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Rotation angle of stem cell division plane controls spiral phyllotaxis in mosses

Abstract

The spiral arrangement (phyllotaxis) of leaves is a shared morphology in land plants, and exhibits diversity constrained to the Fibonacci sequence. Phyllotaxis in vascular plants is produced at a multicellular meristem, whereas bryophyte phyllotaxis emerges from a single apical stem cell (AC) that is embedded in a growing tip of the gametophyte. An AC is asymmetrically divided into itself and a single ‘merophyte’, producing a future leaf and a portion of the stem. Although it has been suggested that the arrangement of merophytes is regulated by a rotation of the division plane of an AC, the quantitative description of the merophyte arrangement and its regulatory mechanism remain unclear. To clarify them, we examined three moss species, Tetraphis pellucida, Physcomitrium patens, and Niphotrichum japonicum, which exhibit 1/3, 2/5, and 3/8 spiral phyllotaxis, respectively. We measured the angle between the centroids of adjacent merophytes relative to the AC centroid on cross-transverse sections. At the outer merophytes, this divergence angle converged to nearly 120\(^\circ\) in T. pellucida, 136\(^\circ\) in N. japonicum, and 141\(^\circ\) in P. patens, which was nearly consistent with phyllotaxis, whereas the divergence angle deviated from the converged angle at the inner merophytes near an AC. A mathematical model, which assumes scaling growth of AC and merophytes and a constant angle of division plane rotation, quantitatively reproduced the sequence of the divergence angles. This model showed that successive relocations of the centroid position of an AC upon its division inevitably result in the transient deviation of the divergence angle. As a result, the converged divergence angle was equal to the rotation angle, predicting that the latter is a major regulator of the spiral phyllotaxis diversity in mosses.

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Acknowledgements

We thank T. Yonekura [Nara Institute of Science and Technology (NAIST), Japan] for valuable discussions and suggestions. This work was supported by Grants-in-Aid for Scientific Research from the Ministry of Education, Culture, Sports, Science and Technology of Japan to KF (17H06386, 16H06378, 20H05415) and MS (20H05419, 25113009).

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Conceptualization: NK, KF, MS; methodology: NK, TT, MS; software: NK; formal analysis: NK; investigation: NK, TT; writing-original draft preparation: NK, KF, MS; writing-review and editing: NK, KF, MS; resources: MS; supervision: KF, MS. All authors read and approved the final manuscript.

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Correspondence to Koichi Fujimoto or Masaki Shimamura.

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Kamamoto, N., Tano, T., Fujimoto, K. et al. Rotation angle of stem cell division plane controls spiral phyllotaxis in mosses. J Plant Res 134, 457–473 (2021). https://doi.org/10.1007/s10265-021-01298-0

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  • DOI: https://doi.org/10.1007/s10265-021-01298-0

Keywords

  • Apical stem cell
  • Cell division plane
  • Moss
  • Niphotrichum japonicum
  • Phyllotaxis
  • Physcomitrium patens