Sie sind auf Seite 1von 23

PY55CH04-Datnoff ARI 8 May 2017 16:51

Review in Advance first posted online


V I E W
E on May 15, 2017. (Changes may
R

still occur before final publication

S
online and in print.)

C E
I N

A
D V A

Silicons Role in Abiotic


and Biotic Plant Stresses
Daniel Debona,1 Fabrcio A. Rodrigues,1
and Lawrence E. Datnoff 2
1
Department of Plant Pathology, Laboratory of Host-Pathogen Interaction, Vicosa Federal
University, Vicosa, Minas Gerais State, Brazil, 36570-900; email: fabricio@ufv.br
Access provided by University of Sherbrooke on 05/15/17. For personal use only.
Annu. Rev. Phytopathol. 2017.55. Downloaded from www.annualreviews.org

2
Department of Plant Pathology & Crop Physiology, Louisiana State University Agricultural
Center, Baton Rouge, Louisiana, 70803; email: ldatnoff@agcenter.lsu.edu

Annu. Rev. Phytopathol. 2017. 55:4.14.23 Keywords


The Annual Review of Phytopathology is online at disease management, drought, foliar diseases, host defense mechanisms,
phyto.annualreviews.org
metal toxicity, pest control, plant nutrition, salt stress, soilborne diseases
https://doi.org/10.1146/annurev-phyto-080516-
035312 Abstract
Copyright  c 2017 by Annual Reviews. Silicon (Si) plays a pivotal role in the nutritional status of a wide variety
All rights reserved
of monocot and dicot plant species and helps them, whether direct or in-
directly, counteract abiotic and/or biotic stresses. In general, plants with a
high root or shoot Si concentration are less prone to suffer from pest at-
tack and exhibit enhanced tolerance to abiotic stresses such as drought, low
temperature, or metal toxicity. However, the most notable effect of Si is the
reduction in the intensities of a number of seedborne, soilborne, and foliar
diseases in many economically important crops that are caused by biotrophic,
hemibiotrophic, and necrotrophic plant pathogens. The reduction in disease
symptom expression is due to the effect of Si on some components of host
resistance, including incubation period, lesion size, and lesion number. The
mechanical barrier formed by the polymerization of Si beneath the cuticle
and in the cell walls was the first proposed hypothesis to explain how this
element reduced the severity of plant diseases. However, new insights have
revealed that many plant species supplied with Si have the phenylpropanoid
and terpenoid pathways potentiated and have a faster and stronger tran-
scription of host defense genes and higher activities of defense enzymes.
Photosynthesis and the antioxidant metabolism involved in the removal of
reactive oxygen species are improved for Si-supplied plants. Although the
current understanding of how this overlooked element affects plants against
pathogen infections, pest attacks, and abiotic stresses has advanced, the exact
mechanism(s) by which it modulates plant physiology through the poten-
tiation of host defense mechanisms still needs further investigation at the
genomic, metabolomic, and proteomic levels.

4.1

Changes may still occur before final publication online and in print
PY55CH04-Datnoff ARI 8 May 2017 16:51

INTRODUCTION
Silicon (Si), a tetravalent metalloid, is the second most abundant element in the Earths crust
after oxygen (43). Most soils contain Si concentrations ranging from 14 to 20 mg Si/L (10).
Concentrations of this magnitude are common for other inorganic nutrients, such as sulfur (S),
potassium (K), and calcium (Ca), and are in excess of phosphorus (P) concentrations in the soil
solution (10, 43, 160). Dissolution of Si from soil minerals is a slow process and its adsorption
or resorption by the soil particles along with a continuous monoculture of crops may cause its
depletion to the point that soil amendment with soluble Si sources is needed to achieve high yields
(31). Some organic soils (histosols) contain little Si in their native state. Some, such as oxisols
and ultisols, are highly weathered, leached, and low in base saturation. Further, soils comprising
mainly quartz sand [silica (SiO2 )] (e.g., sandy entisols) may be high in insoluble Si but are very low
in plant-available Si. Other soil orders considered to be low or limiting are acidic alfisols, acidic
inceptisols, and spodosols (33, 159). Many soilless mixes fall into this category too. These low-
Access provided by University of Sherbrooke on 05/15/17. For personal use only.

soluble Si soil conditions are found in many crop-producing areas of Africa, Asia, the Americas,
Annu. Rev. Phytopathol. 2017.55. Downloaded from www.annualreviews.org

and Europe (33).


Soil weathering processes release SiO2 into the soil solution, surface water, and other natu-
ral water bodies mainly in the form of monosilicic acid (H4 SiO4 ), the prevalent and uncharged
monomeric molecule that exists below pH 9 (160). All plants grown in soil contain a certain con-
centration of Si in their tissues, as reported for more than 44 angiosperm clades that represent
over 100 orders or families (51, 71). When determining whether or not a plant accumulates Si,
past studies have focused primarily on measuring Si concentration in the foliage and not in other
plant organs (71, 154). However, coffee, peppers, and tomatoes concentrate as much, if not more,
Si in the roots as in the shoots (14, 52, 72). Si translocation from roots to shoots dramatically vary
among plant species and growth stage, and shoot Si concentration ranges from 0.1% to 10% on a
dry-weight basis (43). Monocots tend to accumulate more Si in shoots than do dicots. In general,
the Si shoot concentration is from 5% to 7% for wetland grasses, from 0.5% to 1.5% for dryland
grasses, and less than 0.5% for many dicots. At the low end of the range, 0.1% Si corresponds on
a dry-matter basis with macronutrients, such as Ca, magnesium (Mg), P, and S. At the upper end
of 10%, the tissue concentrations of Si exceed those of mineral nutrients such as nitrogen (N) and
K. Clearly, Si is a major mineral constituent of plants and is essential for diatoms, yellow-brown
or golden algae, and the Chrysophyceae and Equisetaceae, and is considered to be quasi-essential
for the growth and development of many plant species (43, 101, 120, 122).
Plants uptake Si from the soil solution as H4 SiO4 and subsequently transport it from roots
to shoots either passively or actively (101). The active mode of Si uptake from roots to shoots
was identified to be due to specific transporter proteins (10). These were first characterized in
certain monocots, such as barley, maize, rice, and wheat (21, 99, 100, 101, 110, 154), but dicots
such as cucumber, pumpkin, and soybean also have been found to have similar transporters (35).
Consequently, the difference in Si shoot concentration among plant species is attributed to their
differential ability to uptake this element by roots (10). Once across the endodermis, Si moves
through the xylem for plant species known to have the Si transporter proteins and/or is driven by
transpirational flow into the root endodermis, the cell membranes of the vascular bundle, and the
leaf cells of the epidermis to be further deposited beneath the cuticle (99, 100). The polymerization
of converting H4 SiO4 into insoluble silica (SiO2 nH2 O, a.k.a. opal, silica gel, or phytoliths) can
occur in the roots but is more prevalent beneath the cuticle and in the plant cell walls.
Plants supplied with Si counteract many types of abiotic (e.g., cold, drought, heat, salinity,
and mineral deficiency or toxicity) and biotic (e.g., plant diseases and herbivores and other pests)
stresses more efficiently (3, 32, 107, 130, 138). The benefits of Si were largely overlooked until the

4.2 Debona Rodrigues Datnoff

Changes may still occur before final publication online and in print
PY55CH04-Datnoff ARI 8 May 2017 16:51

beginning of the twentieth century partly because of the elements abundance in nature and the
lack of visible symptoms of deficiency, and mainly because plant physiologists largely disregarded
the possible effects of this element from any meaningful experiments. However, in field and
greenhouse environments, plants are constantly exposed to different types of stresses and seem
to suffer more when grown in soils low or limiting in plant-available Si. An awareness of Si
deficiency in soils has become recognized since the 1980s as being a limiting factor in overall plant
development and crop yield (33). Although world conferences on Si in agriculture have been held
in the United States (1999), Japan (2002), Brazil (2005), South Africa (2008), China (2011), and
Sweden (2014), with the overarching theme of providing a forum in which the benefits of Si in
agriculture are discussed among plant scientists, agricultural managers, and companies producing
Si materials, the use of this element in agricultural production has been slow to materialize in many
countries. This review aims to provide the current status of the potential of Si in ameliorating
both abiotic and biotic stress in important economic crops.
Access provided by University of Sherbrooke on 05/15/17. For personal use only.
Annu. Rev. Phytopathol. 2017.55. Downloaded from www.annualreviews.org

SILICON AND ALLEVIATION OF ABIOTIC STRESS

Metal Toxicity
Si is recognized for decreasing metal toxicity, and some mechanisms have been suggested to explain
this effect (3). The decrease in availability of phytotoxic metals in soil might be due to the increase
in pH and changes in the speciation (i.e., chemical and physical form) of metals in the soil solution
by the formation of silicate complexes (3). Sodium metasilicate increased soil pH and decreased
exchangeable lead (Pb), thus reducing soil Pb availability (87). Increases in soil pH and reduction in
bioavailable cadmium (Cd) also were reported as a result of applying amorphous silica (87% SiO2 )
(131). Cadmium in soil was also found to be in the form of specific adsorbed (bound to carbonates)
or iron (Fe)-manganese (Mn) oxidebound fractions in Si-amended soil (93). Exogenously applied
Si decreased chromium (Cr) availability in the soil by promoting precipitation-bound and organic
matterbound Cr fractions (36). Formation of hydroxyaluminum silicate is thought to be involved
in Si-mediated detoxification of aluminum (Al) in plants (70). Si-rich biochar was demonstrated
to reduce the amount of soil-exchangeable Al and prevent its migration to the plant (119). The
reduced availability and phytotoxicity of metals afforded by corn cob silica were related to the
formation of insoluble Pb silicate, as revealed by X-ray diffraction analysis, and to an increase in
soil pH, which further promoted binding of the heavy metals to carbonates, Fe and Mn oxides,
organic matter, and S in the soil (145). Taken collectively, these results suggest that pH and changes
in metal speciation are targets for Si in alleviating metal toxicity. However, Si-modulated changes
in the rhizosphere rather than in the bulk soil and the effect of Si sources and its concentration
need to be explored to better understand the effect of this element in the immobilization of metals
(3).
Plants exposed to abiotic stress (e.g., drought, metal, and saline stresses) show an increased
concentration of reactive oxygen species (ROS), such as superoxide radical (O2 ), hydroxyl radical
(OH ), and hydrogen peroxide (H2 O2 ), that damage biomolecules such as nucleic acids, photosyn-
thetic pigments, and proteins (3, 96, 130, 144). A decrease in ROS production and an enhancement
in the antioxidant system for Si-supplied plants may account for their increased tolerance to abiotic
stresses. Application of Si and Si nanoparticles (SiNP) decreased O2 , H2 O2 , and malondialde-
hyde (MDA) concentrations in maize leaves by increasing activities of ascorbate peroxidase (APX),
dehydroascorbate reductase (DHAR), or glutathione (GSH) reductase (GR) under arsenic (As)
stress. This finding demonstrated that rising ascorbate (AsA)-GSH cycle components are one of
the key mechanisms to counteract As (157). Increases in the activities of APX, catalase (CAT),

www.annualreviews.org Silicons Role in Abiotic and Biotic Plant Stresses 4.3

Changes may still occur before final publication online and in print
PY55CH04-Datnoff ARI 8 May 2017 16:51

peroxidase (POX), and superoxide dismutase (SOD) in roots and leaves of cotton plants also were
related to Si-mediated reductions in H2 O2 and MDA concentrations under zinc (Zn) stress (5). A
similar mechanism was found to be operating in the Si-afforded alleviation of boron, Cd, Cr, Fe,
Pb, and Mn toxicity in several plant species (3).
The compartmentalization of metals in roots and shoots is another Si-mediated tolerance
mechanism. In early studies, Si was demonstrated to alleviate Mn toxicity without reducing its
foliar concentration in barley plants. Mn was found to be more evenly distributed in Si-supplied
plants rather than being concentrated within necrotic spots (165). Si increased metal concentration
in roots and, consequently, lowered shoot concentration. Increased copper (Cu) adsorption was
observed at the outer thin layer (<100 A) root surface and immobilized in the central cylinder of
the root epidermis, and translocation was limited through an enhanced thickening of a Si-loaded
endodermis (79). In addition, Si-treated cucumber plants displayed less Mn in the symplast than
in the cell wall (136). However, Si-induced Mn sequestration in nonphotosynthetic tissues was
suggested as a mechanism of tolerance in maize (39).
Access provided by University of Sherbrooke on 05/15/17. For personal use only.
Annu. Rev. Phytopathol. 2017.55. Downloaded from www.annualreviews.org

Metal toxicity has also been reported to be decreased by coprecipitation of Si with metals
in roots and leaves. In rice, lowered Cd, Cu, Pb, and Zn translocation from culm to leaf by Si
amendments was attributed to their coprecipitation with this element (59). Si was also proposed
to form precipitates with Zn as well as change Zn2+ into nonphytotoxic forms in the cell wall of
less bioactive tissues, especially in sclerenchyma of roots (60). Similarly, a hemicellulose-bound,
complexing Cd form of Si with net negative charge was suggested to inhibit Cd uptake by rice
root cells (97).
Some studies also have reported that chelation of flavonoid-phenolics or organic acids with
metals takes place in mitigation of heavy metal stress by Si. In maize, higher exudation of Al-
chelating catechin and quercetin, as well as malic acid, was observed in Si plus Al-exposed maize
compared to Al alone (80). Furthermore, Si increased the proportion of inorganic and organic
anion ligands such as aconitate that increased Cu sequestration into a less toxic form (79).
Recently, Si was reported to not affect the expression of two metal chelators [MsPCS1 (phy-
tochelatin synthase) and MsMT2 (metallothionein)], but it increased that of Fe-related genes
[MsIRT1 (Fe transporter), MsNramp1 (metal transporter), and OsFRO1 (ferric chelate reductase)]
under Cd stress in alfalfa roots. This finding suggested that limiting Fe uptake rather than metal
sequestration is important in Si-mediated alleviation of Cd toxicity (76). Genes, e.g., PCS1, SAP1,
and SAP14, encoding members of the stress-associated protein (SAP) family and the transcription
factor genes AP2/Erf020, Hsf31, and NAC6 were upregulated in roots of Cd-stressed rice plants
but downregulated in the presence of Si and indicated that post-stress addition of Si was able to
reverse Cd stress (44). A study of the rice leaf proteome under Cd stress showed that 50 proteins,
including those associated with photosynthesis, redox homeostasis, protein regulation/synthesis,
pathogen response, and chaperone activity, were upregulated by Si, whereas a class III POX and
a thaumatin-like protein were found to be upregulated by Si irrespective of Cd (113). Therefore,
Si appears to regulate gene expression to alleviate metal toxicity.

Drought and Salt Stress


Si has been shown to decrease drought stress in plants through different mechanisms, which in-
clude an increase in mineral nutrient uptake, modification of gas exchange attributes, osmotic
adjustment, reduction in oxidative stress, modification of gene expression, and regulation of com-
patible solutes and phytohormone synthesis (130). Si-induced increases in a balanced mineral
nutrient uptake and translocation may account for observed beneficial effects. In rice, Si mitigated
the adverse effects of drought while increasing K and total P concentrations in straw (41). Si uptake

4.4 Debona Rodrigues Datnoff

Changes may still occur before final publication online and in print
PY55CH04-Datnoff ARI 8 May 2017 16:51

was strongly correlated with K under water deficit in Rhodes grass (Chloris gayana), Timothy grass
(Phleum pratense), Sudan grass (Sorghum sudanense), and tall fescue (Festuca arundinacea) (42). Sim-
ilarly, Si increased Ca, K, and Mg concentrations in tomato seedlings under salt stress improving
their tolerance to salinity (86).
Impairments in gas exchange attributes and leaf relative water content (RWC) are among the
primary mechanisms by which drought and salt stress reduce crop productivity. Si has been demon-
strated to nullify such stress-induced impairments. For example, photosynthesis, transpiration rate,
and leaf water content under water stress were preserved in leaves of tomato plants supplied with
Si, suggesting that increased water uptake/transport rather than decreased transpiration was be-
hind Si-alleviated stress (144). Conversely, a Si-induced increase in water-use efficiency (WUE) in
maize subjected to water stress was related to a reduced transpiration rate through stomata, indi-
cating that Si affected stomatal aperture (54), which might be species-dependent. The increases in
RWC or WUE due to increased silicification of leaves or root endodermis that prevent water from
escaping through plant tissues are thought to be involved in Si-alleviated osmotic stress (130). Si
Access provided by University of Sherbrooke on 05/15/17. For personal use only.
Annu. Rev. Phytopathol. 2017.55. Downloaded from www.annualreviews.org

alleviates salinity stress in tomato seedlings by increasing photosynthesis, leaf transpiration rate,
and stomatal conductance and by decreasing the concentrations of Na+ and Cl in the leaves stem
and roots (86). Photosynthesis, stomatal conductance, transpiration rate, WUE, the number of
stomata, and stomatal size in okra plants exposed to salt stress were increased by foliarly applying
Si (150 mg/L) (1). Cucumber plants supplied with Si and exposed to salt stress displayed increased
photosynthesis, transpiration rate, leaf water content, and root hydraulic conductance, a fact that
was ascribed to a decrease in Na+ and an increase in K+ concentrations in the leaves (163). Si is
known to reduce Na+ uptake by stimulating the root plasma membrane H+ -ATPase activity (166)
and to reduce Na+ translocation by promoting its binding to cell walls, thus reducing Na+ in the
leaf apoplast (63).
Salt toxicity and water deficit are known to induce lipid peroxidation by ROS in plants, and
Si was able to alleviate salt- and drought-induced oxidative stress by stimulating the antioxidant
system (1, 86, 96, 144). Tomato plants supplied with Si and submitted to water stress displayed
increased CAT and SOD activities, high levels of AsA and GSH, lowered electrolyte leakage and
O2 and H2 O2 concentrations, and no changes in the plasma membrane integrity as compared
with control plants (144). The H2 O2 and lipid peroxidation levels from drought-stressed wheat
plants supplied with Si were reduced and the concentrations of AsA, GSH, total phenolics, and
total flavonoids increased (96). In salt-stressed roots of tomato seedlings, CAT and SOD activities
and the concentrations of nonprotein thiols and AsA were increased, whereas H2 O2 and membrane
oxidative damage were decreased by Si (86). The CAT, POD, and SOD activities increased and
lipid peroxidation was reduced for both a salt-tolerant and a salt-sensitive okra genotype supplied
with Si and subjected to NaCl stress (1).
Regulation of compatible solutes and phytohormone synthesis, including abscisic acid (ABA),
glycine betaine, indole-butyric acid (IAA), jasmonic acid ( JA), polyamines (PAs), proline, and sal-
icylic acid (SA) may enhance plant tolerance to salt or water stress (1, 168). Proline and glycine
betaine concentrations increased for pepper plants supplied with Si and exposed to drought stress.
Furthermore, Si increased nitrate reductase activity, indicating that this element can also in-
crease drought tolerance by enhancing N assimilation (116). Levels of soluble sugars and levels of
both free and conjugated PAs, including putrescine, spermidine, and spermine increased, whereas
1-aminocyclopropane-1-carboxylic acid (ACC), the precursor of ethylene (ET) decreased upon
Si treatment of drought-stressed sorghum plants (168). Similarly, Si application reversed the
decrease in the concentrations of the PAs putrescine and spermine in the roots of salt-stressed
cucumbers (163). The higher accumulation of glycine betaine, proline, total free amino acids, total
soluble sugars, and total phenolics under Si supply indicated its effect in improving the osmotic

www.annualreviews.org Silicons Role in Abiotic and Biotic Plant Stresses 4.5

Changes may still occur before final publication online and in print
PY55CH04-Datnoff ARI 8 May 2017 16:51

adjustment capacity and antioxidant activity of okra plants under saline conditions (1). Short-term
Si applications downregulated JA and upregulated ABA after 6 and 12 h in rice plants under salinity
stress (82). In soybean, Si alleviated the adverse effects of NaCl on plant growth by enhancing
endogenous gibberellic acid and decreasing ABA levels (85). In another study, both JA and salicylic
acid (SA) concentrations declined for soybean plants supplied with Si and submitted to drought
stress, whereas JA and SA concentrations decreased and increased, respectively, for Si-supplied
plants under salt stress (64).
Quantitative real-time polymerase chain reaction analysis revealed that Si application increased
the expression of four AsA-GSH cycle genes and five flavonoid biosynthesis pathway genes in
drought-stressed wheat plants and decreased MDA and H2 O2 concentrations, indicating that this
element played a pivotal role in the coordinated transcriptional regulation of multiple antioxidant
defenses in response to drought (96). In sorghum, the Si-mediated upregulation of several root
aquaporin genes was thought to increase root hydraulic conductance and improve root water up-
take under osmotic stress (95), whereas an upregulation of key PA synthesis genes was also believed
Access provided by University of Sherbrooke on 05/15/17. For personal use only.
Annu. Rev. Phytopathol. 2017.55. Downloaded from www.annualreviews.org

to be involved in Si-mediated salt tolerance (169). The application of Si in combination with salt
stress transiently increased the expression of the ABA biosynthesis-related genes zeaxanthin epox-
idase and 9-cis-epoxicarotenoid oxygenase 1 and 4 (ZEP, NCED1, and NCED4) in comparison to
that with salt stress alone in rice (82). In tobacco BY-2 cell cultures, Si alleviated the damage of
NaCl stress by increasing ET emission and the expression of ET biosynthesis genes, whereas Si
failed to enhance plant tolerance in the absence of ET (89).

Other Abiotic Stresses


In addition to the stresses reported above, Si was also demonstrated to alleviate stresses caused
by low temperature (75, 91), ultraviolet-B (UV-B) radiation (158), and nutrient deficiency (106,
115). In cucumber plants grown under chilling temperatures (15/8 C), exogenous Si decreased
leaf withering, O2 , H2 O2 , and MDA concentrations through increased APX, GR, GSH POX,
monodehydroascorbate reductase, POX and SOD reductase activities, and the concentrations of
both AsA and GSH (75). In addition, a higher deposition of Si in leaves of chilling-stressed seedlings
played a role in constraining accumulation of MDA and damage to lipid membranes (75). Similarly,
Si-supplied plants from a freezing-susceptible and a freezing-tolerant wheat cultivar grown at
5 C displayed higher water retention, CAT, and SOD activities and higher concentrations of
AsA and GSH, which were related to lowered accumulation of H2 O2 and MDA (91). Recently,
SiNP was found to more effectively alleviate UV-B stress in wheat than Si by triggering the
antioxidant defense system. The reduced membrane lipid peroxidation and electrolyte leakage
and ROS-induced damage to photosynthesis were nitric-oxide-signaling dependent (158).
Regarding mineral nutrient deficiencies, ameliorative effects of Si have been consistently ob-
served for K (17, 106), P (98, 114), and Fe (9, 115), but inconsistent results were reported for
Mn and Zn (9). Addition of sodium silicate increased K concentration in leaves, stems, and roots
of soybean plants under K deficiency and ameliorated K deficiencyinduced reductions in shoot
and root growth. Moreover, Si prevented oxidative stress and lipid peroxidation due to K defi-
ciency by increasing CAT, POX, and SOD activities (106). Si alleviated the decreases in the leaf
gas exchange parameters, whole-plant hydraulic conductance, and root hydraulic conductance as
well as increased K accumulation in the xylem of K-deficient sorghum plants, indicating that Si
improved plant-water status under K deficiency (17). Si was beneficial for rice growth only under
low (0.014 mM) or high (0.70 mM) P levels, an effect that was ascribed to decreases in Fe and
Mn uptake at low P levels and to a reduced P uptake at high P levels (98). Soil P sorption was
reduced by sodium silicate, and Si was involved in the ameliorative effects for maize growth under

4.6 Debona Rodrigues Datnoff

Changes may still occur before final publication online and in print
PY55CH04-Datnoff ARI 8 May 2017 16:51

P deficiency (114). Under Fe-deficient conditions, accumulation of Fe-mobilizing compounds and


expression levels of genes encoding proteins involved in Fe acquisition (FRO2, IRT1, and HA1) in
roots of cucumber were increased by Si (115). The alleviating Si effect in Fe deficiency in cucum-
ber was also linked to an enhanced Fe distribution toward apical shoot parts due to an increased
accumulation of Fe-mobilizing compounds such as citrate and catechin (9). These findings are
consistent with reports showing that Si can increase the accumulation of transcripts related to
both the shikimate and phenylpropanoid pathways (SK and PAL, respectively) in root tips under
Fe deprivation (115).

SILICON: HERBIVORE AND OTHER PEST ATTACKS


Although Si has proven to be effective in controlling a high number of insect herbivores and other
arthropods (90) (Table 1), the exact nature of Si-mediated antiherbivore defense remains largely
unknown (129). Even so, some mechanisms underlying Si-afforded plant resistance to pests are
Access provided by University of Sherbrooke on 05/15/17. For personal use only.
Annu. Rev. Phytopathol. 2017.55. Downloaded from www.annualreviews.org

very similar to what is known about the role this element plays in suppressing plant diseases.
For example, the proposed Si deposition beneath the cuticle acting as a physical barrier against
plant disease appears to also function in defense against a number of herbivores and other pests
(129).
The exposure of Spodoptera exempta to high-Si diets reduced leaf digestibility and caused
mandible wear, which probably impacted herbivore performance (102). Similarly, the reduced
food quality and food conversion efficiencies were suggested to be responsible for a decrease in
the third instars weight gain and pupal weight of the rice leaf folder (Cnaphalocrocis medinalis) at a
high Si rate (65). In rice, lower relative growth rates and reduced boring success of the sugarcane
borer (Diatraea saccharalis) were observed in plants supplied with Si in comparison to controls
(147). High foliar Si concentration was associated with reduced sugarcane stalk larval penetration
by the pyralid borer Eldana saccharina (84). Energy dispersive X-ray microanalysis revealed that Si
concentrations increased in the stalks of sugarcane supplied with Si, but the magnitude of accumu-
lation was tissue dependent. For example, the epidermis of the internode and root band displayed
high Si accumulation, whereas Si was not evident in the bud scale. This finding might explain
why the leaf bud is a preferred entry point for the larval stage of E. saccharina (78). Furthermore,
irrespective of the Si supply, a higher Si accumulation was observed in a borer-resistant sugarcane
cultivar than in a borer-susceptible sugarcane cultivar, suggesting that resistance may be, at least
in part, associated with the plants ability to accumulate Si in the shoots (78).
The first evidence that Si might play an active role in host resistance against herbivores was
reported by McNaughton & Tarrants (104). The authors showed that heavily grazed African
grasses accumulated more Si in their leaf blades than did less heavily grazed plants, indicating
that silicification was probably an inducible defense against mammalian herbivores. In another
study, Si applied to the soil or foliage showed that the greenbug aphids (Schizaphis graminum)
stylet penetration into wheat was not affected, thus challenging the physical barrier hypothesis (58).
Furthermore, biochemical analysis confirmed that Si enhanced wheat defense mechanisms against
the greenbug aphid through an increase in POX, polyphenoloxidase (PPO), and phenylalanine
ammonia lyase (PAL) activities, especially when plants received Si before aphid infestation (57).
Ranger and his colleagues (123) observed reductions in total cumulative fecundity and the intrinsic
rate of increase of Myzus persicae on plants of Zinnia elegans supplied with Si. These reductions
were associated with great concentrations of 5-caffeoylquinic acid, p-coumaroylquinic acid, and
rutin in Z. elegans plants supplied with Si as compared to those that were not supplied with Si.
Rice plants grown in a Si-amended soil and infested with the leaf folder (Cnaphalocrocis medinalis)
displayed higher CAT, PAL, POX, PPO, and SOD activities and lower MDA concentration than

www.annualreviews.org Silicons Role in Abiotic and Biotic Plant Stresses 4.7

Changes may still occur before final publication online and in print
PY55CH04-Datnoff ARI 8 May 2017 16:51

Table 1 Herbivores and other pests reported to be suppressed by silicona


Mouthpart Pests
Chewing African armyworm (Spodoptera exempta)
African striped rice stem borer (Chilo zacconius)
Asiatic rice borer (Chilo suppressalis)
Central shoot fly (Atherigonaindica infuscate)
Green rice caterpillar (Naranga aenescens)
Hessian fly (Mayetiola destructor)
Hessian fly (Phytophaga destructor)
Leaf folder (Cnaphalocrocis medinalis)
Pink stalk borer (Sesamia spp.)
Sugarcane borer (Diatraea saccharina)
Stalk borer (Eldana saccharina)
Access provided by University of Sherbrooke on 05/15/17. For personal use only.
Annu. Rev. Phytopathol. 2017.55. Downloaded from www.annualreviews.org

Sunflower caterpillar (Chlosyne lacinia saundersii )


Yellow rice borer (Scirpophaga incertulas)
Weevil (Cylas formicarius)
Piercing-sucking Aphid (Sitobion avenae)
Brown planthopper (Nilaparvata lugens)
Greenbug (Schizaphis graminum)
Green leafhopper (Nephotettix bipunctatus cincticeps)
Green peach aphid (Myzus persicae)
Small brown planthopper (Laodelphax striatellus)
Spider mite (Tetranychus urticae)
White-backed planthopper (Sogatella furcifera)
Whitefly (Bemisia tabaci )

a
Adapted from Reference 90.

plants grown in a nonamended soil. This finding suggested that Si-supplied plants were primed
to enhance antioxidant metabolism and defense mechanisms upon pest attack (66). The level of
transcripts for defense marker genes, JA accumulation, and POX and PPO activities, as well as
the level of trypsin protease inhibitor, increased in rice plants supplied with Si and attacked by
C. medinalis (167). In addition, JA was found to be important in the rice resistance against leaf
borer attack because Si was not able to increase resistance to this insect in plants whose genes
involved in JA biosynthesis or JA perception were silenced (167). Interestingly, Si deposition was
reduced when JA signaling was compromised, indicating a strong interaction between JA-mediated
responses to insect herbivores and Si as well as promotion of Si accumulation and JA (167).
Besides affecting bitrophic (plant-herbivore) interactions, Si has also been shown to affect
tritrophic (plant-herbivorenatural enemy) interactions, which may account for another possible
role in controlling pests (83, 129). In this case, Si may reduce insect feeding either by making them
more vulnerable to their natural enemies (55) or by changing the composition and concentration
of herbivore-induced plant volatiles (HIPVs), thus attracting the insects enemies (83). Although
potassium silicate applied at higher concentrations (0.08 and 0.16%; v/v) alone did not kill mites
(Tetranychus urticae), Beauveria bassianainduced mite mortality was enhanced for beans, cucum-
ber, eggplant, and maize (55). This finding was attributed to Si-primed biochemical defenses in
the plants, making the mites more susceptible to the entomopathogen (55). In rice, a combined

4.8 Debona Rodrigues Datnoff

Changes may still occur before final publication online and in print
PY55CH04-Datnoff ARI 8 May 2017 16:51

application of potassium silicate, B. bassiana, and imidacloprid resulted in the maximum mortality
of C. medinalis (141). Cucumber plants supplied with Si were more attractive to adults of the preda-
tor Dicranolaius bellulus when attacked by larvae of Helicoverpa armigera in comparison to those
not supplied (83). The number of eggs from H. armigera removed from potted cucumber plants
and placed in a lucerne stand with numerous predatory arthropods was higher in the presence of
Si (83). A change in the HIPVs profile produced by Si-supplied cucumber plants when attacked
by the herbivore was thought to be involved in the plants attractiveness to natural enemies (83).
Indeed, considering that JA signaling is activated by Si for plants attacked by pests (167), such
a pathway could provide HIPVs required for the natural enemies attraction (129). Conversely,
even though the preference of the greenbug aphid (S. graminum) for wheat plants supplied with Si
was decreased, the attractiveness of the natural enemies Chrysoperla externa and Aphidius colemani
was not observed (111). Reynolds et al. (129) pointed out that effects of HIPVs might not have be-
come apparent because wheat plants were narrowly spaced and a nonchoice design was employed.
Therefore, Si seems to play an important role in the complex mechanisms involved in decreasing
Access provided by University of Sherbrooke on 05/15/17. For personal use only.
Annu. Rev. Phytopathol. 2017.55. Downloaded from www.annualreviews.org

pests attack, which include physical barriers as well as biochemical and molecular changes that
can either directly reduce pest feeding and development or enhance the plants attractiveness to
natural enemies of pests.

SILICON POTENTIATES HOST DEFENSE MECHANISMS AGAINST


PLANT PATHOGEN INFECTION
A supply of Si to plants has been shown to reduce the intensities of several diseases [e.g., damping
off, leaf blights, leaf spots, galls, powdery mildews, root rots, rusts, and wilts; caused by different
genera of bacteria, fungi, nematodes, and oomycetes as well as a virus (Table 2)] in many eco-
nomically important crops (50, 132). In many of the host-pathogen interactions studied, both final
disease severity and the area under the disease progress curve were reduced as a result of the posi-
tive effect of Si on key components of host resistance, such as the incubation period, latent period,
colony or lesion size, lesion number, lesion expansion, and inoculum production per infection
site (50, 132). Sis impact on components of host resistance has helped to partially explain why

Table 2 Genera of plant pathogens causing seedborne, soilborne, and foliar diseases that had
their infection process impaired by silicona
Pathogens Genera
Fungi Alternaria, Bipolaris, Blumeria, Botrytis, Bremia, Cylindrocladium, Cercospora,
Colletotrichum, Corynespora, Diaporthe, Didymella, Drechslera, Erysiphe, Fusarium,
Ganoderma, Hemileia, Leptosphaeria, Magnaporthe, Microdochium, Monilinia,
Monographela, Mycosphaerella, Oculimacula, Oidiopsis, Oidium, Penicillium,
Pestalotia, Phakopsora, Phomopsis, Podosphaera, Pseudocercospora, Puccinia,
Pyricularia, Ramularia, Rhizoctonia, Sclerospora, Sclerotinia, Septoria, Sphaerotheca,
Trichothecium, Uncinula, and Ustilago
Oomycetes Phytophthora and Pythium
Bacteria Acidovorax, Pseudomonas, Ralstonia and Xanthomonas
Virus Nepovirus
Nematode Meloidogyne

a
A more comprehensive species list of fungi, oomycetes, bacteria and nematodes causing plant diseases that are suppressed
by silicon in a number of economically important crops can be found by consulting the Reference 132.

www.annualreviews.org Silicons Role in Abiotic and Biotic Plant Stresses 4.9

Changes may still occur before final publication online and in print
PY55CH04-Datnoff ARI 8 May 2017 16:51

the resistance of susceptible cultivars may be enhanced to the level of cultivars with race-specific
resistance (128, 134, 139).
The physical barrier hypothesis, which is related to Si deposition and polymerization beneath
the cuticle, in the cell wall, and inside the bulliform cells, was first proposed to explain the reduction
in rice blast severity (Figure 1a). Indeed, this hypothesis was also accepted for explaining the
reductions in disease intensities occurring in other monocots as well as in some dicots species.
In the case of the ricePyricularia oryzae interaction, fungal penetration can be either avoided
(reduction in the number of infection pegs formed by appressoria that pierced the underlying cell

Polymerized silicon Soluble silicon Necrotic cell

a ap
c
gt
Access provided by University of Sherbrooke on 05/15/17. For personal use only.

Homogeneous Si deposition
Annu. Rev. Phytopathol. 2017.55. Downloaded from www.annualreviews.org

High cu
sl
Si
cw

Low ep

No lesions me

Disuniform Si deposition
High

Si

Low

Small lesions

Reduced Si deposition
High

Si

Low

Large lesions

4.10 Debona Rodrigues Datnoff

Changes may still occur before final publication online and in print
PY55CH04-Datnoff ARI 8 May 2017 16:51

wall; consequently, lesions did not develop) or delayed (increase in both incubation and latent
periods and decrease in lesion size) (2, 67, 69, 73, 135, 140, 153, 170). An outer, electron-dense
Si layer embedded in the cellulose microfibrils and an inner electron-translucent layer in the
epidermal cell wall of leaves of rice plants supplied with Si inhibited the colonization by P. oryzae
(81). The disuniformity in Si deposition beneath the cuticle and its further polymerization in the
form of amorphous silica bodies in the rice epidermal cells may allow the narrow penetration
peg of P. oryzae to penetrate (Figure 1b), but a delay in the incubation period and even in the
latent period can occur (12, 81, 112, 135). The reduced Si deposition beneath the cuticle and
the few epidermal cells containing silica bodies allowed penetration by P. oryzae. In this case,
both the incubation period and latent period were shorter, and the sizes of the blast lesions were
larger as a consequence of an unlimited colonization of the epidermal and mesophyll cells by
fungal hyphae (Figure 1c) (135). The silicification of oat epidermal cell walls reduced penetration
by Blumeria graminis f. sp. avenae (15). According to Seebold et al. (140), Si acts more than
as a physical barrier to increase rice resistance to blast because developing leaf lesions were of
Access provided by University of Sherbrooke on 05/15/17. For personal use only.
Annu. Rev. Phytopathol. 2017.55. Downloaded from www.annualreviews.org

reduced size on rice cultivars with different basal levels of resistance. For the Arabidopsis thaliana
Erysiphe cichoracearum, cucumberColletotrichum lagenarium, cucumberPodosphaera xanthii, rice
Monographella albescens, riceRhizoctonia solani, wheatBipolaris sorokiniana, and wheatP. oryzae
interactions, the silicification of the epidermal cells delayed fungal penetration, colonization, and
sporulation (6, 30, 38, 46, 77, 105, 135, 137, 150). Appressoria of B. graminis f. sp. hordei were
unable to penetrate the epidermal cell walls of barley with high Si deposition. However, if fungal
penetration occurred, Si was deposited in the papillae and in the haustorial neck in an attempt to
delay penetration and haustoria formation (15, 74, 171). The deposition of Si along with phenolics
and hydroxyproline-rich glycoproteins in the leaves of French bean and cowpea plants reduced
the number of haustoria formed by Uromyces vignae (68, 117). Papillae formation seemed to be
stimulated in the presence of Si as reported for the rosePodosphaera pannosa and wheatB. graminis
f. sp. tritici interactions (8, 143). The interruption in Si supply resulted in high powdery mildew
and blast severities on the leaves of cucumber and rice plants, respectively. This finding suggested
that a minimal Si concentration and its continuous supply are required in newly formed leaves for


Figure 1
Proposed hypotheses to explain how silicon (Si) suppresses leaf blast, caused by Pyricularia oryzae,
development on rice. (a) The physical barrier hypothesis: The homogeneous Si deposition and
polymerization beneath the cuticle, as determined by X-ray microanalysis, completely block fungal
penetration, and, consequently, blast lesions do not develop. (b) The Si-mediated host defense mechanisms
hypothesis: The disuniformity in Si deposition beneath the cuticle, as determined by X-ray microanalysis,
may allow the narrow penetration peg to penetrate the cuticle and the wall of the epidermal cell. In this case,
there is a delay in both the incubation period (appearance of symptoms) and latent period (fungal
sporulation). Blast lesions are reduced in size owing to limited colonization of the leaf tissues by fungal
hyphae. A delay in fungal penetration allows the cells to counteract against fungal infection more efficiently
through the activation of host defense mechanisms (e.g., production of high amounts of phenolics,
phytoalexins, and lignin as well as high activities of defense enzymes such as chitinases and -1,3-
glucanases). It is believed that the soluble Si at the infection sites may be involved somehow in the
potentiation of these host mechanisms of defense. (c) Plants not supplied with Si: The reduced Si deposition
beneath the cuticle, as determined by X-ray microanalysis, allows fungal penetration. In this case, both the
incubation period and latent period are shorter, and the size of the blast lesion is larger as a consequence of
an unlimited colonization of the epidermal and mesophyll cells by fungal hyphae. In the X-ray microanalysis
images of the adaxial surface of rice leaves, red indicates the highest Si deposition and blue or black indicates
the absence of Si. Abbreviations: ap, appressorium; c, conidium; cu, cuticle; cw, cell wall; ep, epidermis; gt,
germ tube; me, mesophyll; sl, silica layer.

www.annualreviews.org Silicons Role in Abiotic and Biotic Plant Stresses 4.11

Changes may still occur before final publication online and in print
PY55CH04-Datnoff ARI 8 May 2017 16:51

optimal disease control (137, 152). Furthermore, it is postulated that the insoluble Si may not be as
important as the soluble Si at the time of fungal ingress to lower the disease intensity. The physical
barrier hypothesis is probably one tiny facet of how Si suppresses plant disease development, and
one must now take into account that the physiological, biochemical, and molecular data now
available will open new avenues of research to better understand the role of Si as a modulator of
host defense mechanisms.
Microscopic analyses showed that Si potentiated host defense mechanisms as evidenced by the
fact that many leaf cells of cucumber plants supplied with Si rapidly accumulated phenolics in
response to infection by Podosphaera xanthii (105). Biochemical analyses revealed high concen-
trations of flavonoids and phenolic acids in the leaf extracts of cucumber plants supplied with
Si, which also showed reduced powdery mildew symptoms (47). At both histopathological and
ultrastructural levels, many empty hyphae of P. oryzae and M. albescens were found to be evenly
surrounded or trapped in a dense osmiophilic material that also partially occluded epidermal and
mesophyll cells and the vascular bundle of rice plants supplied with Si (6, 135). In contrast to the
Access provided by University of Sherbrooke on 05/15/17. For personal use only.
Annu. Rev. Phytopathol. 2017.55. Downloaded from www.annualreviews.org

Si-supplied plants, the epidermal and mesophyll cells of nonsupplied rice plants were devoid of
organelles, and the cell walls were no longer discernible in the mesophyll. In addition, the vas-
cular bundle was massively colonized by fungal hyphae (6, 135). Intense and rapid deposition of
electron-dense phenolic-like material was found in the root cells of cucumber plants supplied with
Si and infected with Pythium ultimum (20). Cytologically, leaves of wheat plants supplied with Si
reacted against infection by B. graminis f. sp. tritici as evidenced by an intense autofluorescence of
the epidermal cells (an indicator of phenolics) and increased concentration of fungitoxic aglycones
(125). The resistance of wheat plants supplied with Si to powdery mildew was linked to a high
concentration of antifungal methylated forms of trans-aconitate that possibly acted as phytoalexins
(126). Histochemically, Si proved to enhance the deposition of dopamine, flavonoids, lignin, and
phenolics in the sclerenchyma cells and in the metaxylem and phloem vessels in the roots of banana
plants infected with Fusarium oxysporum f. sp. cubense (48). Hyphae of F. oxysporum f. sp. vasinfectum
found in the endodermal cells and vascular vessels in the roots of cotton plants supplied with Si
were degraded due to the deposition of an electron-dense material (164). In the wheatP. oryzae
interaction, the production of phenolics and flavonoids was enhanced in the infected leaves of
Si-supplied plants (22, 30). Glycosylated phenolics, based on cytochemical labeling, were densely
deposited on the extrahaustorial membrane of the fungus and in the cell wall of epidermal cells of
wheat plants supplied with Si and infected with B. graminis f. sp. tritici (8).
In general, the activities of several enzymes related to host defense (e.g., -1,3-glucanase
(GLU), chitinase (CHI), PAL, POX, and PPO increased in plants supplied with Si as reported for
the following host-pathogen interactions: bananaF. oxysporum f. sp. cubense, bananaXanthomonas
campestris pv. musacearum, bitter gourdErysiphe sp., cucumberP. ultimum, cucumberP. xanthii,
coffeeMeloidogyne exigua, cottonColletotrichum gossypii var. cephalosporioides, cottonPhakopsora
gossypii, cottonRamularia areola, melonPodosphaera xanthii, peaMycosphaerella pinodes, perennial
ryegrassP. oryzae, riceB. oryzae, riceM. albescens, riceP. oryzae, riceR. solani, riceXanthomonas
oryzae pv. oryzae, sorghumColletotrichum sublineolum, soybeanPhakopsora pachyrhizi, and tomato
Pseudomonas syringae pv. tomato (4, 13, 19, 23, 25, 2729, 49, 61, 62, 92, 103, 121, 124, 128, 148, 149,
156, 172). Based on two-dimensional electrophoresis maps, Chen et al. (18) found that 26 proteins
were altered (16 increased and 10 decreased) in the roots of tomato plants supplied with Si and
infected with Ralstonia solanacearum, and most of them were associated with both plant metabolism
and defense mechanisms. A high Si concentration in the shoots of plants infected with different
pathogens was associated with a more efficient antioxidant metabolism (high APX, CAT, GR, and
SOD activities), thereby enhancing the removal of ROS (24, 34, 37, 49, 88, 108, 118, 127, 152).
The reduced ROS-dependent cellular damage was indirectly linked to lower MDA concentration

4.12 Debona Rodrigues Datnoff

Changes may still occur before final publication online and in print
PY55CH04-Datnoff ARI 8 May 2017 16:51

due to reduced lipid peroxidation in Si-supplied and pathogen-infected plants (24, 28, 34, 37, 49,
109, 118, 127). Debona et al. (34) reported that wheat plants supplied with Si and infected with
P. oryzae showed lower cellular damage and decreased APX, CAT, GSH-S-transferase, POX, and
SOD activities. Activities of APX, CAT, and SOD decreased in the leaves of wheat plants supplied
with Si and infected with B. graminis f. sp. tritici (109). From a proteomic perspective, Liu et al.
(94) reported that the quantity of APX, DHAR, and SOD increased in rice plants supplied with
Si and infected with P. oryzae.
Si has been shown to potentiate host defenses by enhancing defense-related gene expres-
sion. The genes encoding for GLU, chalcone synthase, CHI, cinnamyl alcohol dehydrogenase,
lipoxygenase, PAL, POX, and PR-1 were all upregulated in the perennial ryegrassP. oryzae,
riceP. oryzae, rosePodosphaera pannosa, and wheatP. oryzae interactions (22, 121, 135, 142).
For snap beans, genes encoding an ET response factor, a polygalacturonase inhibitor protein,
a defense-associated phosphatase, and PR-1 were overexpressed and contributed to resistance
against gray mold (Botrytis cinerea) and cottony rot (Pythium aphanidermatum) (40). The expres-
Access provided by University of Sherbrooke on 05/15/17. For personal use only.
Annu. Rev. Phytopathol. 2017.55. Downloaded from www.annualreviews.org

sion levels of the genes Os03g0109600 (encoding a protein with 175 amino acids and containing
a nuclear localization signal), Prla (PR-1), Rcht2 (chitinase), Lox2 (lipoxygenase), and Pal (phenyl-
alanine ammonia lyase) were high for rice plants supplied with Si and infected with X. oryzae pv.
oryzae, whereas the genes CatA (catalase) and Os03g0126000 (encoding a binding protein with 424
amino acids) had their expression downregulated (149). Many antimicrobial compounds, related
to both primary and secondary metabolism, such as anthocyanins, flavonoids, lignin-thioglycolic
acid derivatives, momilactones, and phenolics, had their concentrations increased in the tissues of
pathogen-infected plants supplied with Si (25, 28, 49, 61, 62, 121, 128, 135, 142, 148, 149, 164,
172).
Some transcriptomic studies have been carried out to elucidate the molecular mechanisms
by which Si potentiates host defense. Fauteux et al. (45) used a 44-K microarray chip to study
the expression of genes of Arabidopsis plants nonsupplied or supplied with Si and infected with
B. graminis f. sp. tritici. The expression of all but two genes was unaffected by Si in noninoculated
plants. Regardless of Si, the expression of a set of nearly 4,000 genes was either upregulated [e.g.,
R genes, stress-related transcription factors, genes involved in signal transduction, the biosynthesis
of stress hormones (SA, JA, and ET) and the metabolism of ROS] or downregulated (genes involved
in primary metabolism) by pathogen infection. The magnitude of downregulation was dramatically
attenuated for the inoculated plants supplied with Si, indicating alleviation of the stress imposed
by the fungus (45). In another study, Chain et al. (16) performed transcriptomic analysis of 55,000
unigenes to compare the response of wheat plants nonsupplied or supplied with Si in the absence
or presence of infection by B. graminis f. sp. tritici. Only 47 genes of diverse functions and with
little evidence of regulation of a specific metabolic process were upregulated for the uninoculated
and Si-supplied plants. Many genes linked to stress and metabolic processes were upregulated, and
genes associated with photosynthesis were downregulated for infected plants not treated with Si.
However, for the infected and Si-supplied plants, genes linked to stress and metabolic processes
were downregulated, and those linked to photosynthesis were upregulated. The expression of
genes associated with JA/ET pathways, oxidative stress, and host defense had their expression
upregulated in the roots of tomato plants supplied with Si and infected with Ralstonia solanacearum
(56).
Brunings and her colleagues (11) used a 44-K gene chip to study gene expression of rice
plants treated with Si and nontreated and then infected by P. oryzae. They found that a
unique number of defense/stress-related genes [ET signaling pathway genes, a gene encoding
a thaumatin/pathogenesis-related protein (Os12g0568900), a class III POX (Os07g0677500) and
a number of transcription factors and protein kinases] were upregulated in the P. oryzae versus

www.annualreviews.org Silicons Role in Abiotic and Biotic Plant Stresses 4.13

Changes may still occur before final publication online and in print
PY55CH04-Datnoff ARI 8 May 2017 16:51

Si + P. oryzae treatment comparisons, highlighting how Si may have changed the plants reaction
to the pathogen. Further, the Si versus Si + P. oryzae comparison had 440 differentially expressed
genes fewer than the control versus P. oryzae comparison, and this comparison had only 236 genes
in common. Si therefore affected the interaction between the host and pathogen at the molecular
level by attenuating the rice response to the pathogen and by the differential expression of a unique
set of genes. Consequently, rice plants supplied with Si were preconditioned to react against this
pathogen stress, and this is further supported by the finding that infection by P. oryzae resulted
in less than half the number of differentially expressed genes in Si-amended plants versus nona-
mended plants (298 versus 738, respectively). All these aforementioned studies were unanimous in
concluding that Si played a pivotal role in the plants transcriptome only upon pathogen infection.
The physiology of plants infected by pathogens is negatively affected as evidenced by changes
in the values of leaf gas exchange parameters, reductions in the amount of healthy leaf area, de-
creases in the concentration of photosynthetic pigments, damage to the chloroplasts, impairments
in energy dissipation via chlorophyll a fluorescence and high foliar temperature (146). Several
Access provided by University of Sherbrooke on 05/15/17. For personal use only.
Annu. Rev. Phytopathol. 2017.55. Downloaded from www.annualreviews.org

studies showed that Si partially preserved the photosynthetic performance of plants infected by
pathogens. For many host-pathogen interactions such as common beanColletotrichum lindemuthi-
anum, cottonR. areola, cottonC. gossypii var. cephalosporioides, riceP. oryzae, riceM. albescens,
sorghumC. sublineolum, and wheatP. oryzae, the Si supply to plants, besides reducing disease
severities, contributed to the preservation of photosynthesis and the concentration of photosyn-
thetic pigments (7, 24, 37, 61, 118, 127, 155). Some photochemical parameters associated with
chlorophyll a fluorescence, such as the quantum yield of photosystem II (PSII) photochemistry
(Fv /Fm ), the photochemical quenching coefficient, and the electron transport rate, were greatly im-
proved for rice plants infected with P. oryzae or M. albescens and wheat plants infected with P. oryzae
if supplied with Si (7, 37, 155). The heat dissipation of chlorophyll excitation energy, based on the
nonphotochemical quenching parameter, decreased for rice and wheat plants infected with either
P. oryzae or M. albescens, respectively, when supplied with Si compared to infected controls. This
finding suggests that the PSII electron transport at the chloroplast level was not impaired, and the
photoprotective processes were preserved by Si treatment (7, 37, 155). Gao et al. (53) also reported
that an increase in rice resistance to blast due to Si was associated with an enhancement in the
photochemical efficiency, specifically by an increase in the values of Fv /Fm and the maximum pri-
mary yield of the photochemistry of PSII. Bipolaris oryzae infection repressed photosynthesis and
nitrate reduction in the leaves of rice plants nonsupplied with Si, triggering premature senescence
and therefore contributing to an increase in brown spot severity (162). By contrast, the expression
of many photorespiratory marker genes was upregulated in Si-supplied plants, indicating that
an increase in photorespiration helped to alleviate the stress imposed by B. oryzae infection by
protecting the rices photosynthetic machinery (162). Several genes involved in photosynthesis
and metabolism of amino acids, carbohydrates, and lipids were downregulated in the leaves of
Arabidopsis thaliana nonsupplied with Si and infected by E. cichoracearum. However, in infected
plants supplied with Si, many of these genes were less responsive (45). For the wheatB. graminis
f. sp. tritici interaction, the supply of Si to plants contributed to the downregulation of genes
associated with stress and metabolic processes and the upregulation of those related to photo-
synthesis (16). Proteins involved in photosynthesis (chlorophyll a/bbinding protein, chloroplast
putative thylakoid lumenal 16.5-kDa protein, sedoheptulose-1,7-bisphosphatase, and ribulose bis-
phosphate carboxylase large subunit) and the tricarboxylic acid and pentose phosphate pathways
were upregulated in rice plants supplied with Si and infected with P. oryzae compared to in-
fected controls without Si (94). According to Dallagnol et al. (26), the inefficiency of the lsi1
(low Si; defective in active Si uptake) rice mutant, which originated from the wild-type cultivar
Oochikara, to actively uptake Si resulted in greater brown spot severity and, consequently, reduced

4.14 Debona Rodrigues Datnoff

Changes may still occur before final publication online and in print
PY55CH04-Datnoff ARI 8 May 2017 16:51

photosynthesis and foliar sugar concentration. By contrast, the high foliar Si concentration de-
creased brown spot symptoms, preserved photosynthesis, and promoted high foliar sugar concen-
tration for the wild-type cultivar Oochikara. Rice resistance to brown spot was independently and
additively affected by Si and soluble sugar concentrations in the leaf tissue (26).
Some studies have linked Si with the plant hormones that modulate defense mechanisms such
as ET, JA, and SA in the ArabidopsisE. cichoracearum interaction (45), ET in the riceP. oryzae
and riceB. oryzae interactions (11, 161), and ET and JA in the tomatoR. solanacearum interaction
(56). Rice resistance to brown spot potentiated by Si was associated with the inability of the ET
produced by B. oryzae to suppress the rice plants innate immune system and, consequently, to
avoid the activation of the basal mechanisms of defense (161).

CONCLUDING REMARKS
Si, a major component of the soil-plant system, plays significant roles in a plants life especially in
Access provided by University of Sherbrooke on 05/15/17. For personal use only.
Annu. Rev. Phytopathol. 2017.55. Downloaded from www.annualreviews.org

alleviating both abiotic and biotic stresses. Unfortunately, the recognition of this quasi-essential
element as one component of fertilizers that could be used in an integrated disease(s)/pest(s)
management strategy is still in its infancy. In general, plants having a high shoot or root Si
concentration are less prone to suffer from pest attack and exhibit enhanced tolerance to abiotic
stresses such as drought, metal toxicity, salinity, low temperature, and UV-B radiation. However,
the most notable effect of Si is the reduction in the intensities of a number of plant diseases caused by
biotrophic, hemibiotrophic, and necrotrophic plant pathogens causing seedborne, soilborne, and
foliar diseases in many crops of great economic importance. The reduction in symptom expression
can be ascribed to the effect of Si on components of host resistance, including incubation period,
latent period, lesion size, lesion number, and inoculum production per infection site. Although
not discussed in this review, the intensities of some diseases for Si-supplied plants are lowered to
the same level achieved with fungicides, and the resistance of susceptible cultivars amended with
Si may achieve a comparable level exhibited by cultivars with race-specific resistance (132).
The polymerization of Si beneath the cuticle and in the wall of epidermal cells is one hypothesis
that explains how this element reduces lesion number and size for some diseases. However, new
insights have revealed that in many plant species supplied with Si, the phenylpropanoid and
terpenoid pathways are greatly potentiated, and there is a faster and stronger transcription of
genes involved in host defense and higher activities of defense enzymes. Antioxidant metabolism
involved in the removal of ROS and photosynthesis were greatly improved in Si-supplied plants
regardless of the type of stress. Although our understanding of how this overlooked element helps
plants counteract pathogen infection and pest attack as well as different types of abiotic stress has
advanced, the exact mechanism(s) by which Si modulates plant physiology through the potentiation
of host defense mechanisms still needs to be investigated in more detail at the genomic, proteomic,
and metabolomic levels.

SUMMARY POINTS
1. A minimum Si concentration in the roots and/or shoots of higher plants, especially mono-
cots, is needed to effectively slow disease development and pest attack and to alleviate
abiotic stresses (e.g., drought, low temperature, metal toxicity, salinity, and UV-B radia-
tion). As the Si concentration (insoluble or soluble) in plant tissue increases, suppression
of both abiotic and biotic stresses occurs more efficiently. However, Si needs to be made
available for plant uptake during their entire life cycle to reduce these stresses.

www.annualreviews.org Silicons Role in Abiotic and Biotic Plant Stresses 4.15

Changes may still occur before final publication online and in print
PY55CH04-Datnoff ARI 8 May 2017 16:51

2. Many components of host resistance (e.g., incubation period, latent period, lesion num-
ber, lesion size, and amount of inoculum produced per infection site) are greatly affected
by Si contributing to reduce the apparent infection rate of a certain disease.
3. In the presence of Si, the resistance of some cultivars known to be susceptible may increase
to the same level of resistance of cultivars exhibiting race-specific resistance.
4. The response of plants against pathogen infection, pest attack, and even abiotic stresses
at the biochemical, physiological, and molecular levels are remarkably similar when Si
is taken up by roots and translocated to shoots, indicating an active role played by this
element in one or more plant defense signaling pathways.

DISCLOSURE STATEMENT
Access provided by University of Sherbrooke on 05/15/17. For personal use only.
Annu. Rev. Phytopathol. 2017.55. Downloaded from www.annualreviews.org

The authors are not aware of any affiliations, memberships, funding, or financial holdings that
might be perceived as affecting the objectivity of this review.

ACKNOWLEDGMENTS
We acknowledge the financial support obtained from CAPES, CNPq, and FAPEMIG to sup-
port the studies investigating the effect of silicon to control plant diseases. Professor Fabrcio A.
Rodrigues thanks CNPq for his fellowship. Professor Lawrence E. Datnoff thanks the Louisiana
State University Agricultural Center for their generous operational and financial support.

LITERATURE CITED
1. Abbas T, Balal RM, Shahid MA, Pervez MA, Ayyub CM, et al. 2015. Silicon-induced alleviation of NaCl
toxicity in okra (Abelmoschus esculentus) is associated with enhanced photosynthesis, osmoprotectants and
antioxidant metabolism. Acta Physiol. Plant. 37:6
2. Abed-Ashtiani F, Kadir JB, Selamat AB, Hanif AHBM, Nasehi A. 2012. Effect of foliar and root appli-
cation of silicon against rice blast fungus in MR219 rice variety. Plant Pathol. J. 28:16471
3. Adrees M, Ali S, Rizwan M, Zia-ur-Rehman M, Ibrahim M, et al. 2015. Mechanisms of silicon-mediated
alleviation of heavy metal toxicity in plants: a review. Ecotoxicol. Environ. Saf. 119:18697
4. Andrade CCL, Resende RS, Rodrigues FA, Ferraz HGM, Moreira WR, et al. 2013. Silicon reduces
bacterial speck development on tomato leaves. Trop. Plant Pathol.38:43642
5. Anwaar SA, Ali S, Ali S, Ishaque W, Farid M, et al. 2014. Silicon (Si) alleviates cotton (Gossypium
hirsutum L.) from zinc (Zn) toxicity stress by limiting Zn uptake and oxidative damage. Environ. Sci.
Pollut. Res. 22:344150
6. Araujo L, Paschoalino RS, Rodrigues FA. 2016. Microscopic aspects of silicon-mediated rice resistance
to leaf scald. Phytopathology 06:13241
7. Aucique-Perez CEA, Rodrigues FA, Moreira WR, DaMatta FM. 2014. Leaf gas exchange and chlorophyll
a fluorescence in wheat plants supplied with silicon and infected with Pyricularia oryzae. Phytopathology
104:14349
8. Belanger RR, Benhamou N, Menzies JG. 2003. Cytological evidence of an active role of silicon in wheat
resistance to powdery mildew (Blumeria graminis f. sp. tritici ). Phytopathology 93:40212
9. Bityutskii N, Pavlovic J, Yakkonen K, Maksimovic V, Nikolic M. 2014. Contrasting effect of silicon on
iron, zinc and manganese status and accumulation of metal-mobilizing compounds in micronutrient-
deficient cucumber. Plant Physiol. Biochem. 74:20511
10. Broadley M, Brown P, Cakmak I, Ma JF, Rengel Z, et al. 2012. Beneficial elements. In Marschners
Mineral Nutrition of Higher Plants, ed. P Marschner, pp. 24969. London: Academic. 3rd ed.

4.16 Debona Rodrigues Datnoff

Changes may still occur before final publication online and in print
PY55CH04-Datnoff ARI 8 May 2017 16:51

11. Brunings AM, Datnoff LE, Ma JF, Mitani N, Nagamura Y, et al. 2009. Differential gene expression of
rice in response to silicon and rice blast fungus Magnaporthe oryzae. Ann. Appl. Biol. 155:16170
12. Cacique IS, Domiciano GP, Moreira WR, Rodrigues FA, Cruz MFA, et al. 2013. Effect of root and leaf
applications of soluble silicon on blast development in rice. Bragantia 72:3049
13. Cai K, Gao D, Luo S, Zeng R, Yang J, et al. 2008. Physiological and cytological mechanisms of silicon-
induced resistance in rice against blast disease. Physiol. Plant.134:32433
14. Carre-Missio V, Rodrigues FA, Schurt DA, Pereira SC, Oliveira MGA, et al. 2009. Ineficiencia do silcio
no controle da ferrugem do cafeeiro em solucao nutritiva. Trop. Plant Pathol. 34:41621
15. Carver TLW, Robbins MP, Thomas BJ, Troth K, Raistrick N, et al. 1998. Silicon deprivation enhances
local autofluorescent responses and phenylalanine ammonia lyase activity in oat attacked by Blumeria
graminis. Physiol. Mol. Plant Pathol. 52:24557
16. Chain F, Cote-Beaulieu C, Belzile F, Menzies JG, Belanger RR. 2009. A comprehensive transcriptomic
analysis of the effect of silicon on wheat plants under control and pathogen stress conditions. Mol.
Plant-Microbe Interact. 22:132330
17. Chen D, Cao B, Wang S, Liu P, Deng X, et al. 2016. Silicon moderated the K deficiency by improving
Access provided by University of Sherbrooke on 05/15/17. For personal use only.
Annu. Rev. Phytopathol. 2017.55. Downloaded from www.annualreviews.org

the plant-water status in sorghum. Sci. Rep. 6:22882


18. Chen Y, Liu M, Wang L, Lin W, Fan X, et al. 2015. Proteomic characterization of silicon-mediated
resistance against Ralstonia solanacearum in tomato. Plant Soil 387:42540
19. Cherif M, Asselin A, Belanger RR. 1994. Defence responses induced by soluble silicon in cucumber roots
infected by Pythium spp. Phytopathology 84:23642
20. Cherif M, Benhamou N, Menzies JG, Belanger RR. 1992. Silicon induced resistance in cucumber plants
against Pythium ultimum. Physiol. Mol. Plant Pathol. 41:41125
21. Chiba Y, Mitani N, Yamaji N, Ma JF. 2009. HvLsi1 is a silicon influx transporter in barley. Plant J.
57:81018
22. Cruz MFA, Debona D, Rios JA, Rodrigues FA. 2015. Potentiation of defense-related gene expression
by silicon increases wheat resistance to leaf blast. Trop. Plant Pathol. 40:394400
23. Cruz MFA, Rodrigues FA, Polanco LR, Curvelo CRS, Nascimento KJT, et al. 2013. Inducers of resis-
tance and silicon on the activity of defense enzymes in the soybeanPhakopsora pachyrhizi interaction.
Bragantia 72:16272
24. Curvelo CRS, Rodrigues FA, Pereira LF, Silva LC, DaMatta FM, et al. 2013. Trocas gasosas e estresse
oxidativo em plantas de algodoeiro supridas com silcio e infectadas porRamularia areola. Bragantia
72:34659
25. Curvelo CRS, Rodrigues FA, Silva LC, Nascimento KJT, Berger PG. 2013. Mecanismos bioqumicos
da defesa do algodoeiro a mancha de ramularia mediados pelo silcio. Bragantia 72:4151
26. Dallagnol LJ, Rodrigues FA, Chaves ARM, Vale FXR, DaMatta FM. 2013. Photosynthesis and sugar
concentration are impaired by the defective active silicon uptake in rice plants infected with Bipolaris
oryzae. Plant Pathol. 62:12029
27. Dallagnol LJ, Rodrigues FA, DaMatta FM, Mielli MVB, Pereira SC. 2011. Deficiency in silicon up-
take affects cytological, physiological, and biochemical events in the rice-Bipolaris oryzae interaction.
Phytopathology 101:92104
28. Dallagnol LJ, Rodrigues FA, Pascholati SF, Fortunato AA, Camargo LEA. 2015. Comparison of root
versus foliar applied potassium silicate in potentiating postinfection defences of melon against powdery
mildew. Plant Pathol. 64:108593
29. Dann EK, Muir S. 2002. Peas grown in media with elevated plant-available silicon levels have higher
activities of chitinases and -1,3-glucanase, are less susceptible to a fungal leaf spot pathogen and accu-
mulate more foliar silicon. Australas. Plant Pathol 31:913
30. da Silva WL, Cruz MFA, Fortunato AA, Rodrigues FA. 2015. Histochemical aspects of wheat resistance
to leaf blast mediated by silicon. Sci. Agric. 72:32227
31. Datnoff LE, Deren CW, Snyder GH. 1997. Silicon fertilization for disease management of rice in
Florida. Crop Prot. 16:52531
32. Datnoff LE, Rodrigues FA. 2005. The role of silicon in suppressing rice diseases. APSnet Features
doi:10.1094/APSnetFeature-2005-0205

www.annualreviews.org Silicons Role in Abiotic and Biotic Plant Stresses 4.17

Changes may still occur before final publication online and in print
PY55CH04-Datnoff ARI 8 May 2017 16:51

33. Datnoff LE, Rodrigues FA. 2015. History of silicon and plant disease. See Ref. 133, pp. 15
34. Debona D, Rodrigues FA, Rios JA, Nascimento KJT, Silva LC. 2014. The effect of silicon on antioxidant
metabolism of wheat leaves infected by Pyricularia oryzae. Plant Pathol. 63:58189
35. Deshmukh RK, Vivancos J, Guerin V, Sonah H, Labbe C, et al. 2013. Identification and functional
characterization of silicon transporters in soybean using comparative genomics of major intrinsic proteins
in Arabidopsis and rice. Plant Mol. Biol. 83:30315
36. Ding X, Zhang S, Li S, Liao X, Wang R. 2013. Silicon mediated the detoxification of Cr on pakchoi
(Brassica chinensis L.) in Cr-contaminated soil. Procedia Environ. Sci. 18:5867
37. Domiciano GP, Cacique IS, Freitas CC, Filippi MC, DaMatta FM, Rodrigues FA, et al. 2015. Alterations
in gas exchange and oxidative metabolism in rice leaves infected by Pyricularia oryzae are attenuated by
silicon. Phytopathology 105:73847
38. Domiciano GP, Rodrigues FA, Guerra AMN, Vale FXR. 2013. Infection process of Bipolaris sorokiniana
on wheat leaves is affected by silicon. Trop. Plant Pathol. 38:25863
39. Doncheva SN, Poschenrieder C, Stoyanova ZI, Georgieva K, Velichkova M, et al. 2009. Silicon ame-
lioration of manganese toxicity in Mn-sensitive and Mn-tolerant maize varieties. Environ. Exp. Bot.
Access provided by University of Sherbrooke on 05/15/17. For personal use only.

65:16997
Annu. Rev. Phytopathol. 2017.55. Downloaded from www.annualreviews.org

40. El-Garhy HAS, Rashid IAS, Abou-Ali RM, Moustafa MMA. 2016. Field application of safe chemical
elicitors induced the expression of some resistance genes against grey mold and cottony rot diseases
during snap bean pods storage. Gene 576:35865
41. Emam MM, Khattab HE, Helal NM, Deraz AE. 2014. Effect of selenium and silicon on yield quality of
rice plant grown under drought stress. Aust. J. Crop Sci. 8:596605
42. Eneji AE, Inanaga S, Muranaka S, Li J, Hattori T, et al. 2008. Growth and nutrient use in four grasses
under drought stress as mediated by silicon fertilizers. J. Plant Nutr. 31:35565
43. Epstein E. 2009. Silicon: its manifold roles in plants. Ann. Appl. Biol. 155:15560
44. Farooq MA, Detterbeck A, Clemens S, Dietz K-J. 2016. Silicon-induced reversibility of cadmium toxicity
in rice. J. Exp. Bot. 67:357385
45. Fauteux F, Chain F, Belzile F, Menzies JG, Belanger RR. 2006. The protective role of silicon in the
Arabidopsispowdery mildew pathosystem. PNAS 103:1755459
46. Fauteux F, Remus-Borel W, Menzies JG, Belanger RR. 2005. Silicon and plant disease resistance against
pathogenic fungi. FEMS Microb. Lett. 249:16
47. Fawe A, Abou-Zaid M, Menzies JG, Belanger RR. 1998. Silicon-mediated accumulation of flavonoid
phytoalexins in cucumber. Phytopathology 88:396401
48. Fortunato AA, da Silva WL, Rodrigues FA. 2014. Phenylpropanoid pathway is potentiated by silicon in
the roots of banana plants during the infection process of Fusarium oxysporum f. sp. cubense. Phytopathology
104:597603
49. Fortunato AA, Rodrigues FA, Baroni JCP, Soares GCB, Rodriguez MAD, et al. 2012. Silicon suppresses
Fusarium wilt development in banana plants. J. Phytopathol. 160:67479
50. Fortunato AA, Rodrigues FA, Datnoff LE. 2015. Silicon control of soil-borne and seed-borne diseases.
See Ref. 133, pp. 5366
51. Frantz JM, Pitchay DDS, Locke JC, Horst LE, Krause CR. 2005. Silicon is deposited in leaves of New
Guinea impatiens. Plant Health Prog. doi:10.1094/php-2005-0217-01-rs
52. French-Monar RD, Rodrigues FA, Korndorfer GH, Datnoff LE. 2010. Silicon suppresses Phytophthora
blight development on bell pepper. J. Phytopathol. 158:55460
53. Gao D, Cai K, Chen J, Luo S, Zeng R, et al. 2011. Silicon enhances photochemical efficiency and adjusts
mineral nutrient absorption in Magnaporthe oryzae infected rice plants. Acta Physiol. Plant. 33:67582
54. Gao X, Zou C, Wang L, Zhang F. 2006. Silicon decreases transpiration rate and conductance from
stomata of maize plants. J. Plant. Nutr. 29:163747
55. Gatarayiha MC, Laing MD, Miller RM. 2010. Combining applications of potassium silicate and Beauveria
bassiana to four crops to control two spotted spider mite, Tetranychus urticae Koch. Int. J. Pest Manag.
56:29197
56. Ghareeb H, Bozso Z, Ott PG, Repenning C, Stahl F, et al. 2011. Transcriptome of silicon-induced
resistance against Ralstonia solanacearum in the silicon non-accumulator tomato implicates priming effect.
Physiol. Mol. Plant Pathol. 75:8389

4.18 Debona Rodrigues Datnoff

Changes may still occur before final publication online and in print
PY55CH04-Datnoff ARI 8 May 2017 16:51

57. Gomes FB, Moraes JCD, Santos CDD, Goussain MM. 2005. Resistance induction in wheat plants by
silicon and aphids. Sci. Agric. 62:54751
58. Goussain MM, Prado E, Moraes JC. 2005. Effect of silicon applied to wheat plants on the biology
and probing behaviour of the greenbug Schizaphis graminum (Rond.) (Hemiptera: Aphididae). Neotrop.
Entomol. 34:80713
59. Gu HH, Qiu H, Tian T, Zhan SS, Deng THB, et al. 2011. Mitigation effects of silicon rich amendments
on heavy metal accumulation in rice (Oryza sativa L.) planted on multi-metal contaminated acidic soil.
Chemosphere 83:123440
60. Gu HH, Zhan S, Wang SZ, Tang YT, Chaney RL, et al. 2012. Silicon-mediated amelioration of zinc
toxicity in rice (Oryza sativa L.) seedlings. Plant Soil 350:193204
61. Guerra AMNM, Rodrigues FA, Berger PG, Barros AF, Rodrigues YC, et al. 2013. Resistencia do algo-
doeiro a ferrugem tropical potencializada pelo silcio. Bragantia 72:27991
62. Guerra AMNM, Rodrigues FA, Berger PG, Barros AF, Silva YCR, et al. 2013. Aspectos bioqumicos da
resistencia do algodoeiro a ramulose potencializada pelo silcio. Bragantia 72:292303
63. Habibi G, Norouzi F, Hajiboland R. 2014. Silicon alleviates salt stress in pistachio plants. Prog. Biol. Sci.
Access provided by University of Sherbrooke on 05/15/17. For personal use only.

4:189202
Annu. Rev. Phytopathol. 2017.55. Downloaded from www.annualreviews.org

64. Hamayun M, Sohn F-Y, Khan SA, Shinwari ZK, Khan AL, et al. 2010. Silicon alleviates the adverse
effects of salinity and drought stress on growth and endogenous plant growth hormones of soybean
(Glycine max L.). Pak. J. Bot. 42:171322
65. Han Y, Lei W, Wen L, Hou M. 2015. Silicon-mediated resistance in a susceptible rice variety to the
rice leaf folder, Cnaphalocrocis medinalis Guenee (Lepidoptera:Pyralidae). PLOS ONE 10:e0120557
66. Han Y, Li P, Gong S, Yang L, Wen L, Hou M. 2016. Defense responses in rice induced by silicon
amendment against infestation by the leaf folder Cnaphalocrocis medinalis. PLOS ONE 11:e0153918
67. Hayasaka T, Fujii H, Ishiguro K. 2008. The role of silicon in preventing appressorial penetration by the
rice blast fungus. Phytopathology 98:103844
68. Heath MC, Stumpf MA. 1986. Ultrastructural observations of penetration sites of the cowpea rust fungus
in untreated and silicon-depleted French bean cells. Physiol. Mol. Plant Pathol. 29:2739
69. Hemmi T, Abe T, Inoue Y. 1941. Studies on the rice blast disease: relation of the environment to the
development of blast disease and races of the blast fungus. Noji Kairyo Shiryo 157:1232
70. Hodson MJ, Evans DE. 1995. Aluminium/silicon interactions in higher plants. J. Exp. Bot. 46:16171
71. Hodson MJ, White PJ, Mead A, Broadley MR. 2005. Phylogenetic variation in the silicon composition
of plants. Ann. Bot. 96:102746
72. Huang C-H, Roberts PD, Datnoff LE. 2011. Silicon suppresses Fusarium crown and root rot of tomato.
J. Phytopathol. 159:54654
73. Ito S, Hayashi H. 1931. On the relation of silica supply to rice blast. J. Sapporo Soc. Agric. Sci. 103:46061
74. Jiang D. 1993. The role of silicon in barley resistance to powdery mildew (Erysiphe graminis f. sp. hordei).
PhD Thesis, Univ. Minn., St. Paul
75. Jiao-Jing L, Shao-Hang L, Pei-Lei X, Xiu-Juan W, Ji-Gang B. 2009. Effects of exogenous silicon on the
activities of antioxidant enzymes and lipid peroxidation in chilling-stressed cucumber leaves. Agric. Sci.
China 8:107586
76. Kabir AH, Hossain MM, Khatun MA, Mandal A, Haider SA. 2016. Role of silicon counteracting cadmium
toxicity in alfalfa (Medicago sativa L.). Front. Plant Sci. 7:1117
77. Kauss H, Seehaus K, Franke R, Gilbert S, Dietrich RA, et al. 2003. Silica deposition by a strongly cationic
proline-rich protein from systemically resistant cucumber plants. Plant J. 33:8795
78. Keeping MG, Kvedaras OL, Bruton AG. 2009. Epidermal silicon in sugarcane: cultivar differences and
role in resistance to sugarcane borer Eldana saccharina. Environ. Exp. Bot. 66:5460
79. Keller C, Rizwan M, Davidian JC, Pokrovsky OS, Bovet N, et al. 2015. Effect of silicon on wheat seedlings
(Triticum turgidum L.) grown in hydroponic sand exposed to 0 to 30 M Cu. Planta 241:84760
80. Kidd PS, Llugany M, Poschenrieder C, Gunse B, Barcelo J. 2001. The role of root exudates in aluminum
resistance and silicon-induced amelioration of aluminum toxicity in three varieties of maize (Zea mays L.).
J. Exp. Bot. 52:133953
81. Kim SG, Kim KW, Park EW, Choi D. 2002. Silicon-induced cell wall fortification of rice leaves: a
possible cellular mechanism of enhanced host resistance to blast. Phytopathology 92:1095103

www.annualreviews.org Silicons Role in Abiotic and Biotic Plant Stresses 4.19

Changes may still occur before final publication online and in print
PY55CH04-Datnoff ARI 8 May 2017 16:51

82. Kim YH, Khan AL, Waqas M, Shim JK, Kim DH, et al. 2014. Silicon application to rice root zone
influenced the phytohormonal and antioxidant responses under salinity stress. J. Plant Growth Regul.
33:13749
83. Kvedaras OL, An M, Choi YS, Gurr GM. 2010. Silicon enhances natural enemy attraction and biological
control through induced plant defences. Bull. Entomol. Res. 100:36771
84. Kvedaras OL, Keeping MG. 2007. Silicon impedes stalk penetration by the borer Eldana saccharina in
sugarcane. Entomol. Exp. Appl. 125:10310
85. Lee SK, Sohn EY, Hamayun M, Yoon JY, Lee IJ. 2010. Effect of silicon on growth and salinity stress of
soybean plant grown under hydroponic system. Agrofor. Syst. 80:33340
86. Li H, Zhu Y, Hu Y, Han W, Gong H. 2015. Beneficial effects of silicon in alleviating salinity stress of
tomato seedlings grown under sand culture. Acta Physiol. Plant. 37:71
87. Li L, Zheng C, Fu Y, Wu D, Yang X, et al. 2012. Silicate-mediated alleviation of Pb toxicity in banana
grown in Pb-contaminated soil. Biol. Trace Elem. Res. 145:1018
88. Li W, Bi Y, Ge Y, Li Y, Wang J, Wang Y. 2012. Effects of postharvest sodium silicate treatment on
pink rot disease and oxidative stressantioxidative system in muskmelon fruit. Eur. Food Res. Technol.
Access provided by University of Sherbrooke on 05/15/17. For personal use only.
Annu. Rev. Phytopathol. 2017.55. Downloaded from www.annualreviews.org

234:13745
89. Liang X, Wang H, Hu Y, Mao L, Sun L, et al. 2015. Silicon does not mitigate cell death in cultured
tobacco BY-2 cells subjected to salinity without ethylene emission. Plant Cell Rep. 34:33143
90. Liang Y, Nikolic M, Belanger R, Gong H, Song A. 2015. Silicon in Agriculture, from Theory to Practice.
Amsterdam: Springer Sci.
91. Liang Y, Zhu J, Li Z, Chu G, Ding Y, et al. 2008. Role of silicon in enhancing resistance to freezing
stress in two contrasting winter wheat cultivars. Environ. Exp. Bot. 64:28694
92. Liang YC, Sun WC, Si J, Romheld V. 2005. Effects of foliar- and root-applied silicon on the enhancement
of induced resistance to powdery mildew in Cucumis sativus. Plant Pathol. 54:67885
93. Liang YC, Wong JWC, Long W. 2005. Silicon-mediated enhancement of cadmium tolerance in maize
(Zea mays L.) grown in cadmium contaminated soil. Chemosphere 58:47583
94. Liu M, Cai K, Chen Y, Luo S, Zhang Z, et al. 2014. Proteomic analysis of silicon-mediated resistance
to Magnaporthe oryzae in rice (Oryza sativa L.). Eur. J. Plant Pathol. 139:57992
95. Liu P, Yin L, Deng X, Wang S, Tanaka K, et al. 2014. Aquaporin-mediated increase in root hydraulic
conductance is involved in silicon-induced improved root water uptake under osmotic stress in Sorghum
bicolor L. J. Exp. Bot. 65:474756
96. Ma D, Sun D, Wang C, Qin H, Ding H, et al. 2016. Silicon application alleviates drought stress in wheat
through transcriptional regulation of multiple antioxidant defense pathways. J. Plant Growth Regul. 35:1
10
97. Ma J, Cai H, He C, Zhang W, Wang L. 2015. A hemicellulose-bound form of silicon inhibits cadmium
ion uptake in rice (Oryza sativa) cells. New Phytol. 206:106374
98. Ma J, Takahashi E. 1990. Effect of silicon on the growth and phosphorus uptake of rice. Plant Soil
126:11519
99. Ma JF, Tamai K, Yamaji N, Mitani N, Konishi S, et al. 2006. A silicon transporter in rice. Nature
440:68891
100. Ma JF, Yamaji N, Mitani N, Tamai K, Konishi S, et al. 2007. An efflux transporter of silicon in rice.
Nature 448:20912
101. Ma JF, Yamaji N, Mitani-Ueno N. 2011. Transport of silicon from roots to panicles in plants. Proc. Jpn.
Acad. Ser. B. 87:37785
102. Massey FP, Hartley SE. 2009. Physical defences wear you down: progressive and irreversible impacts of
silica on insect herbivores. J. Anim. Ecol. 78:28191
103. Mburu K, Oduor R, Mgutu A, Tripathi L. 2016. Silicon application enhances resistance to Xanthomonas
wilt disease in banana. Plant Pathol. 65:80718
104. McNaughton SJ, Tarrants JL. 1983. Grass leaf silicification: natural selection for an inducible defense
against herbivores. PNAS80:79091
105. Menzies JG, Ehret DL, Glass ADM, Helmer T, Koch C, et al. 1991. Effects of soluble silicon on the
parasitic fitness of Sphaerotheca fuliginea on Cucumis sativus. Phytopathology 81:8488

4.20 Debona Rodrigues Datnoff

Changes may still occur before final publication online and in print
PY55CH04-Datnoff ARI 8 May 2017 16:51

106. Miao BH, Han XG, Zhang WH. 2010. The ameliorative effect of silicon on soybean seedlings grown in
potassium-deficient medium. Ann. Bot. 105:96773
107. Miyake Y, Takahashi E. 1983. Effect of silicon on the growth of solution-cultured cucumber plant. Soil
Sci. Plant Nutr. 29:7183
108. Mohaghegh P, Khoshgoftarmanesh AH, Shirvani M, Sharifnabi B, Nili N. 2011. Effect of silicon nutri-
tion on oxidative stress induced by Phytophthora melonis infection in cucumber. Plant Dis. 95:45560
109. Moldes CA, Lima Filho OF, Merini LJ, Tsai SM, Camina JM. 2016. Occurrence of powdery mildew
disease in wheat fertilized with increasing silicon doses: a chemometric analysis of antioxidant response.
Acta Physiol. Plant. 38:206
110. Montpetit J, Vivancos J, Mitani-Ueno N, Yamaji N, Remus-Borel W, et al. 2012. Cloning, functional
characterization and heterologous expression of TaLsi1, a wheat silicon transporter gene. Plant Mol. Biol.
79:3546
111. Moraes JC, Goussai MM, Basagli MAB, Carvalho GA, Ecole CC, et al. 2004. Silicon influence on the
tritrophic interaction: wheat plants, the greenbug Schizaphis graminum (Rondani) (Hemiptera: Aphi-
didae), and its natural enemies, Chrysoperla externa (Hagen) (Neuroptera: Chrysopidae) and Aphidius
Access provided by University of Sherbrooke on 05/15/17. For personal use only.

colemani viereck (Hymenoptera: Aphidiidae). Neotrop. Entomol. 33:61924


Annu. Rev. Phytopathol. 2017.55. Downloaded from www.annualreviews.org

112. Motomura H, Fujii T, Suzuki M. 2004. Silica deposition in relation to ageing of leaf tissues in Sasa
veitchii (Carriere) Rehder (Poaceae: Bambusoideae). Ann. Bot. 93:23548
113. Nwugo CC, Huerta AJ. 2010. The effect of silicon on the leaf proteome of rice (Oryza sativa L.) plants
under cadmium-stress. J. Proteom. Res.10:51828
114. Owino-Gerroh C, Gascho GJ. 2004. Effect of silicon on low pH soil phosphorus sorption and on uptake
and growth of maize. Commun. Soil Sci. Plant Anal. 35:236978
115. Pavlovic J, Samardzic J, Masimovic V, Timotijevic G, Stevic N, et al. 2013. Silicon alleviates iron
deficiency in cucumber by promoting mobilization of iron in the root apoplast. New Phytol. 198:1096
107
116. Pereira TS, Lobato AKS, Tan DKY, Costa DV, Uchoa EB, et al. 2013. Positive interference of silicon on
water relations, nitrogen metabolism, and osmotic adjustment in two pepper (Capsicum annuum) cultivars
under water deficit. Aust. J. Crop Sci. 7:106471
117. Perumalla CJ, Heath MC. 1991. The effect of inhibitors of various cellular processes on the wall modi-
fications induced in bean leaves by the cowpea rust fungus. Physiol. Mol. Plant Pathol. 38:293300
118. Polanco LR, Rodrigues FA, Nascimento KJT, Cruz MFA, Curvelo CRS, et al. 2014. Photosynthetic
gas exchange and antioxidative system in common bean plants infected by Colletotrichum lindemuthianum
and supplied with silicon. Trop. Plant Pathol. 39:3542
119. Qian L, Chen B, Chen M. 2016. Novel alleviation mechanisms of aluminum phytotoxicity via released
biosilicon from rice straw-derived biochars. Sci. Rep. 6:29346
120. Rafi MM, Epstein E. 1999. Silicon absorption by wheat (Triticum aestivum L.). Plant Soil 211:22330
121. Rahman A, Wallis CM, Uddin W. 2015. Silicon-induced systemic defense responses in perennial ryegrass
against infection by Magnaporthe oryzae. Phytopathology 105:74857
122. Rains DW, Epstein E, Zasoski RJ, Aslam M. 2006. Active silicon uptake by wheat. Plant Soil 280:22328
123. Ranger CM, Singh AP, Frantz JM, Canas L, Locke JC, et al. 2009. Influence of silicon on resistance of
Zinnia elegans to Myzus persicae (Hemiptera: Aphididae). Environ. Entomol. 38:12936
124. Ratnayake RMRNK, Daundasekera WAM, Ariyarathne HM, Ganehenege MY. 2016. Some biochemical
defense responses enhanced by soluble silicon in bitter gourd-powdery mildew pathosystem. Australas.
Plant Pathol. 45:42533
125. Remus-Borel W, Menzies JG, Belanger RR. 2005. Silicon induces antifungal compounds in powdery
mildew-infected wheat. Physiol. Mol. Plant Pathol. 66:10815
126. Remus-Borel W, Menzies JG, Belanger RR. 2009. Aconitate and methyl aconitate are modulated by
silicon in powdery mildew-infected wheat plants. J. Plant Physiol. 166:141322
127. Resende RS, Rodrigues FA, Cavatte PC, Martins SCV, Moreira WR, et al. 2012. Leaf gas exchange
and oxidative stress in sorghum plants supplied with silicon and infected by Colletotrichum sublineolum.
Phytopathology 102:89298
128. Resende RS, Rodrigues FA, Costa RV, Silva DD. 2013. Silicon and fungicide effects on anthracnose in
moderately resistant and susceptible sorghum lines. J. Phytopathol. 161:1117

www.annualreviews.org Silicons Role in Abiotic and Biotic Plant Stresses 4.21

Changes may still occur before final publication online and in print
PY55CH04-Datnoff ARI 8 May 2017 16:51

129. Reynolds OL, Padula MP, Zeng R, Gurr GF. 2016. Silicon: potential to promote direct and indirect
effects on plant defense against arthropod pests in agriculture. Front. Plant Sci. 7:744
130. Rizwan M, Ali S, Ibrahim M, Farid M, Adrees M, et al. 2015. Mechanisms of silicon-mediated alleviation
of drought and salt stress in plants: a review. Environ. Sci. Pollut. Res. 22:1541631
131. Rizwan M, Meunier JD, Miche H, Keller C. 2012. Effect of silicon on reducing cadmium toxicity in
durum wheat (Triticum turgidum L. cv. Claudio W.) grown in a soil with aged contamination. J. Hazard.
Mater. 209210:32634
132. Rodrigues FA, Dallagnol LJ, Duarte HSS, Datnoff LE. 2015. Silicon control of foliar diseases in mono-
cots and dicots. See Ref. 133, pp. 67108
133. Rodriques FA, Datnoff LE. 2015. Silicon and Plant Disease. Cham, Switz.: Springer
134. Rodrigues FA, Datnoff LE, Korndorfer GH, Seebold KW, Rush MC. 2001. Effect of silicon and host
resistance on sheath blight development in rice. Plant Dis. 85:82732
135. Rodrigues FA, Resende RS, Dallagnol LJ, Datnoff LE. 2015. Silicon potentiates host defense mecha-
nisms against infection by plant pathogens. See Ref. 133, pp. 10938
136. Rogalla H, Romheld V. 2002. Role of leaf apoplast in silicon-mediated manganese tolerance of Cucumic
Access provided by University of Sherbrooke on 05/15/17. For personal use only.
Annu. Rev. Phytopathol. 2017.55. Downloaded from www.annualreviews.org

sativus L. Plant Cell Environ. 25:54955


137. Samuels AL, Glass ADM, Ehret DL, Menzies JG. 1991. Mobility and deposition of silicon in cucumber
plants. Plant Cell Environ. 41:48592
138. Savant NK, Synder GH, Datnoff LE. 1997. Silicon management and sustainable rice production. Adv.
Agron. 58:15191
139. Seebold KW, Datnoff LE, Correa-Victoria FJ, Kucharek TA, Snyder GH. 2000. Effect of silicon rate
and host resistance on blast, scald, and yield of upland rice. Plant Dis. 84:87176
140. Seebold KW, Kucharek TA, Datnoff LE, Correa-Victoria FJ, Marchetti MA. 2001. The influence of
silicon on components of resistance to blast in susceptible, partially resistance, and resistant cultivars of
rice. Phytopathology 91:6369
141. Shakir HU, Saeed M, Anjum NA, Farid A, Khan IA, et al. 2015. Combined effect of entomopathogenic
fungus (Beauveria bassiana), imidacloprid and potassium silicate against Cnaphalocrocis medinalis Guenee
(Lepidoptera: Pyralidae) in rice crop. J. Entomol. Zool. Stud. 3:17377
142. Shetty R, Frette X, Jensen B, Shetty NP, Jensen JD, et al. 2011. Silicon-induced changes in antifungal
phenolic acids, flavonoids, and key phenylpropanoid pathway genes during the interaction between
miniature roses and the biotrophic pathogen Podosphaera pannosa. Plant Physiol. 157:2194205
143. Shetty R, Jensen B, Shetty NP, Hansen M, Hansen CW, et al. 2012. Silicon induced resistance against
powdery mildew of roses caused by Podosphaera pannosa. Plant Pathol. 61:12031
144. Shi Y, Zhang Y, Han W, Feng R, Hu Y, et al. 2016. Silicon enhances water stress tolerance by improving
root hydraulic conductance in Solanum lycopersicum L. Front. Plant Sci. 7:196
145. Shim J, Shea PJ, Oh BT. 2014. Stabilization of heavy metals in mining site soil with silica extracted from
corn cob. Water Air Soil Pollut. 225:112
146. Shtienberg D. 1992. Effects of foliar diseases on gas exchange processes: a comparative study. Phytopathol-
ogy 82:76065
147. Sidhu JK, Stout MJ, Datnoff LE. 2013. Effect of silicon soil amendment on performance of sugarcane
borer, Diatraea saccharalis (Lepidoptera: Crambidae) on rice. Bull. Entomol. Res. 103:65664
148. Silva RV, Oliveira RDL, Nascimento KJT, Rodrigues FA. 2010. Biochemical responses of coffee resis-
tance against Meloidogyne exigua mediated by silicon. Plant Pathol. 59:58693
149. Song A, Xue G, Cui P, Fan F, Liu H, et al. 2016. The role of silicon in enhancing resistance to bacterial
blight of hydroponic- and soil-cultured rice. Sci. Rep. 6:24640
150. Sousa RS, Rodrigues FA, Schurt DA, Souza NFA, Cruz MFA. 2013. Cytological aspects of the infection
process of Pyricularia oryzae on leaves of wheat plants supplied with silicon. Trop. Plant Pathol. 38:47277
151. Stanley JN, Baqir HA, McLaren TI. 2014. Effect on larval growth of adding finely ground silicon-bearing
minerals (wollastonite or olivine) to artificial diets for Helicoverpa spp. (Lepidoptera: Noctuidae). Austral.
Entomol. 53:43643
152. Sun W, Zhang J, Fan Q, Xue G, Li Z, et al. 2010. Silicon-enhanced resistance to rice blast is attributed
to silicon mediated defence resistance and its role as physical barrier. Eur. J. Plant Pathol. 128:3949

4.22 Debona Rodrigues Datnoff

Changes may still occur before final publication online and in print
PY55CH04-Datnoff ARI 8 May 2017 16:51

153. Suzuki H. 1940. On the relationship between rice susceptibility and penetration into host plants. Ngyo
Oyobi Engei 10:19992010
154. Takahashi E, Ma JF, Miyake Y. 1990. The possibility of silicon as an essential element for higher plants.
Comm. Agric. Food Chem. 2:99122
155. Tatagiba SD, DaMatta FM, Rodrigues FA. 2016. Silicon partially preserves the photosynthetic perfor-
mance of rice plants infected by Monographella albescens. Ann. Appl. Biol. 168:11121
156. Tatagiba SD, Rodrigues FA, Filippi MCC, Silva GB, Silva LC. 2014. Physiological responses of rice
plants supplied with silicon to Monographella albescens infection. J. Phytopathol. 162:596606
157. Tripathi DK, Singh S, Singh VP, Prasad SM, Chauhan DK, Dubey NK. 2016. Silicon nanoparticles
more efficiently alleviate arsenate toxicity than silicon in maize cultivar and hybrid differing in arsenate
tolerance. Front. Environ. Sci. 4:46
158. Tripathi DK, Singh S, Singh VP, Prasad SM, Dubey NK, Chauhan DK. 2017. Silicon nanoparticles
more effectively alleviated UV-B stress than silicon in wheat (Triticum aestivum) seedlings. Plant Physiol.
Biochem. 110:7081
159. Tubana BS, Babu T, Datnoff LE. 2016. A review of silicon in soils and plants and its role in us agriculture:
Access provided by University of Sherbrooke on 05/15/17. For personal use only.
Annu. Rev. Phytopathol. 2017.55. Downloaded from www.annualreviews.org

history and future perspectives. Soil Sci. 181:393411


160. Tubana BS, Heckman JR. 2015. Silicon in soils and plants. See Ref. 133, pp. 751
161. Van Bockhaven J, Spchal L, Novak O, Strnad M, Asano T, et al. 2015. Silicon induces resistance to the
brown spot fungus Cochliobolus miyabeanus by preventing the pathogen from hijacking the rice ethylene
pathway. New Phytol. 206:76173
162. Van Bockhaven J, Steppe K, Bauweraerts I, Kikuchi S, Asano T, et al. 2015. Primary metabolism plays
a central role in moulding silicon-inducible brown spot resistance in rice. Mol. Plant Pathol. 16:81124
163. Wang S, Liu P, Chen D, Yin L, Li H, et al. 2015. Silicon enhanced salt tolerance by improving the root
water uptake and decreasing the ion toxicity in cucumber. Front. Plant Sci. 6:759
164. Whan JA, Dann EK, Aitken EAB. 2016. Effects of silicon treatment and inoculation with Fusarium
oxysporum f. sp. vasinfectum on cellular defences in root tissues of two cotton cultivars. Ann. Bot. 118:219
26
165. Williams ED, Vlamis J. 1957. The effect of silicon on yield and manganese-54 uptake and distribution
in the leaves of barley plants grown in culture solutions. Plant Physiol. 32:4049
166. Xu CX, Ma YP, Liu YL. 2015. Effects of silicon (Si) on growth, quality and ionic homeostasis of aloe
under salt stress. S. Afr. J. Bot. 98:2636
167. Ye M, Songa Y, Longa J, Wanga R, Baersonc SR, et al. 2013. Priming of jasmonate-mediated antiher-
bivore defense responses in rice by silicon. PNAS 110:363139
168. Yin L, Wang S, Liu P, Wang W, Cao D, et al. 2014. Silicon-mediated changes in polyamine and
1-aminocyclopropane-1-carboxylic acid are involved in silicon-induced drought resistance in Sorghum
bicolor L. Plant Physiol. Biochem. 80:26877
169. Yin L, Wang S, Tanaka K, Fujihara S, Itai A, et al. 2016. Silicon-mediated changes in polyamines
participate in silicon-induced salt tolerance in Sorghum bicolor L. Plant Cell Environ. 39:24558
170. Yoshida S, Ohnishi Y, Kitagishi K. 1962. Chemical forms, mobility, and deposition of silicon in the rice
plant. Soil Sci. Plant Nutr. 8:10711
171. Zeyen RJ, Ahlstrand GG, Carver TLW. 1993. X-ray microanalysis of frozen-hydrated, freeze-dried,
and critical point dried leaf specimens: determination of soluble and insoluble chemical elements at
Erysiphe graminis epidermal cell papilla sites in barley isolines containing Ml-o and ml-o alleles. Can. J.
Bot. 71:28496
172. Zhang G, Cui Y, Ding X, Dai Q. 2013. Stimulation of phenolic metabolism by silicon contributes to
rice resistance to sheath blight. J. Plant Nutr. Soil Sci. 176:11824

www.annualreviews.org Silicons Role in Abiotic and Biotic Plant Stresses 4.23

Changes may still occur before final publication online and in print