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Electrical signals in prayer plants (marantaceae)? Insights into the trigger mechanism of the explosive style movement.

Jerominek M, Claßen-Bockhoff R - PLoS ONE (2015)

Bottom Line: In both species, chemical and electric stimulations do not release the style movement.It is concluded that the style movement in Marantaceae is released mechanically by relieving the tissue pressure.Accordingly, the variation potential is an effect of the movement and not its cause.

View Article: PubMed Central - PubMed

Affiliation: Institut für Spezielle Botanik und Botanischer Garten, Johannes Gutenberg-Universität, Mainz, Germany.

ABSTRACT
The explosive pollination mechanism of the prayer plants (Marantaceae) is unique among plants. After a tactile stimulus by a pollinator, the style curls up rapidly and mediates pollen exchange. It is still under discussion whether this explosive movement is released electrophysiologically, i.e. by a change in the membrane potential (as in Venus flytrap), or purely mechanically. In the present study, electrophysiological experiments are conducted to clarify the mechanism. Artificial release experiments (chemical and electrical) and electrophysiological measurements were conducted with two phylogenetically distant species, Goeppertia bachemiana (E. Morren) Borchs. & S. Suárez and Donax canniformis (G. Forst.) K. Schum. Electric responses recorded after style release by extracellular measurements are characterised as variation potentials due to their long repolarization phase and lack of self-perpetuation. In both species, chemical and electric stimulations do not release the style movement. It is concluded that the style movement in Marantaceae is released mechanically by relieving the tissue pressure. Accordingly, the variation potential is an effect of the movement and not its cause. The study exemplarily shows that fast movements in plants are not necessarily initiated by electric changes of the membrane as known from the Venus flytrap.

No MeSH data available.


Positions for the extracellular measurements.Unreleased styles of Donax canniformis (A) and Goeppertia bachemiana (B). Measuring positions of the microelectrode (me) are indicated by black triangles that mark the distance (= D) to the basal plate in 1 mm steps. White triangles are omitted. The microelectrode is located at D = 5 mm in both schemata. Moving and non-moving part of the style is separated by a dotted line.
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pone.0126411.g004: Positions for the extracellular measurements.Unreleased styles of Donax canniformis (A) and Goeppertia bachemiana (B). Measuring positions of the microelectrode (me) are indicated by black triangles that mark the distance (= D) to the basal plate in 1 mm steps. White triangles are omitted. The microelectrode is located at D = 5 mm in both schemata. Moving and non-moving part of the style is separated by a dotted line.

Mentions: The fixed flowers were transferred to a faraday cage. Using a dissecting microscope and a screw micromanipulator, an apoplastic voltage electrode (Fig 3, me) was slightly inserted into the upper epidermal layer of the style to measure the extracellular voltage. To avoid a damage of the electrode due to the style movement, measurements were restricted to positions proximal to the bending tissue (Fig 4, black triangles). Measurements in the moving tissue of the style were only feasible in Donax canniformis that has a lower roll up angle of the style. The minimum distance (= D) between the electrode and the rim of the basal plate was 2 mm in Donax canniformis (Fig 4A) and 4 mm in Goeppertia bachemiana (Fig 4B). To close the circuit, the ovary side of the style was connected to the reference electrode (Fig 3, re) by covering both with tab water. Microelectrodes were made from borosilicate glass capillaries (OD = 1.5 mm, ID = 0.75 mm, with 0.2 mm filament; manufacturer: Hilgenberg) using a two-stage puller (L/M-3P-A, List-Medical) according to Felle and Zimmerman [27] and filled with 0.5 M KCl. To exclude intracellular recording the tip of the electrode was shortened up to 100 μm in diameter. For measurements a high-impedance (1015 Ω) Electrometer (FD223, World Precision Instruments, Sarasota, FL, USA) was used. Electric changes were traced on a chart recorder (W&W Recorder, Model 314) and analysed manually.


Electrical signals in prayer plants (marantaceae)? Insights into the trigger mechanism of the explosive style movement.

Jerominek M, Claßen-Bockhoff R - PLoS ONE (2015)

Positions for the extracellular measurements.Unreleased styles of Donax canniformis (A) and Goeppertia bachemiana (B). Measuring positions of the microelectrode (me) are indicated by black triangles that mark the distance (= D) to the basal plate in 1 mm steps. White triangles are omitted. The microelectrode is located at D = 5 mm in both schemata. Moving and non-moving part of the style is separated by a dotted line.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4440630&req=5

pone.0126411.g004: Positions for the extracellular measurements.Unreleased styles of Donax canniformis (A) and Goeppertia bachemiana (B). Measuring positions of the microelectrode (me) are indicated by black triangles that mark the distance (= D) to the basal plate in 1 mm steps. White triangles are omitted. The microelectrode is located at D = 5 mm in both schemata. Moving and non-moving part of the style is separated by a dotted line.
Mentions: The fixed flowers were transferred to a faraday cage. Using a dissecting microscope and a screw micromanipulator, an apoplastic voltage electrode (Fig 3, me) was slightly inserted into the upper epidermal layer of the style to measure the extracellular voltage. To avoid a damage of the electrode due to the style movement, measurements were restricted to positions proximal to the bending tissue (Fig 4, black triangles). Measurements in the moving tissue of the style were only feasible in Donax canniformis that has a lower roll up angle of the style. The minimum distance (= D) between the electrode and the rim of the basal plate was 2 mm in Donax canniformis (Fig 4A) and 4 mm in Goeppertia bachemiana (Fig 4B). To close the circuit, the ovary side of the style was connected to the reference electrode (Fig 3, re) by covering both with tab water. Microelectrodes were made from borosilicate glass capillaries (OD = 1.5 mm, ID = 0.75 mm, with 0.2 mm filament; manufacturer: Hilgenberg) using a two-stage puller (L/M-3P-A, List-Medical) according to Felle and Zimmerman [27] and filled with 0.5 M KCl. To exclude intracellular recording the tip of the electrode was shortened up to 100 μm in diameter. For measurements a high-impedance (1015 Ω) Electrometer (FD223, World Precision Instruments, Sarasota, FL, USA) was used. Electric changes were traced on a chart recorder (W&W Recorder, Model 314) and analysed manually.

Bottom Line: In both species, chemical and electric stimulations do not release the style movement.It is concluded that the style movement in Marantaceae is released mechanically by relieving the tissue pressure.Accordingly, the variation potential is an effect of the movement and not its cause.

View Article: PubMed Central - PubMed

Affiliation: Institut für Spezielle Botanik und Botanischer Garten, Johannes Gutenberg-Universität, Mainz, Germany.

ABSTRACT
The explosive pollination mechanism of the prayer plants (Marantaceae) is unique among plants. After a tactile stimulus by a pollinator, the style curls up rapidly and mediates pollen exchange. It is still under discussion whether this explosive movement is released electrophysiologically, i.e. by a change in the membrane potential (as in Venus flytrap), or purely mechanically. In the present study, electrophysiological experiments are conducted to clarify the mechanism. Artificial release experiments (chemical and electrical) and electrophysiological measurements were conducted with two phylogenetically distant species, Goeppertia bachemiana (E. Morren) Borchs. & S. Suárez and Donax canniformis (G. Forst.) K. Schum. Electric responses recorded after style release by extracellular measurements are characterised as variation potentials due to their long repolarization phase and lack of self-perpetuation. In both species, chemical and electric stimulations do not release the style movement. It is concluded that the style movement in Marantaceae is released mechanically by relieving the tissue pressure. Accordingly, the variation potential is an effect of the movement and not its cause. The study exemplarily shows that fast movements in plants are not necessarily initiated by electric changes of the membrane as known from the Venus flytrap.

No MeSH data available.