Home LiteratureArticle Details
PMID: 33020606 Published · ppublish English Journal Article

Calcium dynamics during trap closure visualized in transgenic Venus flytrap.

Nature plants ·Vol. 6 ·No. 10 ·2020-00-00 ·Pages 1219-1224

Suda H, Mano H, Toyota M, Fukushima K, Mimura T, Tsutsui I, Hedrich R, Tamada Y, Hasebe M

Abstract

The leaves of the carnivorous plant Venus flytrap, Dionaea muscipula (Dionaea) close rapidly to capture insect prey. The closure response usually requires two successive mechanical stimuli to sensory hairs on the leaf blade within approximately 30 s (refs. 1-4). An unknown biological system in Dionaea is thought to memorize the first stimulus and transduce the signal from the sensory hair to the leaf blade2. Here, we link signal memory to calcium dynamics using transgenic Dionaea expressing a Ca2+ sensor. Stimulation of a sensory hair caused an increase in cytosolic Ca2+ concentration ([Ca2+]cyt) starting in the sensory hair and spreading to the leaf blade. A second stimulus increased [Ca2+]cyt to an even higher level, meeting a threshold that is correlated to the leaf blade closure. Because [Ca2+]cyt gradually decreased after the first stimulus, the [Ca2+]cyt increase induced by the second stimulus was insufficient to meet the putative threshold for movement after about 30 s. The Ca2+ wave triggered by mechanical stimulation moved an order of magnitude faster than that induced by wounding in petioles of Arabidopsis thaliana5 and Dionaea. The capacity for rapid movement has evolved repeatedly in flowering plants. This study opens a path to investigate the role of Ca2+ in plant movement mechanisms and their evolution.

MeSH Terms
Calcium/metabolism Droseraceae/metabolism Physical Stimulation Plant Leaves/metabolism,physiology Plants, Genetically Modified
Chemicals
Calcium
Authors & Affiliations
9 authors, click to expand affiliations / ORCID
Suda Hiraku ORCID
National Institute for Basic Biology, Okazaki, Japan. | Department of Basic Biology, The Graduate University for Advanced Studies (SOKENDAI), Okazaki, Japan.
Mano Hiroaki ORCID
National Institute for Basic Biology, Okazaki, Japan. | Department of Basic Biology, The Graduate University for Advanced Studies (SOKENDAI), Okazaki, Japan. | JST, PRESTO, Saitama, Japan.
Toyota Masatsugu ORCID
Department of Biochemistry and Molecular Biology, Graduate School of Science and Engineering, Saitama University, Saitama, Japan. | Department of Botany, University of Wisconsin, Madison, WI, USA.
Fukushima Kenji ORCID
National Institute for Basic Biology, Okazaki, Japan. | Department of Basic Biology, The Graduate University for Advanced Studies (SOKENDAI), Okazaki, Japan. | Institute for Molecular Plant Physiology and Biophysics, University of Würzburg, Würzburg, Germany.
Mimura Tetsuro
Department of Biology, Graduate School of Science, Kobe University, Kobe, Japan.
Tsutsui Izuo
Graduate School of Business Administration, Hitotsubashi University, Kunitachi, Japan.
Hedrich Rainer ORCID
Institute for Molecular Plant Physiology and Biophysics, University of Würzburg, Würzburg, Germany. | Zoology Department, College of Science, King Saud University, Riyadh, Saudi Arabia.
Tamada Yosuke ORCID
National Institute for Basic Biology, Okazaki, Japan. | Department of Basic Biology, The Graduate University for Advanced Studies (SOKENDAI), Okazaki, Japan. | School of Engineering, Utsunomiya University, Utsunomiya, Japan.
Hasebe Mitsuyasu ORCID
National Institute for Basic Biology, Okazaki, Japan. mhasebe@nibb.ac.jp. | Department of Basic Biology, The Graduate University for Advanced Studies (SOKENDAI), Okazaki, Japan. mhasebe@nibb.ac.jp.
References (28)
28 references, click to expand
  1. Macfarlane, J. M. Contributions to the history of Dionaea muscipula Ellis. Contr. Bot. Lab. Univ. Pennsylvania 1, 7–44 (1892).
  2. Juniper, B. B. E., Robins, R. J. & Joel, D. M. The Carnivorous Plants (Academic Press, 1989).
  3. Brown, W. H. & Sharp, L. W. The closing response in Dionaea. Bot. Gaz. 49, 290–302 (1910). DOI
  4. Burri, J. T. et al. A single touch can provide sufficient mechanical stimulation to trigger Venus flytrap closure. PLoS Biol. 18, e3000740 (2020). DOI
  5. Toyota, M. et al. Glutamate triggers long-distance, calcium-based plant defense signaling. Science 361, 1112–1115 (2018). DOI
  6. Taiz, L., Zeiger, E., Møller, I. M. & Murphy, A. Plant Physiology and Development 6th edn (Oxford Univ. Press, 2018).
  7. Benolken, R. M. & Jacobson, S. L. Response properties of a sensory hair excised from Venus’s flytrap. J. Gen. Physiol. 56, 64–82 (1970). DOI
  8. Action potentials in plant organs.
    Sibaoka, T. Action potentials in plant organs. Symp. Soc. Exp. Biol. 20, 49–73 (1966). PMID: 5958369
  9. Hodick, D. & Sievers, A. On the mechanism of trap closure of Venus flytrap (Dionaea muscipula Ellis). Planta 179, 32–42 (1989). DOI
  10. Hodick, D. & Sievers, A. The action potential of Dionaea muscipula Ellis. Planta 174, 8–18 (1988). DOI
  11. Fagerberg, W. R. & Allain, D. A quantitative study of tissue dynamics during closure in the traps of Venus’s flytrap Dionaea muscipula Ellis. Am. J. Bot. 78, 647–657 (1991). DOI
  12. Hedrich, R. & Neher, E. Venus flytrap: how an excitable, carnivorous plant works. Trends Plant Sci. 23, 220–234 (2018). DOI
  13. Chiu, W. et al. Engineered GFP as a vital reporter in plants. Curr. Biol. 6, 325–330 (1996). DOI
  14. Maekawa, T. et al. Polyubiquitin promoter-based binary vectors for overexpression and gene silencing in Lotus japonicus. Mol. Plant Microbe Interact. 21, 375–382 (2008). DOI
  15. Mano, H., Fujii, T., Sumikawa, N., Hiwatashi, Y. & Hasebe, M. Development of an Agrobacterium-mediated stable transformation method for the sensitive plant Mimosa pudica. PLoS ONE 9, e88611 (2014). DOI
  16. Chen, T.-W. et al. Ultrasensitive fluorescent proteins for imaging neuronal activity. Nature 499, 295–300 (2013). DOI
  17. Knight, H. & Knight, M. R. Imaging spatial and cellular characteristics of low temperature calcium signature after cold acclimation in Arabidopsis. J. Exp. Bot. 51, 1679–1686 (2000). DOI
  18. Pavlovič, A., Jakšová, J. & Novák, O. Triggering a false alarm: wounding mimics prey capture in the carnivorous Venus flytrap (Dionaea muscipula). New Phytol. 216, 927–938 (2017). DOI
  19. Forterre, Y., Skotheim, J. M., Dumais, J. & Mahadevan, L. How the Venus flytrap snaps. Nature 433, 421–425 (2005). DOI
  20. Sibaoka, T. in Plant Growth Substances (Ed. Skoog, F.) 462–469 (Springer, 1980).
  21. Volkov, A. G. Signaling in electrical networks of the Venus flytrap (Dionaea muscipula Ellis). Bioelectrochemistry 125, 25–32 (2019). DOI
  22. Pavlovič, A., Demko, V. & Hudák, J. Trap closure and prey retention in Venus flytrap (Dionaea muscipula) temporarily reduces photosynthesis and stimulates respiration. Ann. Bot. 105, 37–44 (2010). DOI
  23. Pavlovič, A., Slovaková, L., Pandolfi, C. & Mancuso, S. On the mechanism underlying photosynthetic limitation upon trigger hair irritation in the carnivorous plant Venus flytrap (Dionaea muscipula Ellis). J. Exp. Bot. 62, 1991–2000 (2011). DOI
  24. Jensen, M. K. et al. Transcriptome and genome size analysis of the Venus flytrap. PLoS ONE 10, e0123887 (2015). DOI
  25. Komari, T. et al. in Agrobacterium Protocols (ed. Wang, K.) 15–42 (Humana Press, 2015).
  26. Hellens, R., Mullineaux, P. & Klee, H. Technical focus: a guide to Agrobacterium binary Ti vectors. Trends Plant Sci. 5, 446–451 (2000). DOI
  27. Milliken, G. A., Bates, D. M. & Watts, D. G. Nonlinear regression analysis and its applications. Technometrics 32, 219 (1990). DOI
  28. Escalante-Perez, M. et al. A special pair of phytohormones controls excitability, slow closure, and external stomach formation in the Venus flytrap. Proc. Natl Acad. Sci. USA 108, 15492–15497 (2011). DOI
Article Info
Journal
Nature plants
Abbr.
Nat Plants
ISSN
2055-0278
Published
2020-00-00
Epub
2020-00-05
Pages
1219-1224
Language
English
Region
England
NLM ID
101651677
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com