Carnivorous plants from the order Caryophyllales co-opted plant phytohormones from a group of jasmonates to regulate digestive enzyme activity. However, not all genera of carnivorous plants have been thoroughly explored, and the digestive physiology of Australian carnivorous rainbow plants of the genus Byblis (order Lamiales) is poorly understood. Here, we investigated the composition of digestive enzymes in the secreted fluid of Byblis filifolia using LC/MS, measured enzyme activity, and analysed tissue phytohormone levels after experimental feeding with fruit flies and coronatine application. Several hydrolytic digestive enzymes were identified in the secreted digestive fluid, the levels of which clearly increased in the presence of insect prey. However, in contrast to the sundew Drosera capensis, endogenous jasmonates do not accumulate, and coronatine, a molecular mimic of jasmonates, is unable to trigger enzyme secretion. Our results showed that B. filifolia is fully carnivorous, with its own digestive enzyme repertoire. However, in contrast to carnivorous genera from the Caryophyllales order, these enzymes are not regulated by jasmonates. This indicates that jasmonates have not been repeatedly co-opted to regulate digestive enzyme activity during the evolution of carnivorous plants.
- Keywords
- Byblis, Carnivorous plant, Drosera, digestive enzyme, jasmonic acid, phytohormones, sundew,
- MeSH
- Amino Acids metabolism pharmacology MeSH
- Caryophyllales * enzymology physiology metabolism MeSH
- Cyclopentanes * metabolism MeSH
- Drosera physiology MeSH
- Indenes metabolism pharmacology MeSH
- Carnivorous Plant * enzymology physiology metabolism MeSH
- Oxylipins * metabolism MeSH
- Plant Growth Regulators * metabolism MeSH
- Animals MeSH
- Check Tag
- Animals MeSH
- Publication type
- Journal Article MeSH
- Names of Substances
- Amino Acids MeSH
- coronatine MeSH Browser
- Cyclopentanes * MeSH
- Indenes MeSH
- jasmonic acid MeSH Browser
- Oxylipins * MeSH
- Plant Growth Regulators * MeSH
The carnivorous plants in the order Caryophyllales co-opted jasmonate signalling from plant defence to botanical carnivory. However, carnivorous plants have at least 11 independent origins, and here we ask whether jasmonate signalling has been co-opted repeatedly in different evolutionary lineages. We experimentally wounded and fed the carnivorous plants Sarracenia purpurea (order Ericales), Cephalotus follicularis (order Oxalidales), Drosophyllum lusitanicum (order Caryophyllales), and measured electrical signals, phytohormone tissue level, and digestive enzymes activity. Coronatine was added exogenously to confirm the role of jasmonates in the induction of digestive process. Immunodetection of aspartic protease and proteomic analysis of digestive fluid was also performed. We found that prey capture induced accumulation of endogenous jasmonates only in D. lusitanicum, in accordance with increased enzyme activity after insect prey or coronatine application. In C. follicularis, the enzyme activity was constitutive while in S. purpurea was regulated by multiple factors. Several classes of digestive enzymes were identified in the digestive fluid of D. lusitanicum. Although carnivorous plants from different evolutionary lineages use the same digestive enzymes, the mechanism of their regulation differs. All investigated genera use jasmonates for their ancient role, defence, but jasmonate signalling has been co-opted for botanical carnivory only in some of them.
- Keywords
- Aspartic protease, carnivorous plant, digestive enzymes, electrical signal, jasmonic acid, phytohormone, plant defence, wounding,
- MeSH
- Carnivory * MeSH
- Carnivorous Plant * MeSH
- Proteomics MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Names of Substances
- coronatine MeSH Browser
- jasmonic acid MeSH Browser
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.
- Keywords
- Dionaea, Drosera, Nepenthes, Carnivorous plant, co-option, cost–benefit relationships, digestive enzymes, evolution of carnivory, hunting cycle, mineral nutrient economy, regulation of enzyme secretion, terrestrial and aquatic species,
- MeSH
- Photosynthesis MeSH
- Plant Leaves MeSH
- Carnivory * MeSH
- Plants * genetics MeSH
- Nutrients MeSH
- Animals MeSH
- Check Tag
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
Carnivorous plants within the order Caryophyllales use jasmonates, a class of phytohormone, in the regulation of digestive enzyme activities. We used the carnivorous butterwort Pinguicula × Tina from the order Lamiales to investigate whether jasmonate signaling is a universal and ubiquitous signaling pathway that exists outside the order Caryophyllales. We measured the electrical signals, enzyme activities, and phytohormone tissue levels in response to prey capture. Mass spectrometry was used to identify proteins in the digestive secretion. We identified eight enzymes in the digestive secretion, many of which were previously found in other genera of carnivorous plants. Among them, alpha-amylase is unique in carnivorous plants. Enzymatic activities increased in response to prey capture; however, the tissue content of jasmonic acid and its isoleucine conjugate remained rather low in contrast to the jasmonate response to wounding. Enzyme activities did not increase in response to the exogenous application of jasmonic acid or coronatine. Whereas similar digestive enzymes were co-opted from plant defense mechanisms among carnivorous plants, the mode of their regulation differs. The butterwort has not co-opted jasmonate signaling for the induction of enzyme activities in response to prey capture. Moreover, the presence of alpha-amylase in digestive fluid of P. × Tina, which has not been found in other genera of carnivorous plants, might indicate that non-defense-related genes have also been co-opted for carnivory.
- Keywords
- Pinguicula, Butterwort, carnivorous plant, digestive enzymes, electrical signals, jasmonic acid, protease, variation potential,
- MeSH
- Cyclopentanes MeSH
- Lamiales * MeSH
- Carnivory * MeSH
- Oxylipins MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Names of Substances
- Cyclopentanes MeSH
- jasmonic acid MeSH Browser
- Oxylipins MeSH
BACKGROUND AND AIMS: General anaesthetics are compounds that induce loss of responsiveness to environmental stimuli in animals and humans. The primary site of action of general anaesthetics is the nervous system, where anaesthetics inhibit neuronal transmission. Although plants do not have neurons, they generate electrical signals in response to biotic and abiotic stresses. Here, we investigated the effect of the general volatile anaesthetic diethyl ether on the ability to sense potential prey or herbivore attacks in the carnivorous plant Venus flytrap (Dionaea muscipula). METHODS: We monitored trap movement, electrical signalling, phytohormone accumulation and gene expression in response to the mechanical stimulation of trigger hairs and wounding under diethyl ether treatment. KEY RESULTS: Diethyl ether completely inhibited the generation of action potentials and trap closing reactions, which were easily and rapidly restored when the anaesthetic was removed. Diethyl ether also inhibited the later response: jasmonic acid (JA) accumulation and expression of JA-responsive genes (cysteine protease dionain and type I chitinase). However, external application of JA bypassed the inhibited action potentials and restored gene expression under diethyl ether anaesthesia, indicating that downstream reactions from JA are not inhibited. CONCLUSIONS: The Venus flytrap cannot sense prey or a herbivore attack under diethyl ether treatment caused by inhibited action potentials, and the JA signalling pathway as a consequence.
- Keywords
- Dionaea muscipula, Anaesthesia, Venus flytrap, action potential, anaesthetic, carnivorous plant, diethyl ether, electrical signal, jasmonic acid, plant movement,
- MeSH
- Anesthesia * MeSH
- Cyclopentanes MeSH
- Droseraceae * MeSH
- Ether MeSH
- Oxylipins MeSH
- Animals MeSH
- Check Tag
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Names of Substances
- Cyclopentanes MeSH
- Ether MeSH
- jasmonic acid MeSH Browser
- Oxylipins MeSH
Nepenthes regulates enzyme activities by sensing stimuli from the insect prey. Protein is the best inductor mimicking the presence of an insect prey. Carnivorous plants of the genus Nepenthes have evolved passive pitcher traps for prey capture. In this study, we investigated the ability of chemical signals from a prey (chitin, protein, and ammonium) to induce transcription and synthesis of digestive enzymes in Nepenthes × Mixta. We used real-time PCR and specific antibodies generated against the aspartic proteases nepenthesins, and type III and type IV chitinases to investigate the induction of digestive enzyme synthesis in response to different chemical stimuli from the prey. Transcription of nepenthesins was strongly induced by ammonium, protein and live prey; chitin induced transcription only very slightly. This is in accordance with the amount of released enzyme and proteolytic activity in the digestive fluid. Although transcription of type III chitinase was induced by all investigated stimuli, a significant accumulation of the enzyme in the digestive fluid was found mainly after protein and live prey addition. Protein and live prey were also the best inducers for accumulation of type IV chitinase in the digestive fluid. Although ammonium strongly induced transcription of all investigated genes probably through membrane depolarization, strong acidification of the digestive fluid affected stability and abundance of both chitinases in the digestive fluid. The study showed that the proteins are universal inductors of enzyme activities in carnivorous pitcher plants best mimicking the presence of insect prey. This is not surprising, because proteins are a much valuable source of nitrogen, superior to chitin. Extensive vesicular activity was observed in prey-activated glands.
- Keywords
- Carnivorous plant, Chitin, Chitinase, Enzyme, Nepenthesin, Pitcher plant, Protease,
- MeSH
- Caryophyllales enzymology physiology ultrastructure MeSH
- Chitin metabolism MeSH
- Ammonium Chloride pharmacology MeSH
- Enzymes genetics metabolism MeSH
- Hydrogen-Ion Concentration MeSH
- Carnivory MeSH
- Membrane Potentials MeSH
- Gene Expression Regulation, Plant * MeSH
- Plant Proteins genetics metabolism MeSH
- Serum Albumin, Bovine metabolism MeSH
- Publication type
- Journal Article MeSH
- Names of Substances
- Chitin MeSH
- Ammonium Chloride MeSH
- Enzymes MeSH
- Plant Proteins MeSH
- Serum Albumin, Bovine MeSH
The paper describes the electrical plant response to mechanical stimulation monitored with the help of conducting polymers deposited on cotton fabric. Cotton fabric was coated with conducting polymers, polyaniline or polypyrrole, in situ during the oxidation of respective monomers in aqueous medium. Thus, modified fabrics were again coated with polypyrrole or polyaniline, respectively, in order to investigate any synergetic effect between both polymers with respect to conductivity and its stability during repeated dry cleaning. The coating was confirmed by infrared spectroscopy. The resulting fabrics have been used as electrodes to collect the electrical response to the stimulation of a Venus flytrap plant. This is a paradigm of the use of conducting polymers in monitoring of plant neurobiology.
- Keywords
- Venus flytrap, conducting polymers, plant neurobiology, polyaniline, polypyrrole,
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
BACKGROUND: The cost-benefit model for the evolution of botanical carnivory provides a conceptual framework for interpreting a wide range of comparative and experimental studies on carnivorous plants. This model assumes that the modified leaves called traps represent a significant cost for the plant, and this cost is outweighed by the benefits from increased nutrient uptake from prey, in terms of enhancing the rate of photosynthesis per unit leaf mass or area (AN) in the microsites inhabited by carnivorous plants. SCOPE: This review summarizes results from the classical interpretation of the cost-benefit model for evolution of botanical carnivory and highlights the costs and benefits of active trapping mechanisms, including water pumping, electrical signalling and accumulation of jasmonates. Novel alternative sequestration strategies (utilization of leaf litter and faeces) in carnivorous plants are also discussed in the context of the cost-benefit model. CONCLUSIONS: Traps of carnivorous plants have lower AN than leaves, and the leaves have higher AN after feeding. Prey digestion, water pumping and electrical signalling represent a significant carbon cost (as an increased rate of respiration, RD) for carnivorous plants. On the other hand, jasmonate accumulation during the digestive period and reprogramming of gene expression from growth and photosynthesis to prey digestion optimizes enzyme production in comparison with constitutive secretion. This inducibility may have evolved as a cost-saving strategy beneficial for carnivorous plants. The similarities between plant defence mechanisms and botanical carnivory are highlighted.
- Keywords
- Action potential, Dionaea, Drosera, Nepenthes, Venus flytrap, botanical carnivory, carnivorous plant, cost–benefit, electrical signalling, jasmonates,
- MeSH
- Biological Evolution * MeSH
- Models, Biological * MeSH
- Droseraceae physiology MeSH
- Plant Physiological Phenomena * MeSH
- Signal Transduction MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Review MeSH