Published January 16, 2025 | In Press
Journal Article Open

Single cell derived multicellular meristem: insights into male-to-hermaphrodite conversion and de novo meristem formation in ceratopteris

  • 1. ROR icon Purdue University West Lafayette
  • 2. ROR icon California Institute of Technology

Abstract

Land plants alternate between asexual sporophytes and sexual gametophytes. Unlike seed plants, ferns develop free-living gametophytes. Gametophytes of the model fern Ceratopteris exhibit two sex types: hermaphrodites with pluripotent meristems and males lacking meristems. In the absence of the pheromone antheridiogen, males convert to hermaphrodites by forming de novo meristems, though the mechanisms remain unclear. Using long-term time-lapse imaging and computational analyses, we captured male-to-hermaphrodite conversion at single-cell resolution and reconstructed the lineage and division atlas of newly formed meristems. Lineage tracing revealed that the de novo-formed meristem originates from a single non-antheridium cell, the meristem progenitor cell (MPC). During conversion, the MPC lineage showed increased mitotic activity, with marginal cells proliferating faster than inner cells. A mathematical model suggests that stochastic variation in cell division, combined with strong inhibitory signals from dividing marginal cells, is sufficient to explain gametophyte dynamics. Experimental disruption of division timing agreed with the model, showing precise cell cycle progression is essential for MPC establishment and sex-type conversion. These findings reveal cellular mechanisms governing sex conversion and de novo meristem formation in land plants.

Copyright and License

© 2025. Published by The Company of Biologists. Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.

Acknowledgement

The authors thank three anonymous referees for their thoughtful suggestions that improved our manuscript, and the Purdue Bindley Bioscience Facility for access to the ZEISS LSM880 confocal microscope. This work was supported by the NSF grant IOS 1931114 (to Y.Z.). This work was also supported in part by a seed grant (to A.V. and Y.Z.) from the NSF–Simons Center for Quantitative Biology at Northwestern University, through the NSF grant DMS 1764421 and the Simons Foundation/SFARI grant 597491-RWC, both awarded to Northwestern University.

Contributions

X.Y. and Y.Z. conceived the research direction; Y.Z. supervised the research progress; X.Y. performed experiments; X.Y., X.L., and Y.Z. discussed and interpreted experimental results; A.Y., and Y.Z. performed image analysis; X.Y. performed quantitative analysis; A.V. performed mathematical studies and modeling work; A.V. and Y.Z. discussed the model; X.Y., A.V., and Y.Z. wrote the manuscript, and X.L. and A.Y. revised the manuscript. All the authors read and approved the manuscript.

Data Availability

All data supporting the conclusions are included in the manuscript text, figures, or supplementary materials. The model code is publicly available in a GitLab repository
(https://gitlab.com/alexandriavolkening/population-model-for-meristem-dynamics-in-ferns).

Supplemental Material

Supplementary information:

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Additional details

Created:
January 21, 2025
Modified:
January 21, 2025