Abundance of Cysteine Endopeptidase Dionain in Digestive Fluid of Venus Flytrap (Dionaea muscipula Ellis) Is Regulated by Different Stimuli from Prey through Jasmonates

Libiaková, Michaela; Floková, Kristýna; Novák, Ondřej; Slováková, Ľudmila; Pavlovič, Andrej

doi:10.1371/journal.pone.0104424

Cited by 49 publications

(49 citation statements)

References 72 publications

(120 reference statements)

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“…Identified DEGs were mainly enriched for processes controlled or triggered by the stress hormones JA and abscisic acid, followed by ethylene, auxin, and salicylic acid. Corroborating previous findings that the wounding hormone JA plays an important role in carnivorous plants (Escalante-Perez et al 2011;Nakamura et al 2013;Libiakova et al 2014), our analyses now demonstrate that not only JA biosynthesis but also its signaling components were differentially regulated. A detailed inspection showed that insect processing induces JA core components in traps ( Fig.…”

Section: Active Glands In Secretion Modesupporting

confidence: 84%

Venus flytrap carnivorous lifestyle builds on herbivore defense strategies

et al. 2016

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Although the concept of botanical carnivory has been known since Darwin's time, the molecular mechanisms that allow animal feeding remain unknown, primarily due to a complete lack of genomic information. Here, we show that the transcriptomic landscape of the Dionaea trap is dramatically shifted toward signal transduction and nutrient transport upon insect feeding, with touch hormone signaling and protein secretion prevailing. At the same time, a massive induction of general defense responses is accompanied by the repression of cell death–related genes/processes. We hypothesize that the carnivory syndrome of Dionaea evolved by exaptation of ancient defense pathways, replacing cell death with nutrient acquisition.

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Section: Active Glands In Secretion Modesupporting

confidence: 84%

Venus flytrap carnivorous lifestyle builds on herbivore defense strategies

et al. 2016

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“…Several other significantly enriched GOs are associated with this gene family. Cysteine proteases have been identified as major functional components of Venus flytrap (Dionaea muscipula) digestive fluid (72), reported in three D. muscipula transcriptomes (70,73,74), and structurally annotated for both Cape sundew (Drosera capensis) draft genome sequences (75,76) and D. muscipula (77). We found tandem clusters of homologous proteaseencoding genes in the U. gibba genome that had demonstrably undergone tandem duplication both before and after the most recent WGD event in U. gibba's evolutionary history (Fig.…”

Section: Significancementioning

confidence: 90%

Long-read sequencing uncovers the adaptive topography of a carnivorous plant genome

Lan

Renner

Ibarra-Laclette

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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Utricularia gibba, the humped bladderwort, is a carnivorous plant that retains a tiny nuclear genome despite at least two rounds of whole genome duplication (WGD) since common ancestry with grapevine and other species. We used a third-generation genome assembly with several complete chromosomes to reconstruct the two most recent lineage-specific ancestral genomes that led to the modern U. gibba genome structure. Patterns of subgenome dominance in the most recent WGD, both architectural and transcriptional, are suggestive of allopolyploidization, which may have generated genomic novelty and led to instantaneous speciation. Syntenic duplicates retained in polyploid blocks are enriched for transcription factor functions, whereas gene copies derived from ongoing tandem duplication events are enriched in metabolic functions potentially important for a carnivorous plant. Among these are tandem arrays of cysteine protease genes with trap-specific expression that evolved within a protein family known to be useful in the digestion of animal prey. Further enriched functions among tandem duplicates (also with trap-enhanced expression) include peptide transport (intercellular movement of broken-down prey proteins), ATPase activities (bladder-trap acidification and transmembrane nutrient transport), hydrolase and chitinase activities (breakdown of prey polysaccharides), and cell-wall dynamic components possibly associated with active bladder movements. Whereas independently polyploid Arabidopsis syntenic gene duplicates are similarly enriched for transcriptional regulatory activities, Arabidopsis tandems are distinct from those of U. gibba, while still metabolic and likely reflecting unique adaptations of that species. Taken together, these findings highlight the special importance of tandem duplications in the adaptive landscapes of a carnivorous plant genome.

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“…The origin of the essential proteolytic activity associated with an efficient plant carnivorous lifestyle differs between species and reflects independent evolutionary events (1,67). For D. muscipula, cysteine proteases account for the majority of the proteolytic activity in prey digestion (5,41,68), and recent studies strongly link chemical stimulation by the jasmonate phytohormones to the increased production and secretion of the dionains (69). Such results provide evidence for the fine-tuning of digestive fluid proteolytic activity by hormonal stimulation from prey decomposition, in addition to the mechanical stimulation trigged by trap closure.…”

mentioning

confidence: 99%

Enzymatic and Structural Characterization of the Major Endopeptidase in the Venus Flytrap Digestion Fluid

Risør

Thomsen

Sanggaard

et al. 2016

Journal of Biological Chemistry

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Carnivorous plants primarily use aspartic proteases during digestion of captured prey. In contrast, the major endopeptidases in the digestive fluid of the Venus flytrap (Dionaea muscipula) are cysteine proteases (dionain-1 to -4). Here, we present the crystal structure of mature dionain-1 in covalent complex with inhibitor E-64 at 1.5 Å resolution. The enzyme exhibits an overall protein fold reminiscent of other plant cysteine proteases. The inactive glycosylated pro-form undergoes autoprocessing and self-activation, optimally at the physiologically relevant pH value of 3.6, at which the protective effect of the prodomain is lost. The mature enzyme was able to efficiently degrade a Drosophila fly protein extract at pH 4 showing high activity against the abundant Lys-and Arg-rich protein, myosin. The substrate specificity of dionain-1 was largely similar to that of papain with a preference for hydrophobic and aliphatic residues in subsite S 2 and for positively charged residues in S 1 . A tentative structure of the pro-domain was obtained by homology modeling and suggested that a pro-peptide Lys residue intrudes into the S 2 pocket, which is more spacious than in papain. This study provides the first analysis of a cysteine protease from the digestive fluid of a carnivorous plant and confirms the close relationship between carnivorous action and plant defense mechanisms.

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Abundance of Cysteine Endopeptidase Dionain in Digestive Fluid of Venus Flytrap (Dionaea muscipula Ellis) Is Regulated by Different Stimuli from Prey through Jasmonates

Cited by 49 publications

References 72 publications

Venus flytrap carnivorous lifestyle builds on herbivore defense strategies

Venus flytrap carnivorous lifestyle builds on herbivore defense strategies

Long-read sequencing uncovers the adaptive topography of a carnivorous plant genome

Enzymatic and Structural Characterization of the Major Endopeptidase in the Venus Flytrap Digestion Fluid

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