Silicon supplementation improves early blight resistance in Lycopersicon esculentum Mill. by modulating the expression of defense-related genes and antioxidant enzymes

Gulzar, Naveed; Ali, Sajad; Shah, Manzoor A.; Kamili, Azra N.

doi:10.1007/s13205-021-02789-6

Original Article
Published: 22 April 2021

Silicon supplementation improves early blight resistance in Lycopersicon esculentum Mill. by modulating the expression of defense-related genes and antioxidant enzymes

Naveed Gulzar¹,
Sajad Ali¹,
Manzoor A. Shah² &
Azra N. Kamili ORCID: orcid.org/0000-0001-9919-3129¹

3 Biotech volume 11, Article number: 232 (2021) Cite this article

541 Accesses
2 Citations
1 Altmetric
Metrics details

Abstract

Early blight is the most devastating disease in tomato which causes huge yield losses across the globe. Hence, development of specific, efficient and ecofriendly tools are required to increase the disease resistance in tomato plants. Here, we systematically investigate the defensive role and priming effect of silicon (Si) in tomato plants under control and infected conditions. Based on the results, Si-treated tomato plants showed improved resistance to Alternaria solani as there was delay in symptoms and reduced disease severity than non-Si-treated plants. To further examine the Si-mediated molecular priming in tomato plants, expression profiling of defense-related genes like PR1, PR2, WRKYII, PR3, LOXD and JERF3 was studied in control, Si-supplemented, A. solani-inoculated and Si + A. solani-inoculated plants. Interestingly, Si significantly increased the expression of jasmonic acid (JA) marker genes (PR3, LOXD and JERF3) than salicylic acid (SA) marker genes (PR1, PR2 and WRKYII). However, Si + A. solani-inoculated plants showed higher expression levels of defence genes except WRKYII than A. solani-inoculated or Si-treated plants. Furthermore, pre-supplementation of Si to A. solani-infected tomato plants showed increased activity of antioxidant enzymes viz. superoxide dismutase (SOD), catalase (CAT), ascorbate peroxidase (APX), glutathione reductase (GR) and peroxidase (POD) than control, Si-treated and A. solani-inoculated plants. Altogether, present study highlights the defensive role of Si in tomato plants in response to A. solani by increasing not only the transcript levels of defense signature genes, but also the activity of antioxidant enzymes.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

References

Adhikari P, Oh Y, Panthee DR (2017) Current status of early blight resistance in tomato: an update. Int J Mol Sci 18:2019. https://doi.org/10.3390/ijms18102019
CAS Article PubMed Central Google Scholar
Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126. https://doi.org/10.1016/S0076-6879(84)05016-3
CAS Article PubMed Google Scholar
Al-aghabary K, Zhu Z, Shi Q (2005) Influence of silicon supply on chlorophyll content, chlorophyll fluorescence, and antioxidative enzyme activities in tomato plants under salt stress. J Plant Nutr 27:2101–2115. https://doi.org/10.1081/pln-200034641
Article Google Scholar
Al-Huqail AA, Alqarawi AA, Hashem A, Ahmad Malik J (2019) Silicon supplementation modulates antioxidant system and osmolyte accumulation to balance salt stress in Acacia gerrardii Benth. Saudi J Biol Sci 26:1856–1864. https://doi.org/10.1016/j.sjbs.2017.11.049
CAS Article PubMed Google Scholar
Alenazi MM, Shafiq M, Alsadon AA, Alhelal IM, Alhamdan AM, Solieman THI, Ibrahim AA, Shady MR, Al-Selwey WA (2020) Improved functional and nutritional properties of tomato fruit during cold storage. Saudi J Biol Sci 27:1467–1474. https://doi.org/10.1016/j.sjbs.2020.03.026
CAS Article PubMed PubMed Central Google Scholar
Ali S, Chandrashekar N, Rawat S, Nayanakantha NMC, Mir ZA, Manoharan A, Sultana M, Grover A (2017) Isolation and molecular characterization of pathogenesis related PR2 gene and its promoter from Brassica juncea. Biol Plant 61:763–773. https://doi.org/10.1007/s10535-017-0726-7
CAS Article Google Scholar
Ali S, Mir ZA, Tyagi A, Mehari H, Meena R, Bhat JA, Yadav P, Papalou P, Rawat S, Grover A (2017b) Overexpression of NPR1 in Brassica juncea confers broad spectrum resistance to fungal pathogens. Front Plant Microbe Interact. https://doi.org/10.3389/fpls.2017.01693
Article Google Scholar
Almagro L, Gómez Ros LV, Belchi-Navarro S, Bru R, Ros Barceló A, Pedreño MA (2009) Class III peroxidases in plant defence reactions. J Exp Bot 60:370–399. https://doi.org/10.1093/jxb/ern277
CAS Article Google Scholar
Almutairi ZM (2016) Effect of nano-silicon application on the expression of salt tolerance genes in germinating tomato (Solanum lycopersicum L.) seedlings under salt stress. Plant Omics 9:106–114
CAS Google Scholar
Araujo L, Paschoalino RS, Rodrigues FÁ (2016) Microscopic aspects of silicon-mediated rice resistance to leaf scald. Phytopathology 106:132–141. https://doi.org/10.1094/PHYTO-04-15-0109-R
CAS Article PubMed Google Scholar
Balbi V, Devoto A (2008) Jasmonate signalling network in Arabidopsis thaliana: crucial regulatory nodes and new physiological scenarios. New Phytol 177:301–318. https://doi.org/10.1111/j.1469-8137.2007.02292.x
CAS Article PubMed Google Scholar
Bari R, Jones JDG (2009) Role of plant hormones in plant defence responses. Plant Mol Biol 69:473–488. https://doi.org/10.1007/s11103-008-9435-0
CAS Article PubMed Google Scholar
Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 4:276–287. https://doi.org/10.1016/0003-2697(71)90370-8
Article Google Scholar
Brisson LF, Tenhaken R, Lamb C (1994) Function of oxidative cross-linking of cell wall structural proteins in plant disease resistance. Plant Cell 6:1703–1712. https://doi.org/10.1105/tpc.6.12.1703
CAS Article PubMed PubMed Central Google Scholar
Brunings AM, Datnoff LE, Ma JF, Mitani N, Nagamura Y, Rathinasabapathi B, Kirst M (2009) Differential gene expression of rice in response to silicon and rice blast fungus Magnaporthe oryzae. Ann Appl Biol 155:161–170. https://doi.org/10.1111/j.1744-7348.2009.00347.x
CAS Article Google Scholar
Chaerani R, Voorrips E (2006) Tomato early blight (Alternaria solani): the pathogen, genetics, and breeding for resistance. J Gen Plant Pathol 72:335–347. https://doi.org/10.1007/s10327-006-0299-3
Article Google Scholar
Chance B, Maehly AC (1955) Assay of catalases and peroxidases. {black small square}. Methods Enzymol 2:764–775. https://doi.org/10.1016/S0076-6879(55)02300-8
Article Google Scholar
Chen YY, Lin YM, Chao TC, Wang JF, Liu AC, Ho FI, Cheng CP (2009) Virus-induced gene silencing reveals the involvement of ethylene-, salicylic acid- and mitogen-activated protein kinase-related defense pathways in the resistance of tomato to bacterial wilt. Physiol Plant 136:324–335. https://doi.org/10.1111/j.1399-3054.2009.01226.x
CAS Article PubMed Google Scholar
Cooke J, Leishman MR (2016) Consistent alleviation of abiotic stress with silicon addition: a meta-analysis. Funct Ecol 30:1340–1357. https://doi.org/10.1111/1365-2435.12713
Article Google Scholar
Cruz MFA, Debona D, Rios JA, Barros EG, Rodrigues FA (2015) Potentiation of defense-related gene expression by silicon increases wheat resistance to leaf blast. Trop Plant Pathol 40:394–400. https://doi.org/10.1007/s40858-015-0051-7
Article Google Scholar
Curvêlo CRS, Rodrigues FÁ, Pereira LF, Silva LC, DaMatta FM, Berger PG (2013) Trocas gasosas e estresse oxidativo em plantas de algodoeiro supridas com silício e infectadas por Ramularia areola. Bragantia 72:346–359. https://doi.org/10.1590/brag.2013.053
Article Google Scholar
da Silva WL, Cruz MFA, Fortunato AA, Rodrigues FÁ (2015) Histochemical aspects of wheat resistance to leaf blast mediated by silicon. Sci Agric 72:322–327. https://doi.org/10.1590/0103-9016-2014-0221
Article Google Scholar
Dannon EA, Wydra K (2004) Interaction between silicon amendment, bacterial wilt development and phenotype of Ralstonia solanacearum in tomato genotypes. Physiol Mol Plant Pathol 64:233–243. https://doi.org/10.1016/j.pmpp.2004.09.006
CAS Article Google Scholar
Das K, Roychoudhury A (2014) Reactive oxygen species (ROS) and response of antioxidants as ROS-scavengers during environmental stress in plants. Front Environ Sci 2:53. https://doi.org/10.3389/fenvs.2014.00053
Article Google Scholar
De Vleesschauwer D, Djavaheri M, Bakker PAHM, Höfte M (2008) Pseudomonas fluorescens WCS374r-induced systemic resistance in rice against Magnaporthe oryzae is based on pseudobactin-mediated priming for a salicylic acid-repressible multifaceted defense response. Plant Physiol 148:1996–2012. https://doi.org/10.1104/pp.108.127878
CAS Article PubMed PubMed Central Google Scholar
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 63:581–589. https://doi.org/10.1111/ppa.12119
CAS Article Google Scholar
Deshmukh RK, Vivancos J, Guérin V, Sonah H, Labbé C, Belzile F, Bélanger RR (2013) Identification and functional characterization of silicon transporters in soybean using comparative genomics of major intrinsic proteins in Arabidopsis and rice. Plant Molec Biol 83(4–5):303–315
CAS Article Google Scholar
Deshmukh RK, Vivancos J, Ramakrishnan G, Guérin V, Carpentier G, Sonah H, Labbé C, Isenring P, Belzile FJ, Bélanger RR (2015) A precise spacing between the NPA domains of aquaporins is essential for silicon permeability in plants. Plant J 83:489–500. https://doi.org/10.1111/tpj.12904
CAS Article PubMed Google Scholar
Diogo RVC, Wydra K (2007) Silicon-induced basal resistance in tomato against Ralstonia solanacearum is related to modification of pectic cell wall polysaccharide structure. Physiol Mol Plant Pathol 70:120–129. https://doi.org/10.1016/j.pmpp.2007.07.008
CAS Article Google Scholar
Domiciano GP, Rodrigues FA, Guerra AMN, Vale FXR (2013) Infection process of Bipolaris sorokiniana on wheat leaves is affected by silicon. Trop Plant Pathol 38:258–263. https://doi.org/10.1590/S1982-56762013005000006
Article Google Scholar
Doughari JH (2015) An overview of plant. Immunity 6:322. https://doi.org/10.4172/2157-7471.1000322
CAS Article Google Scholar
Dreher K, Callis J (2007) Ubiquitin, hormones and biotic stress in plants. Ann Bot 99:787–822. https://doi.org/10.1093/aob/mcl255
CAS Article PubMed PubMed Central Google Scholar
Epstein E (1999) Silicon. Annu Rev Plant Physiol Plant Mol Biol 50:641–664. https://doi.org/10.1146/annurev.arplant.50.1.641
CAS Article PubMed Google Scholar
Epstein E (2001) Silicon in plants: facts vs concepts. Elsevier Science, Amsterdam, p 424
Google Scholar
Fahad S, Bajwa AA, Nazir U, Anjum SA, Farooq A, Zohaib A, Sadia S, Nasim W, Adkins S, Saud S, Ihsan MZ, Alharby H, Wu C, Wang D, Huang J (2017) Crop production under drought and heat stress: plant responses and management options. Front Plant Sci 8:1147. https://doi.org/10.3389/fpls.2017.01147
Article PubMed PubMed Central Google Scholar
Fauteux F, Chain F, Belzile F, Menzies JG, Bélanger RR (2006) The protective role of silicon in the Arabidopsis-powdery mildew pathosystem. Proc Natl Acad Sci USA 103:17554–17559. https://doi.org/10.1073/pnas.0606330103
CAS Article PubMed Google Scholar
Fauteux F, Rémus-Borel W, Menzies JG, Bélanger RR (2005) Silicon and plant disease resistance against pathogenic fungi. FEMS Microbiol Lett 249:1–6. https://doi.org/10.1016/j.femsle.2005.06.034
CAS Article PubMed Google Scholar
Ferreira RB, Monteiro S, Freitas R, Santos CN, Chen Z, Batista LM, Duarte J, Borges A, Teixeira AR (2007) The role of plant defence proteins in fungal pathogenesis. Mol Plant Pathol 8:677–700. https://doi.org/10.1111/j.1364-3703.2007.00419.x
CAS Article PubMed Google Scholar
Foolad MR (2007) Genome mapping and molecular breeding of tomato. Int J Plant Genom. https://doi.org/10.1155/2007/64358
Article Google Scholar
Fortunato AA, Rodrigues FÁ, Baroni JCP, Soares GCB, Rodriguez MAD, Pereira OL (2012) Silicon suppresses fusarium wilt development in banana plants. J Phytopathol 160:674–679. https://doi.org/10.1111/jph.12005
CAS Article Google Scholar
Fortunato AA, Rodrigues FA, Datnoff LE (2015) Silicon control of soil-borne and seed-borne diseases. Silicon and plant diseases. Springer, Berlin, pp 53–66
Chapter Google Scholar
Foyer CH, Halliwell B (1976) The presence of glutathione and glutathione reductase in chloroplasts: a proposed role in ascorbic acid metabolism. Planta 133:21–25. https://doi.org/10.1007/BF00386001
CAS Article PubMed Google Scholar
Fraser RSS (2000) Case studies. Mechanisms of resistance to plant diseases. Springer, Dordrecht, pp 1–19
Google Scholar
Gechev TS, Van Breusegem F, Stone JM, Denev I, Laloi C (2006) Reactive oxygen species as signals that modulate plant stress responses and programmed cell death. BioEssays 28:1091–1101. https://doi.org/10.1002/bies.20493
CAS Article PubMed Google Scholar
Gerszberg A, Hnatuszko-Konka K (2017) Tomato tolerance to abiotic stress: a review of most often engineered target sequences. Plant Growth Regul 83:175–198. https://doi.org/10.1007/s10725-017-0251-x
CAS Article Google Scholar
Ghareeb H, Bozsó Z, Ott PG, Repenning C, Stahl F, Wydra K (2011) Transcriptome of silicon-induced resistance against Ralstonia solanacearum in the silicon non-accumulator tomato implicates priming effect. Physiol Mol Plant Pathol 75:83–89. https://doi.org/10.1016/j.pmpp.2010.11.004
CAS Article Google Scholar
Ghosh PP, Mandal D, Laha S, Dasgupta MK (2009) Dynamics and severity model in managing fungal diseases. J Plant Protect Sci 1:55–59
Google Scholar
Glazebrook J (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol 43:205–227. https://doi.org/10.1146/annurev.phyto.43.040204.135923
CAS Article PubMed Google Scholar
Gong H, Zhu X, Chen K, Wang S, Zhang C (2005) Silicon alleviates oxidative damage of wheat plants in pots under drought. Plant Sci 169:313–321. https://doi.org/10.1016/j.plantsci.2005.02.023
CAS Article Google Scholar
Guil-Guerrero JL, Rebolloso-Fuentes MM (2009) Nutrient composition and antioxidant activity of eight tomato (Lycopersicon esculentum) varieties. J Food Compos Anal 22:123–129. https://doi.org/10.1016/j.jfca.2008.10.012
CAS Article Google Scholar
Guoqiang W (2004) Effects of silicon supply and Sphaerotheca fuliginea inoculation on resistance of cucumber seedlings against powdery mildew|request PDF. J Appl Ecol 15:2147–2151
Google Scholar
Hayasaka T, Fujii H, Ishiguro K (2008) The role of silicon in preventing appressorial penetration by the rice blast fungus. Phytopath 98:1038–1044. https://doi.org/10.1094/PHYTO-98-9-1038
CAS Article Google Scholar
He Y, Xiao H, Wang H, Chen Y, Yu M (2010) Effect of silicon on chilling-induced changes of solutes, antioxidants, and membrane stability in seashore Paspalum turfgrass. Acta Physiol Plant 32:487–494. https://doi.org/10.1007/s11738-009-0425-x
CAS Article Google Scholar
Heine G, Tikum G, Horst WJ (2007) The effect of silicon on the infection by and spread of Pythium aphanidermatum in single roots of tomato and bitter gourd. J Exp Bot 58:569–577. https://doi.org/10.1093/jxb/erl232
CAS Article PubMed Google Scholar
Huang CH, Roberts PD, Datnoff LE (2011) Silicon suppresses fusarium crown and root rot of tomato. J Phytopathol 159:546–554. https://doi.org/10.1111/j.1439-0434.2011.01803.x
CAS Article Google Scholar
Ignacimuthu S, Ceasar A (2020) Development of transgenic finger millet (Eleusine coracana (L.) Gaertn.) resistant to leaf blast disease. J Biosci 37:135–147. https://doi.org/10.1007/s12038-011-9178-y
CAS Article Google Scholar
Iwai T, Miyasaka A, Seo S, Ohashi Y (2006) Contribution of ethylene biosynthesis for resistance to blast fungus infection in young rice plants. Plant Physiol 142:1202–1215. https://doi.org/10.1104/pp.106.085258
CAS Article PubMed PubMed Central Google Scholar
Jouili H, Bouazizi H, Ferjani E (2011) Plant peroxidases: biomarkers of metallic stress. Acta Physiol Plant 33:2075–2083. https://doi.org/10.1007/s11738-011-0780-2
CAS Article Google Scholar
Jung HW, Hwang BK (2000) Isolation, partial sequencing, and expression of pathogenesis-related cDNA genes from pepper leaves infected by Xanthomonas campestris pv. vesicatoria. Mol Plant-Microbe Interact 13:136–142. https://doi.org/10.1094/MPMI.2000.13.1.136
CAS Article PubMed Google Scholar
Jung HW, Tschaplinski TJ, Wang L, Glazebrook J, Greenberg JT (2009) Priming in systemic plant immunity. Science 80(324):89–91. https://doi.org/10.1126/science.1170025
CAS Article Google Scholar
Kauss H, Seehaus K, Franke R, Gilbert S, Dietrich RA, Kröger N (2003) Silica deposition by a strongly cationic proline-rich protein from systemically resistant cucumber plants. Plant J 33:87–95. https://doi.org/10.1046/j.1365-313X.2003.01606.x
CAS Article PubMed Google Scholar
Khan MA, Butt SJ, Khan KA, Nadeen F, Yousaf B, Javed HU (2017) Morphological and physico-biochemical characterization of various tomato cultivars in a simplified soilless media. Ann Agric Sci 62:139–143. https://doi.org/10.1016/j.aoas.2017.10.001
Article Google Scholar
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. https://doi.org/10.1007/s11738-015-1818-7
Article Google Scholar
Li J, Brader G, Palva ET (2004) The WRKY70 transcription factor: a node of convergence for jasmonate-mediated and salicylate-mediated signals in plant defense. Plant Cell 16:319–331. https://doi.org/10.1105/tpc.016980
CAS Article PubMed PubMed Central Google Scholar
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 stress-antioxidative system in muskmelon fruit. Eur Food Res Technol 234:137–145. https://doi.org/10.1007/s00217-011-1611-9
CAS Article Google Scholar
Liang Y, Chen Q, Liu Q, Zhang W, Ding R (2003) Exogenous silicon (Si) increases antioxidant enzyme activity and reduces lipid peroxidation in roots of salt-stressed barley (Hordeum vulgare L.). J Plant Physiol 160:1157–1164. https://doi.org/10.1078/0176-1617-01065
CAS Article PubMed Google Scholar
Liang YC, Sun WC, Si J, Römheld V (2005) Effect of foliar- and root-applied silicon on the enhancement of induced resistance to powdery mildew in Cucumis sativus. Plant Pathol 54:678–685. https://doi.org/10.1111/j.1365-3059.2005.01246.x
CAS Article Google Scholar
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2 C T method. Methods 25:402–408. https://doi.org/10.1006/meth.2001.1262
CAS Article PubMed PubMed Central Google Scholar
Ma JF (2004) Role of silicon in enhancing the resistance of plants to biotic and abiotic stresses. Soil Sci Plant Nutr 50:11–18. https://doi.org/10.1080/00380768.2004.10408447
CAS Article Google Scholar
Ma JF, Yamaji N (2006) Silicon uptake and accumulation in higher plants. Trends Plant Sci 11:392–397. https://doi.org/10.1016/j.tplants.2006.06.007
CAS Article Google Scholar
Ma JF, Yamaji N (2008) Functions and transport of silicon in plants. Cell Mol Life Sci 65:3049–3057. https://doi.org/10.1007/s00018-008-7580-x
CAS Article PubMed Google Scholar
Menke FLH, Kang HG, Chen Z, Jeong MP, Kumar D, Klessig DF (2005) Tobacco transcription factor WRKY1 is phosphorylated by the MAP kinase SIPK and mediates HR-like cell death in tobacco. Mol Plant-Microbe Interact 18:1027–1034. https://doi.org/10.1094/MPMI-18-1027
CAS Article PubMed Google Scholar
Mitani-ueno N, Ma JF (2020) Soil science and plant nutrition linking transport system of silicon with its accumulation in different plant species. Soil Sci Plant Nutr. https://doi.org/10.1080/00380768.2020.1845972
Article Google Scholar
Mohaghegh P, Khoshgoftarmanesh AH, Shirvani M, Sharifnabi B, Nili N (2011) Effect of silicon nutrition on oxidative stress induced by Phytophthora melonis infection in cucumber. Plant Dis 95:455–460. https://doi.org/10.1094/PDIS-05-10-0379
CAS Article PubMed Google Scholar
Moldes CA, de Lima Filho OF, Merini LJ, Tsai SM, Camiña JM (2016) Occurrence of powdery mildew disease in wheat fertilized with increasing silicon doses: a chemometric analysis of antioxidant response. Acta Physiol Plant 38:1–9. https://doi.org/10.1007/s11738-016-2217-4
CAS Article Google Scholar
Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880. https://doi.org/10.1093/oxfordjournals.pcp.a076232
CAS Article Google Scholar
Niderman T, Genetet I, Bruyere T, Gees R, Stintzi A, Legrand M, Fritig B, Mosinger E (1995) Pathogenesis-related PR-1 proteins are antifungal. Isolation and characterization of three 14-kilodalton proteins of tomato and of a basic PR-1 of tobacco with inhibitory activity against Phytophthora infestans. Plant Physiol 108:17–27. https://doi.org/10.1104/pp.108.1.17
CAS Article PubMed PubMed Central Google Scholar
Ouellette S, Goyette MH, Labbé C, Laur J, Gaudreau L, Gosselin A, Dorais M, Deshmukh RK, Bélanger RR (2017) Silicon transporters and effects of silicon amendments in strawberry under high tunnel and field conditions. Front Plant Sci 8:949. https://doi.org/10.3389/fpls.2017.00949
Article PubMed PubMed Central Google Scholar
Pandey P, Irulappan V, Bagavathiannan MV, Senthil-Kumar M (2017) Impact of combined abiotic and biotic stresses on plant growth and avenues for crop improvement by exploiting physio-morphological traits. Front Plant Sci 8:537. https://doi.org/10.3389/fpls.2017.00537
Article PubMed PubMed Central Google Scholar
Panthee D, Chen F (2009) Genomics of fungal disease resistance in tomato. Curr Genom 11:30–39. https://doi.org/10.2174/138920210790217927
Article Google Scholar
Pereira Domiciano G, Severino Cacique I, Freitas CC, Filippi MCC, da Matta FM, do Vale FXR, Rodrigues FA (2015) Biochemistry and cell biology alterations in gas exchange and oxidative metabolism in rice leaves infected by Pyricularia oryzae are attenuated by silicon. Biochem Cell Biol 105:738–747. https://doi.org/10.1094/PHYTO-10-14-0280-R
Article Google Scholar
Polanco LR, Rodrigues FA, Nascimento KJT, Cruz MFA, Curvelo CRS, DaMatta FM, Vale FXR (2014) Photosynthetic gas exchange and antioxidative system in common bean plants infected by Colletotrichum lindemuthianum and supplied with silicon. Trop Plant Pathol 39:35–42. https://doi.org/10.1590/S1982-56762014000100005
Article Google Scholar
Resende RS, Rodrigues FÁ, Cavatte PC, Martins SCV, Moreira WR, Chaves ARM, DaMatta FM (2012a) Leaf gas exchange and oxidative stress in sorghum plants supplied with silicon and infected by Colletotrichum sublineolum. Phytopathol 102:892–898. https://doi.org/10.1094/PHYTO-01-12-0014-R
CAS Article Google Scholar
Resende RS, Rodrigues FA, Costa RV, Silva DD (2012b) Silicon and fungicide effects on anthracnose in moderately resistant and susceptible sorghum lines. J Phytopathol 161:11–17. https://doi.org/10.1111/jph.12020
CAS Article Google Scholar
Reynolds OL, Padula MP, Zeng R, Gurr GM (2016) Silicon: potential to promote direct and indirect effects on plant defense against arthropod pests in agriculture. Front Plant Sci 7:744. https://doi.org/10.3389/fpls.2016.00744
Article PubMed PubMed Central Google Scholar
Rodrigues FA, Datnoff LE (2015) Silicon and plant diseases, silicon and plant diseases. Springer, Berlin, pp 1–5
Book Google Scholar
Rodrigues FÁ, Datnoff LE, Korndörfer GH, Seebold KW, Rush MC (2001) Effect of silicon and host resistance on sheath blight development in rice. Plant Dis 85:827–832. https://doi.org/10.1094/pdis.2001.85.8.827
CAS Article Google Scholar
Rodrigues TTMS, Maffia LA, Dhingra OD, Mizubuti ESG (2010) Produção in vitro de con? Dios dev Alternaria solani. Trop Plant Pathol 35:203–212. https://doi.org/10.1590/S1982-56762010000400001
Article Google Scholar
Samuels AL, Adm G, Menzies JG, Ehret DL (1994) Silicon in cell walls and papillae of Cucumis sativus during infection by Sphaerotheca fuliginea. Physiol Mol Plant Pathol 44:237–242. https://doi.org/10.1016/S0885-5765(05)80027
CAS Article Google Scholar
Samuels AL, Glass ADM, Ehret DM, Menzies JG (1991) Distribution of silicon in cucumber leaves during infection by powdery mildew fungus. Can J Bot 69:140–146
CAS Article Google Scholar
Seebold KW, Datnoff LE, Correa-Victoria FJ, Kucharek TA, Snyder GH (2004) Effects of silicon and fungicides on the control of leaf and neck blast in upland rice. Plant Dis 88:253–258. https://doi.org/10.1094/PDIS.2004.88.3.253
CAS Article PubMed Google Scholar
Shekari F, Abbasi A, Mustafavi SH (2017) Effect of silicon and selenium on enzymatic changes and productivity of dill in saline condition. J Saudi Soc Agric Sci 16:367–374. https://doi.org/10.1016/j.jssas.2015.11.006
Article Google Scholar
Shi Y, Zhang Y, Han W, Feng R, Hu Y, Guo J, Gong H (2016) Silicon enhances water stress tolerance by improving root hydraulic conductance in Solanum lycopersicum L. Front Plant Sci 7:196. https://doi.org/10.3389/fpls.2016.00196
Article PubMed PubMed Central Google Scholar
Shi Y, Zhang Y, Yao H, Wu J, Sun H, Gong H (2014) Silicon improves seed germination and alleviates oxidative stress of bud seedlings in tomato under water deficit stress. Plant Physiol Biochem 78:27–36. https://doi.org/10.1016/j.plaphy.2014.02.009
CAS Article PubMed Google Scholar
Shwethakumari U, Prakash NB (2018) Effect of foliar application of silicic acid on soybean yield and seed quality under field conditions. J Indian Soc Soil Sci 66:406–414. https://doi.org/10.5958/0974-0228.2018.00051.8
Article Google Scholar
Sies H, Berndt C, Jones DP (2017) Oxidative stress. Annu Rev Biochem 86:715–748. https://doi.org/10.1146/annurev-biochem-061516-045037
CAS Article PubMed Google Scholar
Singh P, Goyal GK (2008) Dietary lycopene: its properties and anticarcinogenic effects. Compr Rev Food Sci Food Saf 7:255–270. https://doi.org/10.1111/j.1541-4337.2008.00044.x
CAS Article PubMed Google Scholar
Song A, Xue G, Cui P, Fan F, Liu H, Yin C, Sun W, Liang Y (2016) The role of silicon in enhancing resistance to bacterial blight of hydroponic- and soil-cultured rice. Sci Rep 6:1–13. https://doi.org/10.1038/srep24640
CAS Article Google Scholar
Sousa RS, Rodrigues FÁ, 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 38:472–477. https://doi.org/10.1590/S1982-56762013000600002
Article Google Scholar
Story EN, Kopec RE, Schwartz SJ, Keith Harris G (2010) An update on the health effects of tomato lycopene. Annu Rev Food Sci Technol 1:189–210. https://doi.org/10.1146/annurev.food.102308.124120
CAS Article PubMed Google Scholar
Sun H, Duan Y, Mitani-Ueno N, Che J, Jia J, Liu J, Guo J, Ma JF, Gong H (2020) Tomato roots have a functional silicon influx transporter but not a functional silicon efflux transporter. Plant Cell Environ 43:732–744. https://doi.org/10.1111/pce.13679
CAS Article PubMed Google Scholar
Sun W, Zhang J, Fan Q, Xue G, Li Z, Liang Y (2010) Silicon-enhanced resistance to rice blast is attributed to silicon-mediated defence resistance and its role as physical barrier. Eur J Plant Pathol 128:39–49. https://doi.org/10.1007/s10658-010-9625-x
CAS Article Google Scholar
Thannickal VJ, Fanburg BL (2000) Reactive oxygen species in cell signaling. Am J Physiol Lung Cell Mol Physiol. https://doi.org/10.1152/ajplung.2000.279.6.l1005
Article PubMed Google Scholar
Thines B, Katsir L, Melotto M, Niu Y, Mandaokar A, Liu G, Nomura K, He SY, Howe GA, Browse J (2007) JAZ repressor proteins are targets of the SCFCOI1 complex during jasmonate signalling. Nature 448:661–665. https://doi.org/10.1038/nature05960
CAS Article PubMed Google Scholar
Thirthamallappa LHC (2000) Genetics of resistance to early blight (Alternaria solani Sorauer) in tomato (Lycopersicon esculentum L.). Euphytica 113:187–193. https://doi.org/10.1023/A:1003929303632
Article Google Scholar
Torres MA, Jones JDG, Dangl JL (2006) Reactive oxygen species signaling in response to pathogens. Plant Physiol 148:373–378. https://doi.org/10.1104/pp.106.079467
CAS Article Google Scholar
Tripathi DK, Singh VP, Prasad SM, Chauhan DK, Dubey NK (2015) Silicon nanoparticles (SiNp) alleviate chromium (VI) phytotoxicity in Pisum sativum (L.) seedlings. Plant Physiol Biochem 96:189–198. https://doi.org/10.1016/j.plaphy.2015.07.026
CAS Article PubMed Google Scholar
Tripathy BC, Oelmüller R (2012) Reactive oxygen species generation and signaling in plants. Plant Signal Behav 7:16–21. https://doi.org/10.4161/psb.22455
CAS Article Google Scholar
Tubana BS, Babu T, Datnoff LE (2016) A review of silicon in soils and plants and its role in US agriculture. Soil Sci 181:1. https://doi.org/10.1097/SS.0000000000000179
CAS Article Google Scholar
Tubaña BS, Heckman JR (2015) Silicon in soils and plants. Springer, Cham
Book Google Scholar
Van Bockhaven J, De Vleesschauwer D, Höfte M (2013) Towards establishing broad-spectrum disease resistance in plants: silicon leads the way. J Exp Bot 64:1281–1293. https://doi.org/10.1093/jxb/ers329
CAS Article PubMed PubMed Central Google Scholar
Van Bockhaven J, Steppe K, Bauweraerts I, Kikuchi S, Asano T, Höfte M, De Vleesschauwer D (2015) Primary metabolism plays a central role in moulding silicon-inducible brown spot resistance in rice. Mol Plant Pathol 16:811–824. https://doi.org/10.1111/mpp.12236
CAS Article PubMed PubMed Central Google Scholar
Vivancos J, Labbé C, Menzies JG, Bélanger RR (2015) Silicon-mediated resistance of Arabidopsis against powdery mildew involves mechanisms other than the salicylic acid (SA)-dependent defence pathway. Mol Plant Pathol 16:572–582. https://doi.org/10.1111/mpp.12213
CAS Article PubMed Google Scholar
Wiese J, Wiese H, Schwartz J, Schubert S (2005) Osmotic stress and silicon act additively in enhancing pathogen resistance in barley against barley powdery mildew. J Plant Nutr Soil Sci 168:269–274. https://doi.org/10.1002/jpln.200420490
CAS Article Google Scholar
Ye M, Song Y, Long J, Wang R, Baerson SR, Pan Z, Zhu-Salzman K, Xie J, Cai K, Luo S, Zeng R (2013) Priming of jasmonate-mediated antiherbivore defense responses in rice by silicon. Proc Natl Acad Sci USA 38:110. https://doi.org/10.1073/pnas.1305848110
Article Google Scholar
Zhang GL, Dai QG, Zhang HC (2006) Silicon application enhances resistance to sheath blight (Rhizoctonia solani) in rice. J Plant Physiol Mol Biol 32:600–606
CAS Google Scholar
Zhang H, Zhang D, Chen J, Yang Y, Huang Z, Huang D, Wang XC, Huang R (2004) Tomato stress-responsive factor TSRF1 interacts with ethylene responsive element GCC box and regulates pathogen resistance to Ralstonia solanacearum. Plant Mol Biol 55:825–834. https://doi.org/10.1007/s11103-004-2140-8
CAS Article PubMed Google Scholar
Zhang Y, Shi Y, Gong H et al (2018) Beneficial effects of silicon on photosynthesis of tomato seedlings under water stress. J Integr Agric 17:2151–2159. https://doi.org/10.1016/S2095-3119(18)62038-6
CAS Article Google Scholar
Zhu Z, Wei G, Li J, Qian Q, Yu J (2004) Silicon alleviates salt stress and increases antioxidant enzymes activity in leaves of salt-stressed cucumber (Cucumis sativus L.). Plant Sci 167:527–533. https://doi.org/10.1016/j.plantsci.2004.04.020
CAS Article Google Scholar

Download references

Acknowledgement

The authors would like to acknowledge the support by Centre of research for development (CORD), University of Kashmir, Srinagar. I am also thankful to the Council of Scientific & Industrial Research for financial support in the form of Junior and Senior Research Fellowships.

Author information

Affiliations

Centre of Research for Development, University of Kashmir, Srinagar, Jammu and Kashmir, 190006, India
Naveed Gulzar, Sajad Ali & Azra N. Kamili
Department of Botany, University of Kashmir, Srinagar, Jammu and Kashmir, 190006, India
Manzoor A. Shah

Authors

Naveed Gulzar
View author publications
You can also search for this author in PubMed Google Scholar
Sajad Ali
View author publications
You can also search for this author in PubMed Google Scholar
Manzoor A. Shah
View author publications
You can also search for this author in PubMed Google Scholar
Azra N. Kamili
View author publications
You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Azra N. Kamili.

Ethics declarations

Conflict of interest

The authors declare that there is no conflict of interest.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Gulzar, N., Ali, S., Shah, M.A. et al. Silicon supplementation improves early blight resistance in Lycopersicon esculentum Mill. by modulating the expression of defense-related genes and antioxidant enzymes. 3 Biotech 11, 232 (2021). https://doi.org/10.1007/s13205-021-02789-6

Download citation

Received: 02 November 2020
Accepted: 12 April 2021
Published: 22 April 2021
DOI: https://doi.org/10.1007/s13205-021-02789-6

Keywords

Lycopersicon esculentum
Silicon
PR genes
Early blight
Alternaria solani
Antioxidant enzymes