The Protein Composition of the Digestive Fluid from the Venus Flytrap Sheds Light on Prey Digestion Mechanisms

Schulze WX, Sanggaard KW, Kreuzer I, Knudsen AD, Bemm F, Thogersen IB, Bräutigam A, Thomsen LR, Schliesky S, Dyrlund TF, Escalante-Perez M, et al. (2012)
Molecular & Cellular Proteomics 11(11): 1306-1319.

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Abstract / Bemerkung
The Venus flytrap (Dionaea muscipula) is one of the most well-known carnivorous plants because of its unique ability to capture small animals, usually insects or spiders, through a unique snap-trapping mechanism. The animals are subsequently killed and digested so that the plants can assimilate nutrients, as they grow in mineral-deficient soils. We deep sequenced the cDNA from Dionaea traps to obtain transcript libraries, which were used in the mass spectrometry-based identification of the proteins secreted during digestion. The identified proteins consisted of peroxidases, nucleases, phosphatases, phospholipases, a glucanase, chitinases, and proteolytic enzymes, including four cysteine proteases, two aspartic proteases, and a serine carboxypeptidase. The majority of the most abundant proteins were categorized as pathogenesis-related proteins, suggesting that the plant's digestive system evolved from defense-related processes. This in-depth characterization of a highly specialized secreted fluid from a carnivorous plant provides new information about the plant's prey digestion mechanism and the evolutionary processes driving its defense pathways and nutrient acquisition. Molecular & Cellular Proteomics 11: 10.1074/mcp.M112.021006, 1306-1319, 2012.
Molecular & Cellular Proteomics


Schulze WX, Sanggaard KW, Kreuzer I, et al. The Protein Composition of the Digestive Fluid from the Venus Flytrap Sheds Light on Prey Digestion Mechanisms. Molecular & Cellular Proteomics. 2012;11(11):1306-1319.
Schulze, W. X., Sanggaard, K. W., Kreuzer, I., Knudsen, A. D., Bemm, F., Thogersen, I. B., Bräutigam, A., et al. (2012). The Protein Composition of the Digestive Fluid from the Venus Flytrap Sheds Light on Prey Digestion Mechanisms. Molecular & Cellular Proteomics, 11(11), 1306-1319. doi:10.1074/mcp.M112.021006
Schulze, W. X., Sanggaard, K. W., Kreuzer, I., Knudsen, A. D., Bemm, F., Thogersen, I. B., Bräutigam, A., Thomsen, L. R., Schliesky, S., Dyrlund, T. F., et al. (2012). The Protein Composition of the Digestive Fluid from the Venus Flytrap Sheds Light on Prey Digestion Mechanisms. Molecular & Cellular Proteomics 11, 1306-1319.
Schulze, W.X., et al., 2012. The Protein Composition of the Digestive Fluid from the Venus Flytrap Sheds Light on Prey Digestion Mechanisms. Molecular & Cellular Proteomics, 11(11), p 1306-1319.
W.X. Schulze, et al., “The Protein Composition of the Digestive Fluid from the Venus Flytrap Sheds Light on Prey Digestion Mechanisms”, Molecular & Cellular Proteomics, vol. 11, 2012, pp. 1306-1319.
Schulze, W.X., Sanggaard, K.W., Kreuzer, I., Knudsen, A.D., Bemm, F., Thogersen, I.B., Bräutigam, A., Thomsen, L.R., Schliesky, S., Dyrlund, T.F., Escalante-Perez, M., Becker, D., Schultz, J., Karring, H., Weber, A., Hojrup, P., Hedrich, R., Enghild, J.J.: The Protein Composition of the Digestive Fluid from the Venus Flytrap Sheds Light on Prey Digestion Mechanisms. Molecular & Cellular Proteomics. 11, 1306-1319 (2012).
Schulze, Waltraud X., Sanggaard, Kristian W., Kreuzer, Ines, Knudsen, Anders D., Bemm, Felix, Thogersen, Ida B., Bräutigam, Andrea, Thomsen, Line R., Schliesky, Simon, Dyrlund, Thomas F., Escalante-Perez, Maria, Becker, Dirk, Schultz, Joerg, Karring, Henrik, Weber, Andreas, Hojrup, Peter, Hedrich, Rainer, and Enghild, Jan J. “The Protein Composition of the Digestive Fluid from the Venus Flytrap Sheds Light on Prey Digestion Mechanisms”. Molecular & Cellular Proteomics 11.11 (2012): 1306-1319.
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33 Zitationen in Europe PMC

Daten bereitgestellt von Europe PubMed Central.

Discovery of digestive enzymes in carnivorous plants with focus on proteases.
Ravee R, Mohd Salleh F', Goh HH., PeerJ 6(), 2018
PMID: 29888132
3D electron tomographic and biochemical analysis of ER, Golgi and trans Golgi network membrane systems in stimulated Venus flytrap (Dionaea muscipula) glandular cells.
Gergely ZR, Martinez DE, Donohoe BS, Mogelsvang S, Herder R, Staehelin LA., J Biol Res (Thessalon) 25(), 2018
PMID: 30116723
Molecular characterization and evolution of carnivorous sundew (Drosera rotundifolia L.) class V β-1,3-glucanase.
Michalko J, Renner T, Mészáros P, Socha P, Moravčíková J, Blehová A, Libantová J, Polóniová Z, Matušíková I., Planta 245(1), 2017
PMID: 27580619
Structural and functional characterisation of a class I endochitinase of the carnivorous sundew (Drosera rotundifolia L.).
Jopcik M, Moravcikova J, Matusikova I, Bauer M, Rajninec M, Libantova J., Planta 245(2), 2017
PMID: 27761648
The role of electrical and jasmonate signalling in the recognition of captured prey in the carnivorous sundew plant Drosera capensis.
Krausko M, Perutka Z, Šebela M, Šamajová O, Šamaj J, Novák O, Pavlovič A., New Phytol 213(4), 2017
PMID: 27933609
The carnivorous Venus flytrap uses prey-derived amino acid carbon to fuel respiration.
Fasbender L, Maurer D, Kreuzwieser J, Kreuzer I, Schulze WX, Kruse J, Becker D, Alfarraj S, Hedrich R, Werner C, Rennenberg H., New Phytol 214(2), 2017
PMID: 28042877
Insect haptoelectrical stimulation of Venus flytrap triggers exocytosis in gland cells.
Scherzer S, Shabala L, Hedrich B, Fromm J, Bauer H, Munz E, Jakob P, Al-Rascheid KAS, Kreuzer I, Becker D, Eiblmeier M, Rennenberg H, Shabala S, Bennett M, Neher E, Hedrich R., Proc Natl Acad Sci U S A 114(18), 2017
PMID: 28416693
Long-read sequencing uncovers the adaptive topography of a carnivorous plant genome.
Lan T, Renner T, Ibarra-Laclette E, Farr KM, Chang TH, Cervantes-Pérez SA, Zheng C, Sankoff D, Tang H, Purbojati RW, Putra A, Drautz-Moses DI, Schuster SC, Herrera-Estrella L, Albert VA., Proc Natl Acad Sci U S A 114(22), 2017
PMID: 28507139
Dynamics of amino acid redistribution in the carnivorous Venus flytrap (Dionaea muscipula) after digestion of 13 C/15 N-labelled prey.
Kruse J, Gao P, Eibelmeier M, Alfarraj S, Rennenberg H., Plant Biol (Stuttg) 19(6), 2017
PMID: 28727249
Complementary Proteomic and Biochemical Analysis of Peptidases in Lobster Gastric Juice Uncovers the Functional Role of Individual Enzymes in Food Digestion.
Bibo-Verdugo B, O'Donoghue AJ, Rojo-Arreola L, Craik CS, García-Carreño F., Mar Biotechnol (NY) 18(2), 2016
PMID: 26613762
Enzymatic and Structural Characterization of the Major Endopeptidase in the Venus Flytrap Digestion Fluid.
Risør MW, Thomsen LR, Sanggaard KW, Nielsen TA, Thøgersen IB, Lukassen MV, Rossen L, Garcia-Ferrer I, Guevara T, Scavenius C, Meinjohanns E, Gomis-Rüth FX, Enghild JJ., J Biol Chem 291(5), 2016
PMID: 26627834
The Venus Flytrap Dionaea muscipula Counts Prey-Induced Action Potentials to Induce Sodium Uptake.
Böhm J, Scherzer S, Krol E, Kreuzer I, von Meyer K, Lorey C, Mueller TD, Shabala L, Monte I, Solano R, Al-Rasheid KA, Rennenberg H, Shabala S, Neher E, Hedrich R., Curr Biol 26(3), 2016
PMID: 26804557
Proteome analysis of digestive fluids in Nepenthes pitchers.
Rottloff S, Miguel S, Biteau F, Nisse E, Hammann P, Kuhn L, Chicher J, Bazile V, Gaume L, Mignard B, Hehn A, Bourgaud F., Ann Bot 117(3), 2016
PMID: 26912512
Venus flytrap carnivorous lifestyle builds on herbivore defense strategies.
Bemm F, Becker D, Larisch C, Kreuzer I, Escalante-Perez M, Schulze WX, Ankenbrand M, Van de Weyer AL, Krol E, Al-Rasheid KA, Mithöfer A, Weber AP, Schultz J, Hedrich R., Genome Res 26(6), 2016
PMID: 27197216
Characterization of the gila monster (Heloderma suspectum suspectum) venom proteome.
Sanggaard KW, Dyrlund TF, Thomsen LR, Nielsen TA, Brøndum L, Wang T, Thøgersen IB, Enghild JJ., J Proteomics 117(), 2015
PMID: 25603280
Carnivorous plants.
Hedrich R., Curr Biol 25(3), 2015
PMID: 25649824
Fluid physico-chemical properties influence capture and diet in Nepenthes pitcher plants.
Bazile V, Le Moguédec G, Marshall DJ, Gaume L., Ann Bot 115(4), 2015
PMID: 25672361
Transcriptome and genome size analysis of the Venus flytrap.
Jensen MK, Vogt JK, Bressendorff S, Seguin-Orlando A, Petersen M, Sicheritz-Pontén T, Mundy J., PLoS One 10(4), 2015
PMID: 25886597
Calcium sensor kinase activates potassium uptake systems in gland cells of Venus flytraps.
Scherzer S, Böhm J, Krol E, Shabala L, Kreuzer I, Larisch C, Bemm F, Al-Rasheid KA, Shabala S, Rennenberg H, Neher E, Hedrich R., Proc Natl Acad Sci U S A 112(23), 2015
PMID: 25997445
Discovering New Biology through Sequencing of RNA.
Weber AP., Plant Physiol 169(3), 2015
PMID: 26353759
Strategy of nitrogen acquisition and utilization by carnivorous Dionaea muscipula.
Kruse J, Gao P, Honsel A, Kreuzwieser J, Burzlaff T, Alfarraj S, Hedrich R, Rennenberg H., Oecologia 174(3), 2014
PMID: 24141381
Secreted major Venus flytrap chitinase enables digestion of Arthropod prey.
Paszota P, Escalante-Perez M, Thomsen LR, Risør MW, Dembski A, Sanglas L, Nielsen TA, Karring H, Thøgersen IB, Hedrich R, Enghild JJ, Kreuzer I, Sanggaard KW., Biochim Biophys Acta 1844(2), 2014
PMID: 24275507
Mechano-stimulation triggers turgor changes associated with trap closure in the Darwin plant Dionaea muscipula.
Escalante-Pérez M, Scherzer S, Al-Rasheid KA, Döttinger C, Neher E, Hedrich R., Mol Plant 7(4), 2014
PMID: 24285093
Open stomata 1 (OST1) kinase controls R-type anion channel QUAC1 in Arabidopsis guard cells.
Imes D, Mumm P, Böhm J, Al-Rasheid KA, Marten I, Geiger D, Hedrich R., Plant J 74(3), 2013
PMID: 23452338
Glucan-rich diet is digested and taken up by the carnivorous sundew (Drosera rotundifolia L.): implication for a novel role of plant β-1,3-glucanases.
Michalko J, Socha P, Mészáros P, Blehová A, Libantová J, Moravčíková J, Matušíková I., Planta 238(4), 2013
PMID: 23832529
The Dionaea muscipula ammonium channel DmAMT1 provides NH₄⁺ uptake associated with Venus flytrap's prey digestion.
Scherzer S, Krol E, Kreuzer I, Kruse J, Karl F, von Rüden M, Escalante-Perez M, Müller T, Rennenberg H, Al-Rasheid KA, Neher E, Hedrich R., Curr Biol 23(17), 2013
PMID: 23954430
S-like ribonuclease gene expression in carnivorous plants.
Nishimura E, Kawahara M, Kodaira R, Kume M, Arai N, Nishikawa J, Ohyama T., Planta 238(5), 2013
PMID: 23959189

57 References

Daten bereitgestellt von Europe PubMed Central.

Darwin C.., 1875
Evolving Darwin's 'most wonderful' plant: ecological steps to a snap-trap.
Gibson TC, Waller DM., New Phytol. 183(3), 2009
PMID: 19573135
How the Venus flytrap snaps.
Forterre Y, Skotheim JM, Dumais J, Mahadevan L., Nature 433(7024), 2005
PMID: 15674293
Active movements in plants: Mechanism of trap closure by Dionaea muscipula Ellis.
Markin VS, Volkov AG, Jovanov E., Plant Signal Behav 3(10), 2008
PMID: 19513230
Trap-closing chemical factors of the Venus flytrap (Dionaea muscipulla Ellis).
Ueda M, Tokunaga T, Okada M, Nakamura Y, Takada N, Suzuki R, Kondo K., Chembiochem 11(17), 2010
PMID: 20963745
Leaf closure in the venus flytrap: an Acid growth response.
Williams SE, Bennett AB., Science 218(4577), 1982
PMID: 17752873
A special pair of phytohormones controls excitability, slow closure, and external stomach formation in the Venus flytrap.
Escalante-Perez M, Krol E, Stange A, Geiger D, Al-Rasheid KA, Hause B, Neher E, Hedrich R., Proc. Natl. Acad. Sci. U.S.A. 108(37), 2011
PMID: 21896747
Electrical memory in Venus flytrap.
Volkov AG, Carrell H, Baldwin A, Markin VS., Bioelectrochemistry 75(2), 2009
PMID: 19356999
Victims of the Venus flytrap
Griggs R.., 1935
Prey capture and factors controlling trap narrowing in Dionaea (Droseraceae)
Lichtner F., Williams S.., 1977
Mineral nutrition of carnivorous plants: a review
Adamec L.., 1997
Comparative studies on the acid proteinase activiteis in the digestive fluids of NEPENTHES, CEPHALOTOUS, DIONAEA, and DROSERA
Takahashi K., Matsumoto K., Nishi W., Muramatsu M., Kubota K.., 2009
The secretory cycle of Dionaea-muscipula ellis. IV. The enzymology of the secretion
Robins R., Juniper B.., 1980
Digestive Secretion of Dionaea muscipula (Venus's Flytrap).
Scala J, Iott K, Schwab DW, Semersky FE., Plant Physiol. 44(3), 1969
PMID: 16657071
A cysteine endopeptidase (“dionain”) is involved in the digestive fluid of Dionaea muscipula (Venus's fly-trap)
Takahashi K., Suzuki T., Nishii W., Kubota K., Shibata C., Isobe T., Dohmae N.., 2011
Dissection of symbiosis and organ development by integrated transcriptome analysis of lotus japonicus mutant and wild-type plants.
Hogslund N, Radutoiu S, Krusell L, Voroshilova V, Hannah MA, Goffard N, Sanchez DH, Lippold F, Ott T, Sato S, Tabata S, Liboriussen P, Lohmann GV, Schauser L, Weiller GF, Udvardi MK, Stougaard J., PLoS ONE 4(8), 2009
PMID: 19662091
CrossWork: software-assisted identification of cross-linked peptides.
Rasmussen MI, Refsgaard JC, Peng L, Houen G, Hojrup P., J Proteomics 74(10), 2011
PMID: 21600323
Probability-based protein identification by searching sequence databases using mass spectrometry data.
Perkins DN, Pappin DJ, Creasy DM, Cottrell JS., Electrophoresis 20(18), 1999
PMID: 10612281
Poplar extrafloral nectaries: two types, two strategies of indirect defenses against herbivores.
Escalante-Perez M, Jaborsky M, Lautner S, Fromm J, Muller T, Dittrich M, Kunert M, Boland W, Hedrich R, Ache P., Plant Physiol. 159(3), 2012
PMID: 22573802
Analysis of protein and peptide mixtures—evaluation of three sodium dodecyl sulfate-polyacrylamide gel-electrophoresis buffer systems
Bury A.., 1981
In-gel digestion for mass spectrometric characterization of proteins and proteomes.
Shevchenko A, Tomas H, Havlis J, Olsen JV, Mann M., Nat Protoc 1(6), 2006
PMID: 17406544
The TSG-6 and I alpha I interaction promotes a transesterification cleaving the protein-glycosaminoglycan-protein (PGP) cross-link.
Sanggaard KW, Karring H, Valnickova Z, Thogersen IB, Enghild JJ., J. Biol. Chem. 280(12), 2005
PMID: 15653696
Global quantification of mammalian gene expression control.
Schwanhausser B, Busse D, Li N, Dittmar G, Schuchhardt J, Wolf J, Chen W, Selbach M., Nature 473(7347), 2011
PMID: 21593866
MEROPS: the peptidase database.
Rawlings ND, Barrett AJ, Bateman A., Nucleic Acids Res. 38(Database issue), 2009
PMID: 19892822
Significance of inducible defense-related proteins in infected plants.
van Loon LC, Rep M, Pieterse CM., Annu Rev Phytopathol 44(), 2006
PMID: 16602946
Proteome analysis of pitcher fluid of the carnivorous plant Nepenthes alata.
Hatano N, Hamada T., J. Proteome Res. 7(2), 2008
PMID: 18183948
Molecular characterization of a senescence-associated gene encoding cysteine proteinase and its gene expression during leaf senescence in sweet potato.
Chen GH, Huang LT, Yap MN, Lee RH, Huang YJ, Cheng MC, Chen SC., Plant Cell Physiol. 43(9), 2002
PMID: 12354916
Effect of pH upon proteolysis by papain.
HOOVER SR, KOKES EL., J. Biol. Chem. 167(1), 1947
PMID: 20281639
Processing of the papain precursor. The ionization state of a conserved amino acid motif within the Pro region participates in the regulation of intramolecular processing.
Vernet T, Berti PJ, de Montigny C, Musil R, Tessier DC, Menard R, Magny MC, Storer AC, Thomas DY., J. Biol. Chem. 270(18), 1995
PMID: 7738022
Cathepsin L1, the major protease involved in liver fluke (Fasciola hepatica) virulence: propetide cleavage sites and autoactivation of the zymogen secreted from gastrodermal cells.
Collins PR, Stack CM, O'Neill SM, Doyle S, Ryan T, Brennan GP, Mousley A, Stewart M, Maule AG, Dalton JP, Donnelly S., J. Biol. Chem. 279(17), 2004
PMID: 14754899
Enzymic and structural characterization of nepenthesin, a unique member of a novel subfamily of aspartic proteinases.
Athauda SB, Matsumoto K, Rajapakshe S, Kuribayashi M, Kojima M, Kubomura-Yoshida N, Iwamatsu A, Shibata C, Inoue H, Takahashi K., Biochem. J. 381(Pt 1), 2004
PMID: 15035659
Nepenthesin, a unique member of a novel subfamily of aspartic proteinases: enzymatic and structural characteristics.
Takahashi K, Athauda SB, Matsumoto K, Rajapakshe S, Kuribayashi M, Kojima M, Kubomura-Yoshida N, Iwamatsu A, Shibata C, Inoue H., Curr. Protein Pept. Sci. 6(6), 2005
PMID: 16381601
Structural basis for inhibition of Aspergillus niger xylanase by triticum aestivum xylanase inhibitor-I. J
Sansen S., De C., Gebruers K., Brijs K., Courtin C., Delcour J., Rabijns A.., 2004
Isolation and characterization of carboxypeptidase III from germinating triticale grains.
Drzymala A, Bielawski W., Acta Biochim. Biophys. Sin. (Shanghai) 41(1), 2009
PMID: 19129952
Mechanism of antifeedant activity of plumbagin, a compound concerning the chemical defense in carnivorous plant
Tokunaga T., Takada N., Ueda M.., 2004
The secretory cycle of Dionaea-muscipula ellis. II. Storage and synthesis of the secretory proteins
Robins R., Juniper B.., 1980
Next-generation DNA sequencing
Shendure J., Ji H.., 2008
RNA-Seq: a revolutionary tool for transcriptomics.
Wang Z, Gerstein M, Snyder M., Nat. Rev. Genet. 10(1), 2009
PMID: 19015660
Whole transcriptome analysis of the fasting and fed Burmese python heart: insights into extreme physiological cardiac adaptation.
Wall CE, Cozza S, Riquelme CA, McCombie WR, Heimiller JK, Marr TG, Leinwand LA., Physiol. Genomics 43(2), 2010
PMID: 21045117
Digestive proteases of blood-feeding nematodes.
Williamson AL, Brindley PJ, Knox DP, Hotez PJ, Loukas A., Trends Parasitol. 19(9), 2003
PMID: 12957519
A multienzyme network functions in intestinal protein digestion by a platyhelminth parasite.
Delcroix M, Sajid M, Caffrey CR, Lim KC, Dvorak J, Hsieh I, Bahgat M, Dissous C, McKerrow JH., J. Biol. Chem. 281(51), 2006
PMID: 17028179
Cellular proteolysis. An overview.
Barrett AJ., Ann. N. Y. Acad. Sci. 674(), 1992
PMID: 1288356
Carnivorous pitcher plant uses free radicals in the digestion of prey.
Chia TF, Aung HH, Osipov AN, Goh NK, Chia LS., Redox Rep. 9(5), 2004
PMID: 15606978
Carnivorous pitcher plants: insights in an old topic.
Mithofer A., Phytochemistry 72(13), 2010
PMID: 21185041
Oases: robust de novo RNA-seq assembly across the dynamic range of expression levels
Schulz M., Zerbino D., Vingron M., Birney E.., 2012
MS Data Miner: a web-based software tool to analyze, compare and share mass spectrometry protein identifications
Dyrlund T., Poulsen E., Scavenius C., Sanggaard K., Enghild J.., 2012


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