Role of Silicon on Enhancing Disease Resistance in Tropical Fruits and Vegetables : A Review

Silicon (Si) has proven to enhance disease resistance in a wide range of tropical fruits and vegetables. It has been used in controlling various diseases: mildews, rots, moulds, wilt, blight, anthracnose and leaf spots. However, the highest number of records was available on reducing diseases of powdery mildews on fruits and vegetables belonging to the family Cucurbitaceae. Siliconmediated defense responses in plant pathosystems are mainly attributed to the physical resistance, which involves reduced penetrability and/or increased hardness and abrasiveness of plant tissues because of silica deposition. The main mechanism is the chemical resistance, which involves chemical defenses to pathogen attack through the enhanced production of defensive enzymes and the production of antifungal compounds such as phenolic metabolism products, phytoalexins and pathogenesis related proteins. Silicon has been applied as soluble silicates to the substrate or to soilless media at pre-harvest level on reducing disease susceptibility. Post-harvest dips of fresh produce in silicate solutions and use of Si combined with a biocontrol agent are other aspects of silicon application in controlling diseases in fruits and vegetables.


Introduction
Silicon (Si) is taken up by plants at concentrations similar to the *Correspondence should be addressed to Dr. Darshani Weerahewa Department of Botany, The Open University Sri Lanka, Nawala, Sri Lanka (Email: hlwee@ou.ac.lk) essential nutrients.However, persistent chemical fertilization and crop removal from the field tend to the depletion of Si availability for plants.As a result, Si has been identified as a limiting factor for Siaccumulating plants, as well as for the plants grown in soils deficient with Si (Epstein, 1999).The beneficial effects of Si have been observed in a wide variety of plant species including enhanced insect and disease resistance, reduced mineral toxicity, increased photosynthetic activity, superior nutrient imbalance, and enhanced drought and frost tolerance (Ma, 2004).Though silicon has not been recognized as an essential element for plant growth, plants deprived of Si are often weaker structurally and more prone to abnormalities of growth, development and reproduction.Silicon is considered as the only nutrient element which is not detrimental when collected in excess in plants (Ma and Takahashi, 2002).
Silicon is absorbed to plants from the soil solution with concentrations ranging from 0.1 to 0.6 mM as monosilicic acid, H4SiO4 (Ma and Takahashi, 2002).The Si concentrations vary widely in above ground plant parts, ranging from 0.1 to 10.0% on dry weight basis (Liang et al., 2005).Plant species are considered as Si 'Accumulators' when the concentration of Si of its dry weight is greater than 1%.'Intermediates' have Si amounts less than 0.1% in their biomass.Plants containing Si concentration below 0.5% of the bio mass are considered as 'Excluders' (Ma and Takahashi, 2002).
Silicon has been found to effectively control many of the diseases found in tropical fruits.However, diseases, such as blue mould and gray mould were reduced in fruits grown in temperate countries.
Silicon has been applied as a form of pre-harvest or post-harvest application, or root or foliar application.The research has also been done on silicon application in combination with yeast or phosphorus acid or hot water treatment.Different sources of silicon i.e. sodium silicate, calcium silicate, calcium silicate, rice hull (raw or partially burnt) have been used as sources for providing Si to the fruits and vegetables.
The following sections describe the disease control by application of silicon in tropical fruits and vegetables.Some records were available on reducing anthracnose disease in tomato and capsicum grown in Sri Lanka.

Powdery mildew
A noticeable inhibitory effect against powdery mildew has been reported by silicon application in cucurbits.A majority of the alleviative effects studies has been accounted in cucumber powdery mildew caused by Sphaerotheca fuliginea (Samuels et al., 1993;Menzies et al., 1991;1992;Fawe et al., 1998;JungSup et al., 2000;Schuerger and Hammer, 2003;Wei et al., 2004;Liang et al., 2005;QiuJu et al., 2009;Buttaro et al., 2009;Wolff et al., 2012) and by Sphaerotheca fuliginea (Liang et al., 2005).Effective suppression of the disease could be observed in some other cucurbits such as melons caused by S. fuliginea and/or Erysiphe cucurbitacearum (Menzies et al., 1992;Yurong et al., 2005;Guo et al., 2005;Chen et al., 2010).Root applied Si induced the resistance against Podosphaera xanthii reducing the disease severity in melon.Supplying silicon in nutrient solutions reduced the severity and incidence of powdery mildew in two varieties of melon, carosello and barattiere (Buttaro et al., 2009).Furthermore, powdery mildew in zucchini squash caused by E. cichoracearum and Podosphaera xanthii pumpkin caused by P. xanthii (Heckman et al., 2003) was lessened by pre-harvest silicon application.Palmer et al. (2006) reported that powdery mildew caused by Sphaerotheca aphanis in strawberry can effectively be suppressed by foliar application of potassium silicate.Silicon had beneficial effects on strawberry plants and may serve as an alternative to fungicides for controlling powdery mildew when supplied as a foliar spray of potassium and sodium silicate.Kanto et al. (2004Kanto et al. ( , 2007) ) and Wang and Galletta (1996) have recorded similar results about the strawberry-powdery mildew patho-system.However, root application of silicon could not reduce the disease severity in strawberry (Bowen et al., 1992).Similar suppressive effects of Si against Uncinula necator were stated by Reynolds et al. (1996) and Blaich and Grundhofer (1998) in grapes.Foliar applied potassium silicate was found to exhibit inhibitory effects on Leveillula taurica, the powdery mildew causing fungi in tomato (Yanar et al., 2013).

Downy mildew
Foliar application of Si suppressed cucumber downy mildew caused by Pseudoperonospora cubensis (Yu and Du, 2009;Yu et al., 2010).Garibaldi et al. (2012) discovered that electrical conductivity and potassium silicate together significantly influenced downy mildew (Bremia lactucae) incidence and severity on lettuce in hydroponic system.The best results, in terms of disease control, were given by the addition of potassium silicate to the 0.95 g l −1 NaCl solution.

Alternaria fruit rot
The synergistic effects of biocontrol yeasts Cryptococcus laurentii and Rhodotorula glutinis combined with silicon against Alternaria fruit rot (Alternaria alternate) have been investigated in jujube fruit (Chinese date: Zizyphus jujuba).Combinations of C. laurentii and R. glutinis with Si were found to be most effective in controlling the diseases caused by A. alternata in jujube fruit (Shiping et al., 2005).Post harvest sodium silicate treatments could resist the growth of A. alternate in pingguoli pear (Guo et al., 2003).

Other fruit rots
The susceptibility to pink rot caused by Trichothecium roseum was shown to be decreased by postharvest Si application in muskmelon (Li et al., 2012), Chinese cantaloupe (Yurong et al., 2003;Guo et al., 2007) and hami melon (Bi et al., 2006).Yang et al. (2010) have revealed synergistic effects of silicon on disease control in apple brown rot (Monilinia fructicola).Foliar application of Si was effective in controlling tomato fruit rot caused by Phytophthora capsici (Mersha et al., 2012)

Pythium root rot
It was stated that Si is effective in controlling root rot in cucumber caused by Pythium ultimum and P. aphanidermatum (Cherif and Belanger, 1992;Chérif et al., 1994aChérif et al., , 1994b)).However, Heine et al. (2007) revealed that the incidence of root rot in cucumber, tomato and bitter gourd caused by P. aphanidermatum could not be controlled by Silicon application.

Phytophthora root rot
Silicon was effective in controlling cucumber root rot caused by Phytophthora melonis (Mohaghegh et al., 2011).In hydroponic experiments, Khoshgoftarmanesh et al. (2012) have demonstrated that Phytophthora root rot (P.drechsleri) in cucumber could be alleviated by Si application.Bekker et al. (2007) found the efficacy of root application of potassium silicate on controlling the disease (P.cinnamomi) in avocado.

Fusarium root rot
Due to the application of Si to tomato seedlings, the disease severity of root rot caused by Fusarium oxysporum f.sp.radicis-lycopersici was reduced.This inhibitory effect was due to the delaying in onset and initial infection of roots and the movement of the pathogen from roots to stems (Huang et al., 2011).Silicon was also reported to be effective to suppress the disease resulted by F. solani in tomato (El-Samman et al., 2000).Fusarium oxysporum f.sp.radiciscucumerinum, the causative fungi of cucumber root rot, could be effectively controlled by soil applied Si (Safari et al., 2012).The alleviative role of Si on the disease was also recorded in other cucurbits in fact hamimelon: F. semitectum, cantaloupe: Fusarium spp.and rock melon: F. oxysporum f.Sp.Melonis (Bi et al., 2006;Liu et al., 2009;Kumar and McConchie, 2010)

Banana root rot
Using the image analysis program WinRHIZO, Vermeire et al. (2011) exhibited that root-rot fungi Cylindrocladium spathiphylli infection in banana could be mitigated.The Si amendment also alleviated growth reduction caused by the pathogen.

Silicon and mould diseases
Blue mould Ebrahimi et al. (2012) explained that postharvest silicon application was more effective in reducing the lesion diameter of blue mould decay of apples caused by Penicillium expansum in combination with the yeast, Torulaspora delbrueckii than using Si or T. delbrueckii alone.In a consequent study, Ebrahimi et al. (2013) discovered the efficacy of controlling the disease triggered by applying Si together with the yeast, Metschnikowia pulcherrima.Farahani et al. (2012) suggested that the yeast, Candida membranifaciens combined with different concentrations of silicon, improved the effectiveness of yeast in controlling the disease in apple.Similar results have been observed by Farahani et al. (2013) by dual application of silicon and the yeast, Pichiaguillier mondii in apples.Postharvest dips of apples in potassium silicate solution (Moscoso-Ramírez and Palou, 2014) and in Si added hot water (Etebarian et al., 2013) were other means of suppressing the disease.Combinations of the yeast species, Cryptococcus laurentii and Rhodotorula glutinis along with Si was more successful in controlling blue mould caused by P. expansum on jujube fruit (Shiping et al., 2005).

Green mould
Silicon has been reported to prevent the incidence of green mould caused by Penicillium digitatum in a number of citrus fruits (Abraham, 2010;Liu et al., 2010).Mkhize et al. (2013) revealed that pre-and post-harvest Si amendments could upsurge the resistance of lemon to P. digitatum.Postharvest dips of potassium silicate before inoculation the same pathogen on oranges significantly reduced the severity of green mould (Moscoso-Ramírez and Palou, 2014).

White mould
In bean, disease incidence and severity of white mould (Sclerotinia sclerotiorum) were significantly reduced by 52% and 73%, respectively, via applying Si as calcium silicate together with calcium chloride (PaulaJúnior et al., 2009).

Gray mould
On increasing the quality of organically grown strawberry, Prokkola and Kivijärvi (2008) found that silicon is effective in controlling gray mould (Botrytis cinerea), when applied as a combination with Trichoderma spp. in two weeks interval until harvested.Soil application of liquid potassium silicate to cucumber plants notably reduced the incidence of gray mould caused by B. cinerea (O'Neil, 1991).In contrast, post-harvest Si application was found to be ineffective for controlling gray mould (B.cinerea) in strawberry (Lopes et al., 2014).

Bacterial wilt
Soil supplied silicon enhanced the resistance in tomato plants against Ralstonia solanacearum, the causing agent of bacterial wilt (Ghareeb et al., 2011).Silicon amendments were also reported to reduce the disease incidence in tomato when applied to soil (Dannon and Wydra, 2004;Diogo and Wydra, 2007;Kiirika et al., 2013).However, dual application of silicon and a rhizobacteria strain Bacillus pumilis against the disease was not effective as same as application of silicon alone in tomato (Kurabachew and Wydra, 2014).
Recently, it was revealed that Si mediated resistance in tomato against R. solanacearum was associated with the changes of soil microorganism amount and soil enzyme activity (Wang et al., 2013).The uptake of Si was significantly increased in the Si-treated tomato plants, where the Si content was higher in the roots than that in the shoots.The results showed that exogenous 2.0 mM Si treatment reduced the disease index of bacterial wilt by 19.18 % to 52.7 %.Si supply significantly increased soil urease and soil acid phosphatase activity under pathogen-inoculated conditions.After R. solanacearum inoculation, Si amendments significantly increased the amount of soil bacteria and actinomycetes and reduced soil fungi/soil bacteria ratio.The results suggested that Si amendment is an effective approach to control R. solanacearum, and Simediated resistance in tomato against R. solanacearum is associated with the changes of soil microorganism amount and soil enzyme activity (Wang et al., 2013).Silicon amendment significantly reduced bacterial wilt incidence of tomato grown in peat substrate (Diogo and Wydra, 2007) and hydroponic culture (Dannon and Wydra, 2004).et al. (2012) revealed that supplying Si to banana plants at seedling stage had a great potential in reducing the intensity of Fusarium wilt caused by Fusarium oxysporum.The suppressive effect of Si on the disease in cucumber caused by Fusarium oxysporumf.sp.radicis-cucumerinum was also reported by Safari et al. (2012).

Phytophthora blight
In cucumber, root applied liquid potassium silicate notably reduced the incidence of stem blight caused by Didymella bryoniae (O'Neil, 1991).Silicon accumulation in roots followed by Si supply could potentially reduce the severity of Phytophthora blight caused by Phytophthora capsici while enhancing the plant development in bell pepper (French-Monar et al., 2010) as well as in pepper (Lee et al., 2004).Foliar application of soluble silicon could efficiently control the disease in tomato caused P. capsici (Mersha et al., 2012).In addition, silicon nutrition enhanced the resistance to stem blight caused by Phomopsis asparagi in two asparagus cultivars, UC157 and Gynlim (Lu et al., 2008).

Stem blight
Application of liquid potassium silicate through a separate set of drip lines to cucumbers grown on rockwool slabs significantly reduced the incidence of stem blight caused by Didymella bryoniae, and appeared to reduce that of those caused by B. cinerea (O'Neil, 1991).Yang et al. (2008) have revealed that it could control the occurrence of anthracnose (Colletotrichum higginsianum) of flowering Chinese cabbage (Brassica campestris L.) on Si application.Injecting soluble silicon into trees prior to harvest significantly decreased the severity and incidence of postharvest anthracnose in avocado while, a combination of soluble silicon and phosphorous acid was not that effective in controlling of anthracnose (Anderson et al., 2005).The disease in avocado could similarly be controlled effectively by postharvest application of soluble silicon (Bosse et al., 2011).The susceptibly to the disease (C.gloesporioides) in tomato was mitigated by soil application of sodium silicate (David and Weerahewa, 2012;Weerahewa and David 2015), and application of partially burnt rice hull (Somapala et al., 2015).Root and shoot applied Si was proven to be an effective way of reducing the disease severity caused by C. gloesporioides in Capsicum annuum L. 'Muria F1' (Jayawardana et al., 2014(Jayawardana et al., , 2015)).The significant reduction of anthracnose disease was observed in capsicum grown in simplified hydroponics system incorporated with raw rice hull as a supplement of silicon (Jayawardana et al., 2016).Moreover, Si induced the resistance against Fitopatologia Brasileira and C. lindemuthianum in bean (Moraes et al., 2006;Polanco et al., 2012Polanco et al., , 2014)).

Silicon and Leaf spot
Foliar application of potassium silicate, as a source of soluble silicon, decreased angular leaf spot (Pseudocercospora griseola) severity on beans at more alkaline pH (Rodrigues et al., 2010).

Banana sigatoka
The effect of silicon uptake on the susceptibility of banana to Mycosphaerella fijiensis, the causative pathogen of black sigatoka disease was investigated by Kablan et al. (2012).It was revealed that Si supply could alleviate the disease in the plants grown both in hydroponic culture system and in pots filled with compost.

Underlying mechanism/s of disease resistance mediated by silicon
There are mainly two methods by which Si induces the resistance in plants against infections.It is either by the chemical defense owing to the physical defense developed due to Si deposition on plant tissues preventing the pathogen penetration and/or by synthesis of anti-pathogenic compounds.In addition, systemic acquired resistance (SAR) was found to be induced upon silicon application in fruits and vegetables.

Mechanical Resistance
Silicon has been shown to be effective in mitigating biotic stress by means of mechanical resistance in fruits and vegetables in a number of studies.Pre-harvest or post-harvest silicon application had shown a great potential in controlling diseases by inhibiting or delaying the growth and development of the mycelium of the pathogen (Samuels et al., 1993;Bowen et al., 1992;Hu et al., 2008;Yu and Du, 2009;Abraham, 2010) due to silicon deposition at infection sites and hyphae (Reynolds et al., 1996) Si application strongly inhibited spore germination, germ tube formation and development of appresoria and possibly the penetration of fungi were hindered.It was hypothesized that Si inhibits fungal disease by physically inhibiting fungal penetration peg dispersion of the epidermis (Menzies et al., 1991a(Menzies et al., , 1991b;;Bowen et al., 1992;Yurong et al. 2005;Kanto et al., 2007;Liu et al., 2010).Si was translocated laterally through the leaf and surrounded the appressoria of U. necator upon foliar application of Si.Plant leaves that were fed with Si via roots showed a similar deposition of Si surrounding the appressoria making a rigid physical barrier for penetration (Bowen et al., 1992).
It has also been found that the trichome bases on the epidermis tend to become silicified (Belanger et al., 1995;Samuels et al., 1993;Chérif et al., 1994a) changing their morphology against infections.Si deposition in leaf hairs suppressed the fungal penetration as a result of increased density and length (Fatema et al., 2011).Penetration peg incursion was found to be constrained by rapid Si deposition at the external openings like stomata of the leaves (Guo et al, 2007).A fast silicification at intercellular spaces, cuticle layer (Kanto et al., 2007) and along the space between the exocarp and mesocarp (Guo et al., 2007) made it more difficult for pathogen penetration and dispersion.Powdery mildew infected leaf cells of silicate treated plants were exhibited to have extensive silica polymerization enhancing the thickness against the fungi in the halo region surrounding the site of fungal penetration (Menzies et al., 1991b).Altered surface morphology of the host cell walls was observed adjacent to the germinating hyphae (Samuels et al., 1993).Deposition of silicon in host cell walls, papillae, around the haustorial neck and in-between the host cell wall and plasma membrane enhanced induced structural defense reactions (Samuels et al., 1994) against S. fuliginea.
Changes in the pectic polysaccharide structure, is another aspect of silicon-induced mechanical defense.In particular, arabinan side chains of rhamnogalacturonan I increased in some vessel walls and galactan side chains of rhamnogalacturonan I increased in the xylem parenchyma, increasing the mechanical strength of the host against infection (Diogo and Wydra, 2007).Si application increased the cell wall lignin content which made it hard for dispersion of fungal mycelium (Polanco et al., 2012).Silicon-treated plants increased resistance against infections by forming electron-dense layers along primary and secondary cell walls as well as over pit membranes of xylem vessels (Chérif et al., 1994b) making it harder for fungal permeation and dispersion within the plant body.

Biochemical resistance
Silicon-mediated defense reaction is induced in fruits and vegetables by synthesis of secondary metabolites.Secondary metabolites influence the interactions between plants and the organisms that inhabit their environment: insects and other animals, microbes and fungi.They are obnoxious, repellent or downright toxic to biotic attackers of plants (Delhaize et al., 1993).Antioxidant enzymes, phenolic compounds, chitinases and phytoalexins are the common secondary metabolites found related to chemical defense in fruits and vegetables.

Acquired resistance through antioxidant enzymes
Several studies showed that lowering disease severity in the Sitreated plants was in line with higher activity of antioxidant defense enzymes in particular, superoxide dismutase, catalase, peroxidase, ascobate peroxidase, guaiacol peroxidase, β-1, 3-glucanase and glutathione reductase.Plants protect cell and sub cellar systems from the cytotoxic effects of the active oxygen radicals using antioxidant enzymes.Silicon was said to be effective in controlling pre harvest diseases of fruits and vegetables as a result of these antimicrobial enzymes (Wei et al., 2004;Cherif et al., 1994b;Liang et al., 2005).A significant reduction in postharvest diseases by silicon application was noted with respect to enhanced defensive enzyme activity (Qin and Tian, 2005;Bi et al., 2006;Guo et al, 2007;Liu et al., 2009Liu et al., , 2010;;Kumar and McConchie, 2010;Li et al., 2012;Ebrahimi et al., 2012;Polanco et al., 2012;Farahani et al., 2013;Polanco et al., 2014;Kurabachew and Wydra, 2014).Rootapplied Si significantly enhanced the activities of defensive enzymes, for example catalase, peroxidase, polyphenoloxidase and β-1, 3glucanase in two asparagus cultivars, UC157 and Gynlim against stem blight caused by Phomopsis asparagi (Lu et al., 2008).

Synthesis
Silicon could be used to reduce many fungal diseases mildew (Powdery mildew and downy mildew), rots (fusarium root rot, phytophthora root rot, pink rot), mould (Blue mould, green mould, gray mould, white mould), blight (phytophthora blight and stem blight), and wilt (fusarium wilt, and anthracnose) in tropical fruits and vegetables.A few bacterial diseases (bacterial wilt) were also reduced by application of silicon.Many diseases observed in tropical fruits and vegetable were significantly reduced by silicon application.However, gray mould in strawberry and blue mould diseases in some fruits grown in temperate countries (sweet cherry, peach, Jujube, apple, pear, oranges etc) were reduced by application of Silicon.
When considering the types of diseases and resistance enhanced by application of silicon in tropical fruits and vegetables, many records (75% of the published records) were available on reducing the powdery mildew disease in cucumber, muskmelon, Zucchini squash, pumpkin and about 25% of the published findings were available on reducing powdery mildew in disease in strawberry and grapes.
Silicon has been applied as a form of pre or post-harvest to reduce diseases in green mould or gray mould.But the postharvest application was done for reducing blue mould disease.
Foliar application of silicon has been used most effectively to reduce powdery mildew disease.However, blight disease was controlled by application of foliar or root.
The possible mechanism/s on diseases reduced by silicon could possibly be due to the formation of physical barriers by silicon depositions or by biochemical compounds formed or antioxidant defense enzymes formed.
Pre-harvest or post-harvest silicon application had shown a great potential in controlling diseases by inhibiting or delaying the growth and development of the mycelium of the pathogen.Powdery mildew infected leaf cells of silicate treated plants were exhibited to have extensive silica polymerization enhancing the thickness against the fungi in the halo region surrounding the site of fungal penetration

Conclusions
Silicon has proven to be an effective means of reducing diseases in tropical fruits and vegetables.Therefore, the use of silicon could reduce the use of fungicides for controlling diseases.
The remarked alleviative effect of Si was recorded in controlling powdery mildew in cucurbits.Silicon might be effective in suppressing diseases in fruits and vegetables than bacterial diseases since preponderance of the findings were related to Si mediated fungal diseases than bacterial diseases.Silicon-induced resistance against infections is mainly attributed to the mechanical and chemical defense.In addition, SAR like mechanisms were involved in silicon induced defense in fruits and vegetables.