Jasmonate-independent regulation of digestive enzyme activity in the carnivorous butterwort Pinguicula × Tina.

Ivan Petřík,Ondřej Kocáb,René Lenobel,Ivo Chamrád,Ondřej Novák,Jana Jakšová,Andrej Pavlovič,John Lunn

doi:10.1093/jxb/eraa159

Abstract

Carnivorous plants within the order Caryophyllales use jasmonates, a class of phytohormone, in the regulation of digestive enzyme activities. We used the carnivorous butterwort Pinguicula × Tina from the order Lamiales to investigate whether jasmonate signaling is a universal and ubiquitous signaling pathway that exists outside the order Caryophyllales. We measured the electrical signals, enzyme activities, and phytohormone tissue levels in response to prey capture. Mass spectrometry was used to identify proteins in the digestive secretion. We identified eight enzymes in the digestive secretion, many of which were previously found in other genera of carnivorous plants. Among them, alpha-amylase is unique in carnivorous plants. Enzymatic activities increased in response to prey capture; however, the tissue content of jasmonic acid and its isoleucine conjugate remained rather low in contrast to the jasmonate response to wounding. Enzyme activities did not increase in response to the exogenous application of jasmonic acid or coronatine. Whereas similar digestive enzymes were co-opted from plant defense mechanisms among carnivorous plants, the mode of their regulation differs. The butterwort has not co-opted jasmonate signaling for the induction of enzyme activities in response to prey capture. Moreover, the presence of alpha-amylase in digestive fluid of P. × Tina, which has not been found in other genera of carnivorous plants, might indicate that non-defense-related genes have also been co-opted for carnivory.

Highlights

The carnivorous plants have evolved specialized leaves or leaf parts that function as traps for prey capture and digestion to obtain scarce nutrients.This adaptation to low nutrient content in the soil has independently evolved by convergent evolution at least 10 times in several orders of flowering plants (Albert et al, 1992; Givnish et al, 2015; Fleischmann et al, 2018)
We focused on carnivorous plants of the genus Pinguicula, which belongs to the order Lamiales and is distantly related to the Venus flytrap, sundew, and pitcher plant (Albert et al, 1992; Givnish, 2015)
We showed that the butterwort (Pinguicula × Tina, order Lamiales) had increased enzyme activities in digestive fluid from leaves in response to prey capture

Summary

Introduction

The carnivorous plants have evolved specialized leaves or leaf parts that function as traps for prey capture and digestion to obtain scarce nutrients.This adaptation to low nutrient content in the soil has independently evolved by convergent evolution at least 10 times in several orders of flowering plants (Albert et al, 1992; Givnish et al, 2015; Fleischmann et al, 2018). The mechanism by which the secretion of these digestive enzymes is regulated by stimuli from prey remained unknown until Escalanté-Pérez et al (2011) found that a phytohormone from the group of jasmonates, 12-oxo-phytodienoic acid (OPDA), was responsible for activation of the digestive process in Venus flytrap (Dionaea muscipula). The studies to date have generally been confined to three genera of carnivorous plants (Drosera, Dionaea, and Nepenthes), which all are within the order Caryophyllales (or, according to some authors, the separate order Nepenthales; Fleischmann et al, 2018) and are monophyletic. It remains unclear whether the jasmonate signaling pathway is a universal and ubiquitous signaling pathway in other phylogenetic lineages of carnivorous plants

Objectives

Methods

Results

Discussion

Conclusion