Is the co-option of jasmonate signalling for botanical carnivory a universal trait for all carnivorous plants?

. 2024 Jan 01 ; 75 (1) : 334-349.

Jazyk angličtina Země Anglie, Velká Británie Médium print

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid37708289

Grantová podpora
MZE-RO0423 Ministry of Agriculture of the Czech Republic

The carnivorous plants in the order Caryophyllales co-opted jasmonate signalling from plant defence to botanical carnivory. However, carnivorous plants have at least 11 independent origins, and here we ask whether jasmonate signalling has been co-opted repeatedly in different evolutionary lineages. We experimentally wounded and fed the carnivorous plants Sarracenia purpurea (order Ericales), Cephalotus follicularis (order Oxalidales), Drosophyllum lusitanicum (order Caryophyllales), and measured electrical signals, phytohormone tissue level, and digestive enzymes activity. Coronatine was added exogenously to confirm the role of jasmonates in the induction of digestive process. Immunodetection of aspartic protease and proteomic analysis of digestive fluid was also performed. We found that prey capture induced accumulation of endogenous jasmonates only in D. lusitanicum, in accordance with increased enzyme activity after insect prey or coronatine application. In C. follicularis, the enzyme activity was constitutive while in S. purpurea was regulated by multiple factors. Several classes of digestive enzymes were identified in the digestive fluid of D. lusitanicum. Although carnivorous plants from different evolutionary lineages use the same digestive enzymes, the mechanism of their regulation differs. All investigated genera use jasmonates for their ancient role, defence, but jasmonate signalling has been co-opted for botanical carnivory only in some of them.

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Adamec L, Matušíková I, Pavlovič A.. 2021. Recent ecophysiological, biochemical and evolutional insights into plant carnivory. Annals of Botany 128, 241–259. PubMed PMC

Adlassnig W, Peroutka M, Lendl T.. 2011. Traps of carnivorous pitcher plants as a habitat: composition of the fluid, biodiversity and mutualistic activities. Annals of Botany 107, 181–194. PubMed PMC

An J-P, Xu R-R, Liu X, Zhang J-C, Wang X-F, You C-X, Hao Y-J.. 2021. Jasmonate induces biosynthesis of anthocyanin and proanthocyanidin in apple by mediating the JAZ1–TRB1–MYB9 complex. The Plant Journal 106, 1414–1430. PubMed

Anderson B. 2005. Adaptations to foliar absorption of faeces: a pathway in plant carnivory. Annals of Botany 95, 757–761. PubMed PMC

Athauda SB, Matsumoto K, Rajapakshe S, Kuribayashi M, Kojima M, Kubomura-Yoshida N, Iwamatsu A, Shibata C, Inoue H, Takahashi K.. 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 defence strategies. Genome Research 26, 812–825. PubMed PMC

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

Böhm J, Scherzer S, Shabala S, Krol E, Neher E, Mueller TD, Hedrich R.. 2016b. Venus flytrap HKT1-type channel provides for prey sodium uptake into carnivorous plant without conflicting with electrical excitability. Molecular Plant 9, 428–436. PubMed PMC

Buch F, Kaman WE, Bikker FJ, Yilamujiang A, Mithöfer A.. 2015. Nepenthesin protease activity indicates digestive fluid dynamics in carnivorous Nepenthes plants. PLoS One 10, e0118853. 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

Chamrád I, Simerský R, Bérešová L, Strnad M, Šebela M, Lenobel R.. 2014. Proteomic identification of a candidate sequence of wheat cytokinin-binding protein 1. Journal of Plant Growth Regulation 33, 896–902.

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

Chini A, Monte I, Zammareño AM, García-Mina JM, Solano R.. 2023. Evolution of the jasmonate ligands and their biosynthetic pathways. New Phytologist 238, 2236–2246. PubMed

Dávila-Lara A, Rahman-Soad A, Reichelt M, Mithöfer A.. 2021. Carnivorous Nepenthes × ventrata plants use a naphthoquinone as phytoanticipin against herbivory. PLoS One 16, e0258235. PubMed PMC

de Vries S, de Vries J.. 2020. Plant genome evolution: Meat lovers expanded gene families for carnivory and dropped the rest. Current Biology 30, R700–R702. PubMed

Ellis AG, Midgley JJ.. 1996. A new plant-animal mutualism involving a plant with sticky leaves and a resident hemipteran insect. Oecologia 106, 478–481. PubMed

Farmer EE, Gao Y-Q, Lenzon G, Wolfender J-C, Wu Q.. 2020. Wound- and mechanostimulated electrical signals control hormone responses. New Phytologist 227, 1037–1050. PubMed

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, 23–41.

Fonseca S, Chini A, Hamberg M, Adie B, Porzel A, Kramell R, Miersch O, Wasternack C, Solano R.. 2009. (+)-7-iso-Jasmonoyl-L-isoleucine is the endogenous bioactive jasmonate. Nature Chemical Biology 5, 344–350. 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, e0059. PubMed

Gallie DR, Chang SC.. 1997. Signal transduction in the carnivorous plant Sarracenia purpurea. Regulation of secretory hydrolase expression during development and in response to resources. Plant Physiology 115, 1461–1471. PubMed PMC

Gilroy S, Suzuki N, Miller G, Choi WG, Toyota M, Devireddy AR, Mittler R.. 2014. A tidal wave of signals: calcium and ROS at the forefront of rapid systemic signalling. Trends in Plant Science 19, 623–630. PubMed

Goh H-H, Baharin A, Salleh FIM, Ravee R, Wan Zakaria WNA, Noor NM.. 2020. Transcriptome-wide shift from photosynthesis and energy metabolism upon endogenous fluid protein depletion in young Nepenthes ampullaria pitchers. Scientific Reports 10, 6575. PubMed PMC

Green S, Green TL, Heslop-Harrison Y.. 1979. Seasonal heterophylly and leaf gland features in Triphyophyllum (Dioncophyllaceae), a new carnivorous plant genus. Botanical Journal of the Linnean Society 78, 99–116.

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

Jaffe K, Michelangeli F, Gonzalez JM, Miras B, Ruiz MC.. 1996. Carnivory in pitcher plants of the genus Heliamphora (Sarraceniaceae). New Phytologist 122, 733–744.

Jakšová J, Libiaková M, Bokor B, Petřík I, Novák O, Pavlovič A.. 2020. Taste for protein: chemical signal from prey stimulates enzyme secretion through jasmonate signalling in the carnivorous plant Venus fytrap. Plant Physiology and Biochemistry 146, 90–97. PubMed

Jakšová J, Novák O, Adamec L, Pavlovič A.. 2021. Contrasting effect of prey capture on jasmonate accumulation in two genera of aquatic carnivorous plants (Aldrovanda, Utricularia). Plant Physiology and Biochemistry 166, 459–465. PubMed

Kocáb O, Jakšová J, Novák O, Petřík I, Lenobel R, Chamrád I, Pavlovič A.. 2020. Jasmonate-independent regulation of digestive enzyme activity in the carnivorous butterwort Pinguicula × Tina. Journal of Experimental Botany 71, 3749–3758. PubMed PMC

Koller-Peroutka M, Krammer S, Pavlik A, Edlinger M, Lang I, Adlassnig W.. 2019. Endocytosis and digestion in carnivorous pitcher plants of the family Sarraceniaceae. Plants 8, 367. PubMed PMC

Koo AJK, Gao X, Jones AD, Howe AG.. 2009. A rapid wound signal activates the systemic synthesis of bioactive jasmonates in Arabidopsis. The Plant Journal 59, 974–986. PubMed

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

Lee L, Zhang Y, Ozar B, Sensen CW, Schriemer DC.. 2017. Carnivorous nutrition in pitcher plants (Nepenthes spp.) via an unusual complement of endogenous enzymes. Journal of Proteome Research 15, 3108–3117. PubMed

Li M, Wang F, Li S, Yu G, Wang L, Li Q, Zhu X, Li Z, Yuan L, Liu P.. 2020. Importers drive leaf-to-leaf jasmonic acid transmission in wound-induced systemic immunity. Molecular Plant 13, 1485–1498. PubMed

Li Y-X, Chen A, Leu W-M.. 2023. Sessile trichomes play major roles in prey digestion and absorption, while stalked trichomes function in prey predation in Byblis guehoi. International Journal of Molecular Sciences 24, 5305. PubMed PMC

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

Lin Q, Ané C, Givnish TJ, Graham SW.. 2021. A new carnivorous plant lineage (Triantha) with a unique sticky-inflorescence trap. Proceedings of the National Academy of Sciences, USA 118, e2022724118. PubMed PMC

Ljung K, Sandberg G, Moritz T.. 2010. Methods of plant hormone analysis. In: Davies PJ, ed. Plant hormones. Dordrecht: Springer, 717–740.

Luciano CS, Newell SJ.. 2017. Effects of prey, pitcher age, and microbes on acid phosphatase activity in fluid from pitchers of Sarracenia purpurea (Sarraceniaceae). PLoS One 12, e0181252. PubMed PMC

Matsumura M, Nomoto M, Itaya T, et al. . 2022. Mechanosensory trichome cells evoke a mechanical stimuli-induced immune response in Arabidopsis thaliana. Nature Communications 13, 1216. PubMed PMC

Matušíková I, Salaj J, Moravčíková 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

Miller G, Schlauch K, Tam R, Cortes D, Torres MA, Shualev V, Dangl JL, Mittler R.. 2009. The plant NADPH oxidase RBOHD mediates rapid systemic signalling in response to diverse stimuli. Science Signaling 2, ra45. PubMed

Mithöfer A. 2011. Carnivorous pitcher plants: insights in an old topic. Phytochemistry 72, 1678–1682. PubMed

Mithöfer A, Reichelt M, Nakamura Y.. 2014. Wound and insect-induced jasmonate accumulation in carnivorous Drosera capensis: two sides of the same coin. Plant Biology 16, 982–987. PubMed

Monte I, Ishida S, Zammareño AM.. 2018. Ligand-receptor co-evolution shaped the jasmonate pathway in land plants. Nature Chemical Biology 14, 480–488. PubMed

Mousavi SA, Chauvin A, Pascaud F, Kellenberger S, Farmer EE.. 2013. Glutamate receptor-like genes mediate leaf-to-leaf wound signalling. Nature 500, 422–426. PubMed

Murray JR, Hackett WP.. 1991. Dihydroflavonol reductase activity in relation to differential anthocyanin accumulation in juvenile and mature phase Hedera helix L. Plant Physiology 97, 343–351. PubMed PMC

Nakamura Y, Reichelt M, Mayer VE, Mithöfer A.. 2013. Jasmonates trigger prey-induced formation of ‘outer stomach’ in carnivorous sundew plants. Proceedings of 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

Palfalvi G, Hackl T, Terhoeven N, et al. . 2020. Genomes of the Venus flytrap and close relatives unveil the roots of plant carnivory. Current Biology 30, 2312–2320.e5. PubMed PMC

Pavlovič A. 2022. How the sensory system of carnivorous plants has evolved. Plant Communications 3, 100462. PubMed PMC

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, 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

Pavlovič A, Vrobel O, Tarkowski P.. 2023. Water cannot activate traps of the carnivorous sundew plant Drosera capensis: On the trail of Darwin’s 150-years-old mystery. Plants 12, 1820. PubMed PMC

Plachno B, Adamec L, Huet H.. 2009. Mineral nutrient uptake from prey and glandular phosphatase activity as a dual test of carnivory in semi-desert plants with glandular leaves suspected of carnivory. Annals of Botany 104, 649–654. PubMed PMC

Pratiwi P, Tanaka G, Takahashi T, Xie X, Yoneyama K, Matsuura H, Takahashi K.. 2017. Identification of jasmonic acid and jasmonoyl-isoleucine, and characterization of AOS, AOC, OPR and JAR1 in the model lycophyte Selaginella moellendorffii. Plant & Cell Physiology 58, 789–801. PubMed

Procko C, Radin I, Hou C, Richardson RA, Haswell ES, Chory J.. 2022. Dynamic calcium signals mediate the feeding response of the carnivorous sundew plant. Proceedings of the National Academy of Sciences, USA 119, e2206433119. PubMed PMC

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

Rembold K, Irmer A, Poppinga S, Rischer H, Bringmann G.. 2010. Propagation of Triphyophyllum peltatum (Dioncophyllaceae) and observations on its carnivory. Carnivorous Plant Newsletter 39, 71–77.

Renner T, Lan T, Farr KM, Ibarra-Laclette E, Herrera-Estrella L, Schuster SC, Hasebe M, Fukushima K, Albert VA.. 2018. In: Ellison AM, Adamec L, eds. Carnivorous plants: physiology, ecology, and evolution. Oxford: Oxford University Press, 135–153.

Renner T, Specht CD.. 2011. A sticky situation: assessing adaptations for plant carnivory in the Caryophyllales by means of stochastic character mapping. International Journal of Plant Sciences 172, 889–901.

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 & Cellular Proteomics 11, 1306–1319. PubMed PMC

Shan X, Zhang Y, Peng W, Wang Z, Xie D.. 2009. Molecular mechanism for jasmonate-induction of anthocyanin accumulation in Arabidopsis. Journal of Experimental Botany 60, 3849–3860. 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

Sims DA, Gamon JA.. 2002. Relationships between leaf pigment content and spectral reflectance across a wide range of species, leaf structures and developmental stages. Remote Sensing and Environment 81, 337–354.

Šimura J, Antoniadi I, Široká J, Tarkowská D, Strnad M, Ljung K, Novák O.. 2018. Plant hormonomics: Multiple phytohormone profiling by targeted metabolomics. Plant Physiology 177, 476–489. PubMed PMC

Sun G, Xu Y, Liu H, et al. . 2018. Large-scale gene losses underlie the genome evolution of parasitic plant Cuscuta australis. Nature Communications 9, 2683. PubMed PMC

Suzuki N, Miller G, Salazar C, et al. . 2013. Temporal–spatial interaction between reactive oxygen species and abscisic acid regulates rapid systemic acclimation in plants. The Plant Cell 25, 3553–3569. PubMed PMC

Takahashi K, Matsumoto K, Nishii 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, Niu Y, Mandaokar A, Liu G, Nomura K, He SY, Howe GA, Browse J.. 2007. JAZ repressor proteins are targets of the SCFCOI1 complex during jasmonate signalling. Nature 448, 661–665. PubMed

Toyota M, Spencer D, Sawai-Toyota S, Jiaqi W, Zhang T, Koo AJ, Howe GA, Gilroy S.. 2018. Glutamate triggers long-distance, calcium-based plant defence signalling. Science 361, 1112–1115. PubMed

Tran NH, Qiao R, Xin L, Chen X, Liu C, Zhang X, Shan B, Ghodsi A, Li M.. 2018. Deep learning enables de novo peptide sequencing from data-independent-acquisition mass spectrometry. Nature Methods 16, 63–66. PubMed

Vadassery J, Ballhorn DJ, Fleming SR, Mazars C, Pandey SP, Schmidt A, Schuman MC, Yeh K-W, Yilamujiang A, Mithöfer A.. 2019. Neomycin: an effective inhibitor of jasmonate-induced reactions in plants. Journal of Plant Growth Regulation 38, 713–722.

Vassilyev AE. 2005. Dynamics of ultrastructural characters of Drosophyllum lusitanicum Link (Droseraceae) digestive glands during maturation and after stimulation. Taiwania 50, 167–182.

Wan Zakaria WNA, Aizat WM, Goh HH, Mohd Noor N.. 2019. Protein replenishment in pitcher fluids of Nepenthes × ventrata revealed by quantitative proteomics (SWATH-MS) informed by transcriptomics. Journal of Plant Research 132, 681–694. PubMed

Wasternack C, Hause B.. 2013. Jasmonates: biosynthesis, perception, signal transduction and action in plant stress response, growth and development. An update to the 2007 review. Annals of Botany 111, 1021–1058. PubMed PMC

Williams SE. 1976. Comparative sensory physiology of the Droseraceae – the evolution of a plant sensory system. Proceedings of the American Philosophical Society 2, 187–204.

Williams SE, Pickard BG.. 1972. Properties of action potentials in Drosera tentacles. Planta 103, 222–240. PubMed

Winkelmann T, Bringmann G, Herwig A, Hedrich R.. 2023. Carnivory on demand: phosphorus deficiency induces glandular leaves in the African liana Triphyophyllum peltatum. New Phytologist 239, 1140–1152. PubMed

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, 369–375. PubMed PMC

Young EB, Sielicki J, Grothjan JJ.. 2018. Regulation of hydrolytic enzyme activity in aquatic microbial communities hosted by carnivorous pitcher plants. Microbial Ecology 76, 885–898. PubMed

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