Callose is integral to the development of permanent tetrads in the liverwort Sphaerocarpos

Abstract

A striking feature of the liverwort Sphaerocarpos is that pairs of male and female spores remain united in permanent tetrads. To identify the nature of this phenomenon and to test the hypothesis that callose is involved, we examined spore wall development in Sphaerocarpos miche lii, with emphasis on the appearance, location and fate of callose vis-à-vis construction of the sculptoderm. All stages of sporogenesis were examined using differential interference contrast optics, and aniline blue fluorescence to locate callose. For precise localization, specimens were immunogold labeled with anti-callose antibody and observed in the transmission electron microscope. Callose plays a role in Sphaerocarpos spore wall development not described in any other plant, including other liverworts. A massive callose matrix forms outside of the sculptured sporocyte plasmalemma that predicts spore wall ornamentation. Consequently, layers of exine form across adjacent spores uniting them. Spore wall development occurs entirely within the callose and involves the production of six layers of prolamellae that give rise to single or stacked tripartite lamellae (TPL). Between spores, an anastomosing network of exine layers forms in lieu of intersporal septum development. As sporopollenin assembles on TPL, callose progressively disappears from the inside outward leaving layers of sporopollenin impregnated exine, the sculptoderm, overlying a thick fibrillar intine. This developmental mechanism provides a direct pathway from callose deposition to sculptured exine that does not involve the intermediary primexine found in pollen wall development. The resulting tetrad, encased in a single wall, provides a simple model for development of permanent dyads and tetrads in the earliest fossil plants.

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Abbreviations

MLL:

Multilamellate layer

TPL:

Tripartite lamellae

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Acknowledgments

We thank Andres Womac, Amelia Merced, Scott Schuette, and Bryan Piatkowski for technical assistance. This work was supported by NSF grants EF 0531751 and DGE 0638722.

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Correspondence to Karen S. Renzaglia.

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Renzaglia, K.S., Lopez, R.A. & Johnson, E.E. Callose is integral to the development of permanent tetrads in the liverwort Sphaerocarpos . Planta 241, 615–627 (2015). https://doi.org/10.1007/s00425-014-2199-7

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Keywords

  • (1,3)-β-Glucan
  • Cryptospore
  • Exine
  • Paleozoic
  • Permanent tetrad
  • Sculptoderm
  • Spores
  • Tripartite lamellae
  • Ultrastructure