Nejvíce citovaný článek - PubMed ID 34166972
Contrasting effect of prey capture on jasmonate accumulation in two genera of aquatic carnivorous plants (Aldrovanda, Utricularia)
Carnivorous plants secrete digestive enzymes for prey degradation. Although carnivorous plants have a polyphyletic origin and evolved several times independently, they surprisingly co-opted similar digestive enzymes during convergent evolution. However, despite having similar digestive enzymes, the mode of their regulation strongly differs across different phylogenetic lineages. But what factors are responsible for such diversity in their digestion? By combining phylogenetic relationships of digestive fluid proteins and biochemical data, the analyses showed that phylogeny seems to be a significant factor determining the regulation of digestion, but environment (water vs terrestrial) and type of trap do not affect regulation. The oldest carnivorous plant lineage, Caryophyllales, co-opted phytohormone jasmonic acid (JA) for regulation of digestive enzyme activity. However, the remaining orders of carnivorous plants do not accumulate JA in response to prey capture, and their digestive enzyme activity is not responsive to exogenous JA application. Instead, they use different modes of regulation, for example, development/senescence, osmotically induced and constitutive. These different modes of regulation can be explained by co-option, albeit of similar genes but different paralogs with different cis regulatory elements that have been fine-tuned during evolution.
- Klíčová slova
- Venus flytrap, carnivorous plants, digestive enzymes, jasmonic acid, pitcher plant,
- MeSH
- biologická evoluce * MeSH
- cyklopentany metabolismus MeSH
- fylogeneze MeSH
- masožravé rostliny * fyziologie enzymologie genetika MeSH
- oxylipiny metabolismus MeSH
- trávení * MeSH
- Publikační typ
- časopisecké články MeSH
- přehledy MeSH
- Názvy látek
- cyklopentany MeSH
- jasmonic acid MeSH Prohlížeč
- oxylipiny MeSH
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
Carnivorous plants of the genus Utricularia (bladderwort) form modified leaves into suction bladder traps. The bladders are metabolically active plant tissue with high rates of mitochondrial respiration (RD). In general, plants possess two mitochondrial electron transport pathways to reduce oxygen to water: cytochrome and an alternative. Due to the high metabolic rate in the bladders, it is tempting to assume that the bladders prefer the cytochrome c oxidative pathway. Surprisingly, we revealed that alternative oxidase (AOX), which yields only a little ATP, is much more abundant in the bladders of Utricularia reflexa in comparison with the shoots. This pattern is similar to the carnivorous plants with passive pitcher traps (e.g. Sarracenia, Nepenthes) and seems to be widespread across many carnivorous taxa. The exact role of AOX in the traps of carnivorous plants remains to be investigated.
- Klíčová slova
- Alternative oxidase, bladderwort, carnivorous plants, cytochrome c oxidase, light harvesting antennae, respiration,
- MeSH
- adenosintrifosfát MeSH
- cytochromy c * MeSH
- kyslík MeSH
- listy rostlin * MeSH
- voda MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- adenosintrifosfát MeSH
- cytochromy c * MeSH
- kyslík MeSH
- voda MeSH
BACKGROUND AND AIMS: Aquatic carnivorous plants have typical rootless linear shoots bearing traps and exhibit steep physiological polarity with rapid apical growth. The aim was to analyse auxin and cytokinin metabolites in traps, leaves/shoots and shoot apices in several species of genera Aldrovanda and Utricularia to elucidate how the hormonal profiles reflect the specific organ functions and polarity. METHODS: The main auxin and cytokinin metabolites were analysed in miniature samples (>2 mg dry weight) of different organs of Aldrovanda vesiculosa and six Utricularia species using ultraperformance liquid chromatography coupled with triple quadrupole mass spectrometry. KEY RESULTS: Total contents of biologically active forms (free bases, ribosides) of all four main endogenously occurring cytokinin types were consistently higher in traps than in leaves in four Utricularia species with monomorphic shoots and/or higher than in shoots in two Utricularia species with dimorphic shoots. In Aldrovanda traps, the total content of different cytokinin forms was similar to or lower than that in shoots. In U. australis leaves, feeding on prey increased all cytokinin forms, while no consistent differences occurred in Aldrovanda. In four aquatic Utricularia species with monomorphic shoots, the content of four auxin forms was usually higher in traps than in leaves. Zero IAA content was determined in U. australis leaves from a meso-eutrophic site or when prey-fed. CONCLUSIONS: Different cytokinin and auxin profiles estimated in traps and leaves/shoots of aquatic carnivorous plants indicate an association with different dominant functions of these organs: nutrient uptake by traps versus photosynthetic function of traps. Interplay of cytokinins and auxins regulates apical dominance in these plants possessing strong polarity.
- Klíčová slova
- Aldrovanda vesiculosa, Utricularia spp, Droseraceae, Lentibulariaceae, Phytohormone profiles, apices, aquatic rootless plants, leaves, physiological polarity, traps,
- MeSH
- cytokininy metabolismus MeSH
- Droseraceae * fyziologie MeSH
- hluchavkotvaré * MeSH
- kyseliny indoloctové metabolismus MeSH
- Magnoliopsida * fyziologie MeSH
- masožravé rostliny MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- cytokininy MeSH
- kyseliny indoloctové 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