The digestive systems of carnivorous plants

Abstract

To survive in the nutrient-poor habitats, carnivorous plants capture small organisms comprising complex substances not suitable for immediate reuse. The traps of carnivorous plants, which are analogous to the digestive systems of animals, are equipped with mechanisms for the breakdown and absorption of nutrients. Such capabilities have been acquired convergently over the past tens of millions of years in multiple angiosperm lineages by modifying plant-specific organs including leaves. The epidermis of carnivorous trap leaves bears groups of specialized cells called glands, which acquire substances from their prey via digestion and absorption. The digestive glands of carnivorous plants secrete mucilage, pitcher fluids, acids, and proteins, including digestive enzymes. The same (or morphologically distinct) glands then absorb the released compounds via various membrane transport proteins or endocytosis. Thus, these glands function in a manner similar to animal cells that are physiologically important in the digestive system, such as the parietal cells of the stomach and intestinal epithelial cells. Yet, carnivorous plants are equipped with strategies that deal with or incorporate plant-specific features, such as cell walls, epidermal cuticles, and phytohormones. In this review, we provide a systematic perspective on the digestive and absorptive capacity of convergently evolved carnivorous plants, with an emphasis on the forms and functions of glands.

Figure 1

Functional similarities between a trap leaf and a digestive tract. A, The spatial differentiation of the digestive system. The sites for eating, digestion, and absorption are spatially separated in the animal system (symbolized by colors), but not in carnivorous plants (overlapping colors). B, Secretory and absorptive pathways that are discussed in the main text and Box 2. Note that the figure shows an imaginary synthetic cell because interspecies and gland-type-specific differences in these processes are often unknown in carnivorous plants. Among the many secretory and absorptive pathways and membrane proteins identified in parietal cells (Yao and Forte, 2003; Engevik et al., 2020), chief cells (Hirschowitz, 1967), and intestinal epithelial cells (Pácha, 2000; Rajendran et al., 2018; Engevik and Engevik, 2021) in animals, only the counterparts of those characterized in carnivorous plants are shown. The cell wall and cuticle are not shown. The organelles are not shown to scale.

Figure 2

Evolution of glandular cells in carnivorous plants. The order-level phylogeny of flowering plants (The Angiosperm Phylogeny Group et al., 2016) is shown on the left, with lineages containing carnivorous plants and their trap types highlighted in red. Branch lengths have no information. Trap leaves and glands of representative species are shown on the right (for scanning electron microscopy, see Supplemental Methods S1). To increase visibility, methylene blue staining was applied to the glands of Cephalotus, Sarracenia, Heliamphora, Darlingtonia, and Roridula (Supplemental Methods S2). Whole or parts of the photographs of Utricularia and Philcoxia were reproduced from the literature (Yang et al., 2009; Pereira et al., 2012). The photographs of Aldrovanda were provided by Dirk Becker. Original pictures (including scale bars for microscopic pictures) are available in figshare (https://doi.org/10.6084/m9.figshare.18271529) under CC BY 4.0 (https://creativecommons.org/licenses/by/4.0/).

Figure 3

Digestive fluid acidity across the tree of life. A, Extracellular pH in the digestive organs of plants and animals. The plant apoplast and phylloplane (i.e. leaf surface) were included for comparison with the digestive fluid of carnivorous plants. The datasets for animal stomachs and plant phylloplane were obtained from the literature (Beasley et al., 2015; Gilbert and Renner, 2021). The source data for the others are available in Supplemental Table S1. When pH was measured at multiple time points or under multiple conditions, only the lowest value was included. The silhouettes of representative organisms were obtained from PhyloPic (http://phylopic.org). The silhouette of Cathartes aura is licensed under CC BY-SA 3.0 (https://creativecommons.org/licenses/by-sa/3.0/) by Sevcik et al. B, pH of the digestive fluids of different carnivorous plant genera. Boxplot elements are defined as follows: center line, median; box limits, upper and lower quartiles; whiskers, 1.5 × interquartile range.