Proc. Natl. Acad. Sci. USAVol. 91, pp. 11-17, January 1994

Review

The anomaly of silicon in plant biologyEmanuel EpsteinDepartment of Land, Air and Water Resources, Soils and Biogeochemistry, University of California, Davis, CA 95616-8627

Contributed by Emanuel Epstein, September 15, 1993

ABSTRACT Silicon is the second mostabundant element in soils, the mineralsubstrate for most of the world's plant life.The soil water, or the "soil solution,"contains silicon, mainly as silicic acid,H4SiO4, at 0.1-0.6 mM-concentrationson the order of those of potassium, cal-cium, and other major plant nutrients,and weli in excess of those of phosphate.Silicon is readily absorbed so that terres-trial plants contain it in appreciable con-centrations, ranging from a fraction of 1%of the dry matter to several percent, and insome plants to 10% or even higher. In spiteof this prominence of silicon as a mineralconstituent of plants, it is not countedamong the elements defined as "essen-tial," qr nutrients, for any terrestrialhigher plants except members of the Eq-uisitaceae. For that reason it is not in-cluded in the formulation of any of thecommonly used nutrient solutions. Theplant physiologist's solution-culturedplants are thus anomalous, containingonly what silicon is derived as a contami-nant of their environment. Ample evi-dence is presented that silicon, whenreadily available to plants, plays a largerole in their growth, mineral nutrition,mechanical strength, and resistance tofungal diseases, herbivory, and adversechemical conditions of the medium. Plantsgrown in conventional nutrient solutionsare thus to an extent experimental arti-facts. Omission of silicon from solutioncultures may lead to distorted results inexperiments on inorganic plant nutrition,growth and development, and responses toenvironmental stress.

"It is to be observed that a definition is,strictly speaking, no part of the subjectin which it occurs." (Alfred NorthWhitehead and Bertrand Russell, Prin-cipia Mathematica)

Soil, dominated for the most part byaluminosilicate minerals, is the source ofthe majority of the chemical elementsthat go into the makeup of terrestrial

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plants and, hence, of their consumers. Itis the solid phase of the soil that is thereservoir of the mineral elements, bothnutrient and non-nutrient, that the rootsof plants ultimately draw upon. The im-mediate source of most of these ele-ments, however, is the soil water, ormore accurately, the soil solution, sup-plied by the solid phase through the pro-cesses of weathering: solution, ion ex-change, desorption-in fact, the wholegamut of processes whereby the solid,liquid, and gaseous phases of the soilceaselessly interact with one another andwith the part of the biosphere that residesthere (1-7). The roots of plants throughtheir interplay with soil minerals play amajor role in the solubilization of Si and,hence, the supply of it in the soil solutionavailable for absorption (6, 8-10).As a result of these processes, Si,

mainly in the form of silicic acid, H4SiO4,is prominent in the soil solution. Actualconcentrations vary widely in space andtime, depending on the particular soilminerals present and many other factors,both abiotic and biotic (11). Concentra-tions on the order of 0.1-0.6 mM may beconsidered in the normal range (1, 11,129). Concentrations of this magnitudeare common for a number of the majorinorganic nutrients such as K+, Ca2+,and SO2- and are far in excess of phos-phate concentrations in the soil solution(12, 13). Si therefore looms large as one ofthe major constituents of the soil solutionin contact with plant roots.

In the form of H4SiO4, Si is readilyabsorbed by plants (14), and all soil-grown plants contain it as an appreciablefraction of the dry matter (Table 1). Thetable lists all the essential (nutrient) min-eral elements, as well as several othersnot known to be generally essential forhigher green plants but essential for somespecies or important for various reasons.(The concept of essentiality is discussedbelow, under that heading.) As is cus-tomary, concentrations are given on adry weight basis and expressed as per-centages for the macronutrient and ppm(mg/kg) for the micronutrient elements.For each element a range of concentra-tions is given because, depending on soilconditions, genotypes, and many otherfactors, the content of any one mineral

element in plant matter varies greatly.The table is based on analyses of cropspecies, and leaf material for the mostpart, because that is the provenance ofmost published values. For any one spe-cies, the range of concentrations wouldbe much narrower. (Values below andabove those listed may be encountered,but most would fall within the rangesindicated.)As for Si, the table reveals a remark-

able feature. Of all the mineral elementslisted that are not known to be generallyessential for green plants, Si alone isconsistently present at concentrationscorresponding to those of the macronu-trient elements. At the low end of therange, 0.1%, Si corresponds in amountper unit of dry plant matter to such mac-ronutrients as P, S, Ca, and Mg. Its uppervalues, 10% or even higher, exceed thetissue concentrations of even the mostabundant mineral nutrients such as K andN. Si thus figures as a major mineralconstituent of plants.

Essentiality

Its quantitative importance as a plantconstituent notwithstanding, Si is notusually listed among the generally essen-tial elements, or nutrients, of plants (12,17-20). Plant physiologists consider anelement essential by two criteria. Thefirst, and classical, definition was laiddown by Amnon and Stout (21): an ele-ment is essential if a deficiency of itmakes it impossible for the plant to com-plete its life cycle and if that effect is notmerely due to the amelioration by theelement of some unfavorable chemical ormicrobiological condition of the sub-strate; i.e., the element must be directlyinvolved in the inorganic nutrition of theplant. A second criterion of essentiality(12) is that the element is part of themolecule of an essential plant constituentor metabolite. It is by the first criterionthat the essentiality of the elements nowknown to be essential has been estab-lished. Conceptually, it is a simple, op-erational definition. In practice, it is notnecessarily easy to apply if, as is the casewith Si, it is difficult to create and main-tain an environment adequately purgedof the element.

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Proc. Natl. Acad. Sci. USA 91 (1994)

Table 1. Mineral elements in crop plantsRange of concentrations

Element (dry weight basis) Remarks

Nitrogen, % 0.5-6Phosphorus, % 0.15-0.5Sulfur, % 0.1-1.5 EssentialPotassium, % 0.8-8 macronutrientsCalcium, % 0.1-6Magnesium, % 0.05-1

Iron, ppm 20-600Manganese, ppm 10-600 1Zinc, ppm 10-250Copper, ppm 2-50 EssentialNickel, ppm 0.05-5 r micronutrientsBoron, ppm 0.2-800Chlorine, ppm 10-80,000 JMolybdenum, ppm 0.1-10

Cobalt, ppm 0.05-10 Essential in allnitrogen-fixingsystems

Sodium, % 0.001-8 } Essential for someSilicon, % 0.1-10 plants; often

beneficial

Aluminum, ppm 0.1-500 Not known to beessential; often toxicto plants on acidsoils

Modified after Epstein (15, 16). p

Si is a "ubiquitous contaminant. It ispresent as an impurity in the macronutri-ent salts used in making up nutrient solu-tions, in the water even if distilled ordemineralized, in containers (glass, ofcourse, must be avoided), and as dust(22). Woolley (23) went to considerablelengths to exclude Si from the environ-ment to determine whether it is an essen-tial element for the tomato, Lycopersiconesculentum. The Si-deprived plants grewas well as those deliberately supplied withthe element. The Si content of the shootsofthe Si-deprived plants was 4.2 ppm, andthat of the roots, 2.8 ppm. These valuesare on the order of levels of Cu generallyconsidered adequate (12). If, then, Si isessential for the tomato plant, its require-ment for the element would be met by theconcentrations found in Woolley's Si-deprived plants. Perhaps Si is a micronu-trient the requirement for which by'solu-tion-cultured plants is generally met bythe inadvertent supply of it usually pre-sent as an environmental contaminant.

In a number ofpublications Miyake andTakahashi have concluded on the basis ofthe responses of plants grown in nutrientsolutions with and without the addition ofSi that omission of the element causesdeficiency symptoms in the tomato (24)and cucumber, Cucumis sativus (25), andmarked adverse effects as well on thegrowth of the soybean, Glycine max (26),and strawberry, Fragaria x ananassa(27). These and other such findings haveled to an implication of Si as an essential

element for higher plants (22, 28). Theclaim needs to be viewed with reserve, fora number of reasons. Cl, an essentialmicronutrient (12, 18), was not included inthe nutrient solutions used by the Japa-nese investigators, except for occasionaladditions ofHCl forpH adjustment. In theexperiments with cucumber (25), the SiO2content of the leaves in the Si-deprivedplants was "extremely low at about 0.1%SiO2" (or about 0.05% Si), or 2 orders ofmagnitude higher than the Si content ofthe tomato plants that were deprived of Siin Woolley's experiments (23). It is pos-sible that the observed effects were due tointeractions between Si and P or Si andCa; such effects have been noted in rice byMa and Takahashi (29, 30). In regard tothe experiments with cucumber (25),Marschner et al. (31) concluded that theresults were due to an interplay betweenZn, P, and Si: in the experiments of Miy-ake and Takahashi (25), the concentra-tions of Zn were low (0.1 ,M or less) andthose of P were high (0.23-2.3 mM). Ad-dition of Si rectified a combination of Zndeficiency and excessive P accumulation.Marschner et al. (31) could achieve thesame rectification by lowering the concen-tration of P in the solution culture orraising that ofZn. Thus the observation byMiyake and Takahashi (25) is an instanceof an element, Si in this case, correctingan unfavorable chemical condition in themedium, and that, according to the clas-sical definition for essentiality laid downby Arnon and Stout (21), does not qualify

the element for "essential" status. Adatiaand Besford (32), also working with cu-cumber but using a balanced, recirculatingnutrient solution, found no extreme ab-normalities but made a number of inter-esting observations (discussed below, un-der Silicon and Growth) indicating posi-tive effects of Si on the growth of theplants.

In view of this and other evidence,claims for the general essentiality of Sifor higher plants cannot presently be sup-ported. Because of the difficulty of de-priving plants of access to Si, the likeli-hood of obtaining adequately Si-purgedmedia is low. One has to agree withVolcani's assessment as quoted in Sang-ster and Hodson (33): "The answer ismost probably, not right now."While for plants in general Si cannot be

considered essential, it is so for certaingroups of plants. Among the algae, Si isessential for diatoms and other membersof the yellow-brown or golden algae (34,35). The beautiful "frustules" of diatomsconsist of silica, SiO2rnH2O (36-38). Fora discussion of these and other silicifiedalgae see Round (39). The significance ofdiatom Si in the chemical economy ofnature is impressive (40-43).The only terrestrial plants for which Si is

unquestionably essential are members ofthe Equisitaceae, or "scouring rushes," socalled because in bygone days their ash,containing abundant gritty silica, was usedto scour pots and pans. Chen and Lewin(44) showed that plants of the species Eq-uisetum arvense died in solution culturesto which Si had not been added.

In concluding this section let it benoted that Si is an essential element forhigher animals (45).

Silicon in Plants

As already mentioned, Si as H4SiO4 isreadily absorbed by plants, but as indi-cated in Table 1, the Si content of plantsvaries widely. Jones and Handreck (17),in their classic review, distinguishedthree groups of crop plants on the basis ofthe Si content of their tissues. Dicotyle-dons have tissue concentrations at thelow end of the range given in Table 1, onthe order of 0.1% (dry weight basis);dryland grasses such as oats and rye haveabout 1%; and the "wetland" grass, pad-dy-grown rice, has levels on the order of5% or higher. Going beyond crop plants,Takahashi and Miyake (46) have broadlysketched the characteristics of Si distri-bution in the plant kingdom. They did thison the basis of analyses of 175 speciesgrown in the same soil. Of nine elementsanalyzed for (Si, Ca, Mg, K, P, Fe, Mn,B, and Al), Si was the most variable.Plants with more than 1% Si in dry leafmatter were considered as Si accumula-tors, and 34 species, or about 19% of

12 Review: Epstein

Proc. Natl. Acad. Sci. USA 91 (1994)

those in the study, fell in that category,with an average Si content of 1.96%. Thecorresponding value for the nonaccumu-lators (81% of the species) was 0.25%.Leaf matter of herbaceous legumes haslow Si values as a rule. Even genotypeswithin a species may have Si tissue con-centrations that vary by as much as afactor of 3, as shown for barley, Hor-deum vulgare, grown in nutrient solu-tions (47).There is a large literature on the dis-

tribution and eventual deposition of Si inplants. For a discussion of mechanisticaspects of its transport, which are be-yond the scope of this paper, the reviewby Raven (14) is unexcelled. Because theuptake of undissociated H4SiO4 may benonselective and energetically passive,and its transport from root to shoot is inthe transpiration stream in the xylem, theassumption has sometimes been madethat the movement of Si follows that ofwater (48). The evidence for that corre-lation was held to be best for drylandgrasses (14). On the basis of nonselec-tive, passive uptake of Si, the Si contentof plants might serve as a convenienttracer for water uptake (48), but recentevidence lends little support to a directlyproportional relationship between waterand Si uptake, even for dryland grasses(49-51). During its passage through thexylem Si has to remain in solution-i.e.,it must remain unpolymerized. Themechanisms preventing polymerizationare not well understood; they may in-volve association with organic com-pounds (52, 53).The form in which Si is ultimately de-

posited is mainly amorphous SiO2rnH20,or "opal." Once deposited in this form, Siis immobile and not redistributed (14, 54).The hydrated, amorphous silica may bedeposited in cell lumens, cell walls, andintercellular spaces or external layers(31). It is present in roots (55-61), leaves(62-70), and inflorescence bracts of cere-als (71-75).

In the roots, silica is deposited to amarked extent in the cell walls, but thereare phylogenetically associated differ-ences in the particulars (57, 59). In youngwheat (Triticum aestivum) leaves theabaxial (lower) epidermal cells are impor-tant sites of silica deposition, but in olderleaves silica is also deposited in the adax-ial (upper) epidermis (68). In inflores-cence bracts ofwheat (lemma and glume)it is the outer epidermal walls that aremost heavily silicified (75). Hairs or tri-chomes are often sites of prominent si-licification (52, 59). Cotton (Gossypiumhirsutum) fibers (technically trichomes)contain Si, which has been postulated toplay a role in their development (76).There are fairly distinct differences in thedistribution and characteristics of silicadepositions between C3 and C4 plants (69,77).

It is the distribution, formation, andform of silica depositions that have at-tracted the attention of most researcherswho have concerned themselves with Siin plants. In the papers discussed aboveit is shown that amorphous silica, or opal,can assume an enormous range of highlycharacteristic morphological configura-tions ("opal phytoliths"). Inasmuch asamorphous silica has no intrinsic mor-phological forms, the multitude of ob-served morphologies must be due to ex-trinsic factors-namely, the organic ma-trices where the silica depositions areformed (78). This is an aspect of biomin-eralization and should be viewed in thatcontext (53, 79-81).

Silicon and Mineral Nutrition

In regard to this and the following sec-tions, an important note is in order con-cerning terminology and rationale. Inkeeping with virtually universal usage,reference will frequently be made to the"effects of Si" on this or that feature orprocess. The reason for that terminologyis the usual omission of Si from formula-tions of nutrient solutions, that being con-sidered the "control" or "standard" con-dition. Addition of Si is then an "experi-mental treatment" the effects ofwhich areexamined. The point of view embodied inthe present review is the opposite. Thepresence of Si in the medium, and conse-quently in the plant, is considered the"control" or "normal" condition, beingthe one that applies to soil-grown plants.It is the omission of Si from the medium,and the growth of plants with abnormallylow Si content, that should be lookedupon as an experimental treatment-atreatment that causes a variety of abnor-malities in mineral nutrition, growth anddevelopment, and resistance to abioticand biotic stresses.An early and striking demonstration of

the significance of Si in plant nutrition wasgiven by Williams and Vlamis in 1957 (82).They found that a concentration ofMn inbarley leaf tissue of300-400 ppm on a dryweight basis was toxic when no Si hadbeen added to the nutrient solution butharmless when the solution contained Siat 0.36 mM. Adding Si to the solution didnot diminish the Mn content ofthe leaves.Rather, in the absence of Si, Mn wasconcentrated in necrotic spots, whereas inthe presence of Si, the distribution ofMnwas more nearly even and no necroticspots appeared. Other Gramineae showedsimilar responses (83).

In view of their chemical affinities,interaction between silicate and phos-phate would be expected. Reference hasalready been made above, under Essen-tiality, to the effect on the growth ofcucumber plants of Si when added tosolutions with a low (0.1 ,M) concentra-tion of Zn and high concentrations of P

(0.23-2.3 mM). Although the original au-thors had concluded that the omission ofSi resulted in Si deficiency, it was shownsubsequently that the positive effect onthe growth of the plants of adding Siresulted from its rectifying an imbalancein Zn and P supply (31).Ma and Takahashi (29) compared phos-

phorus uptake by rice plants from nutrientsolutions without and with addition of Si(1.66 mM H4SiO4), adjusted to pH 5.5.There were three levels of KH2PO4:0.014, 0.21, and 0.70mM. In the treatmentwith Si, the shoots had a content of inor-ganic P (expressed as percent dry weight)on the order of half that ofthe Si-deprivedplants. The shoot concentrations of Feand Mn were also much lower in theSi-treated plants. A confounding factor inthese experiments may have been the useof a nutrient solution whose basic formu-lation did not include Cl, and partial sub-stitution ofKCI for KH2PO4 to maintainKconcentrations in the two lower P treat-ments identical with that having the top(0.70 mM) P concentration. The sameauthors (30) found addition of Si to thenutrient solution to diminish the uptake ofCa by rice plants. The reverse was not thecase: different Ca concentrations in thesolution did not cause differences in Siuptake and deposition.

Solution-cultured young orange trees,Citrus sinensis, on rough lemon, Citruslimon, rootstock, grown without andwith added Si (2.4 mM) differed in the Sicontent of their leaves and feeder roots,and these differences were correlatedwith differences in the concentrations ofseveral other elements in these and otherorgans and tissues (84).

Silicon and Growth

Si plays a major role in the intimateinterplay between the solid phase of thesoil and the soil solution. For this reasonthe present review is largely confined towork with nutrient solutions. They arethe only means by which roots can beexposed to a medium amenable to accu-rate control and monitoring (85). In thissection on growth, however, some ex-periments with soil-grown plants will beincluded because they dramatically illus-trate the importance of Si for the growthof at least some species under field con-ditions.

Plants for which Si has been shown tobe essential fail to grow normally whenthe element is deficient, that being part ofthe very definition of essentiality formu-lated by Arnon and Stout (21). Manyspecies, however, for which Si has notbeen shown to be essential may growbetter in media containing ample Si thanin media, whether solution cultures orsoil, with low concentrations of Si inreadily absorbable form. Such instanceshave been encountered in several of theinvestigations referred to above, under

Rkeview: Epstein

Proc. Natl. Acad. Sci. USA 91 (1994)

the headings Essentiality and Silicon andMineral Nutrition. Thus, the barleyplants in which addition of Si to theculture solution prevented Mn toxicity,in the early experiments of Williams andVlamis (82), also grew better; after 6weeks, the roots of the Si-treated plantshad nearly twice the weight of the Si-deprived ones; the weight of the Si-treated shoots also exceeded that ofthose in the Si-deficient cultures. Thealleviation of Mn toxicity in rice by ad-dition of Si to the nutrient solution alsoimproved the growth of the shoots, butnot that of the roots (86). In other in-stances also in which Si enhanced growththe effect was due to an alleviation by Siof nutrient imbalances. Thus the positiveeffect of Si on the growth of cucumberplants already referred to (31) was shownto be due to the mitigation, by Si, of animbalance in the supply of P and Zn. Inthe experiments of Ma and Takahashi(30), the growth of rice was enhanced bythe addition of Si to the nutrient solutionat 1.66 mM, an effect possibly related tothe Ca concentration of the shoot tissue,whi h was much diminished by the Sitre ment.However, not all instances in which Si

prolnoted growth can be attributed to itseffect in mroderating or alleviating nutri-ent imbalances. Addition of Si at 0.39mM to cultures in which loblolly pine,Pinus taeda, grew for 40 weeks enhancedthe growth of the seedlings; there was noevidence of nutrient imbalance in theSi-deprived plants (87). (The plants weregrown in sand and fritted clay media sothat even the Si-deprived plants hadsom Si available, more so than would bethe lase in pure solution culture withoutany solid substrate.)

In well-controlled experiments in whichcucumber plants were grown in recircu-lating nutrient solutions containing Si at alow (0.17 mM) or high (1.84 mM) concen-tration, Adatia and Besford (32) observeda number of positive effects ofthe high-Sitreatment on the growth of the plants:greater leaf thickness than that of thelow-Si plants, greater dry weight per unitarea of leaf, a small but significant addedincrement in root fresh and dry weight,and less propensity of the leaves to wilt.The lower leaves of the high-Si plantswere darker green and positioned betterfor light interception, and their senes-cence was retarded compared with that ofthe leaves of low-Si plants. The high-Sileaves had 50%o more total chlorophylland, on a unit area basis, 5O0o more ri-bulose-1,5-bisphosphate carboxylase.Even when there is no effect of Si on

the overall growth of plants, specific as-pects of growth or development may bepositively affected when the Si supply isample. For a recent instance, the weightat the late flowering stage ofroots, stems,leaves, and inflorescences of cheat, Bro-

mus secalinus, was the same whether thenutrient solution contained Si at 0.00036mM (the "-Si" control), or at 1.07 or3.57 mM (88). Si added at the two highlevels, however, increased the reproduc-tive output of the plant by markedlyenlarging the number of filled, viableseeds.

In respect to plant growth, however, itis field experiments that provide the mostimpressive evidence for a role of Si.From a plant physiological point of viewthat evidence is not as clearcut as thatfrom experiments with solution culture,because of indirect effects of Si on theplants brought about by interactions of Siwith various soil constituents. Neverthe-less, evidence suggests direct effects ofSi as well. When for at least two majorcrops, rice and sugarcane, fertilizationwith silicate has become commercialpractice, experiments with soil-grownplants cannot be overlooked. Early ob-servations are cited in the review byJones and Handreck (17). Shkolnik (89)has summarized a good deal of literature,including material not readily available inthe West. A few recent examples willdrive home the impact that Si applica-tions can have on the growth of crops.The organic soils (Histosols) of the

Florida Everglades, like many such soils,are low in Si available to crops. Applica-tions of calcium silicate slag raised theyield of sugar from sugarcane, Saccha-rum spp. (90-92). The yield increases(sugar) were large, on the order of 50% toover 100%. Although many soil proper-ties are affected by the application of Simaterials, these and other such field ex-periments nevertheless suggest that thegrowth-promoting effects of these appli-cations were in large measure due to theincreased Si content of the plants. Indi-cations were that for maximal yields, leafSi concentrations had to be in excess of1% (dry weight basis).The highly leached upland soils (Ulti-

sols) of the humid tropics tend to havelow levels of nutrients-i.e., they areinfertile-and their Si content is oftenlow. Applications of Si increased theyield ofrice on such a soil (93). The effectwas apparently direct and not due to theincrease in soil pH caused by the Siapplication. Different rice genotypes re-sponded differentially to Si applications(94). The indica group of genotypes wasmore responsive to Si applications thanwere thejaponicas, both in terms of yieldand in terms of the total amount of Si inthe shoot. The Si application nearly dou-bled the yield of rice over a 2-year period(mean for all eight genotypes in thestudy). The higher yields due to Si appli-cation were correlated with higher flag-leaf Si concentrations. Although markedimprovement of yields due to Si applica-tions have been noted mainly for rice andsugarcane, other Gramineae such as bar-

ley may also benefit from such applica-tions (95).

In experiments with both solution-cultured and soil-grown plants, a recur-ring observation has been that plantssupplied amply with Si resist lodging(drooping, leaning, or even becomingprostrate). The mechanical strength ofplants enabling them to achieve andmaintain an erect habit conducive to lightinterception resides in the cell wall. Re-views on the role of Si in plants thereforestress the association of Si with cell wallsand discuss the increased rigidity of cellwalls of plants grown with ample avail-able Si in terms of that association (14,17).The incorporation of silica into cell

walls has at least two energetically pos-itive effects. First, the role of silica isanalogous to that of lignin in that it is acompression-resistant structural compo-nent of cell walls. Raven (14) has calcu-lated that on a unit weight basis, theenergetic cost of incorporating silica isonly 3.7% that of incorporating lignin.For incorporation of silica comparedwith that of cell-wall carbohydrate, thecorresponding value is 6.7%. Silica isthus an energetically inexpensive struc-tural component of cell walls. Second,the erect habit and the disposition of theleaves of plants amply supplied with Sifavor light interception and, hence, pho-tosynthesis. Thus in the experiment withcucumber plants grown in a recirculatingnutrient solution already referred to (32),the authors found that the responses ofthe leaves of the high-Si plants resembledthose elicited by high levels of solar ra-diation. Although no systematic compar-isons have been made, it is likely thatmany of the positive effects of Si on plantgrowth that have been recorded were dueto increased total energy capture via thefeatures discussed by Adatia and Besford(32). At the very least, then, Si plays animportant supporting role in plant ener-getics and growth. The impregnation ofroot cell walls with silica may also assistin the growth of roots through a mediumdominated by a solid phase.

Silicon and Abiotic and Biotic Stresses

The effect on Mn toxicity of inclusion ofSi in solution cultures of barley plants,discussed under the heading Silicon andMineral Nutrition, may be looked uponas the reversal of a heavy-metal stress bySi. Other such instances have been notedin which inclusion of Si in the medium ofplants (usually crop species) has miti-gated or reversed mineral stress condi-tions. Thus inclusion of Si in solutioncultures of bean plants, Phaseolus vul-garis, mitigated Mn toxicity, not by di-minishing its absorption or translocationto the shoot but by increasing the abilityof leaf tissue to tolerate the Mn absorbed

14 Review: Epstein

Proc. Natl. Acad. Sci. USA 91 (1994)

(96). In rice, also, inclusion of Si in thesolution culture alleviated Mn toxicity(86). Effects of Si on the toxicity of otherheavy metals such as Al are likely (97),but information on the subject is scant.Another mineral stress, salinity, unlike

heavy-metal stress, manifests itself onlyat high concentrations of (mainly) Na+salts. In experiments with rice (98) andwheat (99), addition of Si to the solutioncultures enhanced the resistance of theplants to salinity stress. In both cases theaddition of Si diminished the Na concen-tration in the plants. Soil-grown mes-quite, Prosopis juliflora, irrigated withsaline water (260 mM NaCl) respondedmuch less to the stress in the presence ofSi (0.46mM Na2SiO3) than in the absenceof this amendment (100).There is much interest, and deservedly

so, in the development of plants resistantto the adverse effects of mineral toxici-ties and salinity (101). When geneticscreening and physiological experimen-tation with selected genotypes are doneby the solution culture technique, Si isnot as a rule included in the formulationof these solutions. However, the resultsreferred to above suggest that Si shouldbe included in solution cultures used inresearch on mineral stress. The eventualmedium in which the selected plants areto be grown is soil, and the plants ex-posed to mineral stress will thereforehave Si available and will absorb it. Theirresponses to the stress may then differfrom those elicited by the Si-deficientmedia used in the earlier screening andexperimentation.Evidence that Si affords protection

against the abiotic stresses discussedabove is surpassed by the evidence of itsimportance for resistance to biotic stress-es-mainly, the depredations inflicted byfungi and insects. As long ago as 1940Wagner (102) demonstrated the efficacyof Si applications in protecting cropsagainst fungal attack (cited in ref. 103).

Several positive effects of Si on thegrowth of solution-cultured cucumberplants (32) have already been noted, butin addition there was increased resis-tance of those plants to the powderymildew fungus, Sphaerotheca fuliginea.Even when fungicide was applied repeat-edly, outbreaks of the fungal disease oc-curred in the low-Si plants, whereas theSi-treated plants were virtually free ofthedisease. Similar results had been shownfor both solution-cultured (25) and soil-grown (104) cucumber plants. Still morerecent evidence of the protection fromfungal disease bestowed on cucumberplants by Si has been provided (103, 105,106). In the last paper (106) the evidencewas extended to other vegetable crops,and Si was applied as a foliar spray; it waseffective in reducing the severity of in-fection by powdery mildew. The samemethod proved successful with grape-

vines (107). The mechanisms whereby Siaffects the ability of pathogenic fungi tocolonize plant tissues are not well under-stood (108-111).The dicotyledonous crops discussed

above are notorious for their sensitivityto pathogens. But as long ago as 1967Jones and Handreck (17) were able to citea number of papers in which rice andother cereals were shown to resist fungalattack when amply supplied with Si. Thisis not surprising in view of the normallyhigh Si content ofGramineae. In contrastto the situation with vegetable crops,research on this topic with cereals hasmostly been done in the field, with im-pressive and economically valuable re-sults, especially with rice.Yamauchi and Winslow (93), in their

paper on the growth of rice in Si-poortropical soils, noted not only an increasein yield when Si was applied, as alreadydiscussed, but in addition, a marked re-duction in the incidence of grain discol-oration. This discoloration is the result ofinfection of the husks by several fungi. Ina subsequent investigation (94), a numberofrice disease organisms were identified.Applications of Si to the soil reduced theseverity of all diseases identified; differ-ent rice genotypes respdnded to variousdegrees.

Rice is not only grown on heavilyleached mineral soils low in available Sibut on largely organic low-Si soils aswell. On such soils, also, applications ofSi dramatically reduced the severity offungal diseases (112). The authors com-mented on the scrutiny being bestowedon the use offungicides on environmentalgrounds, and the desirability of exploringalternatives such as Si applications. As isthe case for the dicotyledonous vegetablespecies discussed earlier, the mecha-nisms whereby Si impedes fungal infec-tions of cereals need further study. Inter-esting observations in experiments withbarley are recorded by Carver et al. (113),who also mentioned the possibility ofbreeding crops that absorb Si to highlevels and effectively mobilize it to resistfungal penetration.Not all plant parasites are fungi, nor

are plant shoots the only organs attacked.Striga spp. (Scrophulariaceae), known aswitch weed, is a parasitic flowering plantthat attacks the roots of important cropssuch as rice, sorghum, millet, corn, sug-arcane, and small grains. According toSlife (114), it is the most widespread andserious of all seed plants that are cropparasites. Its haustoria penetrate into thehost roots; the degree to which this takesplace varies depending on the host gen-otype and the thickness of the host rootendodermis and pericycle due to the de-gree of their lignification, silicification,and possibly other factors (115, 116). Noclear-cut correlation has been shown,

however, between the degree of resis-tance and silicification.

Fungal hyphae and parasite haustoriasuccessfully infecting plant cells mustbreach the cell wall, and they do so bychemical means. Herbivores, includingphytophagous insects, have to penetratethe cell wall mechanically. The physicalproperties ofthe wall are factors affectingthe severity of herbivory, as, of course,are the cell contents once the wall hasbeen pierced or macerated. There is ev-idence that plants with a high Si contentare thereby afforded a measure of pro-tection against herbivory (117, 118), animportant effect in view of the huge roleof herbivory in the economy of nature(119).

Solution Culture

Solution culture is the only techniquepermitting exposure of plant roots to amineral substrate whose composition isdetermined by the investigator and capa-ble of being monitored and controlled(85). Of necessity, therefore, solutionculture plays, and must continue to play,a prominent role in plant biological re-search including investigations in mineralplant nutrition, ion transport, mineralmetabolism, water relations, and geno-typic responses to environmental stress-es-indeed, whenever the mineral milieuthat the roots are exposed to must beknown and under control.

This review has summarized ample ev-idence of several important roles that Siplays in plant biology. First, when Si isamply available, as in most soils and insolution cultures to which it has beenadded, plants contain Si in their tissues atlevels comparable to those ofseveral mac-ronutrient elements such as K, Ca, Mg, S,and P. Second, most of the Si absorbed isdeposited in the form ofamorphous silica,SiO2rnH2O, or opal, which is most prom-inently associated with the cell wall, theparticulars of its morphology and patternof deposition depending on both the gen-otype and environmental conditions.Third, Si has major effects on the absorp-tion and translocation of several macro-nutrient and micronutrient elements.Fourth, Si positively affects the growthand development of many plants, mostparticularly by contributing to the me-chanical strength of cell walls and theirfunction of keeping plants erect and theirleaves well positioned for light intercep-tion. Fifth, Si often mitigates and some-times abolishes the adverse effects of ex-cess P or heavy metals or salinity in themedium. Sixth, the impregnation of cellwalls with silica contributes to the resis-tance of plants to attacks by fungi, para-sitic higher plants, and herbivores, includ-ing phytophagous insects.

Together, this evidence amounts to apowerful case for the importance of Si in

Review: Epstein

Proc. Natl. Acad. Sci. USA 91 (1994)

plant biology. Because of the conven-tional wisdom, however, to the effectthat Si is not generally essential forplants, the element is not normally in-cluded in the formulation of nutrient so-lutions used in research in experimentalplant biology. Hoagland and Arnon (120)listed the composition of four nutrientsolutions used by early investigators,from 1860 to 1902. In none ofthem was Siincluded. The most comprehensive list-ing by far of the composition of nutrientsolutions formulated over a period ofmore than a century is that by Hewitt(121). In the tabulation of about 150 ofsuch formulations, Si is mentioned but afew times. Clearly, on the evidencebriefly summarized in this review, theomission of Si from experimental solu-tion cultures needs to be reexamined.The presence, at appreciable concentra-tions, of Si in the medium to which plantroots are normally exposed has such aplethora of diverse effects that its omis-sion amounts to the imposition of anatypical environmental stress. Plantsgrown under these conditions are in im-portant aspects experimental artifacts(122, 123). The definition of essentialityand the evaluation of Si in that frame-work provide no logical basis for omittingthe element from the formulation of nu-trient solftions. The actualities of plantbiology prompt its inclusion. In this lab-oratory, 1 mM Na2SiO3 is included in amodified Hoagland solution (12). Mostcommonly, that solution is used at 0.25times its full concentration, thus contain-ing 0.25 mM Na2SiO3 (123). The recom-mendation that Si be included in theformulation of solution cultures (122,123) is reiterated. Commercial hydro-ponicists should also take notice.

Conclusion: Silicon in Plant Biology andBeyond

The role of Si in experimental plant biol-ogy has implications beyond this fielditself. Hodson and Sangster (74) dis-cussed possible taxonomic, anatomical,archaeological, and medical implica-tions. The taxonomical value of Si lies inthe characteristic morphology of. opal"phytoliths," which may serve as a di-agnostic character. The common associ-ation of silica with cell walls and inter-cellular spaces represents a link to plantanatomy. Silica phytoliths found at ar-chaeological sites may serve to identifycrops grown by their inhabitants. Thearchaeological use of plant silica phyto-liths has been advocated by Piperno(124). Phytoliths bonded to the teeth ofanextinct ape that lived a million years agohave given indications of its diet (125).Dust from wheat and rice containing si-licious fibers poses a health hazard sim-ilar to that due to nonbiogenic siliciousfibrous materials such as asbestos (74).

The deposition of siliceous structures inconjunction with an organic matrix hasimplications for materials science andbiomimetic syntheses (126-128). Agreater awareness of the importance of Siin plants, especially on the part of exper-imental plant biologists, is bound to havebeneficial synergistic effects beyondplant biology per se.

I thank P. H. Brown, R. G. Burau, W. H.Casey, R. A. Dahlgren, J. C. King, and R. 0.Miller, all at this campus, for information anddiscussion. My research during the prepara-tion of this review was supported by GrantDEFG 03 89ER14037 from the Department ofEnergy.

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