Table Of ContentFlora xxx (xxxx) xxx–xxx
ContentslistsavailableatScienceDirect
Flora
journal homepage: www.elsevier.com/locate/flora
☆
Silicon content is a plant functional trait: implications in a changing world
Ofir Katz
TheDeadSeaandAravaScienceCenter,MtMasada,TamarRegionalCouncil86910,Israel
ARTICLE INFO ABSTRACT
EditedbyHermannHeilmeier Plantsilicon(Si)contentisatraitthathasgainedincreasingattentioninrecentyears,andisnowoftensuggested
Keywords: tobeaplantfunctionaltrait.ThispaperreviewstheevidencethatsupportstheinclusionofplantSicontent
Phytolith within the plant functional traits framework. Plant Si contents can vary greatly among plant taxa and en-
Siuptake vironments,reflectingmultiplicityofrolesandfunctionsinplantbiology.PlantSiuptakeandaccumulationalso
Siaccumulation affectsplantcommunityandecosystemproperties,andthusecologicalfunctioningandresponsetoenviron-
Stressadaptation mentalchange.FurtherinvestmentinstudyingplantSicontentasaplantfunctionaltraitanditsrolesineco-
Herbivory logicalprocesseswillimproveourabilitytopredictandmitigatetheconsequencesofclimatechange.
Biogeochemistry
Grasslandorigin
1. Introduction mostlyignoredinplantfunctionaltraitsliterature.Forexample,many
planttaxaareknowntoaccumulatesilicon(Si)intheirtissues,oftenas
Plantfunctionaltraitsaretraitsthatindirectlyinfluencethefitnessof variousamorphousphasesincludingsilicondoublelayers(e.g.,Schaller
an individual via their effects on its growth, reproduction and survival et al., 2013) and microscopic bodies of Opal-A (Si(OH)2·nH2O) called
(Garnier et al., 2016), whose values vary in response to environmental phytoliths(e.g.,Hodsonetal.,2005).Here,Ireviewtheevidencethat
conditions and affect ecosystem functioning (Funk et al., 2017;Garnier plant Si content is a plant trait whose multiple functions in plant re-
etal.,2016),andareoftentakenasanymorphological,physiologicalor sponsetoenvironmentalfactors,effectsonplantperformance,andef-
phenologicalfeature,measurableforindividualplants,atthecelltothe fects on plant communities and ecosystems has gained increasing ap-
whole-plant level (Perez-Harguindeguy et al., 2013). Thus, plant func- preciationinrecentyears.Theaccumulationofsuchevidencesuggests
tional traits are pivotal in linking environmental changes with plant that plant Si content is a plant functional trait that can contribute to
community and ecosystem properties, functioning and responses (Diaz modelsofenvironmentalchangeeffectsonecosystemfunctioningand
etal.,2004;Funketal.,2017;Garnieretal.,2016;Violleetal.,2014). potentially to improve their predictive power. Although this idea has
Therefore,thestudyofplantfunctionaltraitscanenableustoquantita- been expressed both implicitly and explicitly by some (Cooke and
tivelydescribehowenvironmentalvariablesaffectplanttraitvaluesand Leishman,2011a;Cookeetal.,2016;Katz,2014,2015;Schoelynckand
howplanttraitvaluesaffectecosystemfunctioning(Garnieretal.,2016). Struyf, 2016; Schoelynck et al., 2014), elaborate discussions of the
Consequently,suchanalysescanprovideparametersrequiredtodirectly potentialuseofplantSicontentasamediatingplantfunctionaltraitin
modelandpredict–andhopefullymitigate–theeffectsofenvironmental predictive models are missing. I wish to set the step stones to these
changeonecosystemfunctioning(Fig.1).Thisisamajorobjectiveinthese discussionshere.
timesofclimatechange. Inthisshortreview,IdemonstratethecaseforSicontentasaplant
Studiesofplantfunctionaltraitssofarhavefocusedalmostentirely functionaltrait.IfirstdiscussthevariabilityofSicontentsamongplants
on morphological, physiological and phenological traits, or on the and environments, which demonstrates its correspondence with other
contents ofessentialmacronutrients suchasnitrogen andphosphorus plantfunctionaltraitsandresponsetotheenvironment.Ithendiscuss
(e.g., lists in Garnier et al., 2016; Perez-Harguindeguy et al., 2013). plantSi'sroles,fromindividualplantstotheentireecosphere,andhow
Nevertheless, many plants also contain appreciable amounts of non- thistraitanditsfunctionsmayhaveevolvedovergeologictime.Finally,
essentialbutbeneficialnutrientsthatareknowntoaffectplantfitness I discuss major knowledge gaps that, if filled, will improve under-
andenvironment, andwhosecontents withintheindividual plantare standing,monitoring,predictingandmitigatingclimatechangeeffects
driven by (i.e., respond to) the environment. These traits have been onplantcommunitiesandecosystems.
☆Thisarticleispartofaspecialissueentitled:“Functionaltraitsexplainingplantresponsestopastandfutureclimatechanges”publishedatthejournalFlora
254C,2019.
E-mailaddress:[email protected].
https://doi.org/10.1016/j.flora.2018.08.007
Received16January2018;Receivedinrevisedform1August2018;Accepted7August2018
0367-2530/ © 2018 Elsevier GmbH. All rights reserved.
Please cite this article as: Ofir Katz, Flora, https://doi.org/10.1016/j.flora.2018.08.007
O.Katz Flora xxx (xxxx) xxx–xxx
convincingly attributed to plant structural support (Schoelynck et al.,
2010).PlantSicontentwasalsofoundtobenegativelycorrelatedwith
Candphenolcontents(CookeandLeishman,2012;Frewetal.,2016;
JohnsonandHartley,inpress;Schalleretal.,2012a,b),withleafni-
trogen and phosphorus content (Song et al., 2014) and thus to affect
plantstoichiometry(Schalleretal.,2012a,2016a;Songetal.,2014).
Puttogether,thereisareasonablecaseforSipartiallysubstitutingCin
plantbiology(CookeandLeishman,2011a).Nevertheless,evidencefor
Si:Ctrade-offsaremeagreandcomefromonlyafewecosystemsbutnot
from regional- or global-scale analyses (Cooke and Leishman, 2011a;
Klotzbücheretal.,2018;Schoelyncketal.,2010),andsofarlackevi-
dence for clear effects on fitness or explanatory driving mechanisms.
Therefore, further evidence is required to validate the partial sub-
stitutionofCbySi.
Notwithstandingthataplant'sSicontentisdrivenbyitstaxonomy,
phylogeny and physiology, the plant's Si content is also driven by its
environment. Intraspecific variations in plant Si contents have been
studied for many years, mostly in the highly Si-rich grasses. Plant Si
contenthasgenerallybeenshowntoincrease,forexample,withtran-
Fig. 1.A simplified model of the plant functional diversity approach. spiration(Eulissetal.,2005;Faisaletal.,2013;Katzetal.,inpress)and
Environmental variables (and especially abiotic ones) act as filters on plant herbivory intensity (Brizuela et al., 1986; Hartley, 2015; Hartley and
functionaltraitvalues.Inturn,plantfunctionaltraitvaluesdriveplantcom- DeGabriel, 2016; Katz et al., in press; Massey et al., 2008). Plant Si
munity species composition, together with biotic filters (e.g., competition).
contentsresponsestowateravailabilityarelesspredictable,anditmay
Plant community species composition and species functional trait values de-
be that plant Si content increases towards both extremely arid and
termine, together, functional trait indices (for each trait) and community
rainierconditions(Katzetal.,2013;QuigleyandAnderson,2014).
functional diversity indices(fortraitassemblages). Thelatter twodrive eco-
ApartfromtheobviousdependenceonSisupply,mostfocussofar
system properties through the effects of individual species or of species as-
semblages. has been put on the effects of water availability and herbivory (Katz
etal.,2013,2014,inpress).Thisisamirrorreflectionoftheextensive
studiesofplantSi'srolesasanadaptationtoariditybyreducingwater
2. VariabilityofplantSicontents
loss, improving water use efficiency and eliciting stomatal responses
and antioxidant activity (e.g., Coskun et al., 2016; Gong et al., 2005;
Althoughdataisstillmissingformanyplantfamilies(Katz,2015),it
Zhu and Gong, 2014) and as an antiherbivory defence due to its low
isclearnowthatSicontentsvarygreatly(toasmanyas2–3ordersof
nutritionalvalueandtendencytoaccumulateasmicroscopicglass-like
magnitude, from nearly 0% to over 10% of plant dry weight) among
silica particles (Correa et al., 2005; Frew et al., 2016, 2017a, 2017b;
plant families, orders and phyla (Hodson et al., 2005; Katz, 2015;
HartleyandDeGabriel,2016;MasseyandHartley,2006,2009;Massey
Trembath-Reichert et al., 2015). Hodson et al. (2005), for example,
et al., 2007a; Wieczorek et al., 2015a). Although laboratory experi-
foundthattaxonomicorderaccountsfor67%ofinterspecificvariability
ments tend to demonstrate that plant Si contents are higher at high
inSicontentsamongseedplants.Thesourcesofthisvariabilityremain
wateravailability,extremedroughtandstrongherbivorypressure,such
obscureandsomewhatdisputed(Katz,2015;Strömbergetal.,2016).
trendsarelessfrequentlyfoundinnaturallygrowingplants(Katzetal.,
Fromanevolutionaryecologyperspective,onewouldexpectatraitto
2013,2014,inpress).Suchdiscrepanciespossiblyexistbecauseplants
persist within a clade if it confers some advantage expressed in im-
that grow in natural ecosystems are exposed to various other con-
proved fitness. These implies that taxonomic variability can be ex-
founding variables, including soil silicon and nutrient availability,
plained by ecological roles and functions. However, the roles and
temperature, transpiration and interactions with other plants, patho-
functionsofplantSiandthevariationsintheirextentamongtaxawith
gens and animals (in press). They may also stem from interactions
varying Si contents are not always properly understood (Cooke and
among various environmental variables. Moreover, Si may have dif-
Leishman,2011a;Katz,2014,2015;Strömbergetal.,2016).
ferentroles(e.g.,adaptationtoaridity,anti-herbivorydefence,etc.)in
ThevariabilityofplantSicontentsisreflectedinitstrade-offswith
variousecosystems,andtovariousdegrees.ThissuggeststhatplantSi
other plant components. It has long been known that Si contents are
contentinnaturallygrowingplantsmaybeexposedtonaturalselection
higheringrasses–andmoregenerallyinmostcommelinidmonocots–
byvariousagentsthatdonotexistinthelaboratory(Garbuzovetal.,
than in non-commelinid monocots and dicots (Hodson et al., 2005;
2011;HartleyandDeGabriel,2016;Katz,2014;Katzetal.,2013,2014,
Katz, 2015; Trembath-Reichert et al., 2015). In contrast, calcium ox-
inpress;QuigleyandAnderson,2014;Soininenetal.,2013).Likewise,
alate crystals – another inorganic plant component comparable to
short-term controlled experiments can seldom account for long-term
phytoliths in function – are considerably more abundant in non-com-
plantinteractionswiththeenvironmentor fornaturalselection (Katz
melinidmonocotsanddicotsthanincommelinidmonocots(Franceschi
et al., 2014; in press; Quigley and Anderson, 2014; Soininen et al.,
andNakata,2005;PrychidandRudall,1999).Thiscontrastsuggestsa
2013).
trade-off between plant Si and calcium contents, which appears rea-
sonable since phytoliths and calcium oxalate crystals are thought to AtmosphericCO2concentrationsmayalsoaffectplantSiuptakeand
playcomparable rolesinplantstructuralsupportanddefence against accumulation. First and foremost, under higher CO2 concentrations
plantsreducestomatalconductanceandhencetranspirationasamotive
herbivores(seereviewsinCookeandLeishman,2011a;Franceschiand
forceforSiuptake(Eulissetal.,2005;Faisaletal.,2013).Furthermore,
Nakata,2005;andfurtherdiscussionofSirolesinplantsbelow).
Si:Ctrade-offsandputativepartialsubstitutionofCbySisuggestthatat
Nolessstrikingistheevidencefortrade-offsbetweenSiandcarbon
(C)-based plant components. Raven (1983) was among the first to lower CO2 concentrations plantsmay invest more in Si-based adapta-
tions, although this has not been demonstrated empirically so far.
suggest such a trade-off, estimating the metabolic cost of Si-based
mechanical support to be 10–20 times less than that of lignin. Thirty EvidencefortheeffectofelevatedatmosphericCO2concentrationson
plant Si contents are inconsistent (Fulweiler et al., 2015; Frew et al.,
yearslater,atrade-offofSicontentwithligninandcellulosecontents
2017a;JohnsonandHartley,inpress;Lietal.,2014),althoughane-
was found (Klotzbücher et al., 2018; Schoelynck et al., 2010) and
gative effect in grasses (Li et al., 2014) may be explained by C
2
O.Katz Flora xxx (xxxx) xxx–xxx
enrichment relieving postulated Si:C trade-off and allowing plants to foods (Massey and Hartley, 2009; Massey et al., 2006) and to have
relylessonSiasasubstituteforC. slowergrowthrateswhenfeedingonSi-richdiets(Frewetal.,2017a,
Different ecosystem types and biomes are often characterised by 2017b; Massey and Hartley, 2006, 2009; Kvedaras et al., 2007;
differentplantcladesanddifferentstrategies(i.e.,differenttrade-offs). Wieczoreketal.,2015a).
With that addition of intraspecific variabilities in plant Si contents Theotherwayaround,herbivorybyinvertebratesandvertebrates
alongenvironmentalgradients,thissuggeststhatecosystemtypesand (HartleyandDeGabriel,2016;Masseyetal.,2007b)hasbeenshownto
biomeswilldifferinplantcommunitySicontents.CareyandFulweiler induceSiuptakeandaccumulationbygrasses.Althoughthedegreeof
(2012),basedonHodsonetal.(2005),estimatedSipercentagesofthe induction varies among herbivore types and may be masked by the
total plant biomass for the world's biomes, and found that biomes in involvement of other environmental conditions or by grazing history
whichgrassesaremoreabundanttendtobericherinSi(perbiomass) (Katzetal.,2014;QuigleyandAnderson,2014;Soininenetal.,2013),
andmoreproductive.Themechanismsunderlyingthispatternareun- itappearstohaveacumulativeeffectandbestrongerwithincreasing
clearandwerenotmethodicallystudiedsofar,butarelikelyrelatedto herbivory duration or frequency. Festuca ovina and Lolium perenne
theadaptiveroleofSiinsomeplantspeciesandSi’shighcontentsin plants that were subjected to repeated damage by locust and voles
grasses,whicharedominantfast-growingspecies.Nevertheless,atthis contained2–4timesmoreSithanplantsthatweresubjectedtoasingle
point in time, the shortage in global-scale empirical field studies of damageevent(Masseyetal.,2007b).Thisinteractionhassomeintri-
individual plants’ and community-level Si contents along large en- guingoutcomes.First,somegrassspecieshavebeenshowntohaveas
vironmental gradients hinders developing global models ofhow com- much as twice the Si contents in more heavily grazed localities
munity-level Si contents correspond to environmental variables and (Brizuela et al., 1986), while similar patterns are not found in plant
howcommunity-levelSicontentsaffectecosystemfunctioning(Fig.1). species with lower Si contents (Katz et al., 2014). Second, if plant
Oncesuchquantitativeknowledgeexists,itcanbeusedtoparametrise speciesdifferintheirabilitytotakeupandaccumulateSiasadefence,
global models of the effects of environmental variables on ecosystem their competitive ability may depend on Si supply (Garbuzov et al.,
functioning(e.g.,Crameretal.,2001;Diazetal.,2004)andtoimprove 2011).Third,herbivorepopulationcycleshavebeenfoundtobedriven
suchmodels’predictivepower. bygrassSicontentsandtobesynchronisedwithplantSicontentcycles
(Hartley, 2015; Massey et al., 2008; Wieczorek et al., 2015b). Thus,
3. PlantSiasanadaptationtostress plantSicontentdoesnotonlyaffecttheplant,butalsoitsneighbours
andherbivores,andthusecosystem-levelcomponentsandprocesses.
Siliconprovidesplantswithprotectionfrommanystressesthatare
inflictedbytheabioticenvironment(CookeandLeishman,2016)and 4. PlantSiinecosystemsandtheecosphere
bypathogens(Fauteauxetal.,2005;VanBockhavenetal.,2013).Al-
thoughthemechanismsunderlyingsuchprotectiverolesarenotalways Silicon'smanyrolesinplantphysiologysuggestthatinter-andintra-
understood,itisnowknownthatthesemechanismsvaryintheirmode specificvariabilityinplantSicontents,uptakeandaccumulationcap-
ofoperation. Sican inhibit toxicmetal uptakebythe root(Maet al., abilities – as well as Si roles and functions in plant–environment in-
2015)andimprovetheacquisitionorbeneficialandessentialminerals teractions – may affect how plant communities are assembled and
such as phosphorus (Ma and Takahashi, 1990; Gao et al., 2011; Neu partly determine their properties (e.g., structure, species composition
et al., 2017). Likewise, phytoliths act as physical barriers against pa- andinteractionnetworks).Nevertheless,evidenceforthisisstillscanty.
thogenintrusion(Caietal.,2008).Withintheshoot,Sicanbebound Brizuela et al. (1986) demonstrated how higher grazing intensity in-
withtoxicmetalsandthusneutralisethemandtransportthemtospe- creases Si contents in grass species. Garbuzov et al. (2011) demon-
cialisedcompartments(Cockeretal.,1998;Wangetal.,2004),main- stratedhowlocustprefersgrassspecieswithlowerSicontents,which
tain membrane and cell wall stability under stress (He et al., 2010, aremorepalatable,resultinginthemhavingsmallerbiomassandbe-
2015), and mediate apoplastic and symplastic osmotic gradients cominglesscompetitivecomparedwithgrassspeciesthataccumulate
(Coskunetal.,2016).Intheleaf,Sidepositionhasbeenshowntore- more Si under similar conditions. Jacobs et al. (2013) demonstrated
duceultra-violetabsorbance(Gotoetal.,2003;Schalleretal.,2013),to howSiavailabilityfacilitatestheformationandmaintenanceofgrass-
reduceleaftemperature(Wangetal.,2005)andtoparticipateinreg- dominatedvegetationintidalmarshesandestuaries.Finally,observa-
ulatingstomatalconductance(Hattorietal.,2005).Moresystemically, tions that Si-rich habitats are more frequently dominated by grasses
Si has been shown to promote anti-pathogenic (Cai et al., 2008; Van whilecalcium-richhabitatsaremorefrequentlydominatedbylegumes
Bockhaven et al., 2013) and anti-oxidative activity (Fialova et al., in (Schaller et al., 2016b) enabled developing a theoretical model that
press; Gong etal., 2005; He et al.,2010), root growth under drought explains the succession from legume-dominated to grass-dominated
stress (Hattori et al., 2005), stress signalling (Van Bockhaven et al., pasturelands.Calcicmineralsaremoreeasilyerodibleandthuscalcium
2013)andtoregulatetheexpressionofsomegenesthatareassociated is more available in early successional stages providing an advantage
withstresstolerance(Fauteauxetal.,2006;Riosetal.,2017). forlegumes,butovertimecalciumleachesoutoftheecosystemwhile
Phytolithsand otherSi depositswithin planttissuesareknown to Siaccumulates,shiftingtheadvantagetowardsgrasses(Schalleretal.,
have antiherbivoryroles inplants. Thesestructures’ rigidityincreases 2017).
plant tissue abrasiveness (Massey and Hartley, 2006; Massey et al., By extension, the fact that Si uptake, accumulation and functions
2006,2007a;Wieczoreketal.,2015a).Thus,phytolithsandSideposits varyamongtaxa(Katz,2014)suggeststhatSiavailabilitycanpartially
candamageherbivoremouthparts,mostlybyerodingorwearingthem. determinetherelativeabundanceandecologicaladvantageofgrasses
Thishasbeendemonstratedbothoninvertebrate(MasseyandHartley, over species that take up and accumulate less Si and utilise it less.
2009; Massey et al., 2006) and vertebrate (Rivals et al., 2014; Therefore,itcanmodulateplantcommunitystructureandcomposition
Wieczoreketal.,2015a)herbivores,althoughdamagedegreemayvary (e.g.,asproposedbySchalleretal.,2017),andeventuallycommunity-
amongherbivorespecies(Sansonetal.,2007).PlantSistructuresalso level adaptation to abiotic environmental conditions (e.g., Cooke and
physically protect cell contents, hence reducing herbivores' ability to Leishman, 2016) and herbivory (e.g., Massey et al., 2007a). Further-
fullyextractanddigestcells'organiccontent(Huntetal.,2008;Massey more,herbivoresmayprefertograzeinplantcommunitieswithlower
andHartley,2006,2009;Wieczoreketal.,2015a).Moreover,itisalso Si contents (Frew et al., 2016, 2017a; Hunt et al., 2008; Massey and
feasiblethatSithatisingestedbyherbivoresoccupiesstomachvolume Hartley,2006,2009),orthemselvessufferfromlowergrowthratesand
that could have been occupied by nutritional organic compounds, population growth when grazing in plant communities with high Si
hence increasingsatiety sensation relative to actual nutritional value. contents(Hartley,2015;Masseyetal.,2008).Hence,Siavailabilityand
Consequently, some herbivores show low preference for Si-rich plant itsuptakeandaccumulationinplantscanfavourherbivoreandanimal
3
O.Katz Flora xxx (xxxx) xxx–xxx
communitieswithspeciesthataremoreadaptedandlessaffectedbySi- sink but also a source. Likewise, the relative contributions of various
richdiets. biomes to the C cycle through the three abovementioned sinks vary
However, the effects of plant Si uptake and accumulation clearly greatly,assomerecentstudieshaveshown(CareyandFulweiler,2012;
exceedthecommunitylevelandaffectecosystems.Likeotherelements Song et al., 2017). Phytolith carbon sequestration fluxes are approxi-
and nutrients that comprise parts of organismal tissues, Si is also re- mately 1–1.5t CO2km−2 yr−1 in forests and 3–4t CO2km−2 yr−1in
cycled in ecosystems, with plants playing a key role in the process croplands, with little variation among continents, while grassland
(CareyandFulweiler,2012;Struyfetal.,2009).PlantstakeupSifrom fluxes range from approximately 1t CO2km−2 yr−1 in Europe and
thesoilasmonosilicicacid(H4SiO4)andeventuallyreleaseitbackto North America to 2.5–3t CO2km−2 yr−1in South America and Aus-
thesoilindetritusasmonosilicicacidorasamorphoussilica(Alexandre tralia (Song et al., 2017). Therefore, the causal networks underlying
etal.,2011;Cornelisetal.,2010;Farmeretal.,2005).Throughtheir biome- and global-scale processes and variations in Si–C interactions
abilitytotakeupandreleaseSi,plantsmobiliseSiandtakepartinits are still ambiguous. Moreover, the effects of plant Si uptake and ac-
export from terrestrial ecosystems to rivers, lakes and oceans (Carey cumulationontheCcyclearetheresultsofmultiplemechanismsacting
and Fulweiler, 2012; Conley and Carey, 2015; Cornelis et al., 2010; atmultiplescales(fromindividualplantstoecosystems),respondingto
Derryetal.,2005;Struyfetal.,2009).TheamountofdissolvedSire- multipleabioticandbioticvariables,andplayingvariousrolesinplant
leasedfromplantlitterrangesfrom3to8tkm−2yr−1inforestsand biology and ecology (e.g., climate, soil, herbivory and pathogeny).
saltmarshes(Jacobsetal.,2013).InHawaiianforest,forexample,itis Therefore, understanding and predicting how environmental changes
estimated that 68–90% of Si carried by stream water has passed mayaffectplantSiuptakeandaccumulationattheregionaltoglobal
throughphytoliths(Derryetal.,2005).PlantscanthereforeincreaseSi scales and what are the consequences for the C cycle remains a for-
availabilitydownstream,facilitatingconditionsforaquaticSiaccumu- midablechallenge.
lating plants and diatoms (Derry et al., 2005; Farmer et al., 2005;
Jacobs et al., 2013; Ronchi et al., 2013; Schoelynck et al., 2014; 5. Anevolutionaryperspective
Vandevenne et al., 2013). Pastures and grasslands, for example, can
export as much as 2t dissolved Si km−2 yr−1 to adjacent rivers Extantspeciesandecosystemsaretheresultoflong-termdeep-time
(Vandevenneetal.,2013).SuchprocessesofincreasingSiavailability evolutionaryprocesses.Theseprocessescanthereforeexplainwhether
mayhaveplayedaroleinpromotingtheevolutionofSi-accumulating orhowextantspeciesandecosystemsareadaptedandmayrespondto
plantsandalgae(Falkowskietal.,2004;Katz,2015). environmentalchange(BentonandEmerson,2007;Crispetal.,2009;
The global Si and C cycles are sometimes thought to be coupled, Lamsdell et al., 2017; Wiens and Donoghue, 2004). Phytoliths' pre-
sinceplants'roleinSicyclingformsthreeCsinks.First,Siaccumulation servation in soils and sediments makes them a powerful tool for re-
improvesplantperformance(seereviewinprevioussection).Careyand constructing past vegetation formations, mostly during the Cainozoic
Fulweiler (2012)have shown that Si-richbiomes tend tohave higher (e.g.,Bremondetal.,2004;Coeetal.,2017;Fengetal.,2017;Lietal.,
NPPthanSi-poorbiomes,andcalculatedthattheyaccountfor55%of 2018; Strömberg, 2004, 2005; Strömberg et al., 2013) and in archae-
globalterrestrialNPPandCO2regulation.Second,bytakinguplarge ological studies (e.g., Katz et al., 2007; Tsartsidou et al., 2008), and
amounts oflabile(dissolved)Si fromthe soilsandaccumulatingitas potentiallyalsoindeepertime.
amorphous silica, plants may considerably change the stoichiometric Nevertheless, the roles plant Si itself played in the evolutionary
balancebetweendissolvedandmineralSiphasesandacceleratesilicate historyofplants,theiradaptationtoabioticandbioticenvironmental
dissolution (Alexandre et al., 1997; Borrelli et al., 2010; Carey and conditions, and plant–herbivore interactions remain obscure and dis-
Fulweiler, 2016; Cornelis and Delvaux, 2016; Farmer et al., 2005; puted.Avibrantdiscussioninrecentyearsrevolvesaroundthepossible
Hinsinger et al., 2001), a process that consumes atmospheric CO2 roleofplantSiintheglobalexpansionofthegrasslandbiomeonsev-
(Exley,1998;SchuilingandKrijgsman,2006;Songetal.,2012;Street- eral continents during the mid-late Cainozoic (Edwards et al., 2010;
Perrott and Barker, 2008). Third, some of the organic C produced by Strömberg, 2011). Although atmospheric changes (CO2 concentration
plants can be occluded within phytoliths, thus potentially becoming decrease,coolinganddrying)areusuallytakenasthekeyinitiatorsof
sequestered within soils and sediments for as much as millennia thisexpansion,reinforcementbyecologicalprocessesisalsoproposed
(Alexandreetal.,2015,2016;Lietal.,2013;Songetal.,2012,2017). (Beerling and Osborne, 2006; Edwards et al., 2010; Kürschner et al.,
However, the contribution of this latter sink to the global C cycle is 2008).PlantSiissometimesthoughttohaveplayedanappreciablepart
disputed. Santos and Alexandre (2017) suggest that post-depositional in grassland evolution and expansion, due to its roles in protecting
processessuchasoxidationandmineralisationconsiderablyreducethe plantsfromdrought(Coskunetal.,2016;Gongetal.,2005;Zhuand
amount of phytolith-occluded C that is actually stored for such long Gong,2014)andherbivory(Frewetal.,2017a;HartleyandDeGabriel,
time periods. Reyerson et al. (2016) suggest that the source of some 2016;MasseyandHartley,2006,2009;Masseyetal.,2007a).Oneof
phytolith-occluded C is from the soil itself, i.e., that it is transferred the driving and reinforcing ecological processes is a putative co-evo-
between pools rather than reflecting net sequestration. Furthermore, lutionary escalation between Si-rich grasses and large mammalian
Songetal.(2017)estimatedphytolith-relatedCsequestrationinglobal herbivores possessing abrasion-adapted dentition (MacFadden, 1997;
terrestrialbiomesat0.0428GtCyr−1,suggestingitcontributeslittleto Stebbins, 1981). Recent evidence challenge the significance of this
theglobalterrestrialsinkof1.9GtCyr−1(Quereetal.,2016). putative co-evolution. Northern hemisphere grasslands predate mam-
Global models of plant Si effects on the C cycle are still at their malian abrasion-adapted dentition by several million years
infancy, and some major temporal and spatial variations need to be (Mihlbachleretal.,2011;SolouniasandSemprebon,2002;Strömberg,
resolved. In the short run plant Si uptake and accumulation removes 2005, 2006, 2011), whereas in South America mammalian abrasion-
andsequestersatmosphericCO2,whereasinthelongrunitispossible adapted dentition predates grasslands by several million years (Dunn
thatSi'srolesinimprovingplantperformanceandSi:Ctrade-offsmay et al., 2015). Hence, there appears to be no clear coalescence in the
resultinplantsimprovingtheirCuseefficiencyandreducingtheirCO2 evolution of grasslands and mammalian abrasion-adapted dentition,
consumption.Furthermore,siliconuptakeaffectslitterchemicalprop- noraconsistentorderofevents,aswouldbeexpectedifthetwotraits
erties and thus accelerates decomposition rates (Marxen et al., 2015; co-evolvedorifoneevolvedasresultoftheother.
Schaller and Struyf, 2013; Schaller et al., 2014). Schaller and Struyf Morerecently,attemptshavebeenmadetotracetheearlyorigins
(2013)foundthatPhragmitesaustralislittermasslossafter6weekswas andevolutionofSiaccumulationamongangiosperms,usingmolecular
2%and18%forplantsgrownwithoutandwithSi,respectively.Marxen phylogenies.Strömbergetal.(2016)foundthatemergencedatesofSi-
etal.(2015)foundthatricestrawlost60%and68%ofitscarbonafter rich clades do not coalesce with any likely selective force, including
33daysinalitterbag.ThesesuggestthatplantSiuptakeisnotonlyaC herbivory, habitat openness, aridity and atmospheric CO2 decline.
4
O.Katz Flora xxx (xxxx) xxx–xxx
Nevertheless, gene divergence times often overestimate clade diver- Acknowledgements
gence times and do not reflect trait emergence or ecological success
(Katz, 2015, 2018). Taking this into account, Katz (2015) suggested IthankSimchaLev-Yadun(UniversityofHaifa)forencouragingme
thattheindependentearlydiversificationofSi-richangiospermclades to write the manuscript. A discussion with Julia Cooke (Open
may be dated to the Late Cretaceous and be linked in part to the si- University,UK)contributedtothemanuscript'soutlineandscope.Two
multaneous evolution of abrasion-adapted dentition in some dinosaur anonymousreviewersprovidedgoodadvicetoimprovethemanuscript.
andearlymammaliangroups.Ancestralgrassphytolithsinacoprolite
producedbyanherbivorousdinosaurfromtheLateCretaceous(Prasad References
et al., 2005), and more recently and more interestingly the abrasion-
adapteddentitionofanEarlyCretaceousdinosaur(Wuetal.,inpress) Alexandre,A.,Meunier,J.D.,Colin,F.,Koud,J.M.,1997.Plantimpactonthebiogeo-
fitthishypothesis.ImprovingourunderstandingonhowplantSiuptake chemicalcycleofsiliconandrelatedweatheringprocesses.Geochem.Cosmochem.
Acta61,677–682.
and accumulation corresponds to environmental variations and affect
Alexandre,A.,Bouvet,M.,Abbadie,L.,2011.TherolesofsavannasintheterrestrialSi
otherecosystemcomponentswillallowustomorecriticallytestsuch cycle:acase-studyfromLamto,IvoryCoast.Glob.Planet.Change78,162–169.
hypothesesusingquantitativedataandmodels. Alexandre,A.,Basile-Doelsch,I.,Delhaye,T.,Borshneck,D.,Mazur,J.C.,Reyerson,P.,
Santos,G.M.,2015.Newhighlightsofphytolithstructureandoccludedcarbonlo-
The evidence for Si:C trade-offs (Cooke and Leishman, 2012;
cation:3-DX-raymicroscopyandNanoSIMSresults.Biogeosciences12,863–873.
Schalleretal.,2012a,b;Schoelyncketal.,2010),theobservedeffects Alexandre,A.,Balesdent,J.,Cazevieilles,P.,Chevassus-Rosset,C.,Signoret,P.,Mazur,
ofatmosphericCO2concentrationsonplantSicontents(Johnsonand J.C.,Harutyunyan,H.,Doelsch,E.,Basile-Doelsch,I.,Miche,H.,Santos,G.M.,2016.
Directuptakeoforganicallyderivedcarbonbygrassrootsandallocationinleaves
Hartley,inpress)andthatlowatmosphericCO2concentrationremains andphytoliths:13Clabellingevidence.Biogeosicences13,1693–1703.
apossibleprerequisiteforgrasslandexpansion(Strömberg,2011)imply Beerling,D.J.,Osborne,C.P.,2006.Theoriginofthesavannabiome.Glob.ChangeBiol.
thatSiaccumulationcanconferanadvantagetoSi-richcladeslikethe Bioenergy12,2023–2031.
grassesinalowCO2environment.Thisunexploredpossibilitysuggests Bentdoinv,eMrsi.fiJ.c,aEtimonerasocnco,rBd.iCn.g,2to00th7e.Hfooswsildriedcolirfdebaencdommoelseocudlaivreprshey?loTgheenedtyicnsa.micsof
thatthecurrentincreaseinatmosphericCO2concentrationsmayimpair Palaeontology50,23–40.
thecompetitiveabilityofgrassesandotherSi-richplantsworldwide. Borrelli,N.,Alvarez,M.F.,Osterrieth,M.L.,Marcovecchio,J.E.,2010.Silicacontentin
soilsolutionanditsrelationwithphytolithweatheringandsilicabiogeochemical
cycleinTypicalArgiudollsofthePampeanPlain,Argentina–apreliminarystudy.
6. Implicationsandfuturedirections
Int.J.SoilSedimentWater10,983–994.
Bremond,L.,Alexandre,A.,Vela,E.,Guiot,J.,2004.Advantagesanddisadvantagesof
The surge of studies of plant Si accumulation has clearly demon- phytolithanalysisforthereconstructionofMediterraneanvegetation:anassessment
basedonmodernphytoliths,pollenandbotanicaldata(Luberon,France).Rev.
stratedSi'smanyrolesinplantlife–providingthemwithmechanical
Palaeobot.Palynol.129,213–228.
supportandprotectionformamultitudeofabioticandbioticstresses– Brizuela,M.A.,Detling,J.K.,Cid,M.S.,1986.Siliconconcentrationofgrassesgrowingin
and its effects on plant performance, plant community structure and siteswithdifferentgrazinghistories.Ecology67,1098–1101.
Cai,K.,Gao,D.,Luo,S.,Zeng,R.,Yang,J.,Zhu,X.,2008.Physiologicalandcytological
ecosystem- and global-scale processes. Hidden in plain sight, plant Si
mechanismsofsilicon-inducedresistanceinriceagainstblastdisease.Pysiol.Plant.
contentisaplantfunctionaltraitlinkingenvironmentalconditionswith 134,324–333.
ecological functioning. Achieving a better understanding of the me- Carey,J.C.,Fulweiler,R.W.,2012.Theterrestrialsiliconpump.PLoSOne7,e52932.
Carey,J.C.,Fulweiler,R.W.,2016.Humanappropriationofbiogenicsilicon–thein-
chanismsbywhichplantSicontentrespondstoenvironmentalchange
creasingroleofagriculture.Funct.Ecol.30,1331–1339.
and affects ecological functioning at various spatial and temporal Cocker,K.M.,Evans,D.E.,Hodson,M.J.,1998.Theameliorationofaluminiumtoxicityby
scales, will surely improve the predictive power of models of climate siliconinwheat(TriticumaestivumL.):malateexudationasevidenceforaninplanta
change effects on ecosystem structure and functioning (e.g., Cramer mechanism.Planta204,318–323.
Coe,H.H.G.,Souza,R.C.C.L.,Duarte,M.R.,Rickardo,S.D.F.,Mahcado,D.O.B.F.,Macario,
etal.,2001). K.C.D.,Silva,E.P.,2017.Characterisationofphytolithsfromthestratigraphiclayers
However, since research of plant Si is not yet as developed as re- oftheSambaquidaTarioba(RiodasOstras,RJ,Brazil).Flora236–237,1–8.
searchofotherplantfunctionaltraits,sometheoreticalgapsstillhinder Conley,D.J.,Carey,J.C.,2015.Silicacyclingovergeologictime.Nat.Geosci.8,431–432.
Cooke,J.,Leishman,M.R.,2011a.Isplantecologymoresiliceousthanwerealise?Trends
usfromachievingthisgoal.TherolesofplantSiinplantbiologyarenot
PlantSci.16,61–68.
fully explored (Cooke and Leishman, 2011a; Katz, 2014, 2015), and Cooke,J.,Leishman,M.R.,2011b.Siliconconcentrationandleaflongevity:issilicona
may vary among taxa (Katz, 2014). Although understanding the evo- playerintheleafdrymassspectrum?Funct.Ecol.25,1181–1188.
Cooke,J.,Leishman,M.R.,2012.Tradeoffsbetweenfoliarsiliconandcarbon-basedde-
lutionary history of this trait may signify a leap forward in the latter
fences:evidencefromvegetationcommunitiesofcontrastingsoiltypes.Oikos121,
matter,itremainslargelyelusive(Katz,2015;Strömbergetal.,2016). 2052–2060.
Possible interactions of plant Si content with other plant functional Cooke,J.,Leishman,M.R.,2016.Consistentalleviationofabioticstresswithsiliconad-
dition:ameta-analysis.Funct.Ecol.30,1340–1357.
traits have been explored only recently, and their sources and con-
Cooke,J.,DeGabriel,J.L.,Hartley,S.E.,2016.Thefunctionalecologyofplantsilicon:
sequences are little understood (Cooke and Leishman, 2011a, 2011b, geosciencestogenes.Funct.Ecol.30,1270–1276.
2012; Schaller et al., 2012a, 2012b, 2016a; Schoelynck et al., 2010; Cornelis,J.T.,Delvaux,B.,2016.Soilprocessesdrivethebiologicalsiliconfeedbackloop.
Funct.Ecol.30,1298–1310.
Songetal.,2014).Thebiologicalmechanismsthatunderlieintra-spe-
Cornelis,J.T.,Ranger,J.,Iserentant,A.,Delvaux,B.,2010.Treespeciesimpacttheter-
cific variations in plant Si content along environmental gradients are restrialcycleofsiliconthroughvariousuptakes.Biogeochemistry97,231–245.
unclear(Katzetal.,2013,2014,inpress;QuigleyandAnderson,2014; Correa,R.S.B.,Moraes,J.C.,Auad,A.M.,Caravalho,G.A.,2005.Siliconandacibenzolar-
Soininenetal.,2013),inpartduetodiscrepanciesbetweencontrolled S-methylasresistanceinducersincucumber,againstthewhiteflyBemisiatabaci
(Gennadius)(Hemiptera:Aleyrodidae)biotypeB.Neotrop.Entomol.34,429–433.
experimentsandfieldstudies(Katzetal.,inpress).Consequently,we Coskun,D.,Britto,D.B.,Huynh,W.Q.,Kronzucker,H.J.,2016.Theroleofsiliconin
stillhaverelativelylittleunderstandingofhowplantSicontentsvary higherplantsundersalinityanddroughtstress.Front.PlantSci.7,1072.
among ecosystem types and biomes in response to environmental Cramer,W.,Bondeau,A.,Woodward,F.I.,Prentice,I.C.,Betts,R.A.,Brovkin,V.,Cox,
P.M.,Fisher,V.,Foley,J.A.,Friend,A.D.,Kucharik,C.,Lomas,M.R.,Ramankutty,N.,
conditions and how these variations affect variations in ecosystem
Sitch,S.,Smith,B.,White,A.,Young-Molling,C.,2001.Globalresponseofterrestrial
functioning (Carey and Fulweiler, 2012; Jacobs et al., 2013; Schaller ecosystemstructureandfunctiontoCO2andclimatechange:resultsfromsixdy-
etal.,2017).Acquiringsufficientdataandknowledgetofillthesegaps namicglobalvegetationmodels.Glob.ChangeBiol.7,357–373.
Crisp,M.D.,Arroyo,M.T.K.,Cook,L.G.,Ganodlfo,M.A.,Jordan,G.J.,McGlone,M.S.,
willcontributetoourunderstandingofplantcommunityassemblyand
Weston,P.H.,Westoby,M.,Wilf,P.,Linder,H.P.,2009.Phylogeneticbiomecon-
structure and of ecosystem functioning. Incorporating plant Si into servatismonaglobalscale.Nature458,754–758.
models ofecosystems’ and global biogeochemicalcycles’ responsesto Derry,L.A.,Kurtz,A.C.,Ziegler,K.,Chadwick,O.A.,2005.Biologicalcontrolofterrestrial
silicacyclingandexportfluxestowatersheds.Nature433,728–731.
climatechange,onceappropriatedataexists,isverylikelytoimprove
Diaz,S.,Hodgson,J.G.,Thompson,K.,Cabido,M.,Cornelissen,J.H.C.,Jalili,A.,
such models’ predictive power and hence our ability to predict and Montserrat-Marti,G.,Grime,J.P.,Zarrinkamar,F.,Asri,Y.,Band,S.R.,Vasconcelo,
mitigate climate change effects on ecosystems and global biogeo- S.,Castro-Diez,P.,Funes,G.,Hamzehee,B.,Khoshnevi,M.,Perez-Harguindeguy,N.,
Perez-Rontome,M.C.,Shirvany,F.A.,Vendramini,F.,Yazdani,S.,Abbas-Azimi,R.,
chemicalcycles.
5
O.Katz Flora xxx (xxxx) xxx–xxx
Bogaard,A.,Boustani,S.,Charles,M.,Dehghan,M.,deTorres-Espuny,L.,Falczuk,V., siliconcompositionofplants.Ann.Bot.96,1027–1046.
Guerrero-Campo,J.,Hynd,A.,Jones,G.,Kowsary,E.,Kazemi-Saeed,F.,Maestro- Hunt,J.W.,Dean,A.P.,Webster,R.E.,Johnson,G.N.,Ennos,A.R.,2008.Anovelme-
Martinez,M.,Romo-Diez,A.,Shaw,S.,Siavash,B.,Villar-Slavador,P.,Zak,M.R., chanismbywhichsilicadefendsgrassesagainstherbivores.Ann.Bot.102,653–656.
2004.Theplanttraitsthatdriveecosystems:evidencefromthreecontinents.J.Veg. Jacobs,S.,Müller,F.,Teuchies,J.,Oosterlee,L.,Struyf,E.,Meire,P.,2013.Thevege-
Sci.15,295–304. tationsilicapoolinadevelopingtidalfreshwatermarsh.Silicon5,91–100.
Dunn,R.E.,Strömberg,C.A.E.,Madden,R.H.,Kohn,M.J.,Carlini,A.A.,2015.Linked Johnson,S.N.,Hartley,S.E.,2017.Elevatedcarbondioxideandwarmingimpactsilicon
canopy,climateandfaunalevolutionintheCenozoicofPatagonia.Science347, andphenolic-baseddefencesdifferentlyinnativeandexoticgrasses. inpress.Glob.
258–261. ChangeBiol.Bioenergy.
Edwards,E.J.,Osborne,C.P.,Strömberg,C.A.E.,Smith,S.A.,Bond,W.J.,Christin,P.A., Katz,O.,2014.Beyondgrasses:thepotentialbenefitsofstudyingsiliconaccumulationin
Cousins,A.B.,Duvall,M.R.,Fox,D.L.,Freckleton,R.P.,Ghannoum,O.,Hartwell,J., non-grassspecies.Front.PlantSci.5,376.
Huang,Y.,Janis,C.M.,Keely,J.E.,Kellogg,E.A.,Knapp,A.K.,Leakey,A.D.B.,Nelson, Katz,O.,2015.Silicaphytolithsinangiosperms:phylogenyandearlyevolutionaryhis-
D.M.,Saarela,J.M.,Sage,R.F.,Sala,O.E.,Salamin,N.,Still,C.J.,Tipple,B.,2010. tory.NewPhytol.208,642–646.
TheoriginsofC4grasslands:intgratingevolutionaryandecosystemscience.Science Katz,O.,2018.ExtendingthescopeofDarwin’s’abominablemystery’:integrativeap-
328,587–591. proachestounderstandingangiospermoriginsandspeciesrichness.Ann.Bot.
Euliss,K.W.,Dorsey,B.L.,Benke,K.C.,Banks,M.K.,Schwab,A.P.,2005.Theuseofplant 121,1–8.
tissuesiliconcontentforestimatingtranspiration.Ecol.Eng.25,343–348. Katz,O.,Gilead,I.,Bar(Kutiel),P.,Shahack-Gross,R.,2007.Chalcolithicagriculturallife
Exley,C.,1998.Siliconinlife:abioinorganicsolutiontobioorganicessentiality.J.Inorg. atGrar,NorthernNegev,Israel:dryfarmedcerealsanddung-fueledhearts.Paleorient
Biochem.69,139–144. 33,101–116.
Faisal,S.,Callis,K.L.,Slot,M.,Kitajima,K.,2013.Transpiration-dependentpassivesilica Katz,O.,Lev-Yadun,S.,Bar(Kutiel),P.,2013.Plasticityandvariabilityinthepatternsof
accumulationincucumber(Cucumissativus)undervaryingsoilsiliconavailability. phytolithformationinAsteraceaespeciesalongalargerainfallgradientinIsrael.
Botany90,1058–1064. Flora208,438–444.
Falkowski,P.G.,Katz,M.E.,Knoll,A.H.,Quigg,A.,Raven,J.A.,Schofield,O.,Taylor, Katz,O.,Lev-Yadun,S.,Bar(Kutiel),P.,2014.Dophytolithsplayanantiherbivoryrolein
F.J.R.,2004.Theevolutionofmoderneukaryoticphytoplankton.Science305, southwestAsianAsteraceaespeciesandtowhatextent?Flora209,349–358.
354–360. Katz,O.,Lev-Yadun,S.,Bar(Kutiel),P.,2016.Plantsiliconandphytolithcontentsas
Farmer,V.C.,Delbos,E.,Miller,J.D.,2005.Theroleofphytolithformationanddis- affectedbywateravailabilityandherbivory:integratinglaboratoryexperimentation
solutionincontrollingconcentrationsofsilicainsoilsolutionsandstreams. andnaturalhabitatstudies. inpress.Silicon.
Geoderma127,71–79. Klotzbücher,T.,Klotzbücher,A.,Kaiser,K.,Vetterlein,D.,Jahn,R.,Mikutta,R.,2018.
Fauteaux,F.,Remus-Borel,W.,Menzies,J.G.,Belanger,R.R.,2005.Siliconandplant Variablesiliconaccumulationinplantsaffectsterrestrialcarboncyclingbycontrol-
diseaseresistanceagainstpathogenicfungi.FEMSMicrobiol.Lett.249,1–6. lingligninsynthesis.Glob.ChangeBiol.Bioenergy24,e183–e189.
Fauteaux,F.,Chain,F.,Belzile,F.,Menzies,J.G.,Belanger,R.R.,2006.Theprotectiverole Kürschner,W.M.,Kvaček,Z.,Dilcher,D.L.,2008.TheimpactofMioceneatmospheric
ofsiliconintheArabidopsis-powderymildewpathosystem.PNAS103,17554–17559. dioxidefluctuationsonclimateandtheevolutionofterrestrialecosystems.Proc.Natl.
Feng,Y.,Jie,D.,Guo,M.,Dong,S.,Chen,X.,Liu,H.,Liu,L.,Li,N.,2017.Phytolithloss Acad.Sci.U.S.A.105,449–453.
andenrichmentinsoilphytolithassemblagesrevealedbycomparisonsofphytoliths Kvedaras,O.L.,Keeping,M.G.,Goebel,F.R.,Byrne,M.J.,2007.Larvalperformanceofthe
invegetationandsurfacesoilsofaltitudinalbeltsintheChangbaiMountains, pyralidborerEldanasaccharinaWalkerandstalkdamageinsugarcane:influenceof
NortheastChina.Flora236–237,84–93. plantsilicon,cultivarandfeedingsite.Int.J.PestManage.53,183–194.
Fialova,I.,Šimkova,S.,Vaculikova,M.,Luxova,M.,2016.EffectsofSiontheantioxidant Lamsdell,J.C.,Congreve,C.R.,Hopkins,M.J.,Krug,A.Z.,Patzkowsky,M.E.,2017.
defenseofyoungmaizerootsunderNaClstress. inpress.Silicon. Phylogeneticpaleoecology:tree-thinkingandecologyindeeptime.TrendsEcol.
Franceschi,V.R.,Nakata,P.A.,2005.Calciumoxalateinplants:formationandfunction. Evol.32,452–463.
Annu.Rev.PlantBiol.56,41–71. Li,Z.,Song,Z.,Parr,J.F.,Wang,H.,2013.OccludedCinricephytoliths:implicationsto
Frew,A.,Powell,J.R.,Sallam,N.,Allsopp,P.J.,Johnson,S.N.,2016.Trade-offsbetween biogeochemicalcarbonsequestration.PlantSoil370,615–623.
siliconandphenolicdefensesmayexplainenhancedperformanceofrootherbivores Li,N.,Jie,D.,Ge,Y.,Guo,J.,Liu,H.,Liu,L.,Qiao,Z.,2014.Responseofphytolithsin
onphenolic-richplants.J.Chem.Ecol.42,768–771. PhragmitescommunistoelevatedCO2concentrationinSongnenGrassland,China.
Frew,A.,Allsopp,P.J.,Gherlenda,A.N.,Johnson,S.N.,2017a.Increasedrootherbivory Quat.Int.321,97–104.
underelevatedatmosphericcarbondioxideconcentrationsisreversedbysilicon- Li,D.,Jie,D.,Liu,L.,Liu,H.,Gao,G.,Li,N.,2018.Herbaceousphytolithsfromforestand
basedplantdefences.J.Appl.Ecol.54,1310–1319. grasslandinNortheastChina:potentialsignificancefordeterminingpastforest–-
Frew,A.,Powell,J.R.,Hiltpold,I.,Allsopp,P.J.,Sallam,N.,Johnson,S.N.,2017b.Host grasslandboundaries.Flora243,19–31.
plantcolonisationbyarbuscularmycorrhizalfungistimulatesimmunefunction Ma,J.F.,Takahashi,E.,1990.Effectofsilicononthegrowthandphosphorusuptakeof
whereashighrootsiliconconcentrationsdiminishgrowthinasoil-dwellingherbi- rice.PlantSoil126,115–119.
vore.SoilBiol.Biochem.112,117–126. Ma,J.,Cai,H.,He,C.,Zhang,W.,Wang,L.,2015.Ahemicellulose-boundformofsilicon
Fulweiler,R.W.,Maguire,T.J.,Carey,J.C.,Finzi,A.C.,2015.DoeselevatedCO2alter inhibitscadmiumionuptakeinrice(Oryzasativa)cells.NewPhytol.206,
silicauptakeintrees?Front.PlantSci.5,793. 1063–1074.
Funk,J.L.,Larson,J.E.,Ames,G.M.,Butterfield,B.J.,Cavender-Bares,J.,Firn,J., MacFadden,B.J.,1997.OriginandevolutionofthegrazingguildinNewWorldterrestrial
Laughlin,D.C.,Sutton-Grier,A.E.,Williams,L.,Wright,J.,2017.RevisitingtheHoly mammals.TrendsEcol.Evol.12,182–187.
Grail:usingplantfunctionaltraitstounderstandecologicalprocesses.Biol.Rev.92, Marxen,A.,Klotzbücher,T.,Jahn,R.,Kaiser,K.,Nguyen,V.S.,Schmidt,A.,Schädler,M.,
1156–1173. Vetterlein,D.,2015.Interactionbetweensiliconcyclingandstrawdecompositionin
Gao,D.,Cai,K.,Chen,J.,Luo,S.,Zeng,R.,Yang,J.,Zhu,X.,2011.Siliconenhances asilicondeficientriceproductionsystem.PlantSoil398,153–163.
photochemicalefficiencyandadjustsmineralnutrientabsorptioninMagnaporthe Massey,F.P.,Hartley,S.E.,2006.Experimentaldemonstrationoftheantiherbivoreeffects
oryzaeinfectedriceplants.ActaPhysiol.Plant.33,675–682. ofsilicaingrasses:impactsonfoliagedigestibilityandvolegrowthrates.Proc.Roy.
Garbuzov,M.,Reidinger,S.,Hartley,S.E.,2011.Interactiveeffectsofplant-availablesoil Soc.LondonB273,2299–2304.
siliconandherbivoryoncompetitionbetweentwograssspecies.Ann.Bot.108, Massey,F.P.,Hartley,S.E.,2009.Physicaldefenceswearyoudown:progressiveandir-
1355–1363. reversibleimpactsofsilicaoninsectherbivores.J.Appl.Ecol.78,281–291.
Garnier,E.,Navas,M.L.,Grigulis,K.,2016.PlantFunctionalDiversity:OrganismTraits, Massey,F.P.,Ennos,A.R.,Hartley,S.E.,2006.Silicaingrassesasadefenceagainstinsect
CommunityStructure,andEcosystemProperties.OxfordUniversityPress, herbivores:contrastingeffectsonfolivoresandphloemfeeders.J.Anim.Ecol.75,
Oxford,UK. 595–603.
Gong,H.,Zhu,X.,Chen,K.,Wang,S.,Zhang,C.,2005.Siliconalleviatesoxidativeda- Massey,F.P.,Ennos,A.R.,Hartley,S.E.,2007a.Grassesandtheresourceavailability
mageofwheatplantsinpotsunderdrought.PlantSci.169,313–321. hypothesis:theimportanceofsilica-baseddefences.J.Ecol.95,414–424.
Goto,M.,Ehara,H.,Karita,S.,Takabe,K.,Ogawa,N.,Yamada,Y.,Ogawa,S.,Yahaya, Massey,F.P.,Ennos,A.R.,Hartley,S.E.,2007b.Herbivorespecificinductionofsilica-
M.S.,Morita,O.,2003.Protectiveeffectofsilicononphenolicbiosynthesisandul- basedplantdefences.Oecologia152,677–683.
travioletspectralstressinricecrop.PlantSci.164,349–356. Massey,F.P.,Smith,M.J.,Lambin,X.,Hartley,S.E.,2008.Aresilicadefencesingrasses
Hartley,S.E.,2015.Roundandroundincycles?Silicon-basedplantdefencesandvole drivingvolepopulationcycles?Biol.Lett.4,419–422.
populationdynamics.Funct.Ecol.29,151–153. Mihlbachler,M.C.,Rivals,F.,Solounias,N.,Semprebon,G.N.,2011.Dietarychangeand
Hartley,S.E.,DeGabriel,J.L.,2016.Theecologyofherbivore-inducedsilicondefencesin evolutionofhorsesinNorthAmerica.Science331,1178–1181.
grasses.Funct.Ecol.30,1311–1322. Neu,S.,Schaller,J.,Dudel,E.G.,2017.Siliconavailabilitymodifiesnutrientuseeffi-
Hattori,T.,Inanaga,S.,Araki,H.,An,P.,Morita,S.,Luxova,M.,Lux,A.,2005. ciencyandcontent,C:N:Pstoichiometry,andproductivityofwinterwheat(Triticum
ApplicationofsiliconenhancesdroughttoleranceinSorghumbicolor.Physiol.Plant. aestivumL.).Sci.Rep.7,40829.
123,459–466. Perez-Harguindeguy,N.,Diaz,S.,Garnier,E.,Lavorel,S.,Poorter,H.,Jaureguiberry,P.,
He,Y.,Xiao,H.,Wang,H.,Chen,Y.,Yu,M.,2010.Effectofsilicononchilling-induced Bret-Harte,M.S.,Cornwell,W.K.,Craine,J.M.,Gurvich,D.E.,Urcelay,C.,Veneklaas,
changesofsolutes,antioxidants,andmembranestabilityinseashorepaspalum E.J.,Reich,P.B.,Poorter,L.,Wright,I.J.,Ray,P.,Enrico,L.,Pausas,J.G.,deVos,
turfgrass.ActaPhysiol.Plant.32,487–494. A.C.,Buchmann,N.,Funes,G.,Quetier,F.,Hodgson,J.G.,Thompson,K.,Morgan,
He,C.,Ma,J.,Wang,L.,2015.Ahemicellulose-boundformofsiliconwithpotentialto H.D.,terSteege,H.,vanderHeijden,M.G.A.,Sack,L.,Blonder,B.,Poschlod,P.,
improvethemechanicalpropertiesandregenerationofthecellwallofrice.New Vaieretti,M.V.,Conti,G.,Staver,A.C.,Aquino,S.,Cornelissen,J.H.C.,2013.New
Phytol.206,1051–1062. handbookforstandardisedmeasurementofplantfunctionaltraitsworldwide.Aus.J.
Hinsinger,P.,FernandesBarros,O.N.,Benedetti,M.F.,Noack,Y.,Callot,G.,2001.Plant- Bot.61,167–234.
inducedweatheringofabasalticrock:experimentalevidence.Geochem. Prasad,V.,Strömberg,C.A.E.,Alimohammadian,H.,Sahni,A.,2005.Dinosaurcoprolites
Cosmochem.Acta65,137–152. andtheearlyevolutionofgrassesandgrazers.Science310,1177–1180.
Hodson,M.J.,White,P.J.,Mead,A.,Broadley,M.R.,2005.Phylogeneticvariationinthe Prychid,C.J.,Rudall,P.J.,1999.Calciumoxalatecrystalsinmonocotyledons:areviewof
6
O.Katz Flora xxx (xxxx) xxx–xxx
theirstructureandsystematics.Ann.Bot.84,725–739. thanherbivory:levelsofsilica-baseddefencesingrassesvarywithplantspecies,
Quere,C.,Andrew,R.M.,Canadell,J.P.,Sitch,S.,Korsbakken,J.I.,Peters,G.P.,Manning, genotypeandlocation.Oikos122,30–41.
A.C.,Boden,T.A.,Tans,P.P.,Houghton,R.A.,Keeling,R.F.,Alin,S.,Andrews,O.D., Solounias,N.,Semprebon,G.M.,2002.Advancesinthereconstructionofungulateeco-
Anthoni,P.,Barbero,L.,Bopp,L.,Chevallier,F.,Chini,L.P.,Clais,P.,Currie,K., morphologywithapplicationtoearlyfossilequids.Am.MuseumNovitates3366,
Delire,C.,Doney,S.C.,Frielingstein,P.,Gkritzalis,T.,Harris,I.,Hauck,J.,Haverd, 1–49.
V.,Hoppema,M.,Goldewijk,K.K.,Jain,A.K.,Kato,E.,Körtzinger,A.,Landschützer, Song,Z.,Wang,H.,Strong,P.J.,Li,Z.,Jiang,P.,2012.Plantimpactonthecoupled
P.,Lefevre,N.,Lenton,A.,Lienert,S.,Lombardozzi,D.,Melton,J.R.,Metzl,N., biogeochemicalcyclesofsiliconandcarbon:implicationsforbiogeochemicalcarbon
Millero,F.,Moteiro,P.M.,Munro,D.R.,Nabel,J.E.M.S.,Nakaoka,S.,O’Brien,K., sequestration.EarthSci.Rev.115,319–331.
Olsen,A.,Omar,A.M.,Ono,T.,Pierrot,D.,Poulter,B.,Rödenbeck,C.,Salisbury,J., Song,Z.,Liu,H.,Zhao,F.,Xu,C.,2014.EcologicalstoichiometryofN:P:SiinChina’s
Schuster,U.,Schwinger,J.,Seferian,R.,Skjelvan,I.,Stocker,B.D.,Sutton,A.J., grasslands.PlantSoil380,165–179.
Takahashi,T.,Tian,H.,Tilbrook,B.,vanderLaan-Luijkx,I.T.,vanderWerf,G.R., Song,Z.,Liu,H.,Strömberg,C.A.E.,Yang,X.,Zhang,X.,2017.Phytolithcarbonse-
Viovy,N.,Walker,A.P.,Wiltshire,A.J.,Zaehle,S.,2016.Globalcarbonbudget2016. questrationinglobalterrestrialbiomes.Sci.Tot.Environ.603-604,502–509.
EarthSyst.Sci.Data8,605–649. Stebbins,G.L.,1981.Coevolutionofgrassesandherbivores.Ann.Mo.Bot.Gard.68,
Quigley,K.M.,Anderson,T.M.,2014.LeafsilicaconcentrationinSerengetigrassesin- 75–86.
creaseswithwateringbutnotclipping:insightsfromacommongardenstudyand Street-Perrott,F.A.,Barker,P.A.,2008.Biogenicsilica:aneglectedcomponentofthe
literaturesurvey.Front.PlantSci.5,568. coupledglobalcontinentalbiogeochemicalcyclesofcarbonandsilicon.EarthSurf.
Raven,J.A.,1983.Thetransportandfunctionofsiliconinplants.Biol.Rev.58,179–207. Process.Landforms33,1436–1457.
Reyerson,P.E.,Alexandre,A.,Harutyunyan,A.,Corbineau,R.,MartinezdelaTorre,H.A., Strömberg,C.A.E.,2004.Usingphytolithassemblagestoreconstructtheoriginand
Badeck,F.,Cattivelli,L.,Santos,G.M.,2016.Unambiguousevidenceofoldsoil spreadofgrass-dominatedhabitatsintheGreatPlainsduringthelateEocenetoearly
carboningrassbiosilicaparticles.Biogeosciences13,1269–1286. Miocene.Palaeogeog.Palaeoclimatol.Palaeoecol.207,239–275.
Rios,J.J.,Martinez-Ballesta,M.C.,Ruiz,J.M.,Blasco,B.,Carvajal,M.,2017.Silicon- Strömberg,C.A.E.,2005.Decoupledtaxonomicradiationandecologicalexpansionof
mediatedimprovementinplantsalinitytolerance:theroleofaquaporins.Front.Plant open-habitatgrassesintheCenozoicofNorthAmerica.PNAS102,11980–11984.
Sci.8,948. Strömberg,C.A.E.,2006.Theevolutionofhypsodontyinequids:testingahypothesisof
Rivals,F.,Takatsuki,S.,Albert,R.M.,Macia,L.,2014.Bamboofeedingandtoothwearof adaptation.Paleobiology32,236–258.
threesikadeer(Cervusnippon)populationsfromnorthernJapan.J.Mammal.95, Strömberg,C.A.E.,2011.Evolutionofgrasslandsandgrasslandecosystems.Annu.Rev.
1043–1053. EarthPlanet.Sci.39,517–544.
Ronchi,B.,Clymans,W.,Barão,A.L.P.,Vandevenne,F.,Struyf,E.,Batelaan,O., Strömberg,C.A.E.,Dunn,R.E.,Madden,R.H.,Kohn,M.L.,Carlini,A.A.,2013.Decoupling
Dassargues,A.,Govers,G.,2013.TransportofdissolvedSifromsoiltoriver:a thespreadofgrasslandsfromtheevolutionofgrazer-typeherbivoresinSouth
conceptualmechanisticmodel.Silicon5,115–133. America.Nat.Commun.4,1478.
Sanson,G.D.,Kerr,S.A.,Gross,K.A.,2007.Dosilicaphytolithsreallywearmammalian Strömberg,C.A.E.,DiStilio,V.S.,Song,Z.,2016.Functionsofphytolithsinvascular
teeth?J.Archaeol.Sci.34,526–531. plants:anevolutionaryperspective.Funct.Ecol.30,1286–1297.
Santos,G.M.,Alexandre,A.,2017.Thephytolithcarbonsequestrationconcept:factof Struyf,E.,Smis,A.,VanDamme,S.,Meire,P.,Conley,D.J.,2009.Theglobalbiogeo-
fiction?Acommenton“Occurrence,turnoverandcarbonsequestrationpotentialof chemicalsiliconcycle.Silicon1,207–213.
phytolithsinterrestrialecosystems”bySongetal.Earth.Rev.164,251–255.https:// Trembath-Reichert,E.,Wilson,J.P.,McGlynn,S.E.,Fischer,W.W.,2015.Fourhundred
doi.org/10.1016/j.earscirev.2016.04.007. millionyearsofsilicabiomineralizationinlandplants.PNAS112,5449–5454.
Schaller,J.,Struyf,E.,2013.Siliconcontrolsmicrobialdecayandnutrientreleaseofgrass Tsartsidou,G.,Lev-Yadun,S.,Efstratiou,N.,Weiner,S.,2008.Ethnoarchaeologicalstudy
litterduringaquaticdecomposition.Hydrobiologia709,201–212. ofphytolithassemblagesfromanagro-pastoralvillageinnorthernGreece(Sarakini):
Schaller,J.,Brackhage,C.,Dudel,E.G.,2012a.Siliconavailabilitychangesstructural developmentandapplicationofaphytolithdifferenceindex.J.Archaeol.Sci.35,
carbonratioandphenolcontentofgrasses.Environ.Exp.Bot.77,283–287. 600–613.
Schaller,J.,Brackhage,C.,Gessner,M.O.,Bäuker,E.,Dudel,E.G.,2012b.Siliconsupply VanBockhaven,J.,DeVleesschauwer,D.,Höfte,M.,2013.Towardsestablishingbroad-
modifiesC:N:PstoichiometryandgrowthofPhragmitesaustralis.PlantBiol.14, spectrumdiseaseresistanceinplants:siliconleadstheway.J.Exp.Bot.64,
392–396. 1281–1293.
Schaller,J.,Brackhage,C.,Bäucker,E.,Dudel,E.G.,2013.UV-screeningofgrassesby Vandevenne,F.I.,Barão,A.L.,Schoelynck,J.,Smis,A.,Ryken,N.,VanDamme,S.,Meire,
plantsilicalayer?J.Biosci.38,413–416. P.,Struyf,E.,2013.Grazers:biocatalystsofterrestrialsilicacycling.Proc.Roy.Soc.
Schaller,J.,Hines,J.,Brackhage,C.,Bäucker,E.,Gessner,M.O.,2014.Silicadecouples LondonB280(2013),2083.
fungalgrowthandlitterdecompositionwithoutchangingresponsestoclimate Violle,C.,Reich,P.B.,Pacala,S.W.,Enquist,B.J.,Kattge,J.,2014.Theemergenceand
warmingandNenrichment.Ecology95,3181–3189. promiseoffunctionalbiogeography.PNAS111,13690–13696.
Schaller,J.,Shcoelynck,J.,Struyf,E.,Meire,P.,2016a.Siliconaffectsnutrientcontent Wang,Y.,Stass,A.,Horst,W.J.,2004.Apoplasticbindingofaluminumisinvolvedin
andratiosofwetlandplants.Silicon8,479. silicon-inducedameliorationofaluminumtoxicityinmaize.PlantPhysiol.136,
Schaller,J.,Roscher,C.,Hildebrand,H.,Weigelt,A.,Oelmann,Y.,Wilcke,W.,Ebeling, 3762–3770.
A.,Weisser,W.W.,2016b.PlantdiversityandfunctionalgroupsaffectSiandCapools Wang,L.,Nie,Q.,Li,M.,Zhang,F.,Zhuang,J.,Yang,W.,Li,T.,Wang,Y.,2005.
inabovegroundbiomassofgrasslandsystems.Oecologia182,277–286. Biosilicifiedstructuresforcoolingplantleaves:amechanismofhighlyefficient
Schaller,J.,Hodson,M.J.,Struyf,E.,2017.IsrelativeSi/Caavailabilitycrucialtothe midinfraredthermalemission.Appl.Physic.Lett.87,194105.
performanceofgrasslandecosystems?Ecosphere8,e01726. Wieczorek,M.,Szafrańska,P.A.,Labecka,A.M.,Lazaro,J.,Konarzewski,M.,2015a.
Schoelynck,J.,Struyf,E.,2016.Siliconinaquaticvegetation.Funct.Ecol.30, Effectsofabrasivepropertiesofsedgesontheintestinalabsorptivesurfaceand
1323–1330. restingmetabolicrateofrootvole.J.Exp.Biol.218,309–315.
Schoelynck,J.,Bal,K.,Backx,H.,Okruszko,T.,Meire,P.,Struyf,E.,2010.Silicauptake Wieczorek,M.,Zub,K.,Szafrańska,P.A.,Książek,A.,Konarzewski,M.,2015b.Plant-
inaquaticandwetlandmacrophytes:astrategicchoicebetweensilica,ligninand herbivoreinteractions:siliconconcentrationintussocksedgesandpopulationdy-
cellulose?NewPhytol.186,385–391. namicsofrootvoles.Funct.Ecol.29,187–194.
Schoelynck,J.,Müller,F.,Vandevenne,F.,Bal,K.,Barão,A.L.,Smis,A.,Opdekamp,W., Wiens,J.J.,Donoghue,M.J.,2004.Historicalbiogeography,ecologyandspeciesrichness.
Meire,P.,Struyf,E.,2014.Silicon–vegetationinteractioninmultipleecosystems:a TrendsEcol.Evol.19,639–644.
review.J.Veg.Sci.25,301–313. Wu,Y.,You,H.L.,Li,X.Q.,2017.Dinosaur-associatedPoaceaeepidermisandphytoliths
Schuiling,R.D.,Krijgsman,P.,2006.Enhancedweathering:aneffectiveandcheaptoolto fromtheEarlyCretaceousofChina. inpress.Natl.Sci.Rev.
sequesterCO2.Clim.Change74,349–354. Zhu,Y.,Gong,H.,2014.Beneficialeffectsofsilicononsaltanddroughttolerancein
Soininen,E.M.,Bråthen,K.A.,Jusdado,J.G.H.,Reidinger,S.,Hartley,S.E.,2013.More plants.Agron.Sustain.Develop.34,455–472.
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