The carnivorous Venus flytrap uses prey‐derived amino acid carbon to fuel respiration

Abstract

The present study was performed to elucidate the fate of carbon (C) and nitrogen (N) derived from protein of prey caught by carnivorous Dionaea muscipula. For this, traps were fed C/ N-glutamine (Gln). The release of CO was continuously monitored by isotope ratio infrared spectrometry. After 46 h, the allocation of C and N label into different organs was determined and tissues were subjected to metabolome, proteome and transcriptome analyses. Nitrogen of Gln fed was already separated from its C skeleton in the decomposing fluid secreted by the traps. Most of the Gln-C and Gln-N recovered inside plants were localized in fed traps. Among nonfed organs, traps were a stronger sink for Gln-C compared to Gln-N, and roots were a stronger sink for Gln-N compared to Gln-C. A significant amount of the Gln-C was respired as indicated by C-CO emission, enhanced levels of metabolites of respiratory Gln degradation and increased abundance of proteins of respiratory processes. Transcription analyses revealed constitutive expression of enzymes involved in Gln metabolism in traps. It appears that prey not only provides building blocks of cellular constituents of carnivorous Dionaea muscipula, but also is used for energy generation by respiratory amino acid degradation.

Dynamics of amino acid redistribution in the carnivorous Venus flytrap (Dionaea muscipula) after digestion of 13C/15N‐labelled prey

“…Using 13 C‐labelled glutamine, it was previously shown that enhanced energy demand during prey digestion could at least partly be met through catabolic breakdown of C backbones of glutamine taken up from the external stomach (Fasbender et al . ). In the present study, we explored changes in plant amino acid pools, after digestion of 13 C/ 15 N‐labelled insect powder.…”

“…This finding suggests that respiratory degradation of amino acids originating from prey constitutes an important source of energy during prey digestion (Fasbender et al . ). Apparently, unlike initial energy expenditure related to trap closure (Jaffe ; Pavlovič et al .…”

“…; Fasbender et al . ). In the present study, we made an attempt to experimentally mimic conditions that are more closely encountered in nature.…”

Triggering a false alarm: wounding mimics prey capture in the carnivorous Venus flytrap (Dionaea muscipula)

“…On the one hand, after prey digestion and nutrient absorption, the carnivorous plant Venus flytrap can increase its rate of photosynthesis (A N ) and growth. On the other, the electrical signalling associated with prey capture and increased demand for energy during prey digestion results in decreased A N and an increased rate of mitochondrial respiration (Pavlovi c et al, 2010;Kruse et al, 2014;Libiakov a et al, 2014;Pavlovi c & Saganov a, 2015;Fasbender et al, 2017). However, the Venus flytrap has evolved several control mechanisms to optimize this benefit by reducing its associated costs.…”

“…Venus flytrap has a rosette with five to ten leaves that arise from a short, bulb‐like, subterranean stem. The leaves are probably vascularly connected as indicated by isotopic labelling experiments (Fasbender et al ., ) and the exogenous application of coronatine (Escalante‐Pérez et al ., ). To avoid uncertainty about the possible absence of a vascular connection, the three or four traps of a single Venus flytrap plant were fed insects at different time points to intensify a possible systemic response, and the fed traps were harvested at 1, 18, 24 and 168 h (1 wk) after prey capture.…”