Most cited article - PubMed ID 31677265
Anaesthesia with diethyl ether impairs jasmonate signalling in the carnivorous plant Venus flytrap (Dionaea muscipula)
Anaesthetics affect not only humans and animals but also plants. Plants exposed to certain anaesthetics lose their ability to respond adequately to various stimuli such as touch, injury or light. Available results indicate that anaesthetics modulate ion channel activities in plants, e.g. Ca2+ influx. The word anaesthesia means loss of sensation. Plants, as all living creatures, can also sense their environment and they are susceptible to anaesthesia. Although some anaesthetics are often known as drugs with well-defined target to their animal/human receptors, some other are promiscuous in their binding. Both have effects on plants. Application of general volatile anaesthetics (GVAs) inhibits plant responses to different stimuli but also induces strong cellular response. Of particular interest is the ability of GVAs inhibit long-distance electrical and Ca2+ signalling probably through inhibition of GLUTAMATE RECEPTOR-LIKE proteins (GLRs), the effect which is surprisingly very similar to inhibition of nerve impulse transmission in animals or human. However, GVAs act also as a stressor for plants and can induce their own Ca2+ signature, which strongly reprograms gene expression . Down-regulation of genes encoding enzymes of chlorophyll biosynthesis and pigment-protein complexes are responsible for inhibited de-etiolation and photomorphogenesis. Vesicle trafficking, germination, and circumnutation movement of climbing plants are also strongly inhibited. On the other hand, other cellular processes can be upregulated, for example, heat shock response and generation of reactive oxygen species (ROS). Upregulation of stress response by GVAs results in preconditioning/priming and can be helpful to withstand abiotic stresses in plants. Thus, anaesthetic drugs may become a useful tool for scientists studying plant responses to environmental stimuli.
- Keywords
- Anaesthesia, Carnivorous plant, De-etiolation, Electrical signals, Jasmonates, Wounding,
- MeSH
- Anesthetics pharmacology MeSH
- Plant Physiological Phenomena MeSH
- Touch drug effects physiology MeSH
- Gene Expression Regulation, Plant drug effects MeSH
- Plants drug effects metabolism MeSH
- Light * MeSH
- Publication type
- Journal Article MeSH
- Review MeSH
- Names of Substances
- Anesthetics MeSH
The systemic electrical signal propagation in plants (i.e., from leaf to leaf) is dependent on GLUTAMATE RECEPTOR-LIKE proteins (GLRs). The GLR receptors are the homologous proteins to the animal ionotropic glutamate receptors (iGluRs) which are ligand-gated non-selective cation channels that mediate neurotransmission in the animal's nervous system. In this study, we investigated the effect of the general anaesthetic ketamine, a well-known non-competitive channel blocker of human iGluRs, on systemic electrical signal propagation in Arabidopsis thaliana. We monitored the electrical signal propagation, intracellular calcium level [Ca2+]cyt and expression of jasmonate (JA)-responsive genes in response to heat wounding. Although ketamine affected the shape and the parameters of the electrical signals (amplitude and half-time, t1/2) mainly in systemic leaves, it was not able to block a systemic response. Increased [Ca2+]cyt and the expression of jasmonate-responsive genes were detected in local as well as in systemic leaves in response to heat wounding in ketamine-treated plants. This is in contrast with the effect of the volatile general anaesthetic diethyl ether which completely blocked the systemic response. This low potency of ketamine in plants is probably caused by the fact that the critical amino acid residues needed for ketamine binding in human iGluRs are not conserved in plants' GLRs.
- Keywords
- Arabidopsis, anaesthetic, calcium, diethyl ether, jasmonates, ketamine, systemic response,
- Publication type
- Journal Article MeSH
General volatile anesthetic diethyl ether blocks sensation and responsive behavior not only in animals but also in plants. Here, using a combination of RNA-seq and proteomic LC-MS/MS analyses, we investigated the effect of anesthetic diethyl ether on gene expression and downstream consequences in plant Arabidopsis thaliana. Differential expression analyses revealed reprogramming of gene expression under anesthesia: 6,168 genes were upregulated, 6,310 genes were downregulated, while 9,914 genes were not affected in comparison with control plants. On the protein level, out of 5,150 proteins identified, 393 were significantly upregulated and 227 were significantly downregulated. Among the highest significantly downregulated processes in etherized plants were chlorophyll/tetrapyrrole biosynthesis and photosynthesis. However, measurements of chlorophyll a fluorescence did not show inhibition of electron transport through photosystem II. The most significantly upregulated process was the response to heat stress (mainly heat shock proteins, HSPs). Using transgenic A. thaliana expressing APOAEQUORIN, we showed transient increase of cytoplasmic calcium level [Ca2+]cyt in response to diethyl ether application. In addition, cell membrane permeability for ions also increased under anesthesia. The plants pre-treated with diethyl ether, and thus with induced HSPs, had increased tolerance of photosystem II to subsequent heat stress through the process known as cross-tolerance or priming. All these data indicate that diethyl ether anesthesia may partially mimic heat stress in plants through the effect on plasma membrane.
- Keywords
- Arabidopsis, anesthesia, chlorophyll, diethyl ether, heat shock proteins, heat stress, photosystem II,
- Publication type
- Journal Article MeSH
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