Abstract
Silicon (Si) has a physical barrier effect on plant tissues, decreasing nematode infection in different crops. Notwithstanding, research on lettuce is lacking, especially regarding the chemical mechanisms of action of this beneficial element. This study evaluated the effect of Si supply on lettuce plants infested with 0, 6000, and 12,000 eggs and second stage juveniles of Meloidogyne incognita, both in the absence and in the presence of Si (2 mM) in the nutrient solution. Silicon increased phenolic compounds and ascorbic acid, reducing M. incognita population and decreasing oxidative stress. The element also increased chlorophyll content and the quantum efficiency of photosystem II (FV/FM), favoring lettuce growth and production. The use of Si decreased the number of nematodes and affected their reproduction, decreasing the number of eggs and galls on lettuce roots. This indicates that Si may serve as a sustainable alternative for the control of M. incognita. The benefit of using Si appears to be due to the combined effect chemical action from the increase in phenolic compounds and ascorbic acid in plant tissues, improving plant physiology.
Graphical abstract
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abad P, Gouzy J, Aury JM et al (2008) Genome sequence of the metazoan plant-parasitic nematode Meloidogyne incognita. Nat Biotechnol 26:909–915. https://doi.org/10.1038/nbt.1482
Aksakal O, Algur OF, Icoglu Aksakal F, Aysin F (2017) Exogenous 5-aminolevulinic acid alleviates the detrimental effects of UV-B stress on lettuce (Lactuca sativa L) seedlings. Acta Physiol Plant 39:55. https://doi.org/10.1007/s11738-017-2347-3
de Alves R, C, Nicolau MCM, Checchio MV, et al (2020) Salt stress alleviation by seed priming with silicon in lettuce seedlings: An approach based on enhancing antioxidant responses. Bragantia 79:19–29. https://doi.org/10.1590/1678-4499.20190360
Amaral G, Bushee J, Cordani UG et al (2013) Integrated management and biocontrol of vegetable and grain crops nematodes. J Petrol 369:1689–1699. https://doi.org/10.1017/CBO9781107415324.004
AOAC - Chemists O methods of analysis of the association of official analytical (1980) Analytica Chimica Acta: Preface. Anal Chim Acta. https://doi.org/10.1016/j.aca.2005.05.035
Arrigoni O (1979) A biological defense mechanism in plant. In: LAMurT F, TAvt CE, 8 edn. London and New York, pp 457–467
Asgari F, Majd A, Jonoubi P, Najafi F (2018) Effects of silicon nanoparticles on molecular, chemical, structural and ultrastructural characteristics of oat (Avena sativa L.). Plant Physiol Biochem 127:152–160. https://doi.org/10.1016/j.plaphy.2018.03.021
Ashfaque F, Inam A, Inam A et al (2017) Response of silicon on metal accumulation, photosynthetic inhibition and oxidative stress in chromium-induced mustard (Brassica juncea L.). South Afr J Bot 111:153–160. https://doi.org/10.1016/j.sajb.2017.03.002
Barbosa JC, Maldonado Júnior W (2015) Experimentação agronômica & Agroestat - Sistema para análises de ensaios agronômicos, 1th
Coolen WA, D’Herde CJ (1972) A method for quantitative extration of nematodes from plant tissue. Ghent State Nematol end Entomol Res Stn 77
da Silva DL, de Mello PR, Tenesaca LFL et al (2021a) Silicon attenuates calcium deficiency by increasing ascorbic acid content, growth and quality of cabbage leaves. Sci Rep 11:1–9. https://doi.org/10.1038/s41598-020-80934-6
da Silva DL, de Prado RM, Tenesaca LFL, et al (2021b) Silicon attenuates calcium deficiency in rocket plants by increasing the production of non-enzymatic antioxidants compounds. Sci Hortic (amsterdam) 285:110169. https://doi.org/10.1016/j.scienta.2021.110169
Dias-arieira CR, Pl T, Chiamolera FM et al (2012) Comunicação científica, pp 322–326
Dionisio-Sese ML, Tobita S (1998) Antioxidant responses of rice seedlings to salinity stress. Plant Sci 135:1–9. https://doi.org/10.1016/S0168-9452(98)00025-9
Dugui-Es C, Pedroche N, Villanueva L et al (2010) Management of root knot nematode, Meloidogyne incognita in cucumber (Cucumis sativus) using silicon. Commun Agric Appl Biol Sci 75:497–505
Eisenback JD, Hirschmann H, Sasser JN, Triantaphyllou AC (1981) Guide to the four most common species of root-knot nematodes (Meloidogyne species) with a pictorial key
Esbenshade PR, Triantaphyllou AC (1990) Isozyme phenotypes for the identification of Meloidogyne species. J Nematol 22:10–15
Faiq H, Bibi N, Zia Z et al (2018) Silicon mitigates biotic stresses in crop plants: a review. Crop Prot 104:21–34. https://doi.org/10.1016/j.cropro.2017.10.008
Fawe A, Menzies JG, Chérif M, Bélanger RR (2001) Chapter 9 silicon and disease resistance in dicotyledons. Stud Plant Sci 8:159–169. DOI: https://doi.org/10.1016/S0928-3420(01)80013-6
Franchin Sgorlon L, Silva EHC, Soares RS et al (2018) Host status of crispy-leaf lettuce cultivars to root-knot nematodes. Biosci J 34:1319–1325. https://doi.org/10.14393/BJ-v34n5a2018-39387
Galati VC, Guimarães JER, Marques KM et al (2015) Aplicação de silício, em hidroponia, na conservação pós-colheita de alface americana ‘Lucy Brown’ minimamente processada. Cienc Rural 45:1932–1938. https://doi.org/10.1590/0103-8478cr20140334
Guimarães LMP, Pedrosa EMR, Coelho RSB et al (2010) Efficiency and enzymatic activity elicited by methyl jasmonate and potassium silicate on sugarcane under Meloidogyne incognita parasitism. Summa Phytopathol 36:11–15. https://doi.org/10.1590/s0100-54052010000100001
Hajiboland R, Moradtalab N, Eshaghi Z, Feizy J (2018) Effect of silicon supplementation on growth and metabolism of strawberry plants at three developmental stages. New Zeal J Crop Hortic Sci 46:144–161. https://doi.org/10.1080/01140671.2017.1373680
Hasanuzzaman M, Nahar K, Anee TI, Fujita M (2017) Exogenous silicon attenuates cadmium-induced oxidative stress in brassica napus L. by modulating asa-gsh pathway and glyoxalase system. Front Plant Sci 8:1–9. https://doi.org/10.3389/fpls.2017.01061
Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. Circ Calif Agric Exp Stn 347:32
Holbein J, Grundler FMW, Siddique S (2016) Plant basal resistance to nematodes: an update. J Exp Bot 67:2049–2061. https://doi.org/10.1093/jxb/erw005
Hussain M, Kamran M, Singh K et al (2016) Response of selected okra cultivars to Meloidogyne incognita. Crop Prot 82:1–6. https://doi.org/10.1016/j.cropro.2015.12.024
Hussey RS, Barker K (1973) Comparison of methods of collecting inocula of Meloidogyne spp. including a new technique. Plant Dis Report 57:1025–1028
Inanaga S, Okasaka A (1995) Calcium and silicon binding compounds in cell walls of rice shoots. Soil Sci Plant Nutr 41:103–110. https://doi.org/10.1080/00380768.1995.10419563
Jones JT, Haegeman A, Danchin EGJ et al (2013) Top 10 plant-parasitic nematodes in molecular plant pathology. Mol Plant Pathol 14:946–961. https://doi.org/10.1111/mpp.12057
Khan MR, Siddiqui ZA (2020) Use of silicon dioxide nanoparticles for the management of Meloidogyne incognita, Pectobacterium betavasculorum and Rhizoctonia solani disease complex of beetroot (Beta vulgaris L.). Sci Hortic (amsterdam) 265:109211. https://doi.org/10.1016/j.scienta.2020.109211
Korndörfer GH, Pereira HS, Nola A (2004) Análise de silício: solo, planta e fertilizante. Universidade Federal de Uberlândia, Uberlândia
Kraska JE, Breitenbeck GA (2010) Simple, robust method for quantifying silicon in plant tissue. Commun Soil Sci Plant Anal 41:2075–2085. https://doi.org/10.1080/00103624.2010.498537
Liang YC, Sun WC, Si J, Römheld V (2005) Effects 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
Lichtenthaler HK, Buschmann C, Knapp M (2005) How to correctly determine the different chlorophyll fluorescence parameters and the chlorophyll fluorescence decrease ratio RFd of leaves with the PAM fluorometer. Photosynthetica 43:379–393. https://doi.org/10.1007/s11099-005-0062-6
Ma D, Sun D, Wang C 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. https://doi.org/10.1007/s00344-015-9500-2
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
Maareg, M. F., El-Gindi, A. Y., Gohar, I. M.A. and AKM (2014) An ecofriendly root- knot nematode pest management strategy on sugarbeet. Egypt J Agronematol 13:146–159. https://doi.org/10.21608/EJAJ.2014.63691
Maghsoudi K, Emam Y, Pessarakli M (2016) Effect of silicon on photosynthetic gas exchange, photosynthetic pigments, cell membrane stability and relative water content of different wheat cultivars under drought stress conditions. J Plant Nutr 39:1001–1015. https://doi.org/10.1080/01904167.2015.1109108
Mahalik JK, Sahoo NK (2016) Effect of inoculum density of root knot nematode (Meloidogyne incognita) on okra (Abelmoschus esculentus L.). Int J Plant Prot 9:603–607. https://doi.org/10.15740/has/ijpp/9.2/603-607
Mitani N, Yamaji N, Ago Y et al (2011) Isolation and functional characterization of an influx silicon transporter in two pumpkin cultivars contrasting in silicon accumulation. Plant J 66:231–240. https://doi.org/10.1111/j.1365-313X.2011.04483.x
Moens M, Perry RN, Starr JL (2009) Meloidogyne species—A diverse group of novel and important plant parasites. Root-Knot Nematodes. https://doi.org/10.1079/9781845934927.0001
Mou B (2012) Nutritional quality of lettuce. Curr Nutr Food Sci 8:177–187. https://doi.org/10.2174/157340112802651121
Oliveira DF, Costa VA, Terra WC et al (2019) Impact of phenolic compounds on Meloidogyne incognita in vitro and in tomato plants. Exp Parasitol 199:17–23. https://doi.org/10.1016/j.exppara.2019.02.009
Oliveira RM, Ribeiro RCF, Xavier AA et al (2012) Effect of calcium and magnesium silicate on Meloidogyne javanica reproduction and development of banana Prata-Anã seedlings. Rev Bras Frutic 34:409–415. https://doi.org/10.1590/S0100-29452012000200013
Ornat C, Sorribas FJ (2008) Integrated management of root-knot nematodes in mediterranean horticultural crops. In: Ciancio A, Mukerji KG (eds) Integrated management and biocontrol of vegetable and grain crops nematodes. Integrated Management of Plant Pests and Diseases, Springer, Dordrecht. 2:295–319. https://doi.org/10.1007/978-1-4020-6063-2_14
Osman GY (1993) Effect of amino acids and ascorbic acid on Meloidogyne javanica Chitw. (Tylenchidae, Nematoda). Anzeiger Für Schädlingskd Pflanzenschutz Umweltschutz 66:140–142. https://doi.org/10.1007/BF01906844
Pontigo S, Ribera A, Gianfreda L et al (2015) Silicon in vascular plants: Uptake, transport and its influence on mineral stress under acidic conditions. Planta 242:23–37. https://doi.org/10.1007/s00425-015-2333-1
Richmond KE, Sussman M (2003) Got silicon? The non-essential beneficial plant nutrient. Curr Opin Plant Biol 6:268–272. https://doi.org/10.1016/S1369-5266(03)00041-4
Rodrigues FÁ, Jurick WM, Datnoff LE, et al (2005) Silicon influences cytological and molecular events in compatible and incompatible rice-Magnaporthe grisea interactions. Physiol Mol Plant Pathol 66:144–159. https://doi.org/10.1016/j.pmpp.2005.06.002
Rokayya S, Li CJ, Zhao Y et al (2013) Cabbage (Brassica oleracea L. var. capitata) phytochemicals with antioxidant and anti-inflammatory potential. Asian Pacific J Cancer Prev 14:6657–6662. https://doi.org/10.7314/APJCP.2013.14.11.6657
Santos LB, de Souza Júnior JP, de Mello PR et al (2021) Silicon allows halving Cadusafos dose to control Meloidogyne incognita and increase cotton development. SILICON. https://doi.org/10.1007/s12633-021-01126-z
Sato K, Kadota Y, Shirasu K (2019) Plant immune responses to parasitic nematodes. Front Plant Sci 10:1–14. https://doi.org/10.3389/fpls.2019.01165
Shahnaz G, Shekoofeh E, Kourosh D, Moohamadbagher B (2011) Interactive effects of silicon and aluminum on the malondialdehyde (MDA), proline, protein and phenolic compounds in borago officinalis L. J Med Plant Res 5:5818–5827
Siddiqi MY, Glass ADM (1981) Utilization index: A modified approach to the estimation and comparison of nutrient utilization efficiency in plants. J Plant Nutr 4:289–302. https://doi.org/10.1080/01904168109362919
SigmaPlot Version 12.5 (2012) Systat Software Inc.
Silva RV, Oliveira RDL, Nascimento KJT, Rodrigues FA (2010) Biochemical responses of coffee resistance against Meloidogyne exigua mediated by silicon. Plant Pathol 59:586–593. https://doi.org/10.1111/j.1365-3059.2009.02228.x
Singleton VL, Rossi JA (1965) Colorimetry of Total Phenolics with Phosphomolybdic-Phosphotungstic Acid Reagents. Am J Enol Vitic 16:144–158
Song A, Li P, Fan F, et al (2014) The effect of silicon on photosynthesis and expression of its relevant genes in rice (Oryza sativa L.) under high-zinc stress. https://doi.org/10.1371/journal.pone.0113782
Southey J (1970) Laboratory for work with plant and soil nematodes. Minist Agric Fisch 5:148
Souza E, Silva N, Silva M, Siciliano S (2019a) Response of lettuce cultivars to Meloidogyne javanica and Meloidogyne incognita race 1 and 2. Rev Cienc Agron 50:100–106. https://doi.org/10.5935/1806-6690.20190012
Souza JZ, De Mello PR, de Silva SL, O, et al (2019b) Silicon leaf fertilization promotes biofortification and increases dry matter, ascorbate content, and decreases post-harvest leaf water loss of chard and kale. Commun Soil Sci Plant Anal 50:164–172. https://doi.org/10.1080/00103624.2018.1556288
Steel RGD, Torrie JH, Dickey D (1997) Principles and procedures of statistics: a biometrical approach 3rd ed McGraw-Hill New York NY, USA
Taylor DP, Netscher C (1968) An improved technique for preparing perineal patterns of Meloidogyne spp. Nematologica 54:1–343
Voogt W, Sonneveld C (2001) Chapter 6 silicon in horticultural crops grown in soilless culture. Stud Plant Sci 8:115–131. https://doi.org/10.1016/S0928-3420(01)80010-0
Wilcken S, Marchin M, Silva N (2005) Resistência de Alface do Tipo Americana a Meloidogyne incognita raça 2
Zhan LP, Peng DL, Wang XL et al (2018) Priming effect of root-applied silicon on the enhancement of induced resistance to the root-knot nematode Meloidogyne graminicola in rice. BMC Plant Biol 18:1–12. https://doi.org/10.1186/s12870-018-1266-9
Acknowledgements
The Coordenadoria de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), Brazil, Code 001, and Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) process 2020/00195-0, for the scholarship awarded to the first author.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Competing interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Additional information
Communicated by Ivan Hiltpold.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
de Souza Alonso, T.A., da Silva, D.L., de Mello Prado, R. et al. Silicon promotes the control of Meloidogyne incognita in lettuce by increasing ascorbic acid and phenolic compounds. J Pest Sci 95, 1453–1466 (2022). https://doi.org/10.1007/s10340-021-01470-4
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10340-021-01470-4