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What keeps the style under tension? Experimental tests to understand the biomechanics of the explosive style movement in Marantaceae

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  • Mechanical Forces in Plant Growth and Development
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Abstract

Pollination in Marantaceae is mediated by an explosive style movement. Before release, style tension is held by the hooded staminode. When a pollinator touches the trigger appendage of the hooded staminode the latter deforms and the style rapidly curls upwards. This movement has been interpreted as a turgor movement by some authors, but recent studies clearly indicate that setup, hold and release of tension are purely mechanical processes. However, in view of the high diversity of hooded staminodes, the question arises what keeps the tension in species with very thin staminodes. To test the holding mechanisms, we conducted mechanical and physico-chemical release experiments in four species with robust and four species with thin hooded staminodes in their natural tropical environment. We found almost the same response of all species to mechanical treatments, but species-specific reactions to different physico-chemical conditions. This indicates that style release follows the same mechanical principles in all species, but that the sensitivity of the explosive movement depends on material properties like tissue thickness and turgescence. As to the holding mechanisms, we found different degrees of floral synorganization. The hood of the hooded staminode formerly interpreted as an important holding structure does not play a noteworthy role. Instead, the basal plate of the hooded staminode antagonises the pressure of the style head against the holding point of the hooded staminode in species with robust hooded staminodes and well-developed basal plates. In some species with a thin hooded staminode, the latter is closely attached to the style and most likely stabilises tension by adhesive forces. In another species, a morphologically analogous structure adopts the function of the basal plate. We conclude that the holding mechanism of the style tension diversified during the evolution of Marantaceae whereas the release mechanism itself has been conserved throughout the family.

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Fig. 1

© a,b after Pischtschan and Claßen-Bockhoff 2008. c,d based on Claßen-Bockhoff 1991, changed

Fig. 2

© M. Jerominek, Mainz

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Acknowledgements

We thank Dr. Piyakaset Suksathan and Dr. Suyanee Vessabutr for local assistance and arrangements in the Queen Sirikit Botanic Garden (Thailand), and Dr. Zak Zahawi in the Wilson Botanical Garden (Costa Rica). We are grateful to Rodolfo Quirós and Pattarin Nunthamontree for their technical assistance. Thanks are also given to the editor of this special issue, Akitoshi Iwamoto, and to two unknown reviewers for their helpful comments.

Funding

Travel and accommodation expenses were funded by the German Academic Exchange Service (DAAD; D/09/49132).

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Contributions

The project was initiated by RC-B. Both authors contributed to the study conception and design. Material preparation and data collection were performed by MJ. Data analysis and interpretation were conducted by MJ and RC-B. The first draft of the manuscript was written by MJ, the final version by RC-B. Both authors approved the final manuscript.

Corresponding author

Correspondence to Regine Claßen-Bockhoff.

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Supplementary Information

Below is the link to the electronic supplementary material.

V1: Trigger deflection (Goeppertia ecuadoriana) (MP4 9861 KB)

V2: Basal plate slipped away (Goeppertia zebrina var. humilior) (MP4 1174 KB)

V3: Longitudinal cut in distal hood (Goeppertia zebrina var. humilior) (MP4 3020 KB)

V4: Stinging style (Calathea crotalifera) (MP4 10215 KB)

V5: Transverse cut and downward buckling of the style (Goeppertia zebrina var. humilior) (MP4 2206 KB)

V6: Transverse cut and rupture of the style (Goeppertia zebrina var. zebrina) (MP4 5270 KB)

V7: Longitudinal cut at lower side of the style (Calathea crotalifera) (MP4 5383 KB)

V8: Time-lapse (20 min) black colouration after wounding (Goeppertia zebrina var. humilior) (MP4 5546 KB)

V9: Time-lapse (20 min) black colouration in 70% ethanol (Goeppertia zebrina var. zebrina) (MP4 5190 KB)

V10: Time-lapse (10 min) fixation chloroform steam (Stromanthe sanguinea) (MP4 5149 KB)

V11: Time-lapse (30 min) fixation in NaCl (Goeppertia zebrina var. zebrina) (MP4 7539 KB)

V12: Time-lapse (20 min) black colouration after freezing (Goeppertia zebrina var. humilior) (MP4 3036 KB)

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Jerominek, M., Claßen-Bockhoff, R. What keeps the style under tension? Experimental tests to understand the biomechanics of the explosive style movement in Marantaceae. J Plant Res (2024). https://doi.org/10.1007/s10265-024-01535-2

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