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

. 2020 Jun 22 ; 71 (12) : 3749-3758.

Jazyk angličtina Země Anglie, Velká Británie Médium print

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid32219314

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.

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Albert VA, Williams SE, Chase MW. 1992. Carnivorous plants: phylogeny and structural evolution. Science 257, 1491–1495. PubMed

Athauda SB, Matsumoto K, Rajapakshe S, et al. . 2004. Enzymic and structural characterization of nepenthesin, a unique member of a novel subfamily of aspartic proteinases. Biochemical Journal 381, 295–306. PubMed PMC

Bemm F, Becker D, Larisch C, et al. . 2016. Venus flytrap carnivorous lifestyle builds on herbivore defense strategies. Genome Research 26, 812–825. PubMed PMC

Böhm J, Scherzer S, Krol E, et al. . 2016. The Venus flytrap Dionaea muscipula counts prey-induced action potentials to induce sodium uptake. Current Biology 26, 286–295. PubMed PMC

Candiano G, Bruschi M, Musante L, Santucci L, Ghiggeri GM, Carnemolla B, Orecchia P, Zardi L, Righetti PG. 2004. Blue silver: a very sensitive colloidal Coomassie G-250 staining for proteome analysis. Electrophoresis 25, 1327–1333. PubMed

Chi H, Sun RX, Yang B, et al. . 2010. pNovo: de novo peptide sequencing and identification using HCD spectra. Journal of Proteome Research 9, 2713–2724. PubMed

Chini A, Fonseca S, Fernández G, et al. . 2007. The JAZ family of repressors is the missing link in jasmonate signalling. Nature 448, 666–671. PubMed

Darwin C. 1875. Insectivorous plants. London: John Murray.

Eilenberg H, Pnini-Cohen S, Schuster S, Movtchan A, Zilberstein A. 2006. Isolation and characterization of chitinase genes from pitchers of the carnivorous plant Nepenthes khasiana. Journal of Experimental Botany 57, 2775–2784. PubMed

Escalante-Pérez M, Krol E, Stange A, Geiger D, Al-Rasheid KA, Hause B, Neher E, Hedrich R. 2011. A special pair of phytohormones controls excitability, slow closure, and external stomach formation in the Venus flytrap. Proceedings of the National Academy of Sciences, USA 108, 15492–15497. PubMed PMC

Fleischman A, Roccia A. 2018. Systematics and evolution of Lentibulariaceae: I. Pinguicula. In: Ellison AM, Adamec L, eds. Carnivorous plants. Physiology, ecology, and evolution. Oxford: Oxford University Press, 70–80.

Fleischmann A, Schlauer J, Smith SA, Givnish TJ. 2018. Evolution of carnivory in angiosperms. In: Ellison AM, Adamec L, eds. Carnivorous plants. Physiology, ecology, and evolution. Oxford: Oxford University Press, 22–41.

Floková K, Tarkowská D, Miersch O, Strnad M, Wasternack C, Novák O. 2014. UHPLC-MS/MS based target profiling of stress-induced phytohormones. Phytochemistry 105, 147–157. PubMed

Fonseca S, Chini A, Hamberg M, Adie B, Porzel A, Kramell R, Miersch O, Wasternack C, Solano R. 2009. (+)-7-iso-Jasmonyl-l-isoleucine is the endogenous bioactive jasmonate. Nature Chemical Biology 5, 344–350. PubMed

Frank A, Pevzner P. 2005. PepNovo: de novo peptide sequencing via probabilistic network modeling. Analytical Chemistry 77, 964–973. PubMed

Fukushima K, Fang X, Alvarez-Ponce D, et al. . 2017. Genome of the pitcher plant Cephalotus reveals genetic changes associated with carnivory. Nature Ecology Evolution 1, 0059. PubMed

Gallie DR, Chang SC. 1997. Signal transduction in the carnivorous plant Sarracenia purpurea. Plant Physiology 115, 1461–1471. PubMed PMC

Givnish TJ. 2015. New evidence on the origin of carnivorous plants. Proceedings of the National Academy of Sciences, USA 112, 10–11. PubMed PMC

Hanslin HM, Karlsson PS. 1996. Nitrogen uptake from prey and substrate as affected by prey capture level and plant reproductive status in four carnivorous plant species. Oecologia 106, 370–375. PubMed

Harder R, Zemlin I. 1968. Blütenbildung von Pinguicula lusitanica in vitro durch Fütterung mit pollen. Planta 78, 72–78. PubMed

Hatano N, Hamada T. 2008. Proteome analysis of pitcher fluid of the carnivorous plant Nepenthes alata. Journal of Proteome Research 7, 809–816. PubMed

Hatano N, Hamada T. 2012. Proteomic analysis of secreted protein induced by a component of prey in pitcher fluid of the carnivorous plant Nepenthes alata. Journal of Proteomics 75, 4844–4852. PubMed

Heslop-Harrison Y. 2004. Pinguicula L. Journal of Ecology 92, 1071–1118.

Heslop-Harrison Y, Heslop-Harrison J. 1980. Chloride ion movement and enzyme secretion from the digestive glands of Pinguicula. Annals of Botany 45, 729–731.

Heslop-Harrison Y, Heslop-Harrison J. 1981. The digestive glands of Pinguicula: structure and cytochemistry. Annals of Botany 47, 293–319.

Heslop-Harrison Y, Knox RB. 1971. A cytochemical study of the leaf-gland enzymes of insectivorous plants of the genus Pinguicula. Planta 96, 183–211. PubMed

Ilík P, Hlaváčková V, Krchňák P, Nauš J. 2010. A low-noise multichannel device for the monitoring of systemic electrical signal propagation in plants. Biologia Plantarum 54, 185–190.

Iriti M, Faoro F. 2008. Abscisic acid is involved in chitosan-induced resistance to tobacco necrosis virus (TNV). Plant Physiology and Biochemistry 46, 1106–1111. PubMed

Iriti M, Valentina Picchi V, Rossoni M, Gomarasca S, Ludwig N, Gargano M, Faoro F. 2009. Chitosan antitranspirant activity is due to abscisic acid-dependent stomatal closure. Environmental and Experimental Botany 66, 493–500.

Jakšová J, Libiaková M, Bokor B, Petřík I, Novák O, Pavlovič A. 2020. Taste for protein: chemical signal from prey activates jasmonate signalling in the carnivorous plant Venus flytrap (Dionaea muscipula Ellis). Plant Physiology and Biochemistry 146, 90–97. PubMed

Kim SC, Chen Y, Mirza S, Xu Y, Lee J, Liu P, Zhao Y. 2006. A clean, more efficient method for in-solution digestion of protein mixtures without detergent or urea. Journal of Proteome Research 5, 3446–3452. PubMed

Koller-Peroutka M, Lendl T, Watzka M, Adlassnig W. 2015. Capture of algae promotes growth and propagation in aquatic Utricularia. Annals of Botany 115, 227–236. PubMed PMC

Krausko M, Perutka Z, Šebela M, Šamajová O, Šamaj J, Novák O, Pavlovič A. 2017. The role of electrical and jasmonate signalling in the recognition of captured prey in the carnivorous sundew plant Drosera capensis. New Phytologist 213, 1818–1835. PubMed

Laemmli UK. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680–685. PubMed

Legendre L. 2000. The genus Pinguicula L. (Lentibulariaceae): an overview. Acta Botanica Gallica 147, 77–95.

Lee L, Zhang Y, Ozar B, Sensen CW, Schriemer DC. 2016. Carnivorous nutrition in pitcher plants (Nepenthes spp.) via an unusual complement of endogenous enzymes. Journal of Proteome Research 15, 3108–3117. PubMed

Libiaková M, Floková K, Novák O, Slováková L, Pavlovič A. 2014. Abundance of cysteine endopeptidase dionain in digestive fluid of Venus flytrap (Dionaea muscipula Ellis) is regulated by different stimuli from prey through jasmonates. PLoS One 9, e104424. PubMed PMC

Ma B. 2015. Novor: real-time peptide de novo sequencing software. Journal of the American Society for Mass Spectrometry 26, 1885–1894. PubMed PMC

Matušíková I, Salaj J, Moravcíková J, Mlynárová L, Nap JP, Libantová J. 2005. Tentacles of in vitro-grown round-leaf sundew (Drosera rotundifolia L.) show induction of chitinase activity upon mimicking the presence of prey. Planta 222, 1020–1027. PubMed

Michalko J, Renner T, Mészáros P, Socha P, Moravčíková J, Blehová A, Libantová J, Polóniová Z, Matušíková I. 2017. Molecular characterization and evolution of carnivorous sundew (Drosera rotundifolia L.) class V β-1,3-glucanase. Planta 245, 77–91. PubMed

Muth T, Weilnböck L, Rapp E, Huber CG, Martens L, Vaudel M, Barsnes H. 2014. DeNovoGUI: an open source graphical user interface for de novo sequencing of tandem mass spectra. Journal of Proteome Research 13, 1143–1146. PubMed PMC

Nakamura Y, Reichelt M, Mayer VE, Mithöfer A. 2013. Jasmonates trigger prey-induced formation of ‘outer stomach’ in carnivorous sundew plants. Proceedingsof the Royal Society B: Biological Sciences 280, 20130228. PubMed PMC

Nishimura E, Kawahara M, Kodaira R, Kume M, Arai N, Nishikawa J, Ohyama T. 2013. S-like ribonuclease gene expression in carnivorous plants. Planta 238, 955–967. PubMed

Pavlovič A, Jakšová J, Novák O. 2017. Triggering a false alarm: wounding mimics prey capture in the carnivorous Venus flytrap (Dionaea muscipula). New Phytologist 216, 927–938. PubMed

Pavlovič A, Libiaková M, Bokor B, Jakšová J, Petřík I, Novák O, Baluška F. 2020. Anaesthesia with diethyl ether impairs jasmonate signalling in the carnivorous plant Venus flytrap (Dionaea muscipula). Annals of Botany 125, 173–183. PubMed PMC

Pavlovič A, Mithöfer A. 2019. Jasmonate signalling in carnivorous plants: copycat of plant defence mechanisms. Journal of Experimental Botany 70, 3379–3389. PubMed

Pavlovič A, Saganová M. 2015. A novel insight into the cost–benefit model for the evolution of botanical carnivory. Annals of Botany 115, 1075–1092. PubMed PMC

Peroutka M, Adlassnig W, Volgger M, Lendl T, Url WG, Lichtscheidl IK. 2008. Utricularia: a vegetarian carnivorous plant? Plant Ecology 199, 153–162.

Plachno BJ, Wolowski K. 2008. Algae commensal community in Genlisea traps. Acta Societatis Botanicorum Poloniae 77, 77–86.

Rappsilber J, Mann M, Ishihama Y. 2008. Protocol for micro-purification, enrichment, pre-fractionation and storage of peptides for proteomics using StageTips. Nature Protocols 2, 1896–1906. PubMed

Rottloff S, Miguel S, Biteau F, et al. . 2016. Proteome analysis of digestive fluids in Nepenthes pitchers. Annals of Botany 117, 479–495. PubMed PMC

Rottloff S, Stieber R, Maischak H, Turini FG, Heubl G, Mithöfer A. 2011. Functional characterization of a class III acid endochitinase from the traps of the carnivorous pitcher plant genus, Nepenthes. Journal of Experimental Botany 62, 4639–4647. PubMed PMC

Saganová M, Bokor B, Stolárik T, Pavlovič A. 2018. Regulation of enzyme activities in carnivorous pitcher plants of the genus Nepenthes. Planta 248, 451–464. PubMed

Schägger H. 2006. Tricine-SDS-PAGE. Nature Protocols 1, 16–22. PubMed

Schulze WX, Sanggaard KW, Kreuzer I, et al. . 2012. The protein composition of the digestive fluid from the Venus flytrap sheds light on prey digestion mechanisms. Molecular and Cellular Proteomics 11, 1306–1319. PubMed PMC

Šebela M, Štosová T, Havlis J, Wielsch N, Thomas H, Zdráhal Z, Shevchenko A. 2006. Thermostable trypsin conjugates for high-throughput proteomics: synthesis and performance evaluation. Proteomics 6, 2959–2963. PubMed

Sheard LB, Tan X, Mao H, et al. . 2010. Jasmonate perception by inositol-phosphate-potentiated COI1-JAZ co-receptor. Nature 468, 400–405. PubMed PMC

Shevchenko A, Tomas H, Havlis J, Olsen JV, Mann M. 2006. In-gel digestion for mass spectrometric characterization of proteins and proteomes. Nature Protocols 1, 2856–2860. PubMed

Simerský R, Chamrád I, Kania J, Strnad M, Šebela M, Lenobel R. 2017. Chemical proteomic analysis of 6-benzylaminopurine molecular partners in wheat grains. Plant Cell Reports 36, 1561–1570. PubMed

Tabb DL, Ma ZQ, Martin DB, Ham AJ, Chambers MC. 2008. DirecTag: accurate sequence tags from peptide MS/MS through statistical scoring. Journal of Proteome Research 7, 3838–3846. PubMed PMC

Takahashi K, Matsumoto K, Nishi W, Muramatsu M, Kubota K, Shibata C, Athauda SBP. 2009. Comparative studies on the acid proteinase activities in the digestive fluids of Nepenthes, Cephalotus, Dionaea, and Drosera. Carnivorous Plant Newsletter 38, 75–82.

Takahashi K, Nishii W, Shibata C. 2012. The digestive fluid of Drosera indica contains a cysteine endopeptidase (“Droserain”) similar to dionain from Dionaea muscipula. Carnivorous Plant Newsletter 41, 132–134.

Thines B, Katsir L, Melotto M, et al. . 2007. JAZ repressor proteins are targets of the SCF (COI1) complex during jasmonate signalling. Nature 448, 661–665. PubMed

Vassilyev AE, Muravnik LE. 1988a. The ultrastructure of the digestive glands in Pinguicula vulgaris L. (Lentibulariaceae) relative to their function. I. The changes during maturation. Annals of Botany 62, 329–341.

Vassilyev AE, Muravnik LE. 1988b. The ultrastructure of the digestive glands in Pinguicula vulgaris L. (Lentibulariaceae) relative to their function. II. The changes on stimulation. Annals of Botany 61, 343–351.

Yilamujiang A, Reichelt M, Mithöfer A. 2016. Slow food: insect prey and chitin induce phytohormone accumulation and gene expression in carnivorous Nepenthes plants. Annals of Botany 118: 369–735. PubMed PMC

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