Brazilian Journal of Botany

, Volume 42, Issue 1, pp 189–193 | Cite as

Arbuscular mycorrhizal fungi as biotechnology alternative to increase concentrate of secondary metabolites in Zea mays L.

  • Francineyde A. SilvaEmail author
  • Leonor C. Maia
  • Fábio S. B. Silva
Short Communication


Leaves of corn (Zea mays L.) produce secondary metabolism compounds characterizing them as an alternative source of animal food. Plants of this species establish mutualistic symbiosis with arbuscular mycorrhizal fungi (AMF) which provide an increase in the contents of bioactive compounds. These compounds have pharmacological properties and are important to the process of healing diseases. The objective of this paper was to establish whether the association of Z. mays with AMF increases the concentration of phenolic compounds in the leaves. After 70 days of growth, corn leaves were collected and their extract used for phytochemical analyses that included: soluble carbohydrates, proteins, phenols, flavonoids, and total tannins. Plants associated with Claroideoglomus etunicatum (W. N. Becker & Gerdemann) C. Walker & A. Schüssler (UFPE 06), Acaulospora longula Spain & N. C. Schenck (UFPE 21) and Dentiscutata heterogama (T.H. Nicolson & Gerd.) Sieverd., F.A. de Souza & Oehl (UFPE 19) presented an increase in the concentration of soluble carbohydrates of 153.7%, 86.6%, and 79.1%, respectively, in relation to the control. Concentration of flavonoids was higher in plants inoculated with A. longula comparing with the control, while the concentrations of phenols, tannins, and total proteins in the mycorrhizal treatments did not differ from the control. Use of mycorrhizal technology may represent an alternative to enhance the content of some foliar metabolites in Z. mays leading to the production of phytomass with greater phytochemical and nutritional qualities.


Flavonoids Glomeromycotina Maize Phytochemical 



The authors would like to thank the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq—National Council for Scientific and Technological Development) for providing research fellowships to LC Maia and FSB Silva.

Authors’ contributions

FAdaS carried out the evaluation of the experiments and preparation and writing of paper. FSBdaS and LCM contributed to preparation and writing of paper.

Compliance with ethical standards

Conflict of interest

The authors declare no conflict of interest.


  1. Adom KK, Liu RH (2002) Antioxidant activity of grains. J Agric Food Chem 50:6182–6187CrossRefGoogle Scholar
  2. Agra MF, Silva KN, Basílio IJLD, Freitas PF, Barbosa-Filho JM (2008) Survey of medicinal plants used in the region Northeast of Brazil. Rev Bras Farmacogn 18:472–508CrossRefGoogle Scholar
  3. Araújo TAS, Alencar NL, Amorim ELC, Albuquerque UP (2008) A new approach to study medicinal plants with tannins and flavonoids contents from the local knowledge. J Ethnopharmacol 120:72–80CrossRefGoogle Scholar
  4. Assistat (2017) Federal University of Campina Grande, Campina Grande, Paraíba, Brazil. Accessed 17 June 2009
  5. Baslam M, Garmendia I, Goicoechea N (2011) Arbuscular mycorrhizal fungi (AMF) Improved growth and nutritional quality of greenhouse-grown lettuce. J Agric Food Chem 59:5504–5515CrossRefGoogle Scholar
  6. Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254CrossRefGoogle Scholar
  7. Brito HO, Noronha EP, França LM, Brito LMO, Prado SA (2008) Análise da composição fitoquímica do extrato etanólico das folhas de Annona squamosa (ATA). Rev Bras Farm 89:180–184Google Scholar
  8. Ceccarelli N, Curadi M, Martelloni L, Sbrana C, Picciarelli P, Giovannetti M (2010) Mycorrhizal colonization impacts on phenolic content and antioxidant properties of artichoke leaves and flower heads two years after field transplant. Plant Soil 335:311–323CrossRefGoogle Scholar
  9. Coelho IR, Pedone-Bonfim MVL, Silva FSB, Maia LC (2014) Optimization of the production of mycorrhizal inoculum on substrate with organic fertilizer. Braz J Microbiol 45:1173–1178CrossRefGoogle Scholar
  10. Coppeta A, Lingua G, Berta G (2006) Effects of three AM fungi on growth, distribution of glandular hairs, and essential oil production in Ocimum basilicum L. var. genovese. Mycorrhiza 16:485–494CrossRefGoogle Scholar
  11. Dave S, Tarafdar JC (2011) Stimulatory synthesis of saponin by mycorrhizal fungi in safed musli (Chlorophytum borivilianum) tubers. Int Res J Agric Sci Soil Sci 1:137–141Google Scholar
  12. Dubois M, Guiles A, Hamilton JK, Rebers PA, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28:350–355CrossRefGoogle Scholar
  13. Eftekhari M, Alizadeh M, Ebrahimi P (2012) Evaluation of the total phenolics and quercetin content of foliage in mycorrhizal grape (Vitis vinifera L.) varieties and effect of postharvest drying on quercetin yield. Ind Crop Prod 38:160–165CrossRefGoogle Scholar
  14. Giovannetti M, Avio L, Barale R, Ceccarelli N, Cristofani R, Iezzi A, Mignolli F, Picciarelli P, Pinto B, Reali D, Sbrana C, Scarpato R (2012) Nutraceutical value and safety of tomato fruits produced by mycorrhizal plants. Br J Nutr 107:241–251CrossRefGoogle Scholar
  15. González-Muñoz A, Quesille-Villalobos AM, Fuentealba C, Shetty K, Ranilla LG (2013) Potential of chilean native Corn (Zea mays L.) accessions as natural sources of phenolic antioxidants and in vitro bioactivity for hyperglycemia and hypertension management. J Agric Food Chem 61:10995–11007CrossRefGoogle Scholar
  16. Kapoor R, Giri B, Mukerji KG (2002) Glomus macrocarpum: a potential bioinoculant to improve essential oil quality and concentration in dill (Anethum graveolens L.) and darum (Trachyspermum ammi (Linn.) Sprague). World J Microbiol Biotechnol 18:459–463CrossRefGoogle Scholar
  17. Larose G, Chênevert R, Moutoglis P, Gagné 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
  18. Liu A, Hamel C, Hamilton RIMBL, Smith DL (2000) Acquisition of Cu, Zn, Mn and Fe by mycorrhizal maize (Zea mays L.) grown in soil at different P and micronutrient levels. Mycorrhiza 9:331–336CrossRefGoogle Scholar
  19. Maioli-Azevedo V, Fonseca-Kruel VS (2007) Plantas medicinais e ritualísticas vendidas em feiras livres no Município do Rio de Janeiro, RJ, Brasil: estudo de caso nas zonas Norte e Sul. Acta Bot Bras 21:263–275CrossRefGoogle Scholar
  20. Mandal S, Upadhyay S, Wajid S, Ram MJDC, Singh VP, Abdin MZ, Kapoor R (2015) Arbuscular mycorrhiza increase artemisinin accumulation in Artemisia annua by higher expression of key biosynthesis genes via enhanced jasmonic acid levels. Mycorrhiza 25:345–357CrossRefGoogle Scholar
  21. Monteiro JM, Albuquerque UP, Lins Neto EMF, Araújo EL, Albuquerque MM, Amorim ELC (2006) The effects of seasonal climate changes in the Caatinga on tannin levels in Myracrodruon urundeuva (Engl.) Fr. All. and Anadenanthera colubrina (Vell.) Brenan. Braz J Pharmacogn 16:338–344CrossRefGoogle Scholar
  22. Moreira FMS, Siqueira JO (2006) Microbiologia e bioquímica do solo. Editora da UFLA, LavrasGoogle Scholar
  23. Moreira RCT, Costa LCB, Costa RCS, Rocha EA (2002) Abordagem etnobotânica acerca do uso de plantas medicinais na Vila Cachoeira, Ilhéus, Bahia, Brasil. Acta Farm Bonaerense 21:205–211Google Scholar
  24. Oliveira MS, Campos MAS, Albuquerque UP, Silva FSB (2013) Arbuscular mycorrhizal fungi (AMF) affects biomolecules content in Myracrodruon urundeuva seedlings. Ind Crop Prod 50:244–247CrossRefGoogle Scholar
  25. Oliveira MS, Campos MA, Silva FS (2015) Arbuscular mycorrhizal fungi and vermicompost to maximize the production of foliar biomolecules in Passiflora alata Curtis seedlings. J Sci Food Agricul 95:522–528CrossRefGoogle Scholar
  26. Restle J, Neumann M, Brondani IL, Pascoal LL, Silva JHS, Pellegrini LG, Souza ANM (2002) Manipulação da altura de corte da planta de milho (Zea mays L.) para ensilagem visando a produção do novilho superprecoce. Rev Bras Zootec 31:1235–1244CrossRefGoogle Scholar
  27. Santos RI (2003) Metabolismo básico e origem dos metabólitos secundários. In: Simões CMO, Sebenkel EP, Gosmann G, Mello JCP, Mentz LA, Petrovick PR (eds), Farmacognosia: da planta ao medicamento. Porto Alegre/Florianópolis, Editora da UFRG/Editora da UFSC, pp 403–434Google Scholar
  28. Seifi E, Teymoor YS, Alizadeh M, Fereydooni H (2014) Olive mycorrhization: influences of genotype, mycorrhiza, and growing periods. Sci Hortic 180:214–219CrossRefGoogle Scholar
  29. Sheng M, Tang M, Chen H, Yang B, Zhang F, Huang Y (2008) Influence of arbuscular mycorrhizae on photosynthesis and water status of maize plants under salt stress. Mycorrhiza 18:287–296CrossRefGoogle Scholar
  30. Silva FA, Silva FSB (2017) Is the application of arbuscular mycorrhizal fungi an alternative to increase foliar phenolic compounds in seedlings of Mimosa tenuiflora (Wild.) Poir., Mimosoideae? Braz J Bot 40:361–365CrossRefGoogle Scholar
  31. Silva MF, Pescador R, Rebelo RA, Stürmer SL (2008) The effect of arbuscular mycorrhizal solates on the development and oleoresin production of micropropagated Zingiber officinale. Braz J Plant Physiol 20:119–130CrossRefGoogle Scholar
  32. Silva LG, Martins LMV, Silva FSB (2014a) Arbuscular mycorrhizal symbiosis in the maximization of the concentration of foliar biomolecules in pomegranate (Punica granatum L.) seedlings. J Med Plant Res 8:953–957CrossRefGoogle Scholar
  33. Silva FA, Silva FSB, Maia LC (2014b) Biotechnical application of arbuscular mycorrhizal fungi used in the production of foliar biomolecules in ironwood seedlings [Libidibia ferrea (Mart. ex Tul.) L.P.Queiroz var. ferrea]. J Med Plants Res 8:814–819CrossRefGoogle Scholar
  34. Subramanian KS, Charest C (1995) Influence of arbuscular mycorrhizae on the metabolismo of maize under drought stress. Mycorrhiza 5:273–278CrossRefGoogle Scholar
  35. Toussaint JP, Smith FA, Smith SE (2007) Arbuscular mycorrhizal fungi can induce the production of phytochemicals in sweet irrespective of phosphorus nutrition. Mycorrhiza 17:291–297CrossRefGoogle Scholar
  36. Vierheilig H, Gagnon H, Strack D, Maier W (2000) Accumulation of cyclohexenone derivatives in barley, wheats and maize roots in response to inoculation with different arbuscular mycorrhizal fungi. Mycorrhiza 9:291–293CrossRefGoogle Scholar
  37. Zhang Q-R, Zhu H-H, Zhao H-Q, Yao Q (2013) Arbuscular mycorrhizal fungal inoculation increases phenolics synthesis in clover roots via hydrogen peroxide, salicylic acid and nitric oxide signaling pathways. J Plant Physiol 170:74–79CrossRefGoogle Scholar
  38. Zhu X, Song F, Xu H (2010) Influence of arbuscular mycorrhiza on lipid peroxidation and antioxidant enzyme activity of maize plants under temperature stress. Mycorrhiza 20:325–332CrossRefGoogle Scholar
  39. Zuannazzi JAS, Montanha JA (2003) Flavonóides. In: Simões CMO, Sebenkel EP, Gosmann G, Mello JCP, Mentz LA, Petrovick PR (eds) Farmacognosia: da planta ao medicamento. Porto Alegre/Florianópolis, Editora da UFRG/Editora da UFSC, pp 577–614Google Scholar
  40. Zubek S, Mielcarek S, Turnau K (2012) Hipericin and pseudohypericin concentrations of a valuable medicinal plant Hypericum perforatum L. are enhanced by arbuscular mycorrhizal fungi. Mycorrhiza 22:149–156CrossRefGoogle Scholar

Copyright information

© Botanical Society of Sao Paulo 2018

Authors and Affiliations

  • Francineyde A. Silva
    • 1
    Email author
  • Leonor C. Maia
    • 2
  • Fábio S. B. Silva
    • 3
  1. 1.Laboratório de Tecnologia MicorrízicaUniversidade de Pernambuco, Campus PetrolinaPetrolinaBrazil
  2. 2.Departamento de MicologiaUniversidade Federal de PernambucoRecifeBrazil
  3. 3.Laboratório de Análises, Pesquisas e Estudos em Micorrizas e Programa de Pós-Graduação em Biologia Celular e Molecular AplicadaInstituto de Ciências Biológicas – ICB/Universidade de PernambucoRecifeBrazil

Personalised recommendations