ReviewCarnivorous pitcher plants: Insights in an old topic
Graphical abstract
Nepenthes and other pitcher plants obtain many nutrients from caught insect. The mechanisms that are involved in trapping and retaining prey are presented. Moreover, our knowledge of the pitcher fluid composition, which is responsible for prey digestion and making nutrients available for the plant, is summarized and discussed.
Research highlights
► Carnivorous Nepenthes plants attract, trap and digest insect prey for additional nutrients. ► The protein composition of the digestion fluid is reported. ► Secondary metabolites have also been described for the fluid. ► Most enzymes are employed in prey digestion but some show antimicrobial activities.
Introduction
The carnivorous syndrome in plants have fascinated men at least since mid of the 19th century, not only because of Charles Darwin’s pioneer studies on this topic, which have been published in his book ‘Insectivorous Plants’ (Darwin, 1875). Insectivorous, or in a broader sense carnivorous plants, usually grow in nutrient-poor environments and on poor soils and carnivory has evolved as an additional pathway to supplement nutrients such as nitrogen and phosphorus (Adamec, 1997). Carnivory in angiosperms has evolved independently at least six times and carnivorous plants are definitely polyphyletic (Albert et al., 1992, Ellison and Gotelli, 2009). In all cases where the carnivorous syndrome has been established in higher plants it represents a striking example for an integrated interaction of form and function in nature. Interestingly, structural homologies do not necessarily correlate with trap form, and similar trap forms may not be structurally homologous (Albert et al., 1992).
Carnivory involves morphological and anatomical features that are associated with the (i) attraction, (ii) trapping and killing of prey, followed by (iii) its digestion and absorption of the nutrients. These three parameters represent the conditions that must be fulfilled to qualify a plant as carnivorous in the narrower sense in contrast to a basic definition which only relies on the ability of plant tissues to absorb nutrients (Chase et al., 2009). Those features have been realized in carnivorous plants by various specialized forms, including the popular snap-trap of Dionaea muscipula Sol. ex J. Ellis (Venus’ flytrap), the well known flypaper-traps of, for example, Drosera (sundew) and Pinguicula (butterwort) species, the sucking bladder-traps of Utricularia (bladderwort) species as well as the pitfall-traps of Nepenthes (Old World pitcher plant) and other plants employing the same trapping mechanism. Pitcher plants are ideal objects to study plant carnivory because the liquid of the pitcher can be easily harvested; moreover, it directly represents the digestion fluid and it can be collected from closed, prey-free pitches which ensures the presence of solely plant-borne constituents.
The pitcher plant groups evolved three times: (i) Cephalotus follicularis Labill. (Cephalotaceae, Oxalidales), a sole endemic species found in southwestern Australia; (ii) Darlingtonia californica Torr., a sole endemic species found in northwestern USA, Sarracenia spp., found in eastern and northern North America and Heliamphora spp., found in northern South America (all Sarraceniaceae, Ericales); (iii) Nepenthes spp. (Nepenthaceae, Caryophyllales), found mainly in the Old World tropics with a high diversity in southeastern Asia (Fig. 1). All three taxa appear to be only distantly related (Albert et al., 1992). A detailed phylogenetic analysis within Nepenthes has successfully performed using both chloroplast (trnK intron and matK gene; trnK: tRNA for lysine, matK: maturase) and nuclear (PRT1 and a translocated copy of trnK; PRT1: pepticle transferase 1) genes (Meimberg et al., 2001, Meimberg and Heubl, 2006).
As a side note it might be mentioned that Darwin himself never worked on Nepenthes plants. Nevertheless, this review will focus mainly on plants of the genus Nepenthes because these are by far the best studied pitcher plants if not the best studied carnivorous plants at all. In particular, the waxy surface of the inner pitcher as important part of the trapping mechanism is well understood. However, detailed knowledge about biochemical and molecular features and characteristics of carnivory in such plants is still limited, in particular knowledge on the digestion of prey. Only recently, few enzymes involved in this process have been purified and corresponding genes have been cloned. Here, recent findings on the composition of the pitcher fluid will be reviewed; their meaning will be discussed in the context of carnivory. Furthermore, whether and how studies on carnivorous plants might give answers to general questions in plant biology will be addressed.
Section snippets
Pitcher traps: structure and function
Up to now, about 120 species of the genus Nepenthes have been described (McPherson, 2009). Their leaf morphology is very similar and consists of a photosynthetic part of the leaf, originally the enlarged leaf base, and a tendril that at its end might develop a pitfall-trap. These so-called pitchers are formed from a leaf by epiascidiation, i.e. by in-rolling of the adaxial leaf surface followed by marginal fusion (Juniper et al., 1989). The pitcher tissue had no higher respiration rate than the
Protein composition of the digestive fluid
The presence of proteolytic enzyme activities in carnivorous plants is known since the time of Darwin (1875). In the case of the New World pitcher plants, activities of endogenous hydrolytic enzymes that might be involved in prey digestion have been detected only in the pitcher fluid of Sarracenia purpurea L. indicating the presence of a protease, ribonuclease, nuclease, and a phosphatase (Gallie and Chang, 1997, Jaffe et al., 1992) also suggested a protease activity in the pitcher fluid of
Secondary metabolites in the digestion fluid
Similar to pathogenesis-related proteins, low molecular weight compounds of plant origin typically contribute to pathogen resistance in plants as they often possess antimicrobial activities. Although there are several secondary metabolites described from different Nepenthes tissues (Bringmann et al., 2000, Aung et al., 2002, Rischer et al., 2002), up to now there is only one study describing the presence of such compounds in the traps of Nepenthes. Very recently, Eilenberg and coworkers (2010)
Conclusions and outlook
The intention of this review was to summarize our knowledge of prey capture and on the features of the fluid that is responsible for prey digestion in carnivorous pitcher plants. Thus, the focus was clearly on species of the best studied carnivorous pitcher plants belonging to the genus Nepenthes. Although the phenomenon of carnivory in plants is known for more than 150 years, the isolation and identification of the enzymes involved started only recently. We still do not know the complete enzyme
Acknowledgements
I thank Katja Rembold, Nees Institute, Bonn, for providing photographs of Darlingtonia, Heliamphora, Sarracenia, and Cephalotus, Sandy Rottloff and Franziska Buch, MPI for Chemical Ecology, Jena, for the photograph of Nepenthes and Fig. 2, respectively. Work on carnivorous plants has been supported by Wilhelm Boland and the Max Planck Society.
Axel Mithöfer studied Biology in Osnabrück, Germany, and did his Diploma in 1988. In 1992, he received his Ph.D. in Plant Physiology from the Ruhr-Universität Bochum. For his Habilitation in Botany at the Ludwig-Maximilians University Munich in 1999, he worked on physiological and molecular aspects in the Phytophthora sojae – soybean pathosystem together with Prof. J. Ebel. In 2000, he moved to the INRA in Toulouse, France. After returning to Munich for another 2 years he joined the Bioorganic
References (47)
- et al.
Phenolic constituents from the leaves of the carnivorous plant Nepenthes gracilis
Fitoterapia
(2002) - et al.
Droserone from cell cultures of Triphyophyllum peltatum (Dioncophyllaceae) and its biosynthetic origin
Phytochemistry
(2000) A ribonuclease from Nepenthes spp
Biochim. Biophys. Acta
(1960)- et al.
Aspects of pitcher morphology and spectral characteristics of six Bornean Nepenthes pitcher plant species: implications for prey capture
Ann. Bot.
(1999) - et al.
Nepenthes insignis uses a C2-portion of the carbon skeleton of l-alanine acquired via its carnivorous organs, to build up the allelochemical plumbagin
Phytochemistry
(2002) - et al.
Micropreparation of single secretory glands from the carnivorous plant Nepenthes
Anal. Biochem.
(2009) Mineral nutrition of carnivorous plants: a review
Bot. Rev.
(1997)- et al.
Carnivorous plants: phylogeny and structural evolution
Science
(1992) - et al.
Enzymic and structural characterization of nepenthesin, a unique member of a novel subfamily of aspartic proteinases
Biochem. J.
(2004) - et al.
Karnivoren
(2004)
Insect aquaplaning: Nepenthes pitcher plants capture prey with the peristome, a fully wettable water-lubricated anisotropic surface
Proc. Natl. Acad. Sci. USA
Murderous plants: Victorian gothic, Darwin and modern insights into vegetable carnivory
Bot. J. Linn. Soc.
Trap geometry in three giant montane pitcher plant species from Borneo is a function of tree shrew body size
New Phytol.
Tree shrew lavatories: a novel nitrogen sequestration strategy in a tropical pitcher plant
Biol. Lett.
Insectivorous Plants
Isolation and characterization of chitinase genes from pitchers of the carnivorous plant Nepenthes khasiana
J. Exp. Bot.
Induced production of antifungal naphthoquinones in the pitchers of the carnivorous plant Nepenthes khasiana
J. Exp. Bot.
Energetics and the evolution of carnivorous plants-Darwin’s ‘most wonderful plants in the world’
J. Exp. Bot.
Signal transduction in the carnivorous plant Sarracenia purpurea. Regulation of secretory hydrolase expression during development and in response to resources
Plant Physiol.
A viscoelastic deadly fluid in carnivorous pitcher plants
PLoS One
Function of epidermal surfaces in the trapping efficiency of Nepenthes alata pitchers
New Phytol.
Structure and properties of the glandular surfaces in the digestive zone of the pitcher in the carnivorous plant Nepenthes ventrata and its role in insect trapping and retention
J. Exp. Biol.
Proteome analysis of pitcher fluid of the carnivorous plant Nepenthes alata
J. Proteome Res.
Cited by (60)
The antifouling mechanism and application of bio-inspired superwetting surfaces with effective antifouling performance
2024, Advances in Colloid and Interface ScienceContrasting effect of prey capture on jasmonate accumulation in two genera of aquatic carnivorous plants (Aldrovanda, Utricularia)
2021, Plant Physiology and BiochemistryCitation Excerpt :In non-carnivorous plants, JAs accumulate in response to pathogen or herbivore attack and activate plant defense reactions by transcriptional activation (Wasternack and Hause, 2013). It has been suggested that the jasmonate signalling pathway as well as digestive enzymes, which belong to pathogenesis-related proteins, have been co-opted by carnivorous plants from plant defense to prey digestion during evolution (Mithöfer, 2011; Pavlovič and Saganová, 2015; Bemm et al., 2016; Pavlovič and Mithöfer, 2019). The true bioactive compound JA-Ile binds to the CORONATINE INSENSITIVE1 (COI1) protein as a part of a co-receptor complex, mediates the ubiquitin-dependent degradation of JASMONATE ZIM-DOMAIN (JAZ) repressors, resulting in the activation of jasmonate-dependent gene expression (Thines et al., 2007; Fonseca et al., 2009; Sheard et al., 2010); in carnivorous plants, it initiates the expression of carnivory-related genes, mainly for nutrient transport and digestive enzymes (Bemm et al., 2016; Böhm et al., 2016; Krausko et al., 2017; Pavlovič et al., 2017; Jakšová et al., 2020).
A carnivorous plant algorithm for solving global optimization problems
2021, Applied Soft ComputingCitation Excerpt :To gain additional nutrients like nitrogen and phosphorus for growth and reproduction, carnivorous plants attract, trap and consume animals such as flies, butterflies, lizard and mouse with their secreted enzymes [31]. A plant can only be considered as carnivorous if it possesses the abilities of attraction, trapping or killing, and digestion of the prey [32]. Some plants attract the prey for reproduction without killing them, and some immobilize or kill the attackers for defence purposes but do not digest the bodies.
Plumbagin from a tropical pitcher plant (Nepenthes alata Blanco) induces apoptotic cell death via a p53-dependent pathway in MCF-7 human breast cancer cells
2019, Food and Chemical ToxicologyCitation Excerpt :Compound 1 (Fig. 1B) was isolated from the CH2Cl2 fraction by silica gel and RP-C18 column chromatography and identified as plumbagin by comparison of its spectroscopic data with literature values (Buch et al., 2013; Cannon et al., 1980; Rischer et al., 2002). Plumbagin has been previously reported from Nepenthes plants and also identified as a mixture from N. alata (Mithofer, 2011; Raj et al., 2011; Rischer et al., 2002; Schlauer et al., 2005); however, herein it was isolated for the first time from N. alata. Compound 1 was determined to have >98% purity by HPLC analysis.
Nepenthes: State of the art of an inspiring plant for biotechnologists
2018, Journal of BiotechnologyCitation Excerpt :The discovery and the development of new antimicrobial compounds is a key issue to limit new invasive infections. It has been shown that microbial growth is significantly slowdown in the pitcher fluid (Buch et al., 2013; Eilenberg, 2006; Hatano and Hamada, 2008, 2012; Mithofer, 2010). This antibacterial activity might be related to one or more secreted enzyme such as Pathogen-related (PR) proteins.
Ecological interactions of carnivorous plants: beyond the relationship with their prey
2024, Arthropod-Plant Interactions
Axel Mithöfer studied Biology in Osnabrück, Germany, and did his Diploma in 1988. In 1992, he received his Ph.D. in Plant Physiology from the Ruhr-Universität Bochum. For his Habilitation in Botany at the Ludwig-Maximilians University Munich in 1999, he worked on physiological and molecular aspects in the Phytophthora sojae – soybean pathosystem together with Prof. J. Ebel. In 2000, he moved to the INRA in Toulouse, France. After returning to Munich for another 2 years he joined the Bioorganic Chemistry Department of the Max Planck Institute for Chemical Ecology in Jena in 2003 as the leader of the ‘‘Plant Defence Physiology’’ research group. He is associate professor at the Friedrich-Schiller University Jena. His main research interests lies in the field of plants’ interactions with other organisms, mainly herbivorous insects: the processes of signal perception, signal transduction, and induced plant defenses.