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Mapping of cell wall aromatic moieties and their effect on hygroscopic movement in the awns of stork’s bill

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Abstract

The awn in stork’s bill (Erodium gruinum) seed dispersal units coils as it dries. This hygroscopic movement promotes the dissemination and sowing of the seeds. Here we aimed to understand the movement rate, by correlating water dynamics within the awn to the spatial variation in the chemical composition of the awn’s cell walls. We followed the hygroscopic movement visually and measured the kinetics of water adsorption–desorption in segments along the awn. We integrated data from white light, fluorescence, and Raman microscopy, and Matrix Assisted Laser Desorption Ionization imaging to characterize the micro chemical makeup of the awn. We hydrolyzed awns and followed the change in the cell walls’ composition and the effect on the movement. We found that the coil’s top segment is more sensitive to humidity changes than the coil’s base. At the top part of the coil, we found high concentration of modified lignin. In comparison, the base part of the awn contained lower concentration of mostly unmodified lignin. Ferulic acid concentration increased along the awn, apparently cross-linking hemicellulose and strengthening cell-to-cell adhesion. We propose that the high concentration of modified lignin at the coil’s top increased the hydrophobicity of the cell walls, allowed faster water molecules dynamics; thus inducing fast reaction to ambient humidity. Strong cell-to-cell adhesion in this region created a durable tissue required for the awn’s repeated movement that is induced by the diurnal humidity cycles.

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Acknowledgments

We thank Ilana Shtein for the help in preparing and staining the awns’ sections, and Notburga Gierlinger and Peter Fratzl for inspiring discussions. This Research was partly supported by the Israel Science Foundation Grant 598/10.

Author information

Correspondence to Rivka Elbaum.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Close up of the coiling part of the E. gruinum awn at rising humidity (28 to 70% humidity) (WMV 720 kb)

A dry fiber cell put into alkaline solution of 1 M NaOH. The cell first straighten at the cell wall matrix absorbs water and swells. Under alkaline environment bonds within the matrix break, allowing it excessive swelling. The fiber over-swelling results in its coiling in an opposite direction to the dry coiling (MP4 574 kb)

Dry E. gruinum awn put into alkaline solution of 1 M NaOH. Similarly to a single cell reaction (Movie S2), the awn first straighten as it absorbs water. Under the alkaline environment, the cell wall matrix swells excessively. During the movie, at 0.28 s the fibers building the awn over-swell, producing a coiling movement in an opposite direction to the dry coiling. Note that the coil top swells first while the bottom never swell extensively (WMV 38475 kb)

Complete E. gruinum awn experiencing decreasing humidity from 70% to 28% relative humidity. The first 10 s of the video clip show the awn forcing the seed into the surface. In this position, the sharp tip of the mericarp is facing the surface. Next, the dispersal unit roles into a gliding mode with the tightening of the coil (WMV 713 kb)

Supplementary material 1 (PDF 828 kb)

Movie S1

Close up of the coiling part of the E. gruinum awn at rising humidity (28 to 70% humidity) (WMV 720 kb)

Movie S2

A dry fiber cell put into alkaline solution of 1 M NaOH. The cell first straighten at the cell wall matrix absorbs water and swells. Under alkaline environment bonds within the matrix break, allowing it excessive swelling. The fiber over-swelling results in its coiling in an opposite direction to the dry coiling (MP4 574 kb)

Movie S3

Dry E. gruinum awn put into alkaline solution of 1 M NaOH. Similarly to a single cell reaction (Movie S2), the awn first straighten as it absorbs water. Under the alkaline environment, the cell wall matrix swells excessively. During the movie, at 0.28 s the fibers building the awn over-swell, producing a coiling movement in an opposite direction to the dry coiling. Note that the coil top swells first while the bottom never swell extensively (WMV 38475 kb)

Movie S4

Complete E. gruinum awn experiencing decreasing humidity from 70% to 28% relative humidity. The first 10 s of the video clip show the awn forcing the seed into the surface. In this position, the sharp tip of the mericarp is facing the surface. Next, the dispersal unit roles into a gliding mode with the tightening of the coil (WMV 713 kb)

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Abraham, Y., Dong, Y., Aharoni, A. et al. Mapping of cell wall aromatic moieties and their effect on hygroscopic movement in the awns of stork’s bill. Cellulose 25, 3827–3841 (2018) doi:10.1007/s10570-018-1852-x

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Keywords

  • Cell wall
  • Erodium gruinum
  • Ferulic acid
  • Fluorescence microscopy
  • Hygroscopic movement
  • Lignin
  • MALDI-FTICR MS
  • Raman microspectroscopy