Water Cannot Activate Traps of the Carnivorous Sundew Plant Drosera capensis: On the Trail of Darwin's 150-Years-Old Mystery
Status PubMed-not-MEDLINE Language English Country Switzerland Media electronic
Document type Journal Article
Grant support
RO0423
Ministry of Agriculture
PubMed
37176877
PubMed Central
PMC10181276
DOI
10.3390/plants12091820
PII: plants12091820
Knihovny.cz E-resources
- Keywords
- abscisic acid, aspartic protease, carnivorous plant, digestive enzyme, jasmonic acid, sundew,
- Publication type
- Journal Article MeSH
In his famous book Insectivorous plants, Charles Darwin observed that the bending response of tentacles in the carnivorous sundew plant Drosera rotundifolia was not triggered by a drop of water, but rather the application of many dissolved chemicals or mechanical stimulation. In this study, we tried to reveal this 150-years-old mystery using methods not available in his time. We measured electrical signals, phytohormone tissue level, enzyme activities and an abundance of digestive enzyme aspartic protease droserasin in response to different stimuli (water drop, ammonia, mechanostimulation, chitin, insect prey) in Cape sundew (Drosera capensis). Drops of water induced the lowest number of action potentials (APs) in the tentacle head, and accumulation of jasmonates in the trap was not significantly different from control plants. On the other hand, all other stimuli significantly increased jasmonate accumulation; the highest was found after the application of insect prey. Drops of water also did not induce proteolytic activity and an abundance of aspartic protease droserasin in contrast to other stimuli. We found that the tentacles of sundew plants are not responsive to water drops due to an inactive jasmonic acid signalling pathway, important for the induction of significant digestive enzyme activities.
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Williams S.E., Pickard B.G. Properties of action potentials in Drosera tentacles. Planta. 1972;103:222–240. doi: 10.1007/BF00386845. PubMed DOI
Williams S.E., Pickard B.G. Receptor potentials and action potentials in Drosera tentacles. Planta. 1972;103:193–221. doi: 10.1007/BF00386844. PubMed DOI
Williams S.E., Pickard B.G. The role of action potentials in the control of capture movements of Drosera and Dionaea. In: Skoog F., editor. Plant Growth Substances. Springer; Berlin/Heidelberg, Germany: 1980. pp. 470–480.
Williams S.E., Spanswick R.M. Propagation of the neuroid action potential of the carnivorous plant Drosera. J. Comp. Physiol. 1976;108:211–223. doi: 10.1007/BF02169049. DOI
Krausko M., Perutka Z., Šebela M., Šamajová O., Šamaj J., Novák O., Pavlovič A. The role of electrical and jasmonate signalling in the recognition of captured prey in the carnivorous sundew plant Drosera capensis. New Phytol. 2017;213:1818–1835. doi: 10.1111/nph.14352. PubMed DOI
Nakamura Y., Reichelt M., Mayer V.E., Mithöfer A. Jasmonates trigger prey-induced formation of ‘outer stomach’ in carnivorous sundew plants. Proc. R. Soc. B Biol. Sci. 2013;280:20130228. doi: 10.1098/rspb.2013.0228. PubMed DOI PMC
Procko C., Radin I., Hou C., Richardson R.A., Haswell E.S., Chory J. Dynamic calcium signals mediate the feeding response of the carnivorous sundew plant. Proc. Natl. Acad. Sci. USA. 2022;119:e2206433119. doi: 10.1073/pnas.2206433119. PubMed DOI PMC
Mithöfer A., Reichelt M., Nakamura Y. Wound and insect-induced jasmonate accumulation in carnivorous Drosera capensis: Two sides of the same coin. Plant Biol. 2014;5:982–987. doi: 10.1111/plb.12148. PubMed DOI
Matušíková I., Salaj J., Moravčíková J., Mlynárová L., Nap J.P., Libantová J. Tentacles of in vitro-grown round-leaf sundew (Drosera rotundifolia L.) show induction of chitinase activity upon mimicking the presence of prey. Planta. 2005;222:1020–1027. doi: 10.1007/s00425-005-0047-5. PubMed DOI
Okabe T., Yoshimoto I., Hitoshi M., Ogawa T., Ohyama T. An S-like ribonuclease gene is used to generate a trap-leaf enzyme in the carnivorous plant Drosera Adelae. FEBS Lett. 2005;579:5729–5733. doi: 10.1016/j.febslet.2005.09.043. PubMed DOI
Renner T., Specht C.D. Molecular and functional evolution of class I chitinases for plant carnivory in the Caryophyllales. Mol. Biol. Evol. 2012;29:2971–2985. doi: 10.1093/molbev/mss106. PubMed DOI
Takahashi K., Nishii W., Shibata C. The digestive fluid of Drosera indica contains a cysteine endopeptidase (“Droserain”) similar to Dionain from Dionaea muscipula. Carniv. Plant Newsl. 2012;41:132–134. doi: 10.55360/cpn414.kt962. DOI
Nishimura E., Jumyo S., Arai N., Kanna K., Kume M., Nishikawa J., Tanase J., Ohyama T. Structural and functional characteristics of S-like ribonucleases from carnivorous plants. Planta. 2014;240:147–159. doi: 10.1007/s00425-014-2072-8. PubMed DOI
Darwin C. Insectivorous Plants. John Murray; London, UK: 1875.
Jopcik M., Moravciková J., Matusikova I., Bauer M., Rajninec M., Libantova J. Structural and functional characterisation of a class I endochitinase of the carnivorous sundew (Drosera rotundifolia L.) Planta. 2017;245:313–327. doi: 10.1007/s00425-016-2608-1. PubMed DOI
Sprague-Piercy M.A., Bierma J.C., Crosby M.G., Carpenter B.P., Takahashi G.R., Paulino J., Hung I., Zhang R., Kelly J.E., Kozlyuk N., et al. The Droserasin 1 PSI: A Membrane-Interacting Antimicrobial Peptide from the Carnivorous Plant Drosera capensis. Biomolecules. 2020;10:1069. doi: 10.3390/biom10071069. PubMed DOI PMC
Pavlovič A., Jakšová J., Novák O. Triggering a false alarm: Wounding mimics prey capture in the carnivorous Venus flytrap (Dionaea muscipula) N. Phytol. 2017;216:927–938. doi: 10.1111/nph.14747. PubMed DOI
Farmer E.E., Gao Y.-Q., Lenzoni G., Wolfender J.-L., Wu Q. Wound- and mechanostimulated electrical signals control hormone responses. New Phytol. 2020;227:1037–1050. doi: 10.1111/nph.16646. PubMed DOI
Pavlovič A., Saganová M. A novel insight into the cost–benefit model for the evolution of botanical carnivory. Ann. Bot. 2015;115:1075–1092. doi: 10.1093/aob/mcv050. PubMed DOI PMC
Bemm F., Becker D., Larisch C., Kreuzer I., Escalante-Perez M., Schulze W.X., Ankenbrand M., Van de Weyer A.-L., Krol E., Al-Rasheid K.A., et al. Venus flytrap carnivorous lifestyle builds on herbivore defense strategies. Genome Res. 2016;26:812–825. doi: 10.1101/gr.202200.115. PubMed DOI PMC
Pavlovič A., Mithöfer A. Jasmonate signalling in carnivorous plants: Copycat of plant defence mechanisms. J. Exp. Bot. 2019;70:3379–3389. doi: 10.1093/jxb/erz188. PubMed DOI
Adamec L., Matušíková I., Pavlovič A. Recent ecophysiological, biochemical and evolutional insights into plant carnivory. Ann. Bot. 2021;128:241–259. doi: 10.1093/aob/mcab071. PubMed DOI PMC
Jakšová J., Libiaková M., Bokor B., Petřík I., Novák O., Pavlovič A. Taste for protein: Chemical signal from prey stimulates enzyme secretion through jasmonate signalling in the carnivorous plant Venus flytrap. Plant Physiol. Biochem. 2020;146:90–97. doi: 10.1016/j.plaphy.2019.11.013. PubMed DOI
Yilamujiang A., Reichelt M., Mithöfer A. Slow food: Insect prey and chitin induce phytohormone accumulation and gene expression in carnivorous Nepenthes plants. Ann. Bot. 2016;118:369–735. doi: 10.1093/aob/mcw110. PubMed DOI PMC
Saganová M., Bokor B., Stolárik T., Pavlovič A. Regulation of enzyme activities in carnivorous pitcher plants of the genus Nepenthes. Planta. 2018;248:451–464. doi: 10.1007/s00425-018-2917-7. PubMed DOI
Van Moerkercke A., Duncan O., Zander M., Šimura J., Broda M., Bossche R.V., Lewsey M.G., Lama S., Singh K.B., Ljung K., et al. A MYC2/MYC3/MYC4-dependent transcription factor network regulates water spray-responsive gene expression and jasmonate levels. Proc. Natl. Acad. Sci. USA. 2019;116:23345–23356. doi: 10.1073/pnas.1911758116. PubMed DOI PMC
Matsumura M., Nomoto M., Itaya T., Aratani Y., Iwamoto M., Matsuura T., Hayashi Y., Mori T., Skelly M.J., Yamamoto Y.Y., et al. Mechanosensory trichome cells evoke a mechanical stimuli–induced immune response in Arabidopsis thaliana. Nat. Commun. 2022;13:1216. doi: 10.1038/s41467-022-28813-8. PubMed DOI PMC
Pavlovič A. How the sensory system of carnivorous plants has evolved. Plant Commun. 2022;3:100462. doi: 10.1016/j.xplc.2022.100462. PubMed DOI PMC
Ilík P., Hlaváčková V., Krchňák P., Nauš J. A low-noise multi-channel device for the monitoring of systemic electrical signal propagation in plants. Biol. Plant. 2010;54:185–190. doi: 10.1007/s10535-010-0032-0. DOI
Ljung K., Sandberg G., Moritz T. Methods of plant hormone analysis. In: Davies P.J., editor. Plant Hormones. Springer; Berlin/Heidelberg, Germany: 2010. pp. 717–740.
Šimura J., Antoniadi I., Široká J., Tarkowská D., Strnad M., Ljung K., Novák O. Plant hormonomics: Multiple phytohormone profiling by targeted metabolomics. Plant Physiol. 2018;177:476–489. doi: 10.1104/pp.18.00293. PubMed DOI PMC
Schägger H. Tricine-SDS-PAGE. Nat. Protoc. 2006;1:16–22. doi: 10.1038/nprot.2006.4. PubMed DOI