Nejvíce citovaný článek - PubMed ID 28850713
Triggering a false alarm: wounding mimics prey capture in the carnivorous Venus flytrap (Dionaea muscipula)
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.
- Klíčová slova
- Aspartic protease, carnivorous plant, digestive enzymes, electrical signal, jasmonic acid, phytohormone, plant defence, wounding,
- MeSH
- masožravci * MeSH
- masožravé rostliny * MeSH
- proteomika MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- coronatine MeSH Prohlížeč
- jasmonic acid MeSH Prohlížeč
In his famous book Insectivorous plants, Charles Darwin observed that the bending response of tentacles in the carnivorous sundew plant Drosera rotundifolia was not triggered by a drop of water, but rather the application of many dissolved chemicals or mechanical stimulation. In this study, we tried to reveal this 150-years-old mystery using methods not available in his time. We measured electrical signals, phytohormone tissue level, enzyme activities and an abundance of digestive enzyme aspartic protease droserasin in response to different stimuli (water drop, ammonia, mechanostimulation, chitin, insect prey) in Cape sundew (Drosera capensis). Drops of water induced the lowest number of action potentials (APs) in the tentacle head, and accumulation of jasmonates in the trap was not significantly different from control plants. On the other hand, all other stimuli significantly increased jasmonate accumulation; the highest was found after the application of insect prey. Drops of water also did not induce proteolytic activity and an abundance of aspartic protease droserasin in contrast to other stimuli. We found that the tentacles of sundew plants are not responsive to water drops due to an inactive jasmonic acid signalling pathway, important for the induction of significant digestive enzyme activities.
- Klíčová slova
- abscisic acid, aspartic protease, carnivorous plant, digestive enzyme, jasmonic acid, sundew,
- Publikační typ
- časopisecké články 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.
- Klíčová slova
- 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
- fotosyntéza MeSH
- listy rostlin MeSH
- masožravci * MeSH
- rostliny * genetika MeSH
- živiny MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem 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.
- Klíčová slova
- Pinguicula, Butterwort, carnivorous plant, digestive enzymes, electrical signals, jasmonic acid, protease, variation potential,
- MeSH
- cyklopentany MeSH
- hluchavkotvaré * MeSH
- masožravci * MeSH
- oxylipiny MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- cyklopentany MeSH
- jasmonic acid MeSH Prohlížeč
- oxylipiny 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.
- Klíčová slova
- Dionaea muscipula, Anaesthesia, Venus flytrap, action potential, anaesthetic, carnivorous plant, diethyl ether, electrical signal, jasmonic acid, plant movement,
- MeSH
- anestezie * MeSH
- cyklopentany MeSH
- Droseraceae * MeSH
- ether MeSH
- oxylipiny MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- cyklopentany MeSH
- ether MeSH
- jasmonic acid MeSH Prohlížeč
- oxylipiny MeSH
BACKGROUND AND AIMS: Anaesthesia for medical purposes was introduced in the 19th century. However, the physiological mode of anaesthetic drug actions on the nervous system remains unclear. One of the remaining questions is how these different compounds, with no structural similarities and even chemically inert elements such as the noble gas xenon, act as anaesthetic agents inducing loss of consciousness. The main goal here was to determine if anaesthetics affect the same or similar processes in plants as in animals and humans. METHODS: A single-lens reflex camera was used to follow organ movements in plants before, during and after recovery from exposure to diverse anaesthetics. Confocal microscopy was used to analyse endocytic vesicle trafficking. Electrical signals were recorded using a surface AgCl electrode. KEY RESULTS: Mimosa leaves, pea tendrils, Venus flytraps and sundew traps all lost both their autonomous and touch-induced movements after exposure to anaesthetics. In Venus flytrap, this was shown to be due to the loss of action potentials under diethyl ether anaesthesia. The same concentration of diethyl ether immobilized pea tendrils. Anaesthetics also impeded seed germination and chlorophyll accumulation in cress seedlings. Endocytic vesicle recycling and reactive oxygen species (ROS) balance, as observed in intact Arabidopsis root apex cells, were also affected by all anaesthetics tested. CONCLUSIONS: Plants are sensitive to several anaesthetics that have no structural similarities. As in animals and humans, anaesthetics used at appropriate concentrations block action potentials and immobilize organs via effects on action potentials, endocytic vesicle recycling and ROS homeostasis. Plants emerge as ideal model objects to study general questions related to anaesthesia, as well as to serve as a suitable test system for human anaesthesia.
- MeSH
- akční potenciály účinky léků fyziologie MeSH
- anestetika škodlivé účinky MeSH
- Arabidopsis účinky léků fyziologie MeSH
- chlorofyl metabolismus MeSH
- Drosera účinky léků fyziologie MeSH
- Droseraceae účinky léků fyziologie MeSH
- ether škodlivé účinky MeSH
- homeostáza * MeSH
- hrách setý účinky léků fyziologie MeSH
- klíčení účinky léků MeSH
- Lepidium sativum účinky léků fyziologie MeSH
- listy rostlin účinky léků fyziologie MeSH
- Magnoliopsida účinky léků fyziologie MeSH
- Mimosa účinky léků fyziologie MeSH
- organely účinky léků fyziologie MeSH
- reaktivní formy kyslíku metabolismus MeSH
- transportní vezikuly účinky léků fyziologie MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- anestetika MeSH
- chlorofyl MeSH
- ether MeSH
- reaktivní formy kyslíku 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.
- Klíčová slova
- Carnivorous plant, Chitin, Chitinase, Enzyme, Nepenthesin, Pitcher plant, Protease,
- MeSH
- Caryophyllales enzymologie fyziologie ultrastruktura MeSH
- chitin metabolismus MeSH
- chlorid amonný farmakologie MeSH
- enzymy genetika metabolismus MeSH
- koncentrace vodíkových iontů MeSH
- masožravci MeSH
- membránové potenciály MeSH
- regulace genové exprese u rostlin * MeSH
- rostlinné proteiny genetika metabolismus MeSH
- sérový albumin hovězí metabolismus MeSH
- Publikační typ
- časopisecké články MeSH
- Názvy látek
- chitin MeSH
- chlorid amonný MeSH
- enzymy MeSH
- rostlinné proteiny MeSH
- sérový albumin hovězí MeSH