requiring deletion-biased repair mechanisms. While boosting mitochondrial energy output, this genetic mutation compromises genome integrity and may potentially affect recombination rates, illustrating a complex trade-off between evolutionary advantages and disadvantages. Our results highlight the intricate processes by which genetic mutations and environmental pressures shape genome size evolution in carnivorous plants.

2.
J Morphol ; 285(3): e21684, 2024 Mar.
Article in English | MEDLINE | ID: mdl-38439588

ABSTRACT

Among marsupials, the endangered numbat (Myrmecobius fasciatus) is the only obligate myrmecophage with a diet comprised strictly of termites. Like many other specialised myrmecophagous mammals, numbats have a gracile and highly specialised skull morphology with an elongated rostrum and small braincase. Myrmecobiidae is one of four taxonomic families within the Australasian marsupial order Dasyuromorphia, and to date, the muscular anatomy of any member of this group is relatively poorly known. We utilised microdissection and contrast-enhanced microcomputed tomography scanning to provide the first comprehensive qualitative and quantitative descriptions of jaw muscle anatomy in numbats and quolls (Dasuyrus species). The arrangement of the jaw muscles across these species was conservative, both in gross anatomy and muscle proportions, corresponding to a 'generalised' mammalian pattern. In contrast to Dasyurus, the jaw muscles of the numbat were greatly reduced. Many aspects of the muscle anatomy of the numbat were similar to patterns reported in other myrmecophagous species, particularly a greatly reduced temporalis muscle. Unusually, the digastric muscle in the numbat was comprised of a single, large anterior belly while the posterior belly was absent. We propose that the enlarged anterior belly of the digastric may be linked to jaw stabilisation and coordination of tongue movements during feeding. The lateral insertion and fascial connection of the digastric to the tongue in numbats may also aid in distributing stress evenly across the jaw and minimise muscle fatigue. The muscle descriptions and three-dimensional models provided in this study will facilitate further analysis of musculoskeletal adaptation and evolution within the Dasyuromorphia.


Subject(s)
Isoptera , Marsupialia , Humans , Animals , X-Ray Microtomography , Neck Muscles , Skull
3.
Evol Dev ; 26(2): e12469, 2024 Mar.
Article in English | MEDLINE | ID: mdl-38236185

ABSTRACT

Cnidarians-the phylum including sea anemones, corals, jellyfish, and hydroids-are one of the oldest groups of predatory animals. Nearly all cnidarians are carnivores that use stinging cells called cnidocytes to ensnare and/or envenom their prey. However, there is considerable diversity in cnidocyte form and function. Tracing the evolutionary history of cnidocytes may therefore provide a proxy for early animal feeding strategies. In this study, we generated a time-calibrated molecular clock of cnidarians and performed ancestral state reconstruction on 12 cnidocyte types to test the hypothesis that the original cnidocyte was involved in prey capture. We conclude that the first cnidarians had only the simplest and least specialized cnidocyte type (the isorhiza) which was just as likely to be used for adhesion and/or defense as the capture of prey. A rapid diversification of specialized cnidocytes occurred through the Ediacaran (~654-574 million years ago), with major subgroups developing unique sets of cnidocytes to match their distinct feeding styles. These results are robust to changes in the molecular clock model, and are consistent with growing evidence for an Ediacaran diversification of animals. Our work also provides insight into the evolution of this complex cell type, suggesting that convergence of forms is rare, with the mastigophore being an interesting counterexample.


Subject(s)
Scyphozoa , Sea Anemones , Animals
4.
BMC Plant Biol ; 23(1): 660, 2023 Dec 20.
Article in English | MEDLINE | ID: mdl-38124058

ABSTRACT

BACKGROUND: Independent origins of carnivory in multiple angiosperm families are fabulous examples of convergent evolution using a diverse array of life forms and habitats. Previous studies have indicated that carnivorous plants have distinct evolutionary trajectories of plastid genome (plastome) compared to their non-carnivorous relatives, yet the extent and general characteristics remain elusive. RESULTS: We compared plastomes from 9 out of 13 carnivorous families and their non-carnivorous relatives to assess carnivory-associated evolutionary patterns. We identified inversions in all sampled Droseraceae species and four species of Utricularia, Pinguicula, Darlingtonia and Triphyophyllum. A few carnivores showed distinct shifts in inverted repeat boundaries and the overall repeat contents. Many ndh genes, along with some other genes, were independently lost in several carnivorous lineages. We detected significant substitution rate variations in most sampled carnivorous lineages. A significant overall substitution rate acceleration characterizes the two largest carnivorous lineages of Droseraceae and Lentibulariaceae. We also observe moderate substitution rates acceleration in many genes of Cephalotus follicularis, Roridula gorgonias, and Drosophyllum lusitanicum. However, only a few genes exhibit significant relaxed selection. CONCLUSION: Our results indicate that the carnivory of plants have different effects on plastome evolution across carnivorous lineages. The complex mechanism under carnivorous habitats may have resulted in distinctive plastome evolution with conserved plastome in the Brocchinia hechtioides to strongly reconfigured plastomes structures in Droseraceae. Organic carbon obtained from prey and the efficiency of utilizing prey-derived nutrients might constitute possible explanation.


Subject(s)
Droseraceae , Genome, Plastid , Lamiales , Magnoliopsida , Humans , Magnoliopsida/genetics , Carnivory , Lamiales/genetics , Droseraceae/genetics , Phylogeny , Evolution, Molecular
5.
New Phytol ; 239(3): 1140-1152, 2023 08.
Article in English | MEDLINE | ID: mdl-37191044

ABSTRACT

Triphyophyllum peltatum, a rare tropical African liana, is unique in its facultative carnivory. The trigger for carnivory is yet unknown, mainly because the plant is difficult to propagate and cultivate. This study aimed at identifying the conditions that result in the formation of carnivorous leaves. In vitro shoots were subjected to abiotic stressors in general and deficiencies of the major nutrients nitrogen, potassium and phosphorus in particular, to trigger carnivorous leaves' development. Adventitious root formation was improved to allow verification of the trigger in glasshouse-grown plants. Among all the stressors tested, only under phosphorus deficiency, the formation of carnivorous leaves was observed. These glandular leaves fully resembled those found under natural growing conditions including the secretion of sticky liquid by mature capture organs. To generate plants for glasshouse experiments, a pulse of 55.4 µM α-naphthaleneacetic acid was essential to achieve 90% in vitro rooting. This plant material facilitated the confirmation of phosphorus starvation to be essential and sufficient for carnivory induction, also under ex vitro conditions. Having established the cultivation of T. peltatum and the induction of carnivory, future gene expression profiles from phosphorus starvation-induced leaves will provide important insight to the molecular mechanism of carnivory on demand.


Subject(s)
Dioncophyllaceae , Phosphorus , Carnivory , Plants , Plant Leaves
6.
Plants (Basel) ; 12(2)2023 Jan 15.
Article in English | MEDLINE | ID: mdl-36679121

ABSTRACT

Systems biology has been increasingly applied with multiple omics for a holistic comprehension of complex biological systems beyond the reductionist approach that focuses on individual molecules. Different high-throughput omics approaches, including genomics, transcriptomics, metagenomics, proteomics, and metabolomics have been implemented to study the molecular mechanisms of botanical carnivory. This covers almost all orders of carnivorous plants, namely Caryophyllales, Ericales, Lamiales, and Oxalidales, except Poales. Studies using single-omics or integrated multi-omics elucidate the compositional changes in nucleic acids, proteins, and metabolites. The omics studies on carnivorous plants have led to insights into the carnivory origin and evolution, such as prey capture and digestion as well as the physiological adaptations of trap organ formation. Our understandings of botanical carnivory are further enhanced by the discoveries of digestive enzymes and transporter proteins that aid in efficient nutrient sequestration alongside dynamic molecular responses to prey. Metagenomics studies revealed the mutualistic relationships between microbes and carnivorous plants. Lastly, in silico analysis accelerated the functional characterization of new molecules from carnivorous plants. These studies have provided invaluable molecular data for systems understanding of carnivorous plants. More studies are needed to cover the diverse species with convergent evolution of botanical carnivory.

7.
Proc Natl Acad Sci U S A ; 119(43): e2109315119, 2022 10 25.
Article in English | MEDLINE | ID: mdl-36252021

ABSTRACT

The characterization of Neandertals' diets has mostly relied on nitrogen isotope analyses of bone and tooth collagen. However, few nitrogen isotope data have been recovered from bones or teeth from Iberia due to poor collagen preservation at Paleolithic sites in the region. Zinc isotopes have been shown to be a reliable method for reconstructing trophic levels in the absence of organic matter preservation. Here, we present the results of zinc (Zn), strontium (Sr), carbon (C), and oxygen (O) isotope and trace element ratio analysis measured in dental enamel on a Pleistocene food web in Gabasa, Spain, to characterize the diet and ecology of a Middle Paleolithic Neandertal individual. Based on the extremely low δ66Zn value observed in the Neandertal's tooth enamel, our results support the interpretation of Neandertals as carnivores as already suggested by δ15N isotope values of specimens from other regions. Further work could help identify if such isotopic peculiarities (lowest δ66Zn and highest δ15N of the food web) are due to a metabolic and/or dietary specificity of the Neandertals.


Subject(s)
Carnivora , Neanderthals , Tooth , Trace Elements , Animals , Carbon/analysis , Carbon Isotopes/analysis , Collagen , Dental Enamel/chemistry , Diet , Nitrogen Isotopes/analysis , Oxygen/analysis , Spain , Strontium/analysis , Tooth/chemistry , Trace Elements/analysis , Zinc/analysis , Zinc Isotopes/analysis
8.
Int J Mol Sci ; 23(19)2022 Sep 29.
Article in English | MEDLINE | ID: mdl-36232812

ABSTRACT

Carnivorous rainbow plants (Byblis, Byblidaceae, Lamiales) possess sticky flypaper traps for the capture, retention, and digestion of prey (mainly small insects). The trapping system is based on a multitude of millimeter-sized glandular trichomes (also termed stalked glands), which produce adhesive glue drops. For over a century, the trapping system of Byblis was considered passive, meaning that no plant movement is involved. Recently, a remarkable discovery was made: the stalked glands of Byblis are indeed capable of reacting to chemical (protein) stimuli with slow movement responses. This prompted us to investigate this phenomenon further with a series of experiments on the stimulation, kinematics, actuation, and functional morphology of the stalked glands of cultivated Byblis gigantea plants. Measured stalked gland lengths and densities on the trap leaves are similar to the data from the literature. Motion reactions could only be triggered with chemical stimuli, corroborating the prior study on the stalked gland sensitivity. Reaction time (i.e., time from stimulation until the onset of motion) and movement duration are temperature-dependent, which hints towards a tight physiological control of the involved processes. The stalked gland movement, which consist of a sequence of twisting and kinking motions, is rendered possible by the components of the stalk cell wall and is furthermore anatomically and mechanically predetermined by the orientation of cellulose microfibrils in the cell wall. Successive water displacement processes from the stalk cell into the basal cells actuate the movement. The same kinematics could be observed in stalked glands drying in air or submersed in a saturated salt solution. Stimulated and dried stalked glands as well as those from the hypertonic medium were capable of regaining their initial shape by rehydration in water. However, no glue production could be observed afterwards. The long-time overlooked chemonastic movements of stalked glands may help Byblis to retain and digest its prey; however, further research is needed to shed light on the ecological characteristics of the rainbow plant's trapping system.


Subject(s)
Carnivorous Plant , Lamiales , Animals , Cellulose , Insecta/physiology , Plants , Water
9.
Ann Bot ; 130(7): 927-938, 2022 12 31.
Article in English | MEDLINE | ID: mdl-36306274

ABSTRACT

BACKGROUND AND AIMS: While isotopic enrichment of nitrogen (15N) and carbon (13C) is often used to determine whether carnivorous plant species capture and assimilate nutrients from supplemental sources such as invertebrate prey or mammal excreta (heterotrophic nutrition), little is known about how successful the different strategies deployed by carnivorous plants are at obtaining supplemental nutrition. The collection of mammalian faeces by Nepenthes (tropical pitcher plants) is the result of a highly specialized biological mutualism that results in heterotrophic nitrogen gain; however, it remains unknown how effective this strategy is in comparison to Nepenthes species not known to collect mammalian faeces. METHODS: We examined how isotopic enrichment varied in the diverse genus Nepenthes, among species producing pitchers for invertebrate capture and species exhibiting mutualisms for the collection of mammal excreta. Enrichment factors were calculated from δ15N and δ13C values from eight Nepenthes species and naturally occurring hybrids along with co-occurring reference (non-carnivorous) plants from three mountain massifs in Borneo: Mount Kinabalu, Mount Tambuyukon and Mount Trus Madi. RESULTS: All Nepenthes examined, except N. edwardsiana, were significantly enriched in 15N compared to co-occurring non-carnivorous plants, and 15N enrichment was more than two-fold higher in species with adaptations for the collection of mammal excreta compared with other Nepenthes. CONCLUSIONS: The collection of mammal faeces clearly represents a highly effective strategy for heterotrophic nitrogen gain in Nepenthes. Species with adaptations for capturing mammal excreta occur exclusively at high elevation (i.e. are typically summit-occurring) where previous studies suggest invertebrate prey are less abundant and less frequently captured. As such, we propose this strategy may maximize nutritional return by specializing towards ensuring the collection and retention of few but higher-value N sources in environments where invertebrate prey may be scarce.


Subject(s)
Carnivory , Mammals , Animals , Nitrogen
10.
Curr Biol ; 32(19): 4255-4263.e5, 2022 10 10.
Article in English | MEDLINE | ID: mdl-36087579

ABSTRACT

Since the 19th century, it has been known that the carnivorous Venus flytrap is electrically excitable. Nevertheless, the mechanism and the molecular entities of the flytrap action potential (AP) remain unknown. When entering the electrically excitable stage, the trap expressed a characteristic inventory of ion transporters, among which the increase in glutamate receptor GLR3.6 RNA was most pronounced. Trigger hair stimulation or glutamate application evoked an AP and a cytoplasmic Ca2+ transient that both propagated at the same speed from the site of induction along the entire trap lobe surface. A priming Ca2+ moiety entering the cytoplasm in the context of the AP was further potentiated by an organelle-localized calcium-induced calcium release (CICR)-like system prolonging the Ca2+ signal. While the Ca2+ transient persisted, SKOR K+ channels and AHA H+-ATPases repolarized the AP already. By counting the number of APs and long-lasting Ca2+ transients, the trap directs the different steps in the carnivorous plant's hunting cycle. VIDEO ABSTRACT.


Subject(s)
Droseraceae , Action Potentials , Adenosine Triphosphatases , Calcium , Calcium Signaling , Glutamates , Membrane Transport Proteins , RNA , Receptors, Glutamate
11.
Ecol Lett ; 25(9): 2076-2087, 2022 Sep.
Article in English | MEDLINE | ID: mdl-35950788

ABSTRACT

The premise that the intensity of biotic interactions decreases with increasing latitudes and elevations is broadly accepted; however, whether these geographical patterns can be explained within a common theoretical framework remains unclear. Our goal was to identify the general pattern of elevational changes in trophic interactions and to explore the sources of variation among the outcomes of individual studies. Meta-analysis of 226 effect sizes calculated from 134 publications demonstrated a significant but interaction-specific decrease in the intensity of herbivory, carnivory and parasitism with increasing elevation. Nevertheless, this decrease was not significant at high latitudes and for interactions involving endothermic organisms, for herbivore outbreaks or for herbivores living within plant tissues. Herbivory similarly declined with increases in latitude and elevation, whereas carnivory showed a fivefold stronger decrease with elevation than with latitude and parasitism increased with latitude but decreased with elevation. Thus, although these gradients share a general pattern and several sources of variation in trophic interaction intensity, we discovered important dissimilarities, indicating that elevational and latitudinal changes in these interactions are partly driven by different factors. We conclude that the scope of the latitudinal biotic interaction hypothesis cannot be extended to incorporate elevational gradients.


Subject(s)
Herbivory , Plants
12.
Ecol Evol ; 12(7): e9077, 2022 Jul.
Article in English | MEDLINE | ID: mdl-35866021

ABSTRACT

Cichlid fishes of the tribe Tropheini are a striking case of adaptive radiation, exemplifying multiple trophic transitions between herbivory and carnivory occurring in sympatry with other established cichlid lineages. Tropheini evolved highly specialized eco-morphologies to exploit similar trophic niches in different ways repeatedly and rapidly. To better understand the evolutionary history and trophic adaptations of this lineage, we generated a dataset of 532 targeted loci from 21 out of the 22 described Tropheini species. We resolved the Tropheini into seven monophyletic genera and discovered one to be polyphyletic. The polyphyletic genus, Petrochromis, represents three convergent origins of the algae grazing trophic specialization. This repeated evolution of grazing may have been facilitated by adaptive introgression as we found evidence for gene flow among algae grazing genera. We also found evidence of gene flow among algae browsing genera, but gene flow was restricted between herbivorous and carnivorous genera. Furthermore, we observed no evidence supporting a hybrid origin of this radiation. Our molecular evolutionary analyses suggest that opsin genes likely evolved in response to selection pressures associated with trophic ecology in the Tropheini. We found surprisingly little evidence of positive selection in coding regions of jaw-shaping genes in this trophically diverse lineage. This suggests low degrees of freedom for further change in these genes, and possibly a larger role for regulatory variation in driving jaw adaptations. Our study emphasizes Tropheini cichlids as an important model for studying the evolution of trophic specialization and its role in speciation.

13.
Proc Biol Sci ; 289(1970): 20212487, 2022 03 09.
Article in English | MEDLINE | ID: mdl-35232241

ABSTRACT

Predation is a fundamental ecological process that shapes communities and drives evolutionary dynamics. As the world rapidly urbanizes, it is critical to understand how human perturbations alter predation and meat consumption across taxa. We conducted a meta-analysis to quantify the effects of urban environments on three components of trophic ecology in predators: dietary species richness, dietary evenness and stable isotopic ratios (IRs) (δ13C and δ15N IR). We evaluated whether the intensity of anthropogenic pressure, using the human footprint index (HFI), explained variation in effect sizes of dietary attributes using a meta-regression. We calculated Hedges' g effect sizes from 44 studies including 11 986 samples across 40 predatory species in 39 cities globally. The direction and magnitude of effect sizes varied among predator taxa with reptilian diets exhibiting the most sensitivity to urbanization. Effect sizes revealed that predators in cities had comparable diet richness, evenness and nitrogen ratios, though carbon IRs were more enriched in cities. We found that neither the 1993 nor 2009 HFI editions explained effect size variation. Our study provides, to our knowledge, the first assessment of how urbanization has perturbed predator-prey interactions for multiple taxa at a global scale. We conclude that the functional role of predators is conserved in cities and urbanization does not inherently relax predation, despite diets broadening to include anthropogenic food sources such as sugar, wheat and corn.


Subject(s)
Predatory Behavior , Urbanization , Animals , Cities , Diet , Food Chain , Humans , Vertebrates
14.
Proc Natl Acad Sci U S A ; 119(5)2022 02 01.
Article in English | MEDLINE | ID: mdl-35074877

ABSTRACT

The appearance of Homo erectus shortly after 2.0 Ma is widely considered a turning point in human dietary evolution, with increased consumption of animal tissues driving the evolution of larger brain and body size and a reorganization of the gut. An increase in the size and number of zooarchaeological assemblages after the appearance of H. erectus is often offered as a central piece of archaeological evidence for increased carnivory in this species, but this characterization has yet to be subject to detailed scrutiny. Any widespread dietary shift leading to the acquisition of key traits in H. erectus should be persistent in the zooarchaeological record through time and can only be convincingly demonstrated by a broad-scale analysis that transcends individual sites or localities. Here, we present a quantitative synthesis of the zooarchaeological record of eastern Africa from 2.6 to 1.2 Ma. We show that several proxies for the prevalence of hominin carnivory are all strongly related to how well the fossil record has been sampled, which constrains the zooarchaeological visibility of hominin carnivory. When correcting for sampling effort, there is no sustained increase in the amount of evidence for hominin carnivory between 2.6 and 1.2 Ma. Our observations undercut evolutionary narratives linking anatomical and behavioral traits to increased meat consumption in H. erectus, suggesting that other factors are likely responsible for the appearance of its human-like traits.


Subject(s)
Body Size/physiology , Carnivory/physiology , Archaeology/methods , Biological Evolution , Brain/physiology , Diet/methods , Fossils , Humans
15.
Plants (Basel) ; 10(12)2021 Dec 03.
Article in English | MEDLINE | ID: mdl-34961127

ABSTRACT

The genus Utricularia includes around 250 species of carnivorous plants, commonly known as bladderworts. The generic name Utricularia was coined by Carolus Linnaeus in reference to the carnivorous organs (Utriculus in Latin) present in all species of the genus. Since the formal proposition by Linnaeus, many species of Utricularia were described, but only scarce information about the biology for most species is known. All Utricularia species are herbs with vegetative organs that do not follow traditional models of morphological classification. Since the formal description of Utricularia in the 18th century, the trap function has intrigued naturalists. Historically, the traps were regarded as floating organs, a common hypothesis that was maintained by different botanists. However, Charles Darwin was most likely the first naturalist to refute this idea, since even with the removal of all traps, the plants continued to float. More recently, due mainly to methodological advances, detailed studies on the trap function and mechanisms could be investigated. This review shows a historical perspective on Utricularia studies which focuses on the traps and body organization.

16.
FEBS Open Bio ; 11(9): 2576-2585, 2021 09.
Article in English | MEDLINE | ID: mdl-34289256

ABSTRACT

Yellow to red colored betalains are a chemotaxonomic feature of Caryophyllales, while in most other plant taxa, anthocyanins are responsible for these colors. The carnivorous plant family Nepenthaceae belongs to Caryophyllales; here, red-pigmented tissues seem to attract insect prey. Strikingly, the chemical nature of red color in Nepenthes has never been elucidated. Although belonging to Caryophyllales, in Nepenthes, some molecular evidence supports the presence of anthocyanins rather than betalains. However, there was previously no direct chemical proof of this. Using ultra-high-performance liquid chromatography-electrospray ionization-high-resolution mass spectrometry, we identified cyanidin glycosides in Nepenthes species and tissues. Further, we reveal the existence of a complete set of constitutively expressed anthocyanin biosynthetic genes in Nepenthes. Thus, here we finally conclude the long-term open question regarding red pigmentation in Nepenthaceae.


Subject(s)
Anthocyanins/analysis , Carnivorous Plant/chemistry , Pigmentation , Anthocyanins/biosynthesis , Anthocyanins/chemistry , Anthocyanins/isolation & purification , Carnivorous Plant/classification , Carnivorous Plant/genetics , Chemical Fractionation , Chromatography, High Pressure Liquid , Computational Biology/methods , Gene Expression Profiling , Gene Expression Regulation, Plant , Molecular Structure , Phylogeny , Spectrometry, Mass, Electrospray Ionization , Transcriptome
17.
Front Plant Sci ; 12: 643137, 2021.
Article in English | MEDLINE | ID: mdl-34122470

ABSTRACT

The emergence of the carnivory syndrome and traps in plants is one of the most intriguing questions in evolutionary biology. In the present study, we addressed it by comparative transcriptomics analysis of leaves and leaf-derived pitcher traps from a predatory plant Nepenthes ventricosa × Nepenthes alata. Pitchers were collected at three stages of development and a total of 12 transcriptomes were sequenced and assembled de novo. In comparison with leaves, pitchers at all developmental stages were found to be highly enriched with upregulated genes involved in stress response, specification of shoot apical meristem, biosynthesis of sucrose, wax/cutin, anthocyanins, and alkaloids, genes encoding digestive enzymes (proteases and oligosaccharide hydrolases), and flowering-related MADS-box genes. At the same time, photosynthesis-related genes in pitchers were transcriptionally downregulated. As the MADS-box genes are thought to be associated with the origin of flower organs from leaves, we suggest that Nepenthes species could have employed a similar pathway involving highly conserved MADS-domain transcription factors to develop a novel structure, pitcher-like trap, for capture and digestion of animal prey during the evolutionary transition to carnivory. The data obtained should clarify the molecular mechanisms of trap initiation and development and may contribute to solving the problem of its emergence in plants.

18.
Ann Bot ; 128(3): 241-259, 2021 08 26.
Article in English | MEDLINE | ID: mdl-34111238

ABSTRACT

BACKGROUND: Carnivorous plants are an ecological group of approx. 810 vascular species which capture and digest animal prey, absorb prey-derived nutrients and utilize them to enhance their growth and development. Extant carnivorous plants have evolved in at least ten independent lineages, and their adaptive traits represent an example of structural and functional convergence. Plant carnivory is a result of complex adaptations to mostly nutrient-poor, wet and sunny habitats when the benefits of carnivory exceed the costs. With a boost in interest and extensive research in recent years, many aspects of these adaptations have been clarified (at least partly), but many remain unknown. SCOPE: We provide some of the most recent insights into substantial ecophysiological, biochemical and evolutional particulars of plant carnivory from the functional viewpoint. We focus on those processes and traits in carnivorous plants associated with their ecological characterization, mineral nutrition, cost-benefit relationships, functioning of digestive enzymes and regulation of the hunting cycle in traps. We elucidate mechanisms by which uptake of prey-derived nutrients leads to stimulation of photosynthesis and root nutrient uptake. CONCLUSIONS: Utilization of prey-derived mineral (mainly N and P) and organic nutrients is highly beneficial for plants and increases the photosynthetic rate in leaves as a prerequisite for faster plant growth. Whole-genome and tandem gene duplications brought gene material for diversification into carnivorous functions and enabled recruitment of defence-related genes. Possible mechanisms for the evolution of digestive enzymes are summarized, and a comprehensive picture on the biochemistry and regulation of prey decomposition and prey-derived nutrient uptake is provided.


Subject(s)
Carnivory , Plants , Animals , Nutrients , Photosynthesis , Plant Leaves , Plants/genetics
19.
Proc Biol Sci ; 288(1947): 20210079, 2021 03 31.
Article in English | MEDLINE | ID: mdl-33784864

ABSTRACT

Novel behaviours can spur evolutionary change and sometimes even precede morphological innovation, but the evolutionary and developmental contexts for their origins can be elusive. One proposed mechanism to generate behavioural innovation is a shift in the developmental timing of gene-expression patterns underlying an ancestral behaviour, or molecular heterochrony. Alternatively, novel suites of gene expression, which could provide new contexts for signalling pathways with conserved behavioural functions, could promote novel behavioural variation. To determine the relative contributions of these alternatives to behavioural innovation, I used a species of spadefoot toad, Spea bombifrons. Based on environmental cues, Spea larvae develop as either of two morphs: 'omnivores' that, like their ancestors, feed on detritus, or 'carnivores' that are predaceous and cannibalistic. Because all anuran larvae undergo a natural transition to obligate carnivory during metamorphosis, it has been proposed that the novel, predaceous behaviour in Spea larvae represents the accelerated activation of gene networks influencing post-metamorphic behaviours. Based on comparisons of brain transcriptional profiles, my results reject widespread heterochrony as a mechanism promoting the expression of predaceous larval behaviour. They instead suggest that the evolution of this trait relied on novel patterns of gene expression that include components of pathways with conserved behavioural functions.


Subject(s)
Anura , Biological Evolution , Animals , Anura/genetics , Brain , Gene Expression , Larva/genetics
20.
Am J Bot ; 107(11): 1606-1613, 2020 11.
Article in English | MEDLINE | ID: mdl-33145765

ABSTRACT

PREMISE: The association of carnivory (an adaptation to nutrient-poor soils) with fire has been described as a paradox, given increases in nutrient availability that often accompany fire. The nutrients that increase in availability following fire, however, may not be the same as those provided by prey and may not reduce nutrient limitation if accompanied by even greater increases in light. METHODS: Using a factorial experiment in the field, we examined how simulated fire (clipping plus nitrogen-free fertilizer addition) and prey-derived nutrient availability (prey exclusion) interacted to influence carnivorous potential in Sarracenia alata and belowground competition with its neighbors (manipulated via trenching). We hypothesized that simulated fire combined with prey exclusion would (1) increase the potential for prey capture relative to shade avoidance, hereafter, relative prey-capture potential (RPCP), and/or (2) increase belowground competition with neighboring plants. RESULTS: Sarracenia alata increased RPCP in response to the combination of simulated fire and prey exclusion, despite increases in phosphorus and other nutrients associated with the simulated fire treatment, suggesting that prey capture potential increases in response to increased nitrogen limitation resulting from increases in light and/or phosphorus after fire. We found no evidence of belowground competition. CONCLUSIONS: The potential importance of carnivory in Sarracenia alata increases following fire. This result helps to explain the paradoxical association of carnivorous plants with fire by demonstrating the potential for prey-derived nutrient limitation to increase rather than decrease in response to increases in light and nutrients other than nitrogen following fire.


Subject(s)
Fires , Sarraceniaceae , Carnivory , Nitrogen , Phosphorus
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