How the diversity in digestion in carnivorous plants may have evolved

. 2025 Sep ; 247 (6) : 2581-2590. [epub] 20250528

Jazyk angličtina Země Velká Británie, Anglie Médium print-electronic

Typ dokumentu časopisecké články, přehledy

Perzistentní odkaz   https://www.medvik.cz/link/pmid40433787

Carnivorous plants secrete digestive enzymes for prey degradation. Although carnivorous plants have a polyphyletic origin and evolved several times independently, they surprisingly co-opted similar digestive enzymes during convergent evolution. However, despite having similar digestive enzymes, the mode of their regulation strongly differs across different phylogenetic lineages. But what factors are responsible for such diversity in their digestion? By combining phylogenetic relationships of digestive fluid proteins and biochemical data, the analyses showed that phylogeny seems to be a significant factor determining the regulation of digestion, but environment (water vs terrestrial) and type of trap do not affect regulation. The oldest carnivorous plant lineage, Caryophyllales, co-opted phytohormone jasmonic acid (JA) for regulation of digestive enzyme activity. However, the remaining orders of carnivorous plants do not accumulate JA in response to prey capture, and their digestive enzyme activity is not responsive to exogenous JA application. Instead, they use different modes of regulation, for example, development/senescence, osmotically induced and constitutive. These different modes of regulation can be explained by co-option, albeit of similar genes but different paralogs with different cis regulatory elements that have been fine-tuned during evolution.

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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

Arai N, Ohno Y, Jumyo S, Hamaji Y, Ohyama T. 2021. Organ‐specific expression and epigenetic traits of genes encoding digestive enzymes in the lance‐leaf sundew ( 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, Kreuzer I, Escalante‐Perez M, Schulze WX, Ankenbrand M, Van de Weyer A‐L, Krol E, Al‐Rasheid KA PubMed PMC

Buch F, Kaman WE, Bikker FJ, Yilamujiang A, Mithöfer A. 2015. Nepenthesin protease activity indicates digestive fluid dynamics in carnivorous PubMed PMC

Cameron KM, Wurdack KJ, Jobson RW. 2002. Molecular evidence for the common origin of snap‐traps among carnivorous plants. American Journal of Botany 89: 1503–1509. PubMed

Chini A, Fonseca S, Fernández G, Adie B, Chico JM, Lorenzo O, García‐Casado G, López‐Vidriero I, Lozano FM, Ponce MR PubMed

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

Coronado‐Martín A, Martin‐Vásquez C, Jáquez M, Bahaji A, Atarés A. 2024. Micropropagation and genetic transformation of

Darwish E, Ghosh R, Ontiveros‐Cisneros A, Tran HC, Petersson M, De Milde L, Broda M, Goossens A, Van Moerkercke A, Khan K PubMed PMC

Dávila‐Lara A, Rahman‐Soad A, Reichelt M, Mithöfer A. 2021. Carnivorous PubMed PMC

Ding M, Zhou Y, Becker D, Yang S, Krischke M, Scherzer S, Yu‐Strzelczyk J, Mueller MJ, Hedrich R, Nagel G PubMed PMC

Doxey AC, Yaish MWF, Moffatt BA, Griffith M, McConkey BJ. 2007. Functional divergence in the PubMed

Doyle EA, Lane AM, Sides JM, Mudgett MB, Monroe JD. 2007. An alpha‐amylase (At4g25000) in PubMed

Eilenberg H, Pnini‐Cohen S, Schuster S, Movtchan A, Zilberstein A. 2006. Isolation and characterization of chitinase genes from pitchers of the carnivorous plant PubMed

Escalante‐Pérez M, Krol E, Stange A, Geiger D, Al‐Rasheid KAS, 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

Figueiredo L, Santos RB, Figueiredo A. 2021. Defense and offense strategies: the role of aspartic proteases in plant–pathogen interactions. Biology 10: 75. PubMed PMC

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, UK: 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

Frazier CK. 2000. The enduring controversies concerning the process of protein digestion in

Fukushima K, Fang X, Alvarez‐Ponce D, Cai H, Carretero‐Paulet L, Chen C, Chang T‐H, Farr KM, Fujita T, Hiwatashi Y PubMed

Gallie DR, Chang SC. 1997. Signal transduction in the carnivorous plant PubMed PMC

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 PubMed PMC

Häffner E, Konietzki S, Diederichsen E. 2015. Keeping control: the role of senescence and development in plant pathogenesis and defense. Plants 4: 449–488. PubMed PMC

Hatano N, Hamada T. 2008. Proteome analysis of pitcher fluid of the carnivorous plant PubMed

Hatano N, Hamada T. 2012. Proteomic analysis of secreted protein induced by a component of prey in pitcher fluid of the carnivorous plant PubMed

Hedrich R, Gilliham M. 2025. Light‐activated channelrhodopsins: a revolutionary toolkit for the remote control of plant signaling. New Phytologist 245: 982–988. PubMed

Heslop‐Harrison Y. 1975. Enzyme release in carnivorous plants. Frontiers in Biology 43: 525–578. PubMed

Heslop‐Harrison Y, Heslop‐Harrison J. 1980. Chloride ion movement and enzyme secretion from the digestive glands of

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

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 flytrap. 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

Jentsch J. 1972. Isolation of the protease Nepthacin. FEBS Letters 21: 273–276. PubMed

Jílková T. 2023. Under water: signalling in submerged carnivorous plants. Bachelor thesis, Palacký University in Olomouc, Czech Republic, Pp. 40.

Juniper BE, Robins RJ, Joel DM. 1989. The carnivorous plants. London, UK: Academic Press.

Kato Y, Murakami S, Yamamoto Y, Chatani H, Kondo Y, Nakano T, Yokota A, Sato F. 2004. The DNA‐binding protease, CND41, and the degradation of ribulose‐1,5‐bisphosphate carboxylase/oxygenase in senescent leaves of tobacco. Planta 220: 97–104. PubMed

Kimberlin AN, Holtsclaw RE, Zhang T, Mulaudzi T, Koo AJ. 2022. On the initiation of jasmonate biosynthesis in wounded leaves. Plant Physiology 189: 1925–1942. PubMed PMC

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 PubMed PMC

Koo AJK, Howe GA. 2009. The wound hormone jasmonate. Phytochemistry 70: 1571–1580. 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 PubMed

La Porta CAM, Lionetti MC, Bonfanti S, Milan S, Ferrario C, Rayneau‐Kirkhope D, Beretta M, Hanifpour M, Fascio U, Ascagni M PubMed PMC

Lan T, Renner T, Ibarra‐Laclette E, Farr KM, Chang T‐H, Cervantes‐Pérez SA, Zheng C, Sankoff D, Tang H, Purbojati RW PubMed PMC

Lee H‐J, Park J‐S, Shin SY, Kim S‐G, Lee G, Kim H‐S, Jeon JH, Cho HS. 2020. Submergence deactivates wound‐induced plant defence against herbivores. Communications Biology 3: 651. PubMed PMC

Lee L, Zhang Y, Ozar B, Sensen CW, Schriemer DC. 2016. Carnivorous nutrition in pitcher plants ( PubMed

Libantová J, Frátriková M, Jopcík M, Bauer M, Rajninec M. 2021. In silico characterization of β‐1,3‐glucanase promoter from

Libiaková M, Floková K, Novák O, Slováková L, Pavlovič A. 2014. Abundance of cysteine endopeptidase dionain in digestive fluid of Venus flytrap ( PubMed PMC

Lin Q, Ané C, Givnish TJ, Graham SW. 2021. A new carnivorous plant lineage ( PubMed PMC

Loon LC, Rep M, Pieterse CMJ. 2006. Significance of inducible defence‐related proteins in infected plants. Annual Review of Phytopathology 44: 135–162. PubMed

Matsumura M, Nomoto M, Itaya T, Aratani Y, Iwamoto M, Matsuura T, Hayashi Y, Mori T, Skelly MJ, Yamamoto YY PubMed PMC

Matušíková I, Salaj T, Moravčíková J, Mlynárová L, Nap J‐P, Libantová J. 2005. Tentacles of in vitro‐grown round‐leaf sundew ( 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 ( PubMed

Miguel S, Nisse E, Biteau F, Rottloff S, Mignard B, Gontier E, Hehn A, Bourgaud F. 2019. Assessing carnivorous plants for the production of recombinant proteins. Frontiers in Plant Science 10: 793. PubMed PMC

Mikitová V, Jopčík M, Rajninec M, Libantová J. 2025. Complex transcription regulation of acidic chitinase suggests fine‐tuning of digestive processes in PubMed PMC

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

Nishimura E, Jumyo S, Arai N, Kanna K, Kume M, Nishikawa J, Tanase J, Ohyama T. 2014. Structural and functional characteristics of S‐like ribonucleases from carnivorous plants. Planta 240: 147–159. PubMed

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

Oropeza‐Aburto A, Cervantes‐Pérez SA, Albert VA, Herrera‐Estrella L. 2020. PubMed PMC

Palfalvi G, Hackl T, Terhoeven N, Shibata TF, Nishiyama T, Ankenbrand M, Becker D, Förster F, Freund M, Iosip A PubMed PMC

Paniw M, Gil‐Cabeza E, Ojeda F. 2017. Plant carnivory beyond bogs: reliance on prey feeding in PubMed PMC

Pavlovič A. 2022. Photosynthesis in carnivorous plants: from genes to gas exchange of green hunters. Critical Reviews in Plant Sciences 41: 305–320.

Pavlovič A, Jakšová J, Novák O. 2017. Triggering a false alarm: wounding mimics prey capture in the carnivorous Venus flytrap ( PubMed

Pavlovič A, Jílková T, Chamrád I, Lenobel R, Vrobel O, Tarkowski P. 2025. The carnivorous rainbow plant PubMed PMC

Pavlovič A, Koller J, Vrobel O, Chamrád I, Lenobel R, Tarkowski P. 2024. Is the co‐option of jasmonate signalling for botanical carnivory universal trait for all carnivorous plants? Journal of Experimental Botany 75: 334–349. 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

Procko C, Chory J. 2024. Carnivorous plant evolution: is a killer defense always the best option? Journal of Experimental Botany 75: 9–12. PubMed PMC

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

Procko C, Wong WM, Patel J, Mousavi SAR, Dabi T, Duque M, Baird L, Chalasani SH, Chory J. 2023. Mutational analysis of mechanosensitive ion channels in the carnivorous Venus flytrap plant. Current Biology 33: 3257–3264. PubMed PMC

Rea PA, Joel DM, Juniper BE. 1983. Secretion and redistribution of chloride in the digestive glands of Dionaea muscipula Ellis (Venus flytrap) upon secretion stimulation. New Phytologist 94: 359–366.

Renner T, Specht CD. 2012. Molecular and functional evolution of class I chitinases for plant carnivory in the Caryophyllales. Molecular Biology and Evolution 29: 2971–2985. PubMed

Renner T, Specht CD. 2013. Inside the trap: gland morphologies, digestive enzymes, and the evolution of plant carnivory in the Caryophyllales. Current Opinion in Plant Biology 16: 436–442. PubMed PMC

Rentsch JD, Blanco SR, Leebens‐Mack JH. 2024. Comparative transcriptomics of Venus flytrap ( PubMed PMC

Rotloff 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, PubMed PMC

Saul F, Scharmann M, Wakatake T, Rajaraman S, Marques A, Freund M, Bringmann G, Channon L, Becker D, Carroll E PubMed

Sheard LB, Tan X, Mao H, Withers J, Ben‐Nissan G, Hinds TR, Kobayashi Y, Hsu F‐F, Sharon M, Browse J PubMed PMC

Shigeto J, Tsutsumi Y. 2016. Diverse functions and reactions of class III peroxidases. New Phytologist 209: 1395–1402. PubMed

Simões I, Faro C. 2004. Structure and function of plant aspartic proteinases. European Journal of Biochemistry 271: 2067–2075. PubMed

Sirová D, Adamec L, Vrba J. 2003. Enzymatic activities in traps of four aquatic species of the carnivorous genus PubMed

Soares A, Carlton SMR, Simões I. 2019. Atypical and nucellin‐like aspartic proteases: emerging players in plant developmental processes and stress responses. Journal of Experimental Botany 70: 2059–2076. PubMed

Stanley D, Farnden KJF, Macrae EA. 2005. Plant α‐amylases: functions and roles in carbohydrate metabolism. Biologia – Section Cellular and Molecular Biology 16: 65–71.

Steckelberg R, Luttge U, Weigh J. 1967. Reingung der proteinase aus Nepenthes‐Kannensaft (purification of the proteinase from the nepenthes pitcher secretion). Planta 76: 238–241. PubMed

Suda H, Mano H, Toyota M, Fukushima K, Mimura T, Tsutsui I, Hedrich R, Tamada Y, Hasebe M. 2020. Calcium dynamics during trap closure visualized in transgenic Venus flytrap. Nature Plants 6: 1219–1224. PubMed

Sun C, Wei J, Gu XY, Wu ML, Li M, Liu YX, An NK, Wu KM, Wu SS, Wu JQ PubMed PMC

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

Thorogood CJ, Bauer U, Hiscock SJ. 2018. Convergent and divergent evolution in carnivorous pitcher plant traps. New Phytologist 217: 1035–1041. PubMed

Tökes ZA, Woon WC, Chambers SM. 1974. Digestive enzymes secreted by the carnivorous plant PubMed

True JR, Carroll SB. 2002. Gene co‐option in physiological and morphological evolution. Annual Review of Cell and Developmental Biology 18: 53–80. PubMed

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

Xia Y, Suzuki H, Borevitz J, Blount J, Guo Z, Patel K, Dixon RA, Lamb C. 2004. An extracellular aspartic protease functions in Arabidopsis disease resistence signaling. EMBO Journal 23: 980–988. PubMed PMC

Yilamujiang A, Reichelt M, Mithöfer A. 2016. Slow food: insect prey and chitin induce phytohormone accumulation and gene expression in carnivorous PubMed PMC

Yu X, Feng T. 2025. The multifaceted roles of plant aspartic proteases. Journal of Experimental Botany. doi: 10.1093/jxb/eraf147. PubMed DOI

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