Slow food: insect prey and chitin induce phytohormone accumulation and gene expression in carnivorous<i>Nepenthes</i>plants

Yilamujiang, Ayufu; Reichelt, Michael; Mithöfer, Axel

doi:10.1093/aob/mcw110

Cited by 40 publications

(31 citation statements)

References 23 publications

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“…Indeed, prey digestion gave rise to NH 4 + production in carnivorous plants (Scherzer et al, 2013). Another chemical agent that stimulates enzyme production is chitin, which probably acts through a LysM receptor kinase (Matu s ıkov a et al, 2005;Bemm et al, 2016;Yilamujiang et al, 2016).…”

Section: Discussionmentioning

confidence: 99%

The role of electrical and jasmonate signalling in the recognition of captured prey in the carnivorous sundew plant Drosera capensis

et al. 2016

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The carnivorous sundew plant (Drosera capensis) captures prey using sticky tentacles. We investigated the tentacle and trap reactions in response to the electrical and jasmonate signalling evoked by different stimuli to reveal how carnivorous sundews recognize digestible captured prey in their traps. We measured the electrical signals, phytohormone concentration, enzyme activities and Chla fluorescence in response to mechanical stimulation, wounding or insect feeding in local and systemic traps. Seven new proteins in the digestive fluid were identified using mass spectrometry. Mechanical stimuli and live prey induced a fast, localized tentacle-bending reaction and enzyme secretion at the place of application. By contrast, repeated wounding induced a nonlocalized convulsive tentacle movement and enzyme secretion in local but also in distant systemic traps. These differences can be explained in terms of the electrical signal propagation and jasmonate accumulation, which also had a significant impact on the photosynthesis in the traps. The electrical signals generated in response to wounding could partially mimic a mechanical stimulation of struggling prey and might trigger a false alarm, confirming that the botanical carnivory and plant defence mechanisms are related. To trigger the full enzyme activity, the traps must detect chemical stimuli from the captured prey.

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Section: Discussionmentioning

confidence: 99%

The role of electrical and jasmonate signalling in the recognition of captured prey in the carnivorous sundew plant Drosera capensis

et al. 2016

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“…The application of chitin or ammonium salts activated the jasmonate signalling pathway and the expression of digestive enzymes probably through the LysM receptor or the depolarization of the membrane potential in digestive glands, respectively (Matu s ıkov a et al, 2005; Scherzer et al, 2013Scherzer et al, , 2015Libiakov a et al, 2014;Bemm et al, 2016;Jop c ık et al, 2017;Krausko et al, 2017). Chemical sensing is extremely important for inducing the carnivorous response through jasmonate signalling in passive Nepenthes pitcher traps, which are probably not able to generate electrical signals in response to prey capture (Buch et al, 2015;Yilamujiang et al, 2016).…”

Section: New Phytologistmentioning

confidence: 99%

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

2017

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In the carnivorous plant Venus flytrap (Dionaea muscipula), the sequence of events after prey capture resembles the well-known plant defence signalling pathway in response to pathogen or herbivore attack. Here, we used wounding to mimic prey capture to show the similarities and differences between botanical carnivory and plant defence mechanisms. We monitored movement, electrical signalling, jasmonate accumulation and digestive enzyme secretion in local and distal (systemic) traps in response to prey capture, the mechanical stimulation of trigger hairs and wounding. The Venus flytrap cannot discriminate between wounding and mechanical trigger hair stimulation. Both induced the same action potentials, rapid trap closure, hermetic trap sealing, the accumulation of jasmonic acid (JA) and its isoleucine conjugate (JA-Ile), and the secretion of proteases (aspartic and cysteine proteases), phosphatases and type I chitinase. The jasmonate accumulation and enzyme secretion were confined to the local traps, to which the stimulus was applied, which correlates with the propagation of electrical signals and the absence of a systemic response in the Venus flytrap. In contrast to plant defence mechanisms, the absence of a systemic response in carnivorous plant may represent a resource-saving strategy. During prey capture, it could be quite expensive to produce digestive enzymes in the traps on the plant without prey.

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“…The pitchers can detect enzymes in the pitcher fluids and respond accordingly to maintain an optimal cocktail of enzymes so that the benefits from prey digestion outweigh the costs of protein replenishment and pitcher metabolisms. Other studies also revealed that pitchers can regulate enzyme activities 24,46,58 . This is likely involving Ca 2+ and jasmonic acid (JA) signal transduction pathways 22 .…”

Section: Discussionmentioning

confidence: 94%

“…The findings that many proteases, chitinases, and glucanases found in the pitcher fluids can also be classified as PR proteins led to the inference that offensive carnivory mechanism evolved from existing plant defensive mechanism against herbivory 22 . This is also supported by the conserved jasmonate signalling of enzyme secretion during prey capture 23,24 .…”

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confidence: 81%

“…Botanical carnivory for resource acquisition appears to be a costly lifestyle, which suggests that the energetic costs of producing trapping organs, enzymes, waxes, and other secondary meabolites prevent carnivorous plants from being widespread in the plant kingdom over unrestricted habitats 35,36 . Despite recent studies on the prey-induced secretion of digestive enzymes 23,24 , molecular data on the regulation of endogenous protein secretion and replenishment are still lacking to elucidate the molecular and physiological roots of plant carnivory mechanisms. Recently, we reported that certain proteins were replenished even without prey induction in the pitcher fluids of Nepenthes x ventrata within three days of pitcher opening 37 , which indicates molecular regulation of protein secretion in the pitchers in response to protein loss.…”

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confidence: 99%

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Transcriptome-wide shift from photosynthesis and energy metabolism upon endogenous fluid protein depletion in young Nepenthes ampullaria pitchers

Goh

Baharin

Salleh

et al. 2020

Sci Rep

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faris 'imadi Mohd Salleh, Rishiesvari Ravee, Wan nor Adibah Wan Zakaria & normah Mohd noor carnivorous pitcher plants produce specialised pitcher organs containing secretory glands, which secrete acidic fluids with hydrolytic enzymes for prey digestion and nutrient absorption. The content of pitcher fluids has been the focus of many fluid protein profiling studies. These studies suggest an evolutionary convergence of a conserved group of similar enzymes in diverse families of pitcher plants. A recent study showed that endogenous proteins were replenished in the pitcher fluid, which indicates a feedback mechanism in protein secretion. This poses an interesting question on the physiological effect of plant protein loss. However, there is no study to date that describes the pitcher response to endogenous protein depletion. To address this gap of knowledge, we previously performed a comparative RNA-sequencing experiment of newly opened pitchers (D0) against pitchers after 3 days of opening (D3C) and pitchers with filtered endogenous proteins (>10 kDa) upon pitcher opening (D3L). Nepenthes ampullaria was chosen as a model study species due to their abundance and unique feeding behaviour on leaf litters. The analysis of unigenes with top 1% abundance found protein translation and stress response to be overrepresented in D0, compared to cell wall related, transport, and signalling for D3L. Differentially expressed gene (DEG) analysis identified DEGs with functional enrichment in protein regulation, secondary metabolism, intracellular trafficking, secretion, and vesicular transport. the transcriptomic landscape of the pitcher dramatically shifted towards intracellular transport and defence response at the expense of energy metabolism and photosynthesis upon endogenous protein depletion. This is supported by secretome, transportome, and transcription factor analysis with RT-qPCR validation based on independent samples. This study provides the first glimpse into the molecular responses of pitchers to protein loss with implications to future cost/benefit analysis of carnivorous pitcher plant energetics and resource allocation for adaptation in stochastic environments.Carnivorous plants are commonly found in habitats deprived of nutrients, especially nitrogen and phosphorus. To qualify as carnivorous, a plant must have at least one adaptation for active attraction, capture, digestion, and clear nutritional benefit from carnivory 1 . The convergent evolution of passive pitfall traps resulted in carnivorous pitcher plants of diverse orders and families, including Nepenthaceae (Caryophyllales), Cephalotaceae (Oxalidales), and Sarraceniaceae (Ericales) at distant geographical locations but sharing similar digestive fluid proteins 2-4 . A species-rich monotypic group of tropical pitcher plants from genus Nepenthes develop attractive pitchers of diverse shapes and sizes 5 . Recently, two highly conserved leaf developmental regulatory genes, ASYMMETRIC LEAVES1 (AS1) and REVOLUTA (REV), have been shown to be key in pitcher developme...

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Slow food: insect prey and chitin induce phytohormone accumulation and gene expression in carnivorousNepenthesplants

Cited by 40 publications

References 23 publications

The role of electrical and jasmonate signalling in the recognition of captured prey in the carnivorous sundew plant Drosera capensis

The role of electrical and jasmonate signalling in the recognition of captured prey in the carnivorous sundew plant Drosera capensis

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

Transcriptome-wide shift from photosynthesis and energy metabolism upon endogenous fluid protein depletion in young Nepenthes ampullaria pitchers

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