Endocytotic uptake of nutrients in carnivorous plants

Abstract

SUMMARYCarnivorous plants trap, digest and absorb animals in order to supplement their mineral nutrition. Nutrients absorbed by the plant include different nitrogen species, phosphate, potassium, trace elements and small organic compounds. Uptake is usually thought to be performed via specific channels, but this study provides evidence that endocytosis is involved as well. Traps of the carnivorous plants Nepenthes coccinea, Nepenthes ventrata, Cephalotus follicularis, Drosophyllum lusitanicum, Drosera capensis, Dionaea muscipula, Aldrovanda vesiculosa, Genlisea violacea · lobata, Sarracenia psittacina and Sarracenia purpurea were stained with methylene blue in order to identify possible sites of uptake. The permeable parts of the traps were incubated with fluorescein isothiocyanate labelled bovine serum albumin (FITC-BSA) and other fluorescent endocytosis markers, combined with the soluble protein BSA or respiratory inhibitors. Uptake was studied by confocal microscopy. In Nepenthes, small fluorescent vesicles became visible 1 h after incubation with FITC-BSA. These vesicles fused to larger compartments within 30 h. A similar behaviour was found in the related genera Drosera, Dionaea, Aldrovanda and Drosophyllum but also in Cephalotus with glands of different evolutionary origin. In Genlisea and Sarracenia, no evidence for endocytosis was found. We propose that in many carnivorous plants, nutrient uptake by carriers is supplemented by endocytosis, which enables absorption and intracellular digestion of whole proteins. The advantage for the plant of reducing secretion of enzymes for extracellular digestion is evident.

Venus flytrap carnivorous lifestyle builds on herbivore defense strategies

“…S2). That the plasma membrane folding increases toward the basal end of these cells suggests that this cell pole of enlarged surface area is engaged, at least in part, with nutrient resorption (Adlassnig et al 2012). Using the same reasoning, the stimulated cells in layer 2, which are entirely folded in a brush-boarder-like fashion (Supplemental Fig.…”

Nitrogen acquisition in Agave tequilana from degradation of endophytic bacteria

“…However, it is now known that the principal form of N entering soils that do not receive inorganic fertilizer is organic N derived from microbial breakdown of organic matter, including amino acids, di- and tri-peptides, DNA and proteins131415. In addition, some plants can scavenge organic N from insects (carnivorous plants) or by entomopathogenic fungus-mediated N translocation from insects1617. Further, some plants have been shown to consume and degrade bacteria and yeasts through endocytosis3.…”

The mixotrophic nature of photosynthetic plants

“…In legumes, root phosphatase activity is higher than in other forbs regardless of the presence of nodules (Venterink 2011), and soil associated with N 2 fixing plants has higher extracellular phosphatase activity than soil without N 2 fixers (Houlton et al 2008). Root-derived proteases have been described in Hakea (Proteaceae), carnivorous plants, Arabidopsis and other species including crops (Adlassnig et al 2012). Proteases are present in the root apoplast (Tornero et al 1996;Hamilton et al 2003), and the presence of protein degradation products in the apoplast of inner root cortex suggests that proteases are active in the apoplast and at the root surface (Paungfoo- Lonhienne et al 2008).…”

“…2; Raven et al 2009). We do not consider carnivorous angiosperms in detail here, but note that they are photosynthetic (Juniper et al 1989;Raven et al 2009;Król et al 2012), can take up organic C in amino acids and peptides via transporters (Schulze et al 1999) and via endocytosis (Adlassnig et al 2012), but have a significant C cost in trap construction and maintenance and in enzyme secretion (Ellison and Adamec 2011;Sirová et al 2011).…”

“…Recently, endocytosis was identified as a mechanism facilitating entry of proteins into tissues of carnivorous plants. Proteins are absorbed by endosomes which fuse with primary lysosomes which results in larger compartments where degradation takes place (Adlassnig et al 2012). Endocytosis also plays an integral role in the endocytic uptake of Rhizobium bacteria in legume roots, involving internalisation into plant cells (reviewed by Brewin 2004).…”