Advertisement

Silicon influences growth and mycorrhizal responsiveness in strawberry plants

  • Roghieh Hajiboland
  • Narges Moradtalab
  • Nasser Aliasgharzad
  • Zarrin Eshaghi
  • Javad Feizy
Research Article
  • 62 Downloads

Abstract

Effect of silicon (Si) on the response of strawberry (Fragaria × ananassa var. Parus) plants to arbuscular mycorrhizal fungus (AMF) was studied under growth chamber conditions. Plants were grown in perlite irrigated with nutrient solution without (− Si) or with (+ Si) 3 mmol L−1 Si (~ 84 mg L−1 Si as Na2SiO3) in the absence (− AMF) or presence (+ AMF) of fungus. Dry matter production, root colonization rate, photosynthesis rate and water relation parameters were all improved by both Si and AMF, and the highest amounts were achieved by + Si + AMF treatment. Mycorrhizal effectiveness increased by Si treatment associated with higher Si concentration in the + AMF plants. Leaf concentrations of total soluble and cell wall-bound phenolics were increased by Si accompanied by the enhanced activity of phenylalanine ammonia lyase, but not polyphenol oxidase. Profile of phenolics compound revealed that gallic acid, caffeic acid, epicatechin, chlorogenic acid, ellagic acid and kaempferol increased by both Si and AMF treatments, while p-coumaric acid decreased. In addition to vegetative growth, both treatments improved fruit yield and its quality parameters. Our results showed that Si and AMF acted in a synergistic manner and improved growth and biochemical parameters in strawberry plants. However, the mechanism for Si-mediated increase of mycorrhizal effectiveness is not known, thereby needing further elucidation.

Keywords

Silicon Mycorrhizal effectiveness Fragaria × ananassa Rhizophagus clarus Rhizophagus intraradices Glomus versiform 

Abbreviations

AMF

Arbuscular mycorrhizal fungus

CW

Cell wall

PAL

Phenylalanine ammonia-lyase

POD

Peroxidase

PPO

Polyphenol oxidase

RWC

Relative water content

Si

Silicon

Notes

Acknowledgements

The authors would like to thank Dr G. Neumann (University of Hohenheim, Germany) for providing facility of Si analysis and Dr H.R. Beheshti (Testa Quality Control Laboratory, North-East Food Industrial Technology and Biotechnology Park, Mashhad, Iran) and Dr M.S. Nabavi (Department of Agriculture, Payame Noor University, Tehran, Iran) for their assistance in the HPLC analysis.

Authors’ contribution

RH: Project supervisor, responsible for experimental design, interpretation of results, writer of the manuscript. NM: Cultivation of plants, performing all analyses; NA: Project co-supervisor, providing fungal inoculum, involvement in the writing and correction of the paper; ZE: Providing facility and assistance in the HPLC analysis; JF: Providing facility and assistance in the HPLC analysis.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Amil-Ruiz F, Blanco-Portales R, Muñoz-Blanco J, Caballero JL (2011) The strawberry plant defense mechanism: a molecular review. Plant Cell Physiol 52:1873–1903CrossRefPubMedGoogle Scholar
  2. Babu RC, Pathan MS, Blum A, Nguyen HT (1999) Comparison of measurement methods of osmotic adjustment in rice cultivars. Crop Sci 39:150–158CrossRefGoogle Scholar
  3. Borkowska B (2002) Growth and photosynthetic activity of micropropagated strawberry plants inoculated with endomycorrhizal fungi (AMF) and growing under drought stress. Acta Physiol Plant 24:365–370CrossRefGoogle Scholar
  4. Broadley M, Brown P, Cakmak I, Ma JF, Rengel Z, Zhao F (2012) Beneficial elements. In: Marschner P (ed) Marschner’s mineral nutrition of higher plants. Elsevier, Oxford, pp 249–269CrossRefGoogle Scholar
  5. Castellanos-Morales V, Villegas J, Wendelin S, Vierheilig H, Eder R, Cárdenas-Navarro R (2010) Root colonisation by the arbuscular mycorrhizal fungus Glomus intraradices alters the quality of strawberry fruits (Fragaria × ananassa Duch.) at different nitrogen levels. J Sci Food Agric 90:1774–1782PubMedGoogle Scholar
  6. Clark RB, Zeto SK (2000) Mineral acquisition by arbuscular mycorrhizal plants. J Plant Nutr 23:867–902CrossRefGoogle Scholar
  7. Costa FB, Duarte PS, Puschmann R, Finger FL (2011) Quality of fresh-cut strawberry. Hortic Bras 29:477–484CrossRefGoogle Scholar
  8. Etesami H, Jeong BR (2018) Silicon (Si): review and future prospects on the action mechanisms in alleviating biotic and abiotic stresses in plants. Ecotox Environ Safe 147:881–896CrossRefGoogle Scholar
  9. Fawe A, Abou-zaid M, Menzies JG, Bélanger RR (1998) Silicon-mediated accumulation of flavonoid phytoalexins in cucumber. Phytopathology 88:396–401CrossRefPubMedGoogle Scholar
  10. García-garrido JM, Ocampo JA (2002) Regulation of the plant defense response in arbuscular mycorrhizal symbiosis. J Exp Bot 53:1377–1386CrossRefPubMedGoogle Scholar
  11. Garg N, Bhandari P (2016) Silicon nutrition and mycorrhizal inoculations improve growth, nutrient status, K+/Na+ ratio and yield of Cicer arietinum L. genotypes under salinity stress. Plant Growth Regul 78:371–387CrossRefGoogle Scholar
  12. Ghaderi N, Normohammadi S, Javadi T (2015) Morpho-physiological responses of strawberry (Fragaria × ananassa) to exogenous salicylic acid application under drought stress. J Agric Sci Technol 17:167–178Google Scholar
  13. Giampieri F, Alvarez-Suarez JM, Battino M (2014) Strawberry and human health: effects beyond antioxidant activity. J Agric Food Chem 62:3867–3876CrossRefPubMedGoogle Scholar
  14. Giovanetti M, Mosse B (1980) An evaluation of techniques for measuring vesicular–arbuscular mycorrhizal infection in roots. New Phytol 84:489–500CrossRefGoogle Scholar
  15. Giusti MM, Wrolstad RE (2001) Characterization and measurement of anthocyanins by UV–visible spectroscopy. In: Wrolstad RE, Acree TE, An H, Decker EA, Pennere MH, Reid DS, Schwartz SJ, Shoemaker CF, Sporns P (eds) Current protocol in food analytical chemistry. Wiley, New York, pp F1.2.1–F.1.2.13Google Scholar
  16. Grandmaison J, Olah GM, Van Calsteren MR, Furlan V (1993) Characterization and localization of plant phenolics likely involved in the pathogen resistance expressed by endomycorrhizal roots. Mycorrhiza 3:155–164CrossRefGoogle Scholar
  17. Guntzer F, Keller C, Meunier JD (2012) Benefits of plant silicon for crops: a review. Agron Sustain Dev 32:201–213CrossRefGoogle Scholar
  18. Hajiboland R (2012) Effect of micronutrient deficiencies on plant stress responses. In: Ahmad P, Prasad MNV (eds) Abiotic stress responses in plants. Springer, New York, pp 283–329CrossRefGoogle Scholar
  19. Hajiboland R (2013) Role of arbuscular mycorrhiza in amelioration of salinity. In: Ahmad P, Azzoz MM, Prasad MNV (eds) Salt stress in plants, signaling, omics and adaptations. Springer, New York, pp 301–354CrossRefGoogle Scholar
  20. Hajiboland R, Bahrami-rad S, Bastani S (2013) Phenolics metabolism in boron-deficient tea (Camellia sinensis) plants. Acta Biol Hung 64:196–206CrossRefPubMedGoogle Scholar
  21. Hajiboland R, Bahrami-rad S, Poschenrieder C (2017a) Silicon modifies both local and systemic responses to mechanical stress in tobacco leaves. Biol Plant 61:187–191CrossRefGoogle Scholar
  22. Hajiboland R, Moradtalab N, Eshaghi Z, Feizy J (2017b) Effect of silicon supplementation on growth and metabolism of strawberry plants at three developmental stages. N Z J Crop Hortic Sci 46:144–161CrossRefGoogle Scholar
  23. Hassan S, Mathesius U (2012) The role of flavonoids in root–rhizosphere signaling: opportunities and challenges for improving plant–microbe interactions. J Exp Bot 63:3429–3444CrossRefPubMedGoogle Scholar
  24. Helrich K (1990) Official methods of analysis, 15th edn. Association of Official Analytical Chemists (AOAC), ArlingtonGoogle Scholar
  25. Inanaga S, Okasaka A (1995) Calcium and silicon binding compounds in cell walls of rice shoots. Soil Sci Plant Nutr 4:103–110CrossRefGoogle Scholar
  26. Jaiswal PC (2004) Soil, plant and water analysis. Kalyani Publishers, New DelhiGoogle Scholar
  27. Janos DP (2007) Plant responsiveness to mycorrhizas differs from dependence upon mycorrhizas. Mycorrhiza 17:75–91CrossRefPubMedGoogle Scholar
  28. Jugdaohsingh R, Kinrade SD, Powell JJ (2008) Is there a biochemical role for silicon? In: Collery P, Maymard I, Thephanides T, Khassanova L, Collery T (eds) Metal ions in biology and medicine, vol 10. John Libbey Eurotext, Montrouge, pp 45–55Google Scholar
  29. Khaosaad T, Krenn L, Medjakovic S, Ranner A, Lössl A, Nell M et al (2008) Effect of mycorrhization on the isoflavone concentration and the phytoestrogen activity of red clover. J Plant Physiol 165:1161–1167CrossRefPubMedGoogle Scholar
  30. Klopotek Y, Otto K, Böhm V (2005) Processing strawberries to different products alters contents of vitamin C, total phenolics, total anthocyanins, and antioxidant capacity. J Agric Food Chem 53:5640–5646CrossRefPubMedGoogle Scholar
  31. Larose G, Chenevert R, Moutoglis P, Gagne S, Piché Y, Vierheilig H (2002) Flavonoid levels in roots of Medicago sativa are modulated by the developmental stage of the symbiosis and the root colonizing arbuscular mycorrhizal fungus. J Plant Physiol 159:1329–1339CrossRefGoogle Scholar
  32. Maksimovic JD, Bogdanovic J, Maksimovic V, Nikolic M (2007) Silicon modulates the metabolism and utilization of phenolic compounds in cucumber (Cucumis sativus L.) grown at excess manganese. J Plant Nutr Soil Sci 170:739–744CrossRefGoogle Scholar
  33. Mandal SM, Chakraborty D, Dey S (2010) Phenolic acids act as signaling molecules in plant-microbe symbioses. Plant Signal Behav 5:359–368CrossRefPubMedPubMedCentralGoogle Scholar
  34. Merryweather JW, Fitter AH (1991) A modified method for elucidating the structure of the fungal partner in a vesicular ± arbuscular mycorrhiza. Mycol Res 95:1435–1437CrossRefGoogle Scholar
  35. Miyake Y, Takahashi E (1986) Effect of silicon on the growth and fruit production of strawberry plants in a solution culture. Soil Sci Plant Nutr 32:321–326CrossRefGoogle Scholar
  36. Nelwamondo A, Dakora FD (1999) Silicon promotes nodule formation and nodule function in symbiotic cowpea (Vigna unguiculata). New Phytol 142:463–467CrossRefGoogle Scholar
  37. Nour V, Trandafir I, Cosmulescu S (2013) HPLC determination of phenolic acids, flavonoids and juglone in walnut leaves. J Chromatogr Sci 51:883–890CrossRefPubMedGoogle Scholar
  38. Panico AM, Garufi F, Nitto S, Di Mauro R, Longhitano RC, Magrì G, De Guidi G (2009) Antioxidant activity and phenolic content of strawberry genotypes from Fragaria × ananassa. Pharm Biol 47:203–208CrossRefGoogle Scholar
  39. Passardi F, Cosio C, Penel C, Dunand C (2005) Peroxidases have more functions than a Swiss army knife. Plant Cell Rep 24:255–265CrossRefPubMedGoogle Scholar
  40. Porcel R, Aroca R, Ruiz-Lozano JM (2012) Salinity stress alleviation using arbuscular mycorrhizal fungi. A review. Agron Sustain Dev 32:181–200CrossRefGoogle Scholar
  41. Smith SE, Read DJ (2008) Mycorrhizal symbiosis. Academic Press, San DiegoGoogle Scholar
  42. Steinkellner S, Lendzemo V, Langer I, Schweiger P, Khaosaad T, Toussaint JP, Vierheilig H (2007) Flavonoids and strigolactones in root exudates as signals in symbiotic and pathogenic plant-fungus interactions. Molecules 12:1290–1306CrossRefPubMedGoogle Scholar
  43. Swain T, Hillis EE (1959) The phenolic constituents of Prunus domestica I. The quantitative analysis of phenolic constituents. J Sci Food Agric 10:63–68CrossRefGoogle Scholar
  44. Tawaraya K (2003) Arbuscular mycorrhizal dependency of different plant species and cultivars. Soil Sci Plant Nutr 49:655–668CrossRefGoogle Scholar
  45. Van Bockhaven J, De Vleesschauwer D, Höfte M (2012) Towards establishing broad-spectrum disease resistance in plants: silicon leads the way. J Exp Bot 64:1281–1293CrossRefPubMedGoogle Scholar
  46. Vierheilig H (2004) Regulatory mechanisms during the plant—arbuscular mycorrhizal fungus interaction. Can J Bot 82:1166–1176CrossRefGoogle Scholar
  47. Yemm EW, Cocking EC (1955) The determination of amino acids with ninhydrin. Analyst 80:209–213CrossRefGoogle Scholar
  48. Yemm EW, Willis AJ (1954) The estimation of carbohydrates extracts by anthrone. Biochem J 57:508–514CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Prof. H.S. Srivastava Foundation for Science and Society 2018

Authors and Affiliations

  1. 1.Center of Excellence for BiodiversityUniversity of TabrizTabrizIslamic Republic of Iran
  2. 2.Department of Plant ScienceUniversity of TabrizTabrizIslamic Republic of Iran
  3. 3.Department of Soil ScienceUniversity of TabrizTabrizIslamic Republic of Iran
  4. 4.Department of AgriculturePayame Noor UniversityTehranIslamic Republic of Iran
  5. 5.Research Institute of Food Science and TechnologyMashhadIslamic Republic of Iran

Personalised recommendations