A GEOBIOLOGICAL PERSPECTIVE ON THE EVOLUTION OF SILICA BIOMINERALIZATION IN PLANTS

Plants play several major roles in the global silica cycle, including through the production of amorphous silica deposits within their tissues. The phylogenetic distribution and biosynthesis of silica bodies has been primarily studied in monocot angiosperms (e.g., grasses), but the origin of this biomineralization process and its early evolutionary history remain poorly known, with limited paleontological data that can be brought to bear on plant silica’s early history.

We investigated the evolution of silica biomineralization by employing a combined geochemical and molecular comparative biology approach across a deeper diversity of living land plants, with explicit focus on groups with long evolutionary histories that were once far more common in terrestrial ecosystems. We measured silica abundance within photosynthetic tissues collected from a diverse suite of wild and cultivated plants collected throughout Southern California, and then imaged the resulting silica biominerals using electron microscopy and energy dispersive spectroscopy. Results show silica abundance is very high in early-diverging plant groups like ferns, sphenopsids, and some bryophytes; these values are as high or higher on average than many silica-bearing monocot grasses. However, conifers and cycads are low. We combined these observations with analyses from the molecular and structural biology of silicic acid transport proteins, which are the biochemical gatekeepers for silica entry into plant tissues. Results show that silicic acid transporters are derived within a group of nodulin-26-like modified aquaporins and, within angiosperms, these transporters have a single origin descended from a group of arsenite and glycerol transporters present in the earliest land plants. Analysis of silicic acid transporter homologues illustrates multiple origins of silica biomineralization within non-angiosperm silicic acid transporters, including independent origins within lycopsids and Equisetum and an absence within the conifers.

Silica biomineralization was both a feature of early land plants and perhaps evolved several times within the seed plants. Silica cycling in terrestrial ecosystems was likely an important process during the Paleozoic Era, when lycopsids, ferns, and horsetails were abundant and diverse.