Coprophagous features in carnivorous Nepenthes plants: a task for ureases

Publikation: Beitrag in FachzeitschriftArtikelForschungPeer-Review

Autoren

  • Ayufu Yilamujiang
  • Anting Zhu
  • Rodrigo Ligabue-Braun
  • Stefan Bartram
  • Claus-Peter Witte
  • Rainer Hedrich
  • Mitsuyasu Hasabe
  • Caroline R. Schoener
  • Michael G. Schoener
  • Gerald Kerth
  • Celia R. Carlini
  • Axel Mithoefer

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Details

OriginalspracheEnglisch
Aufsatznummer11647
FachzeitschriftScientific reports
Jahrgang7
Ausgabenummer1
PublikationsstatusVeröffentlicht - 14 Sept. 2017

Abstract

Most terrestrial carnivorous plants are specialized on insect prey digestion to obtain additional nutrients. Few species of the genus Nepenthes developed mutualistic relationships with mammals for nitrogen supplementation. Whether dietary changes require certain enzymatic composition to utilize new sources of nutrients has rarely been tested. Here, we investigated the role of urease for Nepenthes hemsleyana that gains nitrogen from the bat Kerivoula hardwickii while it roosts inside the pitchers. We hypothesized that N. hemsleyana is able to use urea from the bats' excrements. In fact, we demonstrate that 15N-enriched urea provided to Nepenthes pitchers is metabolized and its nitrogen is distributed within the plant. As ureases are necessary to degrade urea, these hydrolytic enzymes should be involved. We proved the presence and enzymatic activity of a urease for Nepenthes plant tissues. The corresponding urease cDNA from N. hemsleyana was isolated and functionally expressed. A comprehensive phylogenetic analysis for eukaryotic ureases, including Nepenthes and five other carnivorous plants' taxa, identified them as canonical ureases and reflects the plant phylogeny. Hence, this study reveals ureases as an emblematic example for an efficient, low-cost but high adaptive plasticity in plants while developing a further specialized lifestyle from carnivory to coprophagy.

Zitieren

Coprophagous features in carnivorous Nepenthes plants: a task for ureases. / Yilamujiang, Ayufu; Zhu, Anting; Ligabue-Braun, Rodrigo et al.
in: Scientific reports, Jahrgang 7, Nr. 1, 11647, 14.09.2017.

Publikation: Beitrag in FachzeitschriftArtikelForschungPeer-Review

Yilamujiang, A, Zhu, A, Ligabue-Braun, R, Bartram, S, Witte, C-P, Hedrich, R, Hasabe, M, Schoener, CR, Schoener, MG, Kerth, G, Carlini, CR & Mithoefer, A 2017, 'Coprophagous features in carnivorous Nepenthes plants: a task for ureases', Scientific reports, Jg. 7, Nr. 1, 11647. https://doi.org/10.1038/s41598-017-11999-z
Yilamujiang, A., Zhu, A., Ligabue-Braun, R., Bartram, S., Witte, C.-P., Hedrich, R., Hasabe, M., Schoener, C. R., Schoener, M. G., Kerth, G., Carlini, C. R., & Mithoefer, A. (2017). Coprophagous features in carnivorous Nepenthes plants: a task for ureases. Scientific reports, 7(1), Artikel 11647. https://doi.org/10.1038/s41598-017-11999-z
Yilamujiang A, Zhu A, Ligabue-Braun R, Bartram S, Witte CP, Hedrich R et al. Coprophagous features in carnivorous Nepenthes plants: a task for ureases. Scientific reports. 2017 Sep 14;7(1):11647. doi: 10.1038/s41598-017-11999-z
Yilamujiang, Ayufu ; Zhu, Anting ; Ligabue-Braun, Rodrigo et al. / Coprophagous features in carnivorous Nepenthes plants: a task for ureases. in: Scientific reports. 2017 ; Jahrgang 7, Nr. 1.
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title = "Coprophagous features in carnivorous Nepenthes plants: a task for ureases",
abstract = "Most terrestrial carnivorous plants are specialized on insect prey digestion to obtain additional nutrients. Few species of the genus Nepenthes developed mutualistic relationships with mammals for nitrogen supplementation. Whether dietary changes require certain enzymatic composition to utilize new sources of nutrients has rarely been tested. Here, we investigated the role of urease for Nepenthes hemsleyana that gains nitrogen from the bat Kerivoula hardwickii while it roosts inside the pitchers. We hypothesized that N. hemsleyana is able to use urea from the bats' excrements. In fact, we demonstrate that 15N-enriched urea provided to Nepenthes pitchers is metabolized and its nitrogen is distributed within the plant. As ureases are necessary to degrade urea, these hydrolytic enzymes should be involved. We proved the presence and enzymatic activity of a urease for Nepenthes plant tissues. The corresponding urease cDNA from N. hemsleyana was isolated and functionally expressed. A comprehensive phylogenetic analysis for eukaryotic ureases, including Nepenthes and five other carnivorous plants' taxa, identified them as canonical ureases and reflects the plant phylogeny. Hence, this study reveals ureases as an emblematic example for an efficient, low-cost but high adaptive plasticity in plants while developing a further specialized lifestyle from carnivory to coprophagy.",
author = "Ayufu Yilamujiang and Anting Zhu and Rodrigo Ligabue-Braun and Stefan Bartram and Claus-Peter Witte and Rainer Hedrich and Mitsuyasu Hasabe and Schoener, {Caroline R.} and Schoener, {Michael G.} and Gerald Kerth and Carlini, {Celia R.} and Axel Mithoefer",
note = "Funding information: We thank Birgit Arnold and the whole greenhouse team at the MPI for Chemical Ecology as well as Ingrid Handt, Christian Ehrke and the team of the Botanical Garden in Greifswald for growing N. alata and N. hemsleyana plants, respectively; we also thank Yannick Pauchet for helpful advice and Gerg? P{\'a}lfalvi, Kenji Fukushima, and Yukiko Kabeya for D. spatulata and C. follicularis urease gene sequences. We thank Wilhelm Boland and the Max Planck Society for continuous support. This work was further supported in part by the German Academic Exchange Service (DAAD; PPP Project ID 57142556) (AM), by the Brazilian agency Coordenadoria de Aperfei{\c c}oamento de Pessoal de N{\'i}vel Superior (CAPES), Program PROBRAL 407/2016, grant 23038.006810/2014-51 (CRC), by the German Research Foundation (DFG: KE 746/5-1) (KE) and by the MEXT/ JSPS KAKENHI Grant 22128001 (MH) and 22128002 (MH).",
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AU - Yilamujiang, Ayufu

AU - Zhu, Anting

AU - Ligabue-Braun, Rodrigo

AU - Bartram, Stefan

AU - Witte, Claus-Peter

AU - Hedrich, Rainer

AU - Hasabe, Mitsuyasu

AU - Schoener, Caroline R.

AU - Schoener, Michael G.

AU - Kerth, Gerald

AU - Carlini, Celia R.

AU - Mithoefer, Axel

N1 - Funding information: We thank Birgit Arnold and the whole greenhouse team at the MPI for Chemical Ecology as well as Ingrid Handt, Christian Ehrke and the team of the Botanical Garden in Greifswald for growing N. alata and N. hemsleyana plants, respectively; we also thank Yannick Pauchet for helpful advice and Gerg? Pálfalvi, Kenji Fukushima, and Yukiko Kabeya for D. spatulata and C. follicularis urease gene sequences. We thank Wilhelm Boland and the Max Planck Society for continuous support. This work was further supported in part by the German Academic Exchange Service (DAAD; PPP Project ID 57142556) (AM), by the Brazilian agency Coordenadoria de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), Program PROBRAL 407/2016, grant 23038.006810/2014-51 (CRC), by the German Research Foundation (DFG: KE 746/5-1) (KE) and by the MEXT/ JSPS KAKENHI Grant 22128001 (MH) and 22128002 (MH).

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Y1 - 2017/9/14

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