Physiological response and phenolic metabolism in tomato (Solanum lycopersicum) mediated by silicon under Ralstonia solanacearum infection

doi:10.1016/S2095-3119(18)62036-2

摘要/Abstract

Abstract:

Bacterial wilt, caused by Ralstonia solanacearum (Rs) is a serious soil-borne disease and silicon can enhance tomato resistance against this disease. However, few studies have focused on the mechanisms of Si-mediated pathogen resistance from the rhizosphere perspective. In this study, two tomato genotypes, HYT (susceptible) and H7996 (resistant), were used to investigate the effects of silicon application on disease inhibition, root growth, and organic acid content in both roots and root exudates under R. solanacearum infection. The results showed that Si application significantly suppressed bacterial wilt in HYT, but had no effect in H7996. Silicon concentrations in roots, stems and leaves of tomato were significantly increased by Si treatment under R. solanacearum inoculation. In HYT, Si application increased root dry weight by 22.8–51.6% and leaf photosynthesis by 30.6–208.0%, and reduced the concentrations of citric acid in root exudates by 71.4% and in roots by 83.5%. However, organic acids did not influence R. solanacearum growth. Results also demonstrated that salicylic acid (SA) content in roots was significantly increased by silicon addition for H7996 and exogenous SA application could reduce bacterial wilt disease index. Collectively, these results suggest that Si-modulated phenolic compound metabolism in roots or root exudates, especially citric acid and SA, may be a potential mechanism in the amelioration of bacterial wilt disease by Si.

Key words: silicon , root , root exudates , Solanum lycopersicum , Ralstonia solanacearum , organic acids

. [J]. Journal of Integrative Agriculture, 2018, 17(10): 2160-2171.

FAN Xue-ying, LIN Wei-peng, LIU Rui, JIANG Ni-hao, CAI Kun-zheng. Physiological response and phenolic metabolism in tomato (Solanum lycopersicum) mediated by silicon under Ralstonia solanacearum infection[J]. Journal of Integrative Agriculture, 2018, 17(10): 2160-2171.

参考文献

Afroz A, Khan M R, Ahsan N, Komatsu S. 2009. Comparative proteomic analysis of bacterial wilt susceptible and resistant tomato cultivars. Peptides, 30, 1600–1607.
Akiyama K, Matsuzaki K, Hayashi H. 2005. Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature, 435, 824–827.
Amari T, Lutts S, Taamali M, Lucchini G, Sacchi G A, Abdelly C, Ghnaya T. 2016. Implication of citrate, malate and histidine in the accumulation and transport of nickel in Mesembryanthemum crystallinum and Brassica juncea. Ecotoxicology and Environmental Safety, 126, 122–128.
Araujo L, Paschoalino R S, Rodrigues F A. 2016. Microscopic aspects of silicon-mediated rice resistance to leaf scald. Phytopathology, 106, 132–141.
Baetz U, Martinoia E. 2014. Root exudates: The hidden part of plant defense. Trends in Plant Science, 19, 90–98.
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. Molecular Plant Pathology, 16, 811–824.
Van Bockhaven J, De Vleesschauwer D, Hofte M. 2013. Towards establishing broad-spectrum disease resistance in plants: Silicon leads the way. Journal of Experimental Botany, 64, 1281–1293.
Brunings A M, Datnoff L E, Ma J F, Mitani N, Nagamura Y. 2009. Differential gene expression of rice in response to silicon and rice blast fungus. Annals of Applied Biology, 155, 161–170.
Cai K, Gao D, Luo S, Zeng R, Yang J, Zhu X. 2008. Physiological and cytological mechanisms of silicon-induced resistance in rice against blast disease. Physiologia Plantarum, 134, 324–333.
Chen Y, Liu M, Wang L, Lin W, Fan X, Cai K. 2015. Proteomic characterization of silicon-mediated resistance against Ralstonia solanacearum in tomato. Plant and Soil, 387, 425–440.
Chen Y Y, Lin Y M, Chao T C, Wang J F, Liu A C, Ho F I, Cheng C P. 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. Physiological Plant, 136, 324–335.
Dallagnol L J, Rodrigues F I C A, Damatta F A B M, Mielli M V, Pereira S C. 2011. Deficiency in silicon uptake affects cytological, physiological, and biochemical events in the rice-Bipolaris oryzae interaction. Phytopathology, 101, 92–104.
Dannon E A, Wydra K. 2004. Interaction between silicon amendment, bacterial wilt development and phenotype of Ralstonia solanacearum in tomato genotypes. Physiological and Molecular Plant Pathology, 64, 233–243.
Debona D, Rodrigues F A, Datnoff L E. 2017. Silicon’s role in abiotic and biotic plant stresses. Annual Review of Phytopathology, 55, 85–107.
Diogo R V C, Wydra K. 2007. Silicon-induced basal resistance in tomato against Ralstonia solanacearum is related to modification of pectic cell wall polysaccharide structure. Physiological and Molecular Plant Pathology, 70, 120–129.
Ehsan S, Ali S, Noureen S, Mahmood K, Farid M, Ishaque W, Shakoor M B, Rizwan M. 2014. Citric acid assisted phytoremediation of cadmium by Brassica napus L. Ecotoxicology and Environmental Safety, 106, 164–172.
Fang Z D. 1998. Plant Pathology Research Methods. 3rd ed. China Agriculture Press, Beijing. p. 388. (in Chinese)
Fauteux F, Chain F, Belzile F, Menzies J G, Belanger R R. 2006. The protective role of silicon in the Arabidopsis-powdery mildew pathosystem. Proceedings of the National Academy of Sciences of the United States of America, 103, 17554–17559.
Fauteux F O, Rã Mus-Borel W, Menzies J G, Bélanger R R. 2005. Silicon and plant disease resistance against pathogenic fungi. FEMS Microbiology Letters, 249, 1–6.
Fortunato A A, Rodrigues F A, Do N K. 2012. Physiological and biochemical aspects of the resistance of banana plants to Fusarium wilt potentiated by silicon. Phytopathology, 102, 957–966.
Garibaldi A, Gilardi G, Gullino M L. 2011. Effect of potassium silicate and electrical conductivity in reducing powdery mildew of hydroponically grown tomato. Phytopathologia Mediterranea, 50, 192–202.
Ghareeb H, Bozso Z, Ott P G, Repenning C, Stahl F, Wydra K. 2011. Transcriptome of silicon-induced resistance against Ralstonia solanacearum in the silicon non-accumulator tomato implicates priming effect. Physiological and Molecular Plant Pathology, 75, 83–89.
He C, Wang L, Liu J, Liu X, Li X, Ma J, Lin Y, Xu F. 2013. Evidence for ‘silicon’ within the cell walls of suspension-cultured rice cells. New Phytologist, 200, 700–709.
Heine G, Tikum G, Horst W J. 2007. The effect of silicon on the infection by and spread of Pythium aphanidermatum in single roots of tomato and bitter gourd. Journal of Experimental Botany, 58, 569–577.
Huang C H, Roberts P D, Datnoff L E. 2011. Silicon suppresses fusarium crown and root rot of tomato. Journal of Phytopathology, 159, 546–554.
Huang G, Guo G, Yao S, Zhang N, Hu H. 2016. Organic acids, amino acids compositions in the root exudates and Cu-accumulation in castor (Ricinus communis L.) under Cu stress. International Journal of Phytoremediation, 18, 33–40.
Huang X, Chaparro J M, Reardon K F, Zhang R, Shen Q, Vivanco J M. 2014. Rhizosphere interactions: Root exudates, microbes, and microbial communities. Botany-Botanique, 92, 67–275.
Jayawardana H A R K, Weerahewa H L D, Saparamadu M D J S. 2015. Enhanced resistance to anthracnose disease in chili pepper (Capsicum annuum L.) by amendment of the nutrient solution with silicon. Journal of Horticultural Science & Biotechnology, 90, 557–562.
Kim S G, Kim K W, Park E W, Choi D. 2002. Silicon-induced cell wall fortification of rice leaves: A possible cellular mechanism of enhanced host resistance to blast. Phytopathology, 92, 1095–1103.
Kurabachew H, Stahl F, Wydra K. 2013. Global gene expression of rhizobacteria-silicon mediated induced systemic resistance in tomato (Solanum lycopersicum) against Ralstonia solanacearum. Physiological and Molecular Plant Pathology, 84, 44–52.
Kurabachew H, Wydra K. 2014. Induction of systemic resistance and defense-related enzymes after elicitation of resistance by rhizobacteria and silicon application against Ralstonia solanacearum in tomato (Solanum lycopersicum). Crop Protection, 57, 1–7.
Liang Y, Sun W, Si J, Römheld V. 2005. Effect of foliar- and root-applied silicon on the enhancement of induced resistance in Cucumis sativus to powdery mildew. Plant Pathology, 54, 678–685
Liang Y, Sun W, Zhu Y, Christie P. 2007. Mechanisms of silicon-mediated alleviation of abiotic stresses in higher plants: A review. Environmental Pollution, 147, 422–428.
Liu M, Cai K, Chen Y, Luo S, Zhang Z, Lin W. 2014. Proteomic analysis of silicon-mediated resistance to Magnaporthe oryzae in rice (Oryza sativa L.). European Journal of Plant Pathology, 139, 579–592.
Ma J F, Yamaji N. 2006. Silicon uptake and accumulation in higher plants. Trends in Plant Science, 11, 392–397.
Ma J F, Yamaji N. 2008. Functions and transport of silicon in plants. Cellular and Molecular Life Sciences, 65, 3049–3057.
Ma J F, Yamaji N. 2015. A cooperative system of silicon transport in plants. Trends in Plant Science, 20, 435–442.
Ma J F, Yamaji N, Mitani N, Tamai K, Konishi S, Fujiwara T, Katsuhara M, Yano M. 2007. An efflux transporter of silicon in rice. Nature, 448, 209–212.
Mandal S, Kar I, Mukherjee A K, Acharya P. 2013. Elicitor-induced defense responses in Solanum lycopersicum against Ralstonia solanacearum. The Scientific World Journal, 2013, 561056.
Maqsood M A, Hussain S, Aziz T, Ashraf M. 2011. Wheat-exuded organic acids influence zinc release from calcareous soils. Pedosphere, 21, 657–665.
Polanco L R, Rodrigues F A, Nascimento K J T, Shulman P, Silva L C, Neves F W, Vale F X R. 2012. Biochemical aspects of bean resistance to anthracnose mediated by silicon. Annals of Applied Biology, 161, 140–150.
Raza W, Wang J, Wu Y, Ling N, Wei Z, Huang Q, Shen Q. 2016. Effects of volatile organic compounds produced by Bacillus amyloliquefaciens on the growth and virulence traits of tomato bacterial wilt pathogen Ralstonia solanacearum. Applied Microbiology and Biotechnology, 100, 7639–7650.
Resende R S, Rodrigues F A, Gomes R J, Nascimento K J T. 2013. Microscopic and biochemical aspects of sorghum resistance to anthracnose mediated by silicon. Annals of Applied Biology, 163, 114–123.
Le Roux M, Phiri E, Khan W, Sakiroglu M, Valentine A, Khan S. 2014. Expression of novel cytosolic malate dehydrogenases (cMDH) in Lupinus angustifolius nodules during phosphorus starvation. Journal of Plant Physiology, 171, 1609–1618.
Rudrappa T, Czymmek K J, Pare P W, Bais H P. 2008. Root-secreted malic acid recruits beneficial soil bacteria. Plant Physiology, 148, 1547–1556.
Sahebi M, Hanafi M M, Abdullah S N A, Rafii M Y, Azizi P, Nejat N, Idris A S. 2014. Isolation and expression analysis of novel silicon absorption gene from roots of mangrove (Rhizophora apiculata) via suppression subtractive hybridization. Biomed Research International, 2014, article 971985.
Seo S, Nakaho K, Hong S W, Takahashi H, Shigemori H, Mitsuhara I. 2016. L-Histidine induces resistance in plants to the bacterial pathogen Ralstonia solanacearum partially through the activation of ethylene signaling. Plant and Cell Physiology, 57, 1932–1942.
Shetty R, Frette X, Jensen B, Shetty N P, Jensen J D, Jorgensen H J, Newman M A. 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 Physiology, 157, 2194–2205.
Shetty R, Jensen B, Shetty N P, Hansen M, Hansen C W, Starkey K R, Jørgensen H J L. 2012. Silicon induced resistance against powdery mildew of roses caused by Podosphaera pannosa. Plant Pathology, 61, 120–131.
Silva I T, Rodrigues F Á, Oliveira J R, Pereira S C, Andrade C C L, Silveira P R, Conceição M M. 2010. Wheat resistance to bacterial leaf streak mediated by silicon. Journal of Phytopathology, 158, 253–262.
Silva W L D, Cruz M F A, Fortunato A A, Rodrigues F Á. 2015. Histochemical aspects of wheat resistance to leaf blast mediated by silicon. Scientia Agricola, 72, 322–327.
Song A L, Xue G F, Cui P Y, Fan F L, Liu H F, Yin C, Sun W C, Liang Y C. 2016. The role of silicon in enhancing resistance to bacterial blight of hydroponic- and soil-cultured rice. Scientific Reports, 6, 24640.
Steinkellner S, Mammerler R, Vierheilig H. 2008. Germination of Fusarium oxysporum in root exudates from tomato plants challenged with different Fusarium oxysporum strains. European Journal of Plant Pathology, 122, 395–401.
Sun L, Liang C, Chen Z, Liu P, Tian J, Liu G, Liao H. 2014. Superior aluminium (Al) tolerance of Stylosanthes is achieved mainly by malate synthesis through an Al-enhanced malic enzyme, SgME1. New Phytologist, 202, 209–219.
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. European Journal of Plant Pathology, 128, 39–49.
Takahashi H, Nakaho K, Ishihara T, Ando S, Wada T, Kanayama Y, Asano S, Yoshida S, Tsushima S, Hyakumachi M. 2014. Transcriptional profile of tomato roots exhibiting Bacillus thuringiensis-induced resistance to Ralstonia solanacearum. Plant Cell Reports, 33, 99–110.
Tan S, Yang C, Mei X, Shen S, Raza W, Shen Q, Xu Y. 2013. The effect of organic acids from tomato root exudates on rhizosphere colonization of Bacillus amyloliquefaciens T-5. Applied Soil Ecology, 64, 15–22.
Tesfagiorgis H B, Laing M D, Annegarn H J. 2014. Evaluation of biocontrol agents and potassium silicate for the management of powdery mildew of zucchini. Biological Control, 73, 8–15.
Vivancos J, Labbé C, Menzies J G, Bélanger R R. 2015. Silicon-mediated resistance of Arabidopsis against powdery mildew involves mechanisms other than the salicylic acid (SA)-dependent defence pathway. Molecular Plant Pathology, 16, 572–582.
Wang L, Cai K, Chen Y, Wang G. 2013. Silicon-mediated tomato resistance against Ralstonia solanacearum is associated with modification of soil microbial community structure and activity. Biological Trace Element Research, 152, 275–283.
Wu K, Su L, Fang Z, Yuan S, Wang L, Shen B, Shen Q. 2017. Competitive use of root exudates by Bacillus amyloliquefaciens with Ralstonia solanacearum decreases the pathogenic population density and effectively controls tomato bacterial wilt. Scientia Horticulturae, 218, 132–138.
Wu K, Yuan S, Xun G, Shi W, Pan B, Guan H, Shen B, Shen Q. 2015. Root exudates from two tobacco cultivars affect colonization of Ralstonia solanacearum and the disease index. European Journal of Plant Pathology, 141, 667–677.
Yuan J, Zhang N, Huang Q, Raza W, Li R, Vivanco J M, Shen Q. 2015. Organic acids from root exudates of banana help root colonization of PGPR strain Bacillus amyloliquefaciens NJN-6. Scientific Reports, 5, 13438.
Zhang C, Wang L, Zhang W, Zhang F. 2013. Do lignification and silicification of the cell wall precede silicon deposition in the silica cell of the rice (Oryza sativa L.) leaf epidermis? Plant and Soil, 372, 137–149.
Zhang G, Cui Y, Ding X, Dai Q. 2013. Stimulation of phenolic metabolism by silicon contributes to rice resistance to sheath blight. Journal of Plant Nutrition and Soil Science, 176, 118–124.
Zhang N, Yang D, Wang D, Miao Y, Shao J, Zhou X, Xu Z, Li, Q, Feng H, Li S, Shen Q, Zhang R. 2015. Whole transcriptomic analysis of the plant-beneficial rhizobacterium Bacillus amyloliquefaciens SQR9 during enhanced biofilm formation regulated by maize root exudates. BMC Genomics, 16, 685.