Abstract
Benzoic and cinnamic acid derivatives such as 3-phenylpropionic acid (PA) are the main autotoxins identified from cucumber root exudates. In this study, we investigated the effects of silicon (Si) supplemented on cucumber seed germination under PA-induced stress. Cucumber bud seedlings were harvested at 0, 4, 8, 12, 24, 36, and 48 h after treatment and assessed for plant growth, amylase activity and gene expression, and starch metabolism. Results revealed that PA significantly reduced the seed germination rate, seed vigor, radicle length, number of lateral roots, fresh weight, and soluble sugar content of cucumber bud seedlings. However, PA increased the starch content. The supplement of silicon promoted the growth of PA-treated plants and significantly increased the germination rate, seed vigor, and soluble sugar content of cucumber bud seedlings. Compared with those of the control plants, the levels and activities of α- (AMY) and β-amylase (BMY) during germination significantly decreased after PA treatment. The supplement of silicon significantly improved amylase activity, and total amylase and β-amylase activities reached maximum values at 36 h. PA significantly down-regulated the relative expression levels of AMY and BMY, whereas exogenous silicon significantly increased their transcript levels. These results suggest that supplement of Si alleviated cucumber autotoxicity caused by PA during seed germination at both the physiological and molecular levels.
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References
Akazawa T, Hara-Nishimura I (1985) Topographic aspects of biosynthesis, extracellular secretion, and intracellular storage of proteins in plant cells. Annu Rev Plant Biol 36:441–472
Asaduzzaman M, Asao T (2012) Autotoxicity in beans and their allelochemicals. Sci Hortic 134:26–31
Batish DR, Singh HP, Kaur S, Kohli RK, Yadav SS (2008) Caffeic acid affects early growth, and morphogenetic response of hypocotyl cuttings of mung bean (Phaseolus aureus). J Plant Physiol 165:297–305
Blum U (1996) Allelopathic interactions involving phenolic acids. J Nematol 28:259
Chen W, Yao XQ, Cai KZ, Chen JN (2011) Silicon alleviates drought stress of rice plants by improving plant water status, photosynthesis and mineral nutrient absorption. Biol Trace Elem Res 142:67–76
Chérif M, Asselin A, Bélanger RR (1994) Defense responses induced by soluble silicon in cucumber roots infected by Pythium spp. Phytopathology 84:236–242
Chon S, Choi S, Jung S, Jang H, Pyo B, Kim S (2002) Effects of alfalfa leaf extracts and phenolic allelochemicals on early seedling growth and root morphology of alfalfa and barnyard grass. Crop Prot 21:1077–1082
Dai A, Nie Y, Yu B, Li Q, Lu L, Bai J (2012) Cinnamic acid pretreatment enhances heat tolerance of cucumber leaves through modulating antioxidant enzyme activity. Environ Exp Bot 79:1–10
Ding J, Sun Y, Xiao CL, Shi K, Zhou YH, Yu JQ (2007) Physiological basis of different allelopathic reactions of cucumber and figleaf gourd plants to cinnamic acid. J Exp Bot 58:3765–3773
Epstein E (1994) The anomaly of silicon in plant biology. Proc Natl Acad Sci USA 91:11–17
Epstein E (1999) Silicon. Annu Rev Plant Biol 50:641–664
Epstein E (2009) Silicon: its manifold roles in plants. Ann Appl Biol 155:155–160
Feng JP, Shi QH, Wang XF, Wei M, Yang FJ, Xu HN (2010) Silicon supplementation ameliorated the inhibition of photosynthesis and nitrate metabolism by cadmium (Cd) toxicity in Cucumis sativus L. Sci Hortic 123:521–530
Golisz A, Sugano M, Fujii Y (2008) Microarray expression profiling of Arabidopsis thaliana L. in response to allelochemicals identified in buckwheat. J Exp Bot 59:3099–3109
Gong HJ, Zhu XY, Chen KM, Wang SM, Zhang CL (2005) Silicon alleviates oxidative damage of wheat plants in pots under drought. Plant Sci 169:313–321
Gonzalez VM, Kazimir J, Nimbal C, Weston LA, Cheniae GM (1997) Inhibition of a photosystem II electron transfer reaction by the natural product sorgoleone. J Agric Food Chem 45:1415–1421
Gottardi S, Iacuzzo F, Tomasi N, Cortella G, Manzocco L, Pinton R, Römheld V, Mimmo T, Scampicchio M, Dalla Costa L (2012) Beneficial effects of silicon on hydroponically grown corn salad (Valerianella locusta (L.) Laterr) plants. Plant Physiol Biochem 56:14–23
Hejl AM, Koster KL (2004) The allelochemical sorgoleone inhibits root H+-ATPase and water uptake. J Chem Ecol 30:2181–2191
Hejl AA, Einhellig FA, Rasmussen JA (1993) Effects of juglone on growth, photosynthesis, and respiration. J Chem Ecol 19:559–568
Hiradate S, Morita S, Furubayashi A, Fujii Y, Harada J (2005) Plant growth inhibition by cis-cinnamoyl glucosides and cis-cinnamic acid. J Chem Ecol 31:591–601
Inderjit, Duke SO (2003) Ecophysiological aspects of allelopathy. Planta 217:529–539
Iqbal Z, Hiradate S, Araya H, Fujii Y (2004) Plant growth inhibitory activity of Ophiopogon japonicus Ker-Gawler and role of phenolic acids and their analogues: a comparative study. Plant Growth Regul 43:245–250
Jacobsen JV, Hanson AD, Chandler PC (1986) Water stress enhances expression of an α-amylase gene in barley leaves. Plant Physiol 80:350–359
Jarvis SC (1987) The uptake and transport of silicon by perennial ryegrass and wheat. Plant Soil 97:429–437
Jones LHP, Handreck KA (1967) Silica in soils, plants, and animals. Adv Agron 19:107–149
Kaur S, Gupta AK, Kaur N (1998) Gibberellic acid and kinetin partially reverse the effect of water stress on germination and seedling growth in chickpea. Plant Growth Regul 25:29–33
Kaur S, Gupta AK, Kaur N (2000) Effect of GA3, kinetin and indole acetic acid on carbohydrate metabolism in chickpea seedlings germinating under water stress. Plant Growth Regul 30:61–70
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
Kim YH, Khan AL, Hamayun M, Kang SM, Beom YJ, Lee IJ (2011) Influence of short-term silicon application on endogenous physiohormonal levels of Oryza sativa L under wounding stress. Biol Trace Elem Res 144:1175–1185
Kim YH, Khan AL, Waqas M, Shim JK, Kim DH, Lee KY, Lee IJ (2013) Silicon application to rice root zone influenced the phytohormonal and antioxidant responses under salinity stress. J Plant Growth Regul 33:137–149
Kittock DL, Law AG (1968) Relationship of seedling vigor to respiration and tetrazolium chloride reduction by germinating wheat seeds. Agron J 60:286–288
Liang Y, Si J, Römheld V (2005a) Silicon uptake and transport is an active process in Cucumis sativus. New Phytol 167:797–804
Liang YC, Wong J, Wei L (2005b) Silicon-mediated enhancement of cadmium tolerance in maize (Zea mays L.) grown in cadmium contaminated soil. Chemosphere 58:475–483
Liang YC, Sun WC, Zhu YG, Christie P (2007) Mechanisms of silicon-mediated alleviation of abiotic stresses in higher plants: a review. Environ Pollut 147:422–428
Liang YC, Zhu J, Li ZJ, Chu GX, Ding YF, Zhang J, Sun WC (2008) Role of silicon in enhancing resistance to freezing stress in two contrasting winter wheat cultivars. Environ Exp Bot 64:286–294
Liu P, Yin LN, Wang SW, Zhang MJ, Deng XP, Zhang SQ, Tanaka K (2015) Enhanced root hydraulic conductance by aquaporin regulation accounts for silicon alleviated salt-induced osmotic stress in Sorghum bicolor L. Environ Exp Bot 111:42–51
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2–∆∆CT method. Methods 25:402–408
Ma JF (2004) Role of silicon in enhancing the resistance of plants to biotic and abiotic stresses. Soil Sci Plant Nutr 50:11–18
Ma JF, Yamaji N (2006) Silicon uptake and accumulation in higher plants. Trends Plant Sci 11:392–397
Ma JF, Tamai K, Yamaji N, Mitani N, Konishi S, Katsuhara M, Ishiguro M, Murata Y, Yano M (2006) A silicon transporter in rice. Nature 440:688–691
Ma J, Cai HM, He CW, Zhang WJ, Wang LJ (2015) A hemicellulose-bound form of silicon inhibits cadmium ion uptake in rice (Oryza sativa) cells. New Phytol 206(3):1063–1074
Maksimović JD, Mojović M, Maksimović V, Römheld V, Nikolic M (2012) Silicon ameliorates manganese toxicity in cucumber by decreasing hydroxyl radical accumulation in the leaf apoplast. J Exp Bot 63:2411–2420
Miller GN (1959) Use of dinitrosalicylic acid reagent for the determination of reducing sugar. Anal Chem 81:426–428
Moussa HR (2006) Influence of exogenous application of silicon on physiological response of salt-stressed maize (Zea mays L). Int J Agric Biol 8:293–297
Rajjou L, Duval M, Gallardo K, Catusse J, Bally J, Job C, Job D (2012) Seed germination and vigor. Annu Rev Plant Biol 63:507–533
Romero-Aranda MR, Jurado O, Cuartero J (2006) Silicon alleviates the deleterious salt effect on tomato plant growth by improving plant water status. J Plant Physiol 163:847–855
Rudrappa T, Bonsall J, Gallagher JL, Seliskar DM, Bais HP (2007) Root-secreted allelochemical in the noxious weed Phragmites australis deploys a reactive oxygen species response and microtubule assembly disruption to execute rhizotoxicity. J Chem Ecol 33:1898–1918
Sakamoto T, Murata N (2002) Regulation of the desaturation of fatty acids and its role in tolerance to cold and salt stress. Curr Opin Microbiol 5:206–210
Shi QH, Bao ZY, Zhu ZJ, He Y, Qian QQ, Yu JQ (2005) Silicon-mediated alleviation of Mn toxicity in Cucumis sativus in relation to activities of superoxide dismutase and ascorbate peroxidase. Phytochemistry 66:1551–1559
Shi Y, Zhang Y, Yao HJ, Wu JW, Sun H, Gong HJ (2014) Silicon improves seed germination and alleviates oxidative stress of bud seedlings in tomato under water deficit stress. Plant Physiol Biochem 78:27–36
Singh HP, Batish DR, Kohli RK (1999) Autotoxicity: concept, organisms, and ecological significance. Crit Rev Plant Sci 18:757–772
Song AL, Li ZJ, Zhang J, Xue GF, Fan FL, Liang YC (2009) Silicon-enhanced resistance to cadmium toxicity in Brassica chinensis L. is attributed to Si-suppressed cadmium uptake and transport and Si-enhanced antioxidant defense capacity. J Hazard Mater 172:74–83
Sonobe K, Hattori T, An P, Tsuji W, Eneji AE, Kobayashi S, Kawamura Y, Tanaka K, Inanaga S (2011) Effect of silicon application on sorghum root responses to water stress. J Plant Nutr 34:71–82
Soylemezoglu G, Demir K, Inal A, Gunes A (2009) Effect of silicon on antioxidant and stomatal response of two grapevine (Vitis vinifera L) rootstocks grown in boron toxic, saline and boron toxic-saline soil. Sci Hortic 123:240–246
Todaka D, Matsushima H, Morohashi Y (2000) Water stress enhances β-amylase activity in cucumber cotyledons. J Exp Bot 51:739–745
Tripathi DK, Singh VP, Kumar D, Chauhan DK (2012) Rice seedlings under cadmium stress: effect of silicon on growth, cadmium uptake, oxidative stress, antioxidant capacity and root and leaf structures. J Chem Ecol 28:281–291
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
Vasquez-Tello A, Zuily-Fodil Y, Thi AP, Da Silva JV (1990) Electrolyte and Pi leakages and soluble sugar content as physiological tests for screening resistance to water stress in Phaseolus and Vigna species. J Exp Bot 41:827–832
Wang X, Ou-yang C, Fan ZR, Gao S, Chen F, Tang L (2010) Effects of exogenous silicon on seed germination and antioxidant enzyme activities of Momordica charantia under salt stress. J Anim Plant Sci 6:700–708
Weitbrecht K, Mueller K, Leubner-Metzger G (2011) First off the mark: early seed germination. J Exp Bot 62:3289–3309
Ye SF, Yu JQ, Peng YH, Zheng JH, Zou LY (2004) Incidence of Fusarium wilt in Cucumis sativus L. is promoted by cinnamic acid, an autotoxin in root exudates. Plant Soil 263:143–150
Ye SF, Zhou YH, Sun Y, Zou LY, Yu JQ (2006) Cinnamic acid causes oxidative stress in cucumber roots, and promotes incidence of Fusarium wilt. Environ Exp Bot 56:255–262
Yin LN, Wang SW, Tanaka K, Fujihara S, Itai A, Den XP, Zhang SQ (2016) Silicon-mediated changes in polyamines participate in silicon-induced salt tolerance in Sorghum bicolor L. Plant Cell Environ 39(2):245–258
Yoshida S (1965) Chemical aspect of silicon in physiology of the rice plant. Bull Natl Agric Sci B 15:1–58
Yu JQ, Matsui Y (1994) Phytotoxic substances in root exudates of cucumber (Cucumis sativus L.). J Chem Ecol 20:21–31
Yu JQ, Matsui Y (1997) Effects of root exudates of cucumber (Cucumis sativus) and allelochemicals on ion uptake by cucumber seedlings. J Chem Ecol 23:817–827
Yu JQ, Shou SY, Qian YR, Zhu ZJ, Hu WH (2000) Autotoxic potential of cucurbit crops. Plant Soil 223:149–153
Zeid IM, Shedeed ZA (2006) Response of alfalfa to putrescine treatment under drought stress. Biol Plant 50:635–640
Zhang Y, Gu M, Xia XJ, Shi K, Zhou YH, Yu JQ (2009) Effects of phenylcarboxylic acids on mitosis, endoreduplication and expression of cell cycle-related genes in roots of cucumber (Cucumis sativus L.). J Chem Ecol 35:679–688
Zhang PY, Gao RG, Yang FJ, Wang XF, Wei M, Shi QH, Li Y (2014) Effects of silicon on photosynthetic characteristics and activity of antioxidant enzymes in continuous-cropped cucumber seedlings. Chin J Appl Ecol 25:1733–1738
Zhu YX, Gong HJ (2014) Beneficial effects of silicon on salt and drought tolerance in plants. Agron Sustain Dev 34:455–472
Zhu ZJ, Wei GQ, Li J, Qian QQ, Yu JQ (2004) Silicon alleviates salt stress and increases antioxidant enzymes activity in leaves of salt-stressed cucumber (Cucumis sativus L.). Plant Sci 167:527–533
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This research was financially supported by the National Natural Science Foundation of China (31260493) and the Special Fund for Agro-scientific Research in the Public Interest (201203002).
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Bu, R., Xiao, X., Liao, W. et al. Exogenous Si Alleviation of Autotoxicity in Cucumber (Cucumis sativus L.) Seed Germination is Correlated with Changes in Carbohydrate Metabolism. J Plant Growth Regul 37, 784–793 (2018). https://doi.org/10.1007/s00344-017-9773-8
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DOI: https://doi.org/10.1007/s00344-017-9773-8