Nejvíce citovaný článek - PubMed ID 31734521
Taste for protein: Chemical signal from prey stimulates enzyme secretion through jasmonate signalling in the carnivorous plant Venus flytrap
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.
- Klíčová slova
- Byblis, Carnivorous plant, Drosera, digestive enzyme, jasmonic acid, phytohormones, sundew,
- MeSH
- aminokyseliny metabolismus farmakologie MeSH
- Caryophyllales * enzymologie fyziologie metabolismus MeSH
- cyklopentany * metabolismus MeSH
- Drosera fyziologie MeSH
- indeny metabolismus farmakologie MeSH
- masožravé rostliny * enzymologie fyziologie metabolismus MeSH
- oxylipiny * metabolismus MeSH
- regulátory růstu rostlin * metabolismus MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- Názvy látek
- aminokyseliny MeSH
- coronatine MeSH Prohlížeč
- cyklopentany * MeSH
- indeny MeSH
- jasmonic acid MeSH Prohlížeč
- oxylipiny * MeSH
- regulátory růstu rostlin * 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.
- 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
The field of plant hormonomics focuses on the qualitative and quantitative analysis of the hormone complement in plant samples, akin to other omics sciences. Plant hormones, alongside primary and secondary metabolites, govern vital processes throughout a plant's lifecycle. While active hormones have received significant attention, studying all related compounds provides valuable insights into internal processes. Conventional single-class plant hormone analysis employs thorough sample purification, short analysis and triple quadrupole tandem mass spectrometry. Conversely, comprehensive hormonomics analysis necessitates minimal purification, robust and efficient separation and better-performing mass spectrometry instruments. This review summarizes the current status of plant hormone analysis methods, focusing on sample preparation, advances in chromatographic separation and mass spectrometric detection, including a discussion on internal standard selection and the potential of derivatization. Moreover, current approaches for assessing the spatiotemporal distribution are evaluated. The review touches on the legitimacy of the term plant hormonomics by exploring the current status of methods and outlining possible future trends.
- Klíčová slova
- Hormonomics, Internal standard, Liquid chromatography, Mass spectrometry, Matrix effect, Metabolomics, Omics, Plant hormone, Solid phase extraction,
- Publikační typ
- časopisecké články MeSH
- přehledy MeSH
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