Probing the mechanisms of silicon-mediated pathogen resistance

Abstract

Silicon is the second most abundant mineral element in soil, it has important role in alleviating various environmental stresses and enhancing plant resistance against pathogen, but the exact mechanism by which Si mediates pathogen resistance remains unclear. One of the resistance mechanisms is related to silicon deposition in leaf that acts as a physical barrier to hinder pathogen penetration. But more evidence show that silicon can induce defense responses that are functionally similar to systemic acquired resistance, Si-treated plants can significantly increase antioxidant enzyme activities and the production of antifungal compounds such as phenolic metabolism product, phytoalexins and pathogenesis-related proteins etc. Molecular and biochemical detections show that Si can activate the expression of defense-related genes and may play important role in the transduction of plant stress signal such as salicylic acid, jasmonic acid and ethylene.

Introduction

Although silicon (Si) has not been considered as an essential element for plant nutrition, the beneficial effects of this element on growth and development of many plant species have been demonstrated. Furthermore, the beneficial role of silicon in enhancing plant resistance to various biotic and abiotic stresses is particularly evident. Numerous evidence showed that Si could control plant disease caused by fungi and bacteria, such as blast and sheath blight in rice,^1–4 powdery mildew in wheat, barley, cucumber and Arabiopsis,^5–7 ring spot in sugarcane,⁸ rust in cowpea (Vigna unguiculata)⁵ etc. And the enhanced resistance is associated with the higher deposit of silicon in leaf so as to form physical barrier to impede pathogen penetration^2,9,10 and the activation of host defense response.^11–13 But the exact nature of protective effects by silicon in plants, are uncertain and presently the subject of debate. The objective of this review is to discuss the possible mechanisms for Si-enhanced resistance to disease, and the recommended further studies are also proposed.

Physical Barrier Mechanism

Since Si was found to control plant disease, physical barrier was traditionally used to explain its role in enhancing pathogen resistance. Si can accumulate and deposit beneath the cuticle to form a cuticle-Si double layer and thereby interfere with pathogen's penetration through mechanical barrier.^9,10 A blast-resistant rice cultivar has more silicified cells than a susceptible cultivar.¹⁴ Si manifested its effect to establish blockage to ingress by fungus.¹⁵ Kim et al.,² reported that silicified epidermal cell walls were closely associated with the reduced blast severity in susceptible and partially resistant cultivars. The prevalence of papillae in Si treatment could increase pathogen resistance against B. graminis f.sp. tritici.¹⁶ Cytological evidence showed that Si-induced resistance to M. grisea in rice was correlated with a specific leaf cell reaction that interferes with the development of M. grisea.³ Liang et al.,¹⁷ reported that foliar applied Si only produced physical barrier and osmotic effect, but root applied Si leaded to systemic acquired resistance when Cucumis sativus. plants were infected by powdery mildew pathogen. Studies by Zhang et al.,⁴ demonstrated that Si-treated rice plants infected by sheath blight pathogen Rhizoctonia solani had much more silica cells and papillae. Based on light microscopic observation of the adaxial surface of rice leaves amended with or without Si, Hayasaka et al.,¹⁸ further confirmed that Si in the leaf epidermis may confer resistance against appressorial penetration. Our previous study showed that Si treatment and M. grisea inoculation resulted in higher Si deposit in rice leaves from the zones where fungus grew for both susceptible and resistant near-isogenic lines, and the size of silica cells was larger than that in no Si-treated plants.¹⁹

Biochemical Mechanism

Although early and recent studies partly support the hypothesis of cell silicifiation, silicon deposit and papilla formation to explain enhanced resistance of plants against pathogen, this mechanism has been always strongly doubted. It was demonstrated that insoluble Si could accumulate and polymerize at fungal penetration sites or in epidermal cell walls, but not associated with the increased resistance.^20,21 Prophylactic effect against powdery mildew was lost when Si feeding to cucumber plants was interrupted.⁹ Heine et al.,²² reported that the accumulation of Si in root cell walls did not represent a physical barrier to the spread of Pythium aphanidermatum in roots of bitter gourd and tomato.

When infected with necrotizing pathogens, many plants develop an enhanced resistance to against further pathogen attack, which is referred to as systemic acquired resistance (SAR).²³ Silicon could induce defense responses similar to SAR. Several studies showed that lower disease severity in the Si-treated plants was in line with higher activity of protective enzymes (POD, PPO and PAL) in leaves of rice,¹⁹ wheat²⁴ and cucumber.^17,25 And these enzymes had important role in regulating the production of accumulation of antifungal compounds such as phenolic metabolism product (lignin), phytoalexins and pathogenesis-related proteins in plants. Si application can induce the production the antifungal compounds after the penetration of pathogens enter the epidermal cell.^11,12,25,26 It was demonstrated that Si treatment resulted in the increase of flavonoid phytoalexin in cucumber plants infected by powdery mildew (Podosphaera xanthii).¹¹s Another studies reported that Si-induced resistance to blast (M. grisea) in rice was related to the production of phytoalexin(s), which were mainly momilactones A and B.^12,13 Si can increase the production lignin-carbohydrate complexes in the cell wall of rice epidermal cells.²⁷ Our studies showed that Si-treated infected plants significantly increased lignin content of susceptible rice line compared with no Si-treated plants.¹⁹

Ample evidence showed that Si alone has apparently no effect on the metabolism of plants growing in a controlled unstressed environment, but it will alleviate the stress (including abiotic and biotic stress) and modulates the stress response in plants, and this role is active.^7,19,21,24

Molecular Mechanism

However, silicon mediated pathogen resistance is a complex phenomena that is worthy of more detailed analysis at the molecular and biochemical level.¹³ It was reported that gene expression had no significant difference between Si-treated and non-treated plants in the absence of stress.²⁸ A study by Kauss et al.,²⁹ showed that during the induction of systemic acquired resistance (SAR) mediated by silicon in cucumber, the express of a gene encoding a novel proline-rich protein was enhanced, this protein was associated to cell wall reinforcement at the site of the attempted penetration of fungi into epidermal cells. By using molecular biology techniques such as subtractive cDNA libraries or microarrays, Fauteux et al.,⁷ assessed the defense-related genes expressed in control or infected Arabidopsis plants, their microarray results show that Si-treated plants react to pathogen inoculation through the upregulation of defense- and pathogenesis-related genes, which confirms that silicon plays an active role in enhancing host resistance to pathogen infection.

Where Now?

Although numerous studies on the physiological and biochemical levels have elucidated the possible mechanisms of silicon-mediated pathogen resistance, the detailed mechanism by which Si mediates plant signaling transduction is needed for further exploration. When attacked by pathogen, the infected plant will synthesize antimicrobial compounds together with systemic stress signals such as salicylic acid, jasmonic acid and ethylene. Can silicon modulate the systemic signaling process? What is the interaction between Si and the signal substances? Silicon application can significantly enhance the activity of protective enzymes (POD, PPO and PAL), how silicon regulate gene expression as related to these protective enzymes? What are other new antifungal compounds that silicon may activate? We also need more knowledge on how silicon acid be transported in higher plants. Recently great progress has been made on the cloning and characterization of gene related to Si-transportation in rice.^30–32 This work provides a good basis for further study. The in-depth understanding of silicon in plants will be helpful to effectively use silicon to increase crop yield and enhance pathogen resistance.

Abbreviations

Si

silicon

POD

peroxidase

PPO

polyphenol oxidase

PAL

phenylalanine ammonia-lyase

SAR

system acquired resistance