Matthias Freund, Dorothea Graus, Andreas Fleischmann, Kadeem J Gilbert, Qianshi Lin, Tanya Renner, Christian Stigloher, Victor A Albert, Rainer Hedric

The digestive systems of carnivorous plants

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2023-03-16 10:30:04

Matthias Freund, Dorothea Graus, Andreas Fleischmann, Kadeem J Gilbert, Qianshi Lin, Tanya Renner, Christian Stigloher, Victor A Albert, Rainer Hedrich, Kenji Fukushima, The digestive systems of carnivorous plants, Plant Physiology, Volume 190, Issue 1, September 2022, Pages 44–59, https://doi.org/10.1093/plphys/kiac232

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.

Like an animal’s mouth, carnivorous plants use their trapping structures to “eat” their prey, primarily small arthropods. All carnivorous plants discovered to date capture their prey using modified leaves called “trap leaves,” except for Triantha (false asphodel), which was recently shown to produce flypaper-type traps exclusively on its flower stalks ( Lin et al., 2021). Although trap leaves share many functions with animal digestive tracts, there are striking differences in their spatial arrangements ( Figure 1). Most vertebrate digestive tracts are divided into functionally specialized organs such as the mouth, stomach, and intestines, where food is digested and absorbed in distinct compartments ( Hedrich, 2015). In carnivorous plants, however, the prey does not travel through a digestive tract but instead remains in the same organ where it was captured for subsequent digestion and absorption (comparable to some animals with a blind-ended digestive tract, such as polyps; Steinmetz, 2019). Therefore, in principle, trap leaves are all-in-one organs with multifaceted functions, regardless of trap type ( Figure 2). However, in certain trap types, a spatial split of functions may be observed within the organ (i.e. within a single leaf). A striking example is the eel traps of Genlisea (corkscrew plants), in which bifurcating arm-like trapping organs are well separated from the digestive chamber ( Figure 2).

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