Terrestrial carnivorous plants of genera Drosera, Dionaea and Nepenthes within the order Caryophyllales employ jasmonates for the induction of digestive processes in their traps. Here, we focused on two aquatic carnivorous plant genera with different trapping mechanism from distinct families and orders: Aldrovanda (Droseraceae, Caryophyllales) with snap-traps and Utricularia (Lentibulariaceae, Lamiales) with suction traps. Using phytohormone analyses and simple biotest, we asked whether the jasmonates are involved in the activation of carnivorous response similar to that known in traps of terrestrial genera of Droseraceae (Drosera, Dionaea). The results showed that Utricularia, in contrast with Aldrovanda, does not use jasmonates for activation of carnivorous response and is the second genus in Lamiales, which has not co-opted jasmonate signalling for botanical carnivory. On the other hand, the nLC-MS/MS analyses revealed that both genera secreted digestive fluid containing cysteine protease homologous to dionain although the mode of its regulation may differ. Whereas in Utricularia the cysteine protease is present constitutively in digestive fluid, it is induced by prey and exogenous application of jasmonic acid in Aldrovanda.
BACKGROUND AND AIMS: Carnivorous plants can enhance photosynthetic efficiency in response to prey nutrient uptake, but the underlying mechanisms of increased photosynthesis are largely unknown. Here we investigated photosynthesis in the pitcher plant Nepenthes × ventrata in response to different prey-derived and root mineral nutrition to reveal photosynthetic constrains. METHODS: Nutrient-stressed plants were irrigated with full inorganic solution or fed with four different insects: wasps, ants, beetles or flies. Full dissection of photosynthetic traits was achieved by means of gas exchange, chlorophyll fluorescence and immunodetection of photosynthesis-related proteins. Leaf biochemical and anatomical parameters together with mineral composition, nitrogen and carbon isotopic discrimination of leaves and insects were also analysed. KEY RESULTS: Mesophyll diffusion was the major photosynthetic limitation for nutrient-stressed Nepenthes × ventrata, while biochemistry was the major photosynthetic limitation after nutrient application. The better nutrient status of insect-fed and root-fertilized treatments increased chlorophyll, pigment-protein complexes and Rubisco content. As a result, both photochemical and carboxylation potential were enhanced, increasing carbon assimilation. Different nutrient application affected growth, and root-fertilized treatment led to the investment of more biomass in leaves instead of pitchers. CONCLUSIONS: The study resolved a 35-year-old hypothesis that carnivorous plants increase photosynthetic assimilation via the investment of prey-derived nitrogen in the photosynthetic apparatus. The equilibrium between biochemical and mesophyll limitations of photosynthesis is strongly affected by the nutrient treatment.
- MeSH
- chlorofyl MeSH
- fotosyntéza * MeSH
- listy rostlin MeSH
- masožravci * MeSH
- organické látky MeSH
- oxid uhličitý MeSH
- živiny MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem 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.
- 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
The lipid-derived jasmonate phytohormones (JAs) regulate a wide spectrum of physiological processes in plants such as growth, development, tolerance to abiotic stresses, and defence against pathogen infection and insect attack. Recently, a new role for JAs has been revealed in carnivorous plants. In these specialized plants, JAs can induce the formation of digestive cavities and regulate enzyme production in response to different stimuli from caught prey. Appearing to be a new function for JAs in plants, a closer look reveals that the signalling pathways involved resemble known signalling pathways from plant defence mechanisms. Moreover, the digestion-related secretome of carnivorous plants is composed of many pathogenesis-related (PR) proteins and low molecular weight compounds, indicating that the plant carnivory syndrome is related to and has evolved from plant defence mechanisms. This review describes the similarities between defence and carnivory. It further describes how, after recognition of caught insects, JAs enable the carnivorous plants to digest and benefit from the prey. In addition, a causal connection between electrical and jasmonate signalling is discussed.
- MeSH
- cyklopentany imunologie metabolismus MeSH
- Drosera metabolismus MeSH
- imunita rostlin MeSH
- oxylipiny imunologie metabolismus MeSH
- regulátory růstu rostlin metabolismus MeSH
- Sarraceniaceae metabolismus MeSH
- sekundární metabolismus MeSH
- signální transdukce MeSH
- Viridiplantae metabolismus MeSH
- Publikační typ
- časopisecké články MeSH
- přehledy MeSH
MAIN CONCLUSION: 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.
- 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
The carnivorous sundew plant (Drosera capensis) captures prey using sticky tentacles. We investigated the tentacle and trap reactions in response to the electrical and jasmonate signalling evoked by different stimuli to reveal how carnivorous sundews recognize digestible captured prey in their traps. We measured the electrical signals, phytohormone concentration, enzyme activities and Chla fluorescence in response to mechanical stimulation, wounding or insect feeding in local and systemic traps. Seven new proteins in the digestive fluid were identified using mass spectrometry. Mechanical stimuli and live prey induced a fast, localized tentacle-bending reaction and enzyme secretion at the place of application. By contrast, repeated wounding induced a nonlocalized convulsive tentacle movement and enzyme secretion in local but also in distant systemic traps. These differences can be explained in terms of the electrical signal propagation and jasmonate accumulation, which also had a significant impact on the photosynthesis in the traps. The electrical signals generated in response to wounding could partially mimic a mechanical stimulation of struggling prey and might trigger a false alarm, confirming that the botanical carnivory and plant defence mechanisms are related. To trigger the full enzyme activity, the traps must detect chemical stimuli from the captured prey.
- MeSH
- biologické modely MeSH
- cyklopentany metabolismus MeSH
- Drosera enzymologie fyziologie MeSH
- elektrofyziologické jevy * MeSH
- fotochemické procesy MeSH
- fotosystém II - proteinový komplex metabolismus MeSH
- oxylipiny metabolismus MeSH
- regulátory růstu rostlin metabolismus MeSH
- rostlinné proteiny metabolismus MeSH
- signální transdukce * MeSH
- Publikační typ
- časopisecké články MeSH
In the carnivorous plant Venus flytrap (Dionaea muscipula), the sequence of events after prey capture resembles the well-known plant defence signalling pathway in response to pathogen or herbivore attack. Here, we used wounding to mimic prey capture to show the similarities and differences between botanical carnivory and plant defence mechanisms. We monitored movement, electrical signalling, jasmonate accumulation and digestive enzyme secretion in local and distal (systemic) traps in response to prey capture, the mechanical stimulation of trigger hairs and wounding. The Venus flytrap cannot discriminate between wounding and mechanical trigger hair stimulation. Both induced the same action potentials, rapid trap closure, hermetic trap sealing, the accumulation of jasmonic acid (JA) and its isoleucine conjugate (JA-Ile), and the secretion of proteases (aspartic and cysteine proteases), phosphatases and type I chitinase. The jasmonate accumulation and enzyme secretion were confined to the local traps, to which the stimulus was applied, which correlates with the propagation of electrical signals and the absence of a systemic response in the Venus flytrap. In contrast to plant defence mechanisms, the absence of a systemic response in carnivorous plant may represent a resource-saving strategy. During prey capture, it could be quite expensive to produce digestive enzymes in the traps on the plant without prey.
Photo-reduction of O2to water mediated by flavodiiron proteins (FDPs) represents a safety valve for the photosynthetic electron transport chain in fluctuating light. So far, the FDP-mediated O2photo-reduction has been evidenced only in cyanobacteria and the moss Physcomitrella; however, a recent phylogenetic analysis of transcriptomes of photosynthetic organisms has also revealed the presence of FDP genes in several nonflowering plant groups. What remains to be clarified is whether the FDP-dependent O2photo-reduction is actually operational in these organisms. We have established a simple method for the monitoring of FDP-mediated O2photo-reduction, based on the measurement of redox kinetics of P700 (the electron donor of photosystem I) upon dark-to-light transition. The O2photo-reduction is manifested as a fast re-oxidation of P700. The validity of the method was verified by experiments with transgenic organisms, namely FDP knock-out mutants of Synechocystis and Physcomitrella and transgenic Arabidopsis plants expressing FDPs from Physcomitrella. We observed the fast P700 re-oxidation in representatives of all green plant groups excluding angiosperms. Our results provide strong evidence that the FDP-mediated O2photo-reduction is functional in all nonflowering green plant groups. This finding suggests a major change in the strategy of photosynthetic regulation during the evolution of angiosperms.
Unlike angiosperms, gymnosperms use two different enzymes for the reduction of protochlorophyllide to chlorophyllide: the light-dependent protochlorophyllide oxidoreductase (LPOR) and the dark-operative protochlorophyllide oxidoreductase (DPOR). In this study, we examined the specific role of both enzymes for chlorophyll synthesis in response to different light/dark and temperature conditions at different developmental stages (cotyledons and needles) of Norway spruce (Picea abies Karst.). The accumulation of chlorophyll and chlorophyll-binding proteins strongly decreased during dark growth in secondary needles at room temperature as well as in cotyledons at low temperature (7 °C) indicating suppression of DPOR activity. The levels of the three DPOR subunits ChlL, ChlN, and ChlB and the transcripts of their encoding genes were diminished in dark-grown secondary needles. The low temperature had minor effects on the transcription and translation of these genes in cotyledons, which is suggestive for post-translational control in chlorophyll biosynthesis. Taking into account the higher solubility of oxygen at low temperature and oxygen sensitivity of DPOR, we mimicked low-temperature condition by the exposure of seedlings to higher oxygen content (33%). The treatment resulted in an etiolated phenotype of dark-grown seedlings, confirming an oxygen-dependent control of DPOR activity in spruce cotyledons. Moreover, light-dependent suppression of mRNA and protein level of DPOR subunits indicates that more efficiently operating LPOR takes over the DPOR function under light conditions, especially in secondary needles.
- MeSH
- chlorofyl genetika metabolismus MeSH
- oxidoreduktasy působící na CH-CH vazby biosyntéza metabolismus MeSH
- regulace genové exprese u rostlin MeSH
- smrk enzymologie genetika metabolismus MeSH
- světlo MeSH
- teplota MeSH
- Publikační typ
- časopisecké články MeSH
- Geografické názvy
- Norsko MeSH
Gymnosperms, unlike angiosperms, are able to synthesize chlorophyll and form photosystems in complete darkness. Photosystem I (PSI) formed under such conditions is fully active, but photosystem II (PSII) is present in its latent form with inactive oxygen evolving complex (OEC). In this work we have studied light-induced gradual changes in PSII function in dark-grown cotyledons of Norway spruce (Picea abies) via the measurement of chlorophyll a fluorescence rise, absorption changes at 830 nm, thermoluminescence glow curves (TL) and protein analysis. The results indicate that in dark-grown cotyledons, alternative reductants were able to act as electron donors to PSII with inactive OEC. Illumination of cotyledons for 5 min led to partial activation of PSII, which was accompanied by detectable oxygen evolution, but still a substantial number of PSII centers remained in the so called PSII-Q(B)-non-reducing form. Interestingly, even 24 h long illumination was not sufficient for the full activation of PSII centers. This was evidenced by a weak attachment of PsbP protein and the absence of PsbQ protein in PSII particles, the absence of PSII supercomplexes, the suboptimal maximum yield of PSII photochemistry, the presence of C band in TL curve and also the presence of up-shifted Q band in TL in DCMU-treated cotyledons. This slow light-induced activation of PSII in dark-grown cotyledons could contribute to the prevention of PSII overexcitation before the light-induced increase in PSI/PSII ratio allows effective operation of linear electron flow.
- MeSH
- chlorofyl chemie metabolismus MeSH
- fotosyntéza účinky záření MeSH
- fotosystém I - proteinový komplex metabolismus MeSH
- fotosystém II - proteinový komplex metabolismus MeSH
- kotyledon růst a vývoj metabolismus účinky záření MeSH
- kyslík metabolismus MeSH
- luminiscenční měření metody MeSH
- rostlinné proteiny metabolismus MeSH
- semenáček růst a vývoj metabolismus účinky záření MeSH
- smrk růst a vývoj metabolismus účinky záření MeSH
- světlo * MeSH
- teplota MeSH
- tma * MeSH
- transport elektronů účinky záření MeSH
- tylakoidy metabolismus účinky záření MeSH
- western blotting MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
