title: 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.
authors.affiliation: Division of Geological and Planetary Sciences, California Institute of Technology, Pasadena, CA 91125; e.t.r@caltech.edu.
authors.forename: Elizabeth
authors.initials: E
authors.lastname: Trembath-Reichert
authors.affiliation: Department of Biology, Haverford College, Haverford, PA 19041; and.
authors.forename: Jonathan Paul
authors.initials: JP
authors.lastname: Wilson
authors.affiliation: Division of Geological and Planetary Sciences, California Institute of Technology, Pasadena, CA 91125; Graduate School of Science and Engineering, Tokyo Metropolitan University, Hachioji-shi, Tokyo 192-0397, Japan.
authors.forename: Shawn E
authors.initials: SE
authors.lastname: McGlynn
authors.affiliation: Division of Geological and Planetary Sciences, California Institute of Technology, Pasadena, CA 91125;
authors.forename: Woodward W
authors.initials: WW
authors.lastname: Fischer
mesh_terms: D005075:Biological Evolution; D005580:Fossils; D018521:Plant Physiological Phenomena; D010944:Plants / Q000235:genetics / Q000378:metabolism; D012822:Silicon Dioxide / Q000378:metabolism*
chemical_list: D012822:Silicon Dioxide
keywords: aquaporin; fern; lycophyte; phytolith; silicon
references.citation: Proc Natl Acad Sci U S A. 2002 Aug 6;99(16):10923-8
references.pmid: 12149443
references.citation: BMC Plant Biol. 2010 Nov 20;10:256
references.pmid: 21092127
references.citation: Bioinformatics. 2007 Nov 1;23(21):2947-8
references.pmid: 17846036
references.citation: Proc Natl Acad Sci U S A. 2005 Aug 23;102(34):11980-4
references.pmid: 16099827
references.citation: Science. 1982 Aug 27;217(4562):831-3
references.pmid: 17778314
references.citation: J Exp Bot. 2005 Apr;56(414):1255-61
references.pmid: 15753109
references.citation: BMC Bioinformatics. 2008 Jan 23;9:40
references.pmid: 18215316
references.citation: Plant J. 2012 Oct;72(2):320-30
references.pmid: 22712876
references.citation: Mol Biol Evol. 2002 Apr;19(4):456-61
references.pmid: 11919287
references.citation: Biochim Biophys Acta. 2014 May;1840(5):1468-81
references.pmid: 24355433
references.citation: Bioinformatics. 2009 May 1;25(9):1189-91
references.pmid: 19151095
references.citation: Bioinformatics. 2011 Apr 15;27(8):1164-5
references.pmid: 21335321
references.citation: Mol Syst Biol. 2011 Oct 11;7:539
references.pmid: 21988835
references.citation: Trends Plant Sci. 2011 Feb;16(2):61-8
references.pmid: 21087891
references.citation: Science. 2002 May 3;296(5569):899-904
references.pmid: 11988572
references.citation: Proc Natl Acad Sci U S A. 2006 Oct 17;103(42):15511-6
references.pmid: 17030812
references.citation: Proc Natl Acad Sci U S A. 1994 Jan 4;91(1):11-7
references.pmid: 11607449
references.citation: Nat Protoc. 2010 Apr;5(4):725-38
references.pmid: 20360767
references.citation: Ann Bot. 2005 Nov;96(6):1027-46
references.pmid: 16176944
references.citation: Cell Mol Life Sci. 2008 Oct;65(19):3049-57
references.pmid: 18560761
references.citation: J Exp Bot. 2011 Aug;62(12):4391-8
references.pmid: 21586431
references.citation: PLoS Comput Biol. 2009 Jul;5(7):e1000440
references.pmid: 19609355
references.citation: Front Plant Sci. 2012 Feb 20;3:33
references.pmid: 22639644
references.citation: Nature. 2005 Feb 17;433(7027):728-31
references.pmid: 15716949
references.citation: Nature. 2006 Mar 30;440(7084):688-91
references.pmid: 16572174
references.citation: Genome Res. 2004 Jun;14(6):1188-90
references.pmid: 15173120
references.citation: Biochemistry. 2005 Dec 27;44(51):16826-34
references.pmid: 16363796
references.citation: Nature. 2007 Dec 20;450(7173):1184-9
references.pmid: 18097399
references.citation: Proteins. 2009;77 Suppl 9:100-13
references.pmid: 19768687
references.citation: Science. 2004 Jul 16;305(5682):354-60
references.pmid: 15256663
references.citation: Science. 2010 Apr 30;328(5978):587-91
references.pmid: 20431008
references.citation: PLoS One. 2012;7(12):e52932
references.pmid: 23300825
references.citation: PLoS One. 2010 Mar 10;5(3):e9490
references.pmid: 20224823
references.citation: Science. 2000 Oct 20;290(5491):481-6
references.pmid: 11039922
references.citation: Nucleic Acids Res. 2007;35(10):3375-82
references.pmid: 17478507
references.citation: New Phytol. 2003 Jun;158(3):419-421
references.pmid: 36056512
references.citation: Proc Natl Acad Sci U S A. 2008 Jul 22;105(29):9931-5
references.pmid: 18626020
references.citation: Science. 2005 Nov 18;310(5751):1177-80
references.pmid: 16293759
references.citation: Biol Cell. 2005 Jun;97(6):397-414
references.pmid: 15850454
references.citation: Proc Natl Acad Sci U S A. 2002 Nov 12;99(23):14893-6
references.pmid: 12397183
references.citation: Syst Biol. 2010 May;59(3):307-21
references.pmid: 20525638
references.citation: Am J Bot. 2009 Jan;96(1):228-36
references.pmid: 21628186
references.citation: Pflugers Arch. 2008 Jul;456(4):679-86
references.pmid: 18214526