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

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

BACKGROUND: The cost-benefit model for the evolution of botanical carnivory provides a conceptual framework for interpreting a wide range of comparative and experimental studies on carnivorous plants. This model assumes that the modified leaves called traps represent a significant cost for the plant, and this cost is outweighed by the benefits from increased nutrient uptake from prey, in terms of enhancing the rate of photosynthesis per unit leaf mass or area (AN) in the microsites inhabited by carnivorous plants. SCOPE: This review summarizes results from the classical interpretation of the cost-benefit model for evolution of botanical carnivory and highlights the costs and benefits of active trapping mechanisms, including water pumping, electrical signalling and accumulation of jasmonates. Novel alternative sequestration strategies (utilization of leaf litter and faeces) in carnivorous plants are also discussed in the context of the cost-benefit model. CONCLUSIONS: Traps of carnivorous plants have lower AN than leaves, and the leaves have higher AN after feeding. Prey digestion, water pumping and electrical signalling represent a significant carbon cost (as an increased rate of respiration, RD) for carnivorous plants. On the other hand, jasmonate accumulation during the digestive period and reprogramming of gene expression from growth and photosynthesis to prey digestion optimizes enzyme production in comparison with constitutive secretion. This inducibility may have evolved as a cost-saving strategy beneficial for carnivorous plants. The similarities between plant defence mechanisms and botanical carnivory are highlighted.

• Klíčová slova
• Action potential, Dionaea, Drosera, Nepenthes, Venus flytrap, botanical carnivory, carnivorous plant, cost–benefit, electrical signalling, jasmonates,
• MeSH
• biologická evoluce * MeSH
• biologické modely * MeSH
• Droseraceae fyziologie   MeSH
• fyziologie rostlin * MeSH
• signální transdukce MeSH
• Publikační typ
• časopisecké články MeSH
• práce podpořená grantem MeSH
• přehledy MeSH