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.

• Keywords
• Venus flytrap, carnivorous plants, digestive enzymes, jasmonic acid, pitcher plant,
• MeSH
• Biological Evolution * MeSH
• Cyclopentanes metabolism   MeSH
• Phylogeny MeSH
• Carnivorous Plant * physiology   enzymology   genetics   MeSH
• Oxylipins metabolism   MeSH
• Digestion * MeSH
• Publication type
• Journal Article MeSH
• Review MeSH
• Names of Substances
• Cyclopentanes MeSH
• jasmonic acid MeSH Browser
• Oxylipins 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.

• Keywords
• Byblis, Carnivorous plant, Drosera, digestive enzyme, jasmonic acid, phytohormones, sundew,
• MeSH
• Amino Acids metabolism   pharmacology   MeSH
• Caryophyllales * enzymology   physiology   metabolism   MeSH
• Cyclopentanes * metabolism   MeSH
• Drosera physiology   MeSH
• Indenes metabolism   pharmacology   MeSH
• Carnivorous Plant * enzymology   physiology   metabolism   MeSH
• Oxylipins * metabolism   MeSH
• Plant Growth Regulators * metabolism   MeSH
• Animals MeSH
• Check Tag
• Animals MeSH
• Publication type
• Journal Article MeSH
• Names of Substances
• Amino Acids MeSH
• coronatine MeSH Browser
• Cyclopentanes * MeSH
• Indenes MeSH
• jasmonic acid MeSH Browser
• Oxylipins * MeSH
• Plant Growth Regulators * 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.

• Keywords
• Aspartic protease, carnivorous plant, digestive enzymes, electrical signal, jasmonic acid, phytohormone, plant defence, wounding,
• MeSH
• Carnivory * MeSH
• Carnivorous Plant * MeSH
• Proteomics MeSH
• Publication type
• Journal Article MeSH
• Research Support, Non-U.S. Gov't MeSH
• Names of Substances
• coronatine MeSH Browser
• jasmonic acid MeSH Browser

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.

• Keywords
• 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
• Photosynthesis MeSH
• Plant Leaves MeSH
• Carnivory * MeSH
• Plants * genetics   MeSH
• Nutrients MeSH
• Animals MeSH
• Check Tag
• Animals MeSH
• Publication type
• Journal Article MeSH
• Research Support, Non-U.S. Gov't MeSH