Recent ecophysiological, biochemical and evolutional insights into plant carnivory

Abstract

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.

Fig. 1.

Two sides of the same coin. Sticky organs in plants from the same order Lamiales. (A) The inflorescence of Salvia glutinosa is covered by sticky trichomes, which capture insects for purely defensive purposes, and is not considered carnivorous, whereas (B) sticky leaves of the carnivorous butterwort Pinguicula grandiflora clearly digest captured prey. Such defensive structures might have been a prerequisite for evolution of botanical carnivory.

Fig. 2.

The carnivorous plants capturing their prey by different trapping mechanisms. Pitcher traps: (A) Albany pitcher plant, Cephalotus follicularis (Cephalotaceae), (B) California pitcher plant, Darlingtonia californica (Sarraceniaceae), (C) North American pitcher plant, Sarracenia purpurea ssp. venosa (Sarraceniaceae), (D) marsh pitcher plant, Heliamphora folliculata (Sarraceniaceae), (E) tropical pitcher plant, Nepenthes pervillei (Nepenthaceae), (F) bromelia, Brocchinia hectioides (Bromeliaceae); sticky traps: (G) sundew, Drosera rotundifolia (Droseraceae), (H) butterwort, Pinguicula alpina (Lentibulariaceae); eel traps: (I) corkscrew plant, Genlisea hispidula (Lentibulariaceae); suction traps: (J) bladderwort, Utricularia reflexa (Lentibulariaceae); snap traps: (K) waterwheel plant, Aldrovanda vesiculosa (Droseraceae), (L) Venus flytrap, Dionaea muscipula (Droseraceae).

Fig. 3.

Phenotypic plasticity shown as an example on Sarracenia purpurea ssp. venosa. The production of non-carnivorous leaves is favoured under low light, low water availability, low temperature and high nutrient content. The production of carnivorous pitchers is favoured under high light, high water availability, high temperature and low nutrient content.

Fig. 4.

Anatomy of the Nepenthes × Mixta trap. Semi-thin section of the digestive zone of the trap stained with toluidine blue and basic fuchsin through the digestive zone with digestive glands; digestive gland (1), epidermal ridge protecting the digestive gland (2), endodermoid layer (3), trap mesophyll (4), vascular bundles (5); scale bar = 100 µm.

Fig. 5.

Biochemistry of prey decomposition in the digestive glands in the Dionaea trap. (A) In the resting gland, no enzyme production occurs and free ribosomes are only visible (black dots). (B) In the early phase, prey stimulates mechano-sensitive, chloride-permeable channels (FLYC) by touching the sensory trigger hairs that, with other, possibly Ca²⁺-permeable channels, mediate membrane depolarization. The generated action potentials and Ca²⁺ wave are propagated through plasmodesmata along the outer cell layers and lead to trap closure and activation of the JA signalling pathway in the digestive glands. Similar to non-CPs, jasmonic acid (JA) conjugates with isoleucine (JA-Ile), mediates degradation of JASMONATE ZIM-DOMAIN (JAZ) repressors and soon activates gene expression in the nucleus (N) to produce hydrolases (red dots). (C) In the later phase, substances (stimulants) derived from captured prey (*) penetrate the cuticular gaps. Ammonium ions released by deamination in traps induce H⁺ secretion into the fluid, and extremely low amounts of low molecular weight nitrogenous elicitors (amino acids and amines) enter the gland cell. Specific prey-derived molecules (e.g. chitin) activate receptors with a LysM domain and different kinases (Rec/Kin, blue membrane proteins, respectively), which mediate Ca²⁺-dependent and JA-mediated activation of further downstream responses. Zymogens are also gradually released from the vacuole (V). Enzymes (red dots) released from the cutinized wall directly elicit gap formation in the cuticle and secretion of digestive enzymes. Enzymes stored in the wall of the secretory cells may release active residues from prey proteins that further stimulate the gland. With progressing digestion, hydrolases and various transporters (green membrane channels) are intensively produced. The prey is decomposed in the fluid, which becomes strongly acidic and contains autoactivated proteases and oxidases (red dots). The digestive gland readily absorbs the released nutrients either by transporters or by endocytosis, and polysomes utilize them to synthetize novel proteins on membranes of the endoplasmatic reticulum (ER). By the end of prey decomposition, the digestive gland cells are rich in exporting vesicules from the ER or Golgi apparatus (GA), and absorbed nutrients are also transported symplastically. The time course and overlap (in any) of the individual steps of mechanically (B) and chemically activated processes (C) are not fully imaged, and only the most typical components are indicated in both panels.