Four hundred million years of silica biomineralization in land plants

Abstract

Biomineralization plays a fundamental role in the global silicon cycle. Grasses are known to mobilize significant quantities of Si in the form of silica biominerals and dominate the terrestrial realm today, but they have relatively recent origins and only rose to taxonomic and ecological prominence within the Cenozoic Era. This raises questions regarding when and how the biological silica cycle evolved. To address these questions, we examined silica abundances of extant members of early-diverging land plant clades, which show that silica biomineralization is widespread across terrestrial plant linages. Particularly high silica abundances are observed in lycophytes and early-diverging ferns. However, silica biomineralization is rare within later-evolving gymnosperms, implying a complex evolutionary history within the seed plants. Electron microscopy and X-ray spectroscopy show that the most common silica-mineralized tissues include the vascular system, epidermal cells, and stomata, which is consistent with the hypothesis that biomineralization in plants is frequently coupled to transpiration. Furthermore, sequence, phylogenetic, and structural analysis of nodulin 26-like intrinsic proteins from diverse plant genomes points to a plastic and ancient capacity for silica accumulation within terrestrial plants. The integration of these two comparative biology approaches demonstrates that silica biomineralization has been an important process for land plants over the course of their >400 My evolutionary history.

Additional Information

© 2015 National Academy of Sciences. Freely available online through the PNAS open access option. Edited by Thure E. Cerling, University of Utah, Salt Lake City, UT, and approved February 20, 2015 (received for review January 7, 2015). We thank George Rossman and Victoria Orphan for laboratory equipment, Chi Ma for assistance with electron microscopy and spectroscopy, and Sean Lahmeyer (The Huntington Library, Art Collections, and Botanical Gardens), Loran M. Whitelock (Eagle Rock, CA), and Lucinda McDade (Rancho Santa Ana Botanic Garden) for aid in sample collection. This project was partially supported by an OK Earl Postdoctoral Scholarship (Caltech) and a San Andreas Visiting Fellowship to The Huntington Library, Art Collections, and Botanical Gardens (J.P.W.). S.E.M. was partially supported by the Agouron Institute as a Geobiology Fellow. W.W.F. acknowledges support from the Agouron Institute. Author contributions: E.T.-R., J.P.W., S.E.M., and W.W.F. designed research; E.T.-R., J.P.W., and S.E.M. performed research; E.T.-R., J.P.W., S.E.M., and W.W.F. analyzed data; and E.T.-R., J.P.W., S.E.M., and W.W.F. wrote the paper. The authors declare no conflict of interest. This article is a PNAS Direct Submission. This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1500289112/-/DCSupplemental.

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Supplemental Material - pnas.1500289112.sd04.txt

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