Advertisement

Arbuscular Mycorrhizal Fungi: Effects on Secondary Metabolite Production in Medicinal Plants

  • Devendra K. Pandey
  • Prabhjot Kaur
  • Abhijit Dey
Chapter

Abstract

Medicinal plants are used by 80% of the world population for their primary health care. The medicinal value of plants is primarily attributed to the secondary metabolite content such as terpenoids, alkaloids, and phenolics. These compounds play a crucial role in plant defense, are merchandised valued for their therapeutic applications and ecological role, and are also used as flavoring agents. Arbuscular mycorrhizal fungi (AMF) or Glomeromycota is known to form a symbiotic relationship with many terrestrial plants. AM fungi–plant consortium enhanced the production of plant terpenoids, alkaloids, and phenolics, which are valuable to human health. The potential role of arbuscular mycorrhiza (AM) symbiosis in amplification of the secondary metabolite content has attained enormous recognition for sustainable cultivation of medicinally important crops. AMF–plant symbiosis not only improves the growth and nutrients but also exerts a synergistic effect on accumulation of bioactive compounds with medicinal importance. Current studies have also recognized AM-mediated modulation of morphology, biochemistry, and gene expression in medicinal as well as in the industrial important plants. This chapter provides an appraisal on contemporary finding in the area of AMF investigation with a marked emphasis on the yield of pharmaceutically important plant-derived secondary metabolites.

Keywords

Secondary metabolites Medicinal plants Nutrient uptake AM fungi 

References

  1. Abu-Zeyad R, Khan AG, Khoo C (1999) Occurrence of arbuscular mycorrhiza in Castanospermum australe A. Cunn. & C. Fraser and effects on growth and production of castanospermine. Mycorrhiza 9:111–117Google Scholar
  2. Adams RP, Habte M, Park S, Dafforn MR (2004) Preliminary comparison of vetiver root essential oils from cleansed (bacteria-and fungus-free) versus non-cleansed (normal) vetiver plants. Biochem Syst Ecol 32(12):1137–1144CrossRefGoogle Scholar
  3. Akiyama K, Hayashi H (2002) Arbuscular mycorrhizal fungus-promoted accumulation of two new triterpenoids in cucumber roots. Biosci Biotechnol Biochem 66(4):762–769PubMedCrossRefGoogle Scholar
  4. Allen MF, Moore TS, Christensen M (1980) Phytohormone changes in Bouteloua gracilis infected by vesicular-arbuscular mycorrhizae. I. Cytokinin increases in the host plant. Can J Bot 58:371–374CrossRefGoogle Scholar
  5. Allen MF, Moore TS, Christensen M (1982) Phytohormone changes in Bouteloua gracilis infected by vesicular-arbuscular mycorrhizae. II. Altered levels of gibberellin-like substances and abscisic acid in the host plant. Can J Bot 60:468–471CrossRefGoogle Scholar
  6. Andrade SAL, Malik S, Sawaya ACHF, Bottcher A, Mazzafera P (2013) Association with arbuscular mycorrhizal fungi influences alkaloid synthesis and accumulation in Catharanthus roseus and Nicotiana tabacum plants. Acta Physiol Plant 35(3):867–880CrossRefGoogle Scholar
  7. Araim G, Saleem A, Arnason JT, Charest AC (2009) Root colonization by an arbuscular mycorrhizal (AM) fungus increases growth and secondary metabolism of purple coneflower, Echinacea purpurea (L.) Moench. J Agric Food Chem 57:2255–2258PubMedCrossRefGoogle Scholar
  8. Arpana J, Bagyaraj DJ, Prakasa Rao EVS, Parameswaran TN, Abdul Rahiman BA (2008) Symbiotic response of patchouli [Pogostemon cablin (Blanco) Benth.] to different arbuscular mycorrhizal fungi. Adv Environ Biol 2(1):20–24Google Scholar
  9. Asrar AWA, Elhindi KM (2010) Elhindi. Alleviation of drought stress of marigold (Tagetes erecta) plants by using arbuscular mycorrhizal fungi. Saudi J Biol Sci 18(1):93–98PubMedPubMedCentralCrossRefGoogle Scholar
  10. Augé RM (2001) Water relations, drought and vesicular-arbuscular mycorrhizal symbiosis. Mycorrhiza 11(1):3–42CrossRefGoogle Scholar
  11. Awasthi A, Bharti N, Nair N, Singh R, Shukla AK, Gupta MM, Darokar MP, Kalra A (2011) Synergistic effect of Glomus mosseae and nitrogen fixing Bacillus subtilis strain Daz26 on artemisinin content in Artemisia annua L. Appl Soil Ecol 49:125–130CrossRefGoogle Scholar
  12. Bagheri S, Ebrahimi MA, Davazdahemami S, Minooyi J (2014) Terpenoids and phenolic compounds production of mint genotypes in response to mycorrhizal bio-elicitors. Tech J Eng Appl Sci 4:339–348Google Scholar
  13. Bagyaraj D J, Varma A (1995) Interaction between arbuscular mycorrhizal fungi and plants. In Advances in Microbial Ecology Springer, Boston pp 119–142Google Scholar
  14. Barrios E (2007) Soil biota, ecosystem services and land productivity. Ecol Econ 64:269–285CrossRefGoogle Scholar
  15. Bian XJ, Hu L, Li XL, Zhang FS (2001) Effect of VA mycorrhiza on the turfgrass quality and mineral nutrient uptakes. Acta Pratacul Sin 10(3):42–46Google Scholar
  16. Binet MN, Van Tuinen D, Deprêtre N, Koszela N, Chambon C, Gianinazzi S (2011) Arbuscular mycorrhizal fungi associated with Artemisia umbelliformis Lam, an endangered aromatic species in Southern French Alps, influence plant P and essential oil contents. Mycorrhiza 21:523–535PubMedCrossRefPubMedCentralGoogle Scholar
  17. Boby VU, Bagyaraj DJ (2003) Biological control of root-rot of Coleus forskohlii Briq. using microbial inoculants. World J Microbiol Biotechnol 19(2):175–180CrossRefGoogle Scholar
  18. Boller T, Wiemken A (1986) Dynamics of vacuolar compartmentation. Annu Rev Plant Physiol 37(1):137–164CrossRefGoogle Scholar
  19. Borde M, Dudhane M, Jite PK (2009) Role bioinoculant (AM fungi) increasing in growth, flavor content and yield in Allium sativum L. under field condition. Not Bot Hortic Agrobot Cluj 37(2):124–128Google Scholar
  20. Cai BY, Jie WG, Ge JP, Yan XF (2008) Molecular detection of the arbuscular mycorrhizal fungi in the rhizosphere of Phellodendron amurense. Mycosystema 27(6):884–893Google Scholar
  21. Cao DX, Zhao JL (2007) The investigation of arbuscular mycorrhizal fungi and soil factors from the rhizospere of medicinal plant Angelica dahurica. Acta Agric Boreali-Sin 22:47–50Google Scholar
  22. Copetta 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 16:485–494Google Scholar
  23. Chaudhary V, Kapoor R, Bhatnagar AK (2008) Effectiveness of two arbuscular mycorrhizal fungi on concentrations of essential oil and artemisinin in three accessions of Artemisia annua L. Appl Soil Ecol 40:174–181CrossRefGoogle Scholar
  24. Chen LT, Guo QS, Liu ZY (2009a) Colonization pattern and dynamic change of arbuscular mycorrhizal fungi in Pinellia ternate. Guizhou Agric Sci 37(2):37–39Google Scholar
  25. Chen LT, Liu ZY, Guo QS, Zhu GS (2009b) Advances in studies on arbuscular mycorrhizas in medicinal plants. Chin Tradit Herb Drugs 40(1):156–160Google Scholar
  26. Chen LT, Guo QS, Liu ZY (2010) Arbuscular mycorrhiza of cultivated and wild Pinellia ternate. Chin J Chin Mater Med 35(4):405–410Google Scholar
  27. Cho EJ, Lee DJ, Wee CD, Kim HL, Cheong YH, Cho JS, Sohn BK (2009) Effects of AM FUNGI inoculation on growth of Panax ginseng C.A. Meyer seedlings and on soil structures in mycorrhizosphere. Sci Hortic 122(4):633–637CrossRefGoogle Scholar
  28. Clark RB, Zeto SK (2000) Mineral acquisition by arbuscular mycorrhizal plants. J Plant Nutr 23(7):867–902CrossRefGoogle Scholar
  29. Cordell GA (1995) Changing strategies in natural products chemistry. Phytochem 40(6):1585–1612CrossRefGoogle Scholar
  30. Corizier R (1974) In: Kleinman VS et al. (eds) Medicine in Chinese Culture, Department of Health, Education and Welfare Publications, pp 26Google Scholar
  31. Croteau R, Kutchan TM, Lewis NG (2000) Natural products (secondary metabolites). Biochem Mol Biol 24:1250–1319Google Scholar
  32. David S (2000) The history of WWII medicine. http://home.att.net/~steinert/wwii.htm
  33. De la Rosa-Mera CJ, Ferrera-Cerrato R, Alarcón A, de Jesús Sánchez-Colín M, Muñoz-Muñiz OD (2011) Arbuscular mycorrhizal fungi and potassium bicarbonate enhance the foliar content of the vinblastine alkaloid in Catharanthus roseus. Plant Soil 349(1–2):367–376CrossRefGoogle Scholar
  34. El-Sayed M, Verpoorte R (2007) Catharanthus terpenoid indole alkaloids: biosynthesis and regulation. Phytochem Rev 6(2–3):277–305CrossRefGoogle Scholar
  35. Fan JH, Yang GT, Mu LQ, Zhou JH (2006) Effect of AM fungi on the content of berberine, jatrorrhizine and palmatine of Phellodendron amurense seedings. Prot For Sci Technol 5:24–26Google Scholar
  36. Farahani HA, Lebaschi MH, Hamidi A (2008) Effects of arbuscular mycorrhizal fungi, phosphorus and water stress on quantity and quality characteristics of coriander. J Adv Nat Appl Sci 2(2):55–59Google Scholar
  37. Feng G, Zhang F, Li X, Tian C, Tang C, Rengel Z (2002) Improved tolerance of maize plants to salt stress by arbuscular mycorrhiza is related to higher accumulation of soluble sugars in roots. Mycorrhiza 12(4):185–190PubMedCrossRefGoogle Scholar
  38. Floß DS, Hause B, Lange PR, Küster H, Strack D, Walter MH (2008) Knock-down of the MEP pathway isogene 1-deoxy-d-xylulose 5-phosphate synthase 2 inhibits formation of arbuscular mycorrhiza-induced apocarotenoids, and abolishes normal expression of mycorrhiza-specific plant marker genes. Plant J 56(1):86–100PubMedCrossRefGoogle Scholar
  39. Fransworth NR, Akerele O, Bingel AS, Soejarto DD, Guo Z (1985) Drugs from medicinal plants. Bull WHO 63:965–981Google Scholar
  40. Freitas MSM, Martins MA, Vieira IJC (2004) Yield and quality of essential oils of Mentha arvensis in response to inoculation with arbuscular mycorrhizal fungi. Pesq Agropec Bras 39(9):887–894CrossRefGoogle Scholar
  41. Galbley S, Thiericke R (1999) Drug Discovery FROM Nature. Springer, BerlinGoogle Scholar
  42. Geneva MP, Stancheva IV, Boychinova MM, Mincheva NH, Yonova PA (2010) Effects of foliar fertilization and arbuscular mycorrhizal colonization on Salvia officinalis L. growth, antioxidant capacity, and essential oil composition. J Sci Food Agric 90:696–702PubMedPubMedCentralGoogle Scholar
  43. Gershenzon J, Kreis W (1999) Biochemistry of terpenoids: monoterpenes, sesquiterpenes, diterpenes, sterols, cardiac glycosides and steroid saponins. Biochem Plant Sec Met 2:222–299Google Scholar
  44. Ghisalberti EL (1993) Detection and isolation of bioactive natural products. In: Colegate SM, Molyneux RJ (eds) Bioactive natural products: detection, isolation, and structural determination. CRC Press, Boca Raton, pp 9–57Google Scholar
  45. Gianinazzi S, Gollotte A, Binet MN, Tuinen DV, Redecker D, Wipf D (2010) Agroecology: the key role of arbuscular mycorrhizas in ecosystem services. Mycorrhiza 20:519–530PubMedCrossRefPubMedCentralGoogle Scholar
  46. Gong MQ, Wang FZ, Chen Y (2002) Study on application of arbuscular-mycorrhizas in growing seedling of Aloe vera. J Chin Med Mater 25(1):1–3Google Scholar
  47. Gopal RM (2001) J Med Aromat Plant Sci, 22/4A & 23/1A, 572Google Scholar
  48. Guerrieri E, Lingua G, Digilio MC, Massa N, Berta G (2004) Do interactions between plant roots and the rhizosphere affect parasitoid behaviour? Ecol Entomol 29(6):753–756CrossRefGoogle Scholar
  49. Guo LP, Wang HG, Hang LQ (2006) Effects of arbuscular mycorrhizae on growth and essential oil of Atractylodes lancea. Chin J Chin Mater Med 31(8):1491–1495Google Scholar
  50. Guo QS, Chen LT, Liu ZY (2010) Study on influence of arbuscular mycorrhizal fungi on Pinellia ternata yield and chemical composition. Chin J Chin Med 35(3):333–338Google Scholar
  51. Gupta ML, Prasad A, Ram M, Kumar S (2002) Effect of the vesicular-arbuscular mycorrhizal (VAM) fungus Glomus fasciculatum on the essential oil yield related characters and nutrient acquisition in the crops of different cultivars of menthol mint (Mentha arvensis) under field conditions. Bioresour Technol 81(1):77–79PubMedCrossRefPubMedCentralGoogle Scholar
  52. Hadwiger A, Neimann H, Kaebisch A, Bauer H, Tamura T (1986) Appropriate glucosylation of the FMS gene product is a prerequisite for its transforming potency. EMBO J 5:689–694PubMedPubMedCentralCrossRefGoogle Scholar
  53. Harris JC, Cottrell S, Plummer S, Lloyd D (2001) Antimicrobial properties of Allium sativum (garlic). Appl Microbiol Biotechnol 57:282–286PubMedCrossRefGoogle Scholar
  54. Harrison M (1999) Molecular and cellular aspects of the arbuscular mycorrhizal symbiosis. Annu Rev Plant Biol 50:361–389CrossRefGoogle Scholar
  55. Hart MM, Trevors JT (2005) Microbe management: application of mycorrhyzal fungi in sustainable agriculture. Front Ecol Environ 310:533–539CrossRefGoogle Scholar
  56. Herbert RB (2001) The biosynthesis of plant alkaloids and nitrogenous microbial metabolites. Nat Prod Rep 18(1):50–65PubMedCrossRefGoogle Scholar
  57. He XL, Li J, Gao AX, Zhao LL, Zao JL (2009a) Effects of different host plants on the development of AM fungi in the rhizospere of Salvia miltiorrhiza. J Hebei Univ 29(5):533–537Google Scholar
  58. He XL, Li J, He C (2009b) Effects of AM fungi on the chemical components of Salvia miltiorrhiza Bge. Chin Agric Sci Bull 25(14):182–185Google Scholar
  59. He XL, Liu T, Zhao LL (2009c) Effects of inoculating AM fungi on physiological characters an nutritional components of Astragalus membranaceus under different N application levels. Chin J Appl Ecol 20(9):2118–2122Google Scholar
  60. He XL, Wang LY, Ma J, Zhao LL (2010) AM fungal diversity in the rhizosphere of Salvia miltiorrhiza in Anguo city of Hebei province. Biodivers Sci 18(2):187–194CrossRefGoogle Scholar
  61. Hodge A, Campbell CDFAH (2001) An arbuscular mycorrhizal fungus accelerates decomposition and acquires nitrogen directly from organic material. Nature 413:297–299PubMedCrossRefGoogle Scholar
  62. Hostettmann K, Marston A, Ndjoko K, Wolfender JL (2000) The potential of African plants as a source of drugs. Curr Org Chem 4(10):973–1010CrossRefGoogle Scholar
  63. Huang KC (1999) The pharmacology of Chinese herbs: a brief history of Chinese medicine, 2nd edn. CRC Press, Boca Raton, pp 1–16Google Scholar
  64. Huang YF, Li HH, Chen HY, Li Y (2003) Preliminary study on the mycorrhiza inoculation on the seeding of camptotheca acuminate. Guangdong For Sci Technol 19(1):40–42Google Scholar
  65. Huang LQ, Chen ML, Xiao PG (2004) The modern biological basis and model hypothesis on the research of genuineness of Chinese herbal medicine. Chin J Chin Mater Med 29(6):494–496Google Scholar
  66. Huang JH, Tan JF, Jie HK, Zeng RS (2011) Effects of invoculating arbuscular mycorrhizal fungi on Artemisia annua growth and its officinal components. Chin J Appl Ecol 22(6):1443–1449Google Scholar
  67. Ishibashi A (2002) In: Complementary and alternative medicine in Japan, SY19-4Google Scholar
  68. Janardhanan KK, Abdul-Khaliq K (1995) Influence of vesicular arbuscular mycorrhizal fungi on growth and productivity of German chamomile in alkaline usar soil. In: Adholeya A, Singh S (eds) Mycorrhizae: biofertilizers for the future. Tata Energy Research Institute, New Delhi, pp 410–412Google Scholar
  69. Jeffries P, Gianinazzi S, Peretto S, Turnau K, Barea JM (2003) The contribution of arbuscular mycorrhizal fungi in sustainable maintenance of plant health and soil fertility. Biol Fertil Soils 37:1–16Google Scholar
  70. Jie WG, Cai BY, Ge JP, Yan XF (2007) Identification of arbuscular mycorrhizal fungi of Phellodendren amurense Rupr. Biotechnology 17(6):32–35Google Scholar
  71. Jugran AK, Bahukhandi A, Dhyani P, Bhatt ID, Rawal RS, Nandi SK, Palni LMS (2015) The effect of inoculation with mycorrhiza: AM on growth, phenolics, tannins, phenolic composition and antioxidant activity in Valeriana jatamansi Jones. J Soil Sci Plant Nutr 15(4):1036–1049Google Scholar
  72. Jurkiewicz A, Ryszka P, Anielska T, Waligórski P, Białońska D, Góralska K, Michael MT, Turnau K (2010) Optimization of culture conditions of Arnica montana L.: effects of mycorrhizal fungi and competing plants. Mycorrhiza 20:293–306PubMedCrossRefGoogle Scholar
  73. Kapoor R, Giri B, Mukerji KG (2002a) Glomus macrocarpum: a potential bioinoculant to improve essential oil quality and concentration in Dill (Anethum graveolens L.) and Carum (Trachyspermum ammi (Linn.) Sprague). World J Microbiol Biotechnol 18(5):459–463CrossRefGoogle Scholar
  74. Kapoor R, Giri B, Mukerji KG (2002b) Mycorrhization of coriander (Coriandrum sativum L.) to enhance the concentration and quality of essential oil. J Sci Food Agric 82:339–342CrossRefGoogle Scholar
  75. Kapoor R, Giri B, Mukerji KG (2004) Improved growth and essential oil yield and quality in Foeniculum vulgare mill on mycorrhizal inoculation supplemented with P-fertilizer. Bioresour Technol 93:307–311PubMedCrossRefGoogle Scholar
  76. Kapoor R, Chaudhary V, Bhatnagar AK (2007) Effects of arbuscular mycorrhiza and phosphorus application on artemisinin concentration in Artemisia annua L. Mycorrhiza 17:581–587PubMedCrossRefGoogle Scholar
  77. Karagiannidis N, Thomidisa T, Lazari D, Filotheou EP, Karagiannidou C (2011) Effect of three Greek arbuscular mycorrhizal fungi in improving the growth, nutrient concentration, and production of essential oils of oregano and mint plants. Sci Hortic 129:329–334CrossRefGoogle Scholar
  78. Khaosaad T, Vierheilig H, Nell M, Zitterl-Eglseer K, Novak J (2006) Arbuscular mycorrhiza alter the concentration of essential oils in oregano (Origanum sp., Lamiaceae). Mycorrhiza 16:443–446PubMedCrossRefGoogle Scholar
  79. Koide RT (1991) Nutrient supply, nutrient demand and plant response to mycorrhizal infection. New Phytol 117:365–386CrossRefGoogle Scholar
  80. Koide RT, Schreiner RP (1992) Regulation of the vesicular-arbuscular mycorrhizal symbiosis. Annu Rev Plant Physiol Plant Mol Biol 43:557–581CrossRefGoogle Scholar
  81. Krishna H, Singh S, Sharma RR, Khawale RN, Grover M, Patel VB (2005) Biochemical changes in micropropagated grape (Vitis vinifera L.) plantlets due to arbuscular-mycorrhizal fungi (AMF) inoculation during ex vitro acclimatization. Sci Hort 106(4):554–567CrossRefGoogle Scholar
  82. Lapeyrie F (1988) Oxalate synthesis from soil bicarbonate by fungus Paxillus involutus. Plant Soil 110:3–8CrossRefGoogle Scholar
  83. Leake J, Johnson D, Donnelly D, Muckle G, Boddy L, Read (2004) Networks of power and influence: the role of mycorrhizal mycelium in controlling plant communities and agroecosystem functioning. Can J Bot 82:1016–1045CrossRefGoogle Scholar
  84. Lee J, Scagel CF (2009) Chicoric acid found in basil (Ocimum basilicum L.) leaves. Food Chem 115(2):650–656CrossRefGoogle Scholar
  85. Li CX (2003a) Effect of vesicular-arbuscular mycorrhizal fungi on production of Ginseng. J Chin Med Mater 26(7):475–476Google Scholar
  86. Li CX (2003b) Effects of infecting vesicular-arbuscular mycorrhiza on growth and development of Coix Lachryma-jobi L. J Shanxi Agric Univ 23(4):351–353Google Scholar
  87. Liu T, He XL (2008) Research on the formation course of arbuscular mycorrhizae from Astragalus membranaceus (Fisch.) Bunge seedlings. J Hebei For Orc Res 23(3):311–314Google Scholar
  88. Liu SL, He XL (2009) Effects of AM fungi on growth of Glycyrrhiza inflata Bat under water stress. J Nucl Agric Sci 23(4):692–696Google Scholar
  89. Liu JN, Wu LJ, Wei SL, Xiao X, Su CX, Jiang P, Song ZB, Wang T, Yu ZL (2007) Effects of arbuscular mycorrhizal fungi on the growth, nutrient uptake and glycyrrhizin production of licorice (Glycyrrhiza uralensis Fisch). Plant Growth Regul 52(1):29–39CrossRefGoogle Scholar
  90. Loomis WD, Corteau R (1972) Essential oil biosynthesis. Rec Adv Phytochem 6:147–185CrossRefGoogle Scholar
  91. Lu YQ, He XL (2005) Effects of AM fungi on the chemical composition and growth amount of Atractylodes macrocephala koidz seedling on different N levels. J Hebei Univ 25(6):650–653Google Scholar
  92. Lu YQ, He XL (2008) Effects of AM fungi on photosynthetic pigment of Atractylodes macrocephala under different nitrogen levels. Acta Agric Bor Occi Sin 17(4):314–321Google Scholar
  93. Lu YQ, Cui Y, He XL (2008a) Effects of AM fungi on biomass and nitrogen content of Atractylodes macrocephala under different nitrogen levels. J Henan Agric Sci 4:94–96Google Scholar
  94. Lu YQ, He XL, Li LZ (2008b) Effects of AM fungi on leaf protective enzymes of Atractrlodes macrocephala under different nitrogen levels. Hubei Agric Sci 47(6):659–660Google Scholar
  95. Lu YQ, Wang DX, Lu XL, Li LM, Li Y, He XL (2011) Effects of AM fungi on physiological character and nutritional component of Atractylodes macrocephala under different N levels. Acta Bot Bor Occi Sin 31(2):351–356Google Scholar
  96. Lu FC, Lee CY, Wang CL (2015) The influence of arbuscular mycorrhizal fungi inoculation on yam (Dioscorea spp.) tuber weights and secondary metabolite content. Peer J 3:e1266PubMedCrossRefGoogle Scholar
  97. Ma J, He XL, Jiang ZM, Wang LY (2009) Influence of soil factors on arbuscular mycorrhizal fungal colonization of Salvia miltiorrhiza. Acta Agric Bor Occi Sin 18(5):194–198Google Scholar
  98. Maier W, Schmidt J, Wray V, Walter MH, Strack D (1999) The arbuscular mycorrhizal fungus, Glomus intraradices, induces the accumulation of cyclohexenone derivatives in tobacco roots. Planta 207:620–623CrossRefGoogle Scholar
  99. Mamta G, Rahi P, Pathania V, Gulati A, Singh B, Bhanwra RK, Tewari R (2012) Comparative efficiency of phosphate-solubilizing bacteria under greenhouse conditions for promoting growth and aloin-A content of Aloe barbadensis. Arch Agron Soil Sci 58(4):437–449CrossRefGoogle Scholar
  100. Mandal S, Evelin H, Giri B, Singh VP, Kapoor R (2013) Arbuscular mycorrhiza enhances the production of stevioside and rebaudioside-A in Stevia rebaudiana via nutritional and non-nutritional mechanisms. Appl Soil Ecol 72:187–194CrossRefGoogle Scholar
  101. Mandal A, Mandal S, Park MH (2014) Genome-wide analyses and functional classification of proline repeat-rich proteins: potential role of eIF5A in eukaryotic evolution. PLoS One 9(11):e111800PubMedPubMedCentralCrossRefGoogle Scholar
  102. Mandal S, Upadhyay S, Singh VP, Kapoor R (2015) Enhanced production of steviol glycosides in mycorrhizal plants: a concerted effect of arbuscular mycorrhizal symbiosis on transcription of biosynthetic genes. Plant Physiol Biochem 89:100–106PubMedCrossRefGoogle Scholar
  103. Marschner H (1995) Mineral nutrition of higher plants, 2nd edn. Elsevier Science, San DiegoGoogle Scholar
  104. Marschner H (1998) Mineral nutrition of higher plants. Academic, LondonGoogle Scholar
  105. McGarvey DJ, Croteau R (1995) Terpenoid metabolism. Plant Cell 7(7):1015PubMedPubMedCentralCrossRefGoogle Scholar
  106. Meng JJ, He XL (2011) Effects of AM fungi on growth and nutritional contents of Salvia miltiorrhiza Bge. under drought stress. J Agric Univ Hebei 34(1):51–61Google Scholar
  107. Morone Fortunato I, Avato P (2008) Plant development and synthesis of essential oils in micropropagated and mycorrhiza inoculated plants of Origanum vulgare L. ssp. hirtum (Link) Ietswaart. Plant Cell Tissue Organ 93:139–149CrossRefGoogle Scholar
  108. Nell M, Vötsch M, Vierheilig H, Steinkellner S, Zitterl-Eglseer K, Franz C, Novak J (2009) Effect of phosphorus uptake on growth and secondary metabolites of garden (Salvia officinalis L.). J Sci Food Agric 89:1090–1096CrossRefGoogle Scholar
  109. Nell M, Wawrosh C, Steinkellner S, Vierheilig H, Kopp B, Lössl A, Franz C, Novak J, Zitterl-Eglseer K (2010) Root solonization by symbiotic arbuscular mycorrhizal fungi increases sesquiterpenic acid concentrations in Valeriana of ficinalis L. Planta Med 76:393–398PubMedCrossRefGoogle Scholar
  110. Pan PL, Chen DQ, Chen YT, Zhou FM (2008) The research on the sift and germinate of AM FUNGI spore of Ophiopogon japonicas. Mod Chin Med 10(10):13–14Google Scholar
  111. Pandey DK, Banik RM (2009) The influence of dual inoculation with Glomus mossae and Azotobacter on growth and barbaloin content of Aloe vera. Am Eu J Sust Agric 3(4):703–714Google Scholar
  112. Pandey DK, Banik RM, Dey A, Panwar J (2014) Improved growth and colchicines concentration in Gloriosa superb in mycorrhizal inoculation supplemented with phosphorus – fertilizer. Afr J Tradit Complement Altern Med 11(2):439–446PubMedPubMedCentralCrossRefGoogle Scholar
  113. Peng S, Eissenstat DM, Graham JH, Williams K, Hodge NC (1993) Growth depression in mycorrhizal citrus at high-phosphorus supply: analysis of carbon costs. Plant Physiol 101:1063–1071PubMedPubMedCentralCrossRefGoogle Scholar
  114. Petersen M, Simmonds MSJ (2003) Rosmarinic acid. Phytochemistry 62:121–125PubMedCrossRefPubMedCentralGoogle Scholar
  115. Phillipson JD (1999) New drugs from nature—It could be yew. Phytother Res 13(1):2–8PubMedCrossRefGoogle Scholar
  116. Pozo MJ, Azcón-Aguilar C (2007) Unraveling mycorrhiza-induced resistance. Curr Opin Plant Biol 10(4):393–398PubMedCrossRefGoogle Scholar
  117. Prasad A, Kumar S, Khaliq A, Pandey A (2011) Heavy metals and arbuscular mycorrhizal (AM) fungi can alter the yield and chemical composition of volatile oil of sweet basil (Ocimum basilicum L.). Biol Fertil Soils 47(8):853–861CrossRefGoogle Scholar
  118. Qi GH, Zhang LP, Yang WL, Lu XR, Li CL (2002) Effects of arbuscular mycorrhizal fungi on growth and disease resistance of replanted ginkgo (Ginkgo biloba L.) seedlings. J Hebei For Orch Res 17(1):58–61Google Scholar
  119. Qi GH, Zhang LP, Yang WL, Lv GY (2003) The effects of abruscular mycorrhiza fungi on ginkgo (Ginkgo biloba L.) in the field. Hebei Fruits 19(1):40–42Google Scholar
  120. Rajan SK, Reddy BJD, Bagyaraj DJ (2000) Screening of arbuscular mycorrhizal fungi for their symbiotic efficiency with Tectona grandis. Forest Ecol Manag 126(2):91–95CrossRefGoogle Scholar
  121. Rapparini F, Llusia J, Penuelas J (2008) Effect of arbuscular mycorrhizal (AM) colonization on terpene emission and content of Artemisia annua L. Plant Biol 10:108–122PubMedCrossRefPubMedCentralGoogle Scholar
  122. Rasouli-Sadaghianil MH, Hassani A, Barin M, Danesh YR, Sefidkon F (2010) Effects of arbuscular mycorrhizal (AM) fungi on growth, essential oil production and nutrients uptake in basil. J Med Plant Res 4(21):2222–2228Google Scholar
  123. Rastogi PR, Meharotra BN (1990) (eds) In: Compendium of Indian medicinal plants, publications and information directorate, CSIR, New Delhi, vol.l, p 339Google Scholar
  124. Redecker D, Morton JB, Bruns TD (2000) Ancestral lineages of arbuscular mycorrhizal fungi (Glomales). Mol Phylogenet Evol 14:276–284PubMedCrossRefPubMedCentralGoogle Scholar
  125. Ren JH, Liu RX, Li YL (2007) Study on arbuscular mycorrhizae of Panax notoginseng. Microbiology 34(2):224–227Google Scholar
  126. Ren JH, Zhang JF, Liu RX, Li YQ (2008) Study on arbuscular mycorrhizae in Taxus chinensis var. mairei. Acta Bot Bor Occi Sin 28(7):1468–1473Google Scholar
  127. Roepke J, Salim V, Wu M, Thamm AM, Murata J, Ploss K, Wilhelm B, De Luca V (2010) Vinca drug components accumulate exclusively in leaf exudates of Madagascar periwinkle. Proc Natl Acad Sci 107(34):15287–15292PubMedCrossRefGoogle Scholar
  128. Rojas-Andrade R, Cerda-GarcÍa-Rojas CM, FrÍas-Hernández JT, Dendooven L, Olalde-Portugal V, Ramos-Valdivia AC (2003) Changes in the concentration of trigonelline in a semi-arid leguminous plant (Prosopis laevigata) induced by an arbuscular mycorrhizal fungus during the presymbiotic phase. Mycorrhiza 13:49–52PubMedCrossRefPubMedCentralGoogle Scholar
  129. Sailo GS, Bagyaraj DJ (2005) Influence of different AM-fungi on the growth, nutrition and forskolin content of Coleus forskohlii. Mycol Res 109(7):795–798PubMedCrossRefPubMedCentralGoogle Scholar
  130. Schüßler A, Schwarzott D, Walker C (2001) A new fungal phylum, the Glomeromycota, phylogeny and evolution. Mycol Res 105:1413–1421CrossRefGoogle Scholar
  131. Singh R, Soni SK, Kalra A (2013) Synergy between Glomus fasciculatum and a beneficial Pseudomonas in reducing root diseases and improving yield and forskolin content in Coleus forskohlii Briq. under organic field conditions. Mycorrhiza 23:35–44PubMedCrossRefPubMedCentralGoogle Scholar
  132. Shah V, Bhat SV, Bajwa BS, Domacur H, De SNJ (1980) The occurrence of forskolin in Labiatae. Planta Med 39:183–185CrossRefGoogle Scholar
  133. Shen XL, Guo QS, Liu ZY, Zhu GS, Liu YX (2011) Colonization progress of arbuscular mycorrhizae on tissue-cultured plantlets of Pinellia ternata. Chin J Chin Mater Med 36:93–96Google Scholar
  134. Shibata K, Iwata S, Nakamura M (1923) Baicalin, a new flavone-glucuronic acid compound from the roots of Scutellaria baicalensis. Acta Phytochim 1:105–139Google Scholar
  135. Sieverding E, Friedrichsen J, Suden W (1991) Vesicular-arbuscular mycorrhiza management in tropical agrosystems. Sonderpublikation der GTZ (Germany)Google Scholar
  136. Silva MFD, Pescador R, Rebelo RA, Stürmer SL (2008) The effect of arbuscular mycorrhizal fungal isolates on the development and oleoresin production of micropropagated Zingiber officinale. Braz J Plant Physiol 20(2):119–130CrossRefGoogle Scholar
  137. Silva FA, Ferreira MR, Soares LA, Sampaio EV, Maia LC (2014) Arbuscular mycorrhizal fungi increase gallic acid production in leaves of field grown Libidibia ferrea (Mart. ex Tul.) LP Queiroz. J Med Plant Res 8(36):1110–1115CrossRefGoogle Scholar
  138. Smith SE, Read DJ (1997) Mycorrhizal symbiosis. Academic, LondonGoogle Scholar
  139. Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic, LondonGoogle Scholar
  140. Smith SE, Smith FA, Jakobsen I (2004) Functional diversity in arbuscular mycorrhizal (AM) symbioses: the contribution of the mycorrhizal P uptake pathway is not correlated with mycorrhizal responses in growth or total P uptake. New Phytol 162:511–524CrossRefGoogle Scholar
  141. de Sousa OM, da Silva Campos MA, de Albuquerque UP, da Silva FSB (2013) Arbuscular mycorrhizal fungi (AMF) affects biomolecules content in Myracrodruon urundeuva seedlings. Ind Crop Prod 50:244–247CrossRefGoogle Scholar
  142. Strack D, Fester T, Hause B, Schliemann W, Walter MH (2003) Arbuscular mycorrhiza: biological, chemical, and molecular aspects. J Chem Ecol 29(9):1955–1979PubMedCrossRefGoogle Scholar
  143. Suzuki Y (2002, May 29) In Current status and future directions of alternative medicine, WHO, Geneva, SwitzerlandGoogle Scholar
  144. Swami Tirtha SS (1998) In: Uniyal RC et al (eds) Ayurvedic Encyclopedia, Natural Secrets to Healing, Prevention, and Longevity: history of Ayurvedic Tree, 1st edn. New Delhi, Sai Satguru PublicationsGoogle Scholar
  145. Szakiel A, Pączkowski H (2011a) Influence of environmental biotic factors on the content of saponins in plants. Phytochem Rev 10:493–502CrossRefGoogle Scholar
  146. Szakiel A, Pączkowski H (2011b) Influence of environmental abiotic factors on the content of saponins in plants. Phytochem Rev 10:471–491CrossRefGoogle Scholar
  147. Burni T, Saadia N, Tabassum Y, Sakina B (2013) Arblscular mycorrhizal stuidies in “Aloe vera (l). burm. f.” biologically active and potential medicinal plant. Wudpecker J Agric Res 2(1):039–042Google Scholar
  148. Tang W, Eisenbrand G (1992) In: Chinese drugs of plant origin, SpingerVerlag, Berlin, p 127Google Scholar
  149. Teng HR, He XL (2005) Effects of different AM fungi and N levels on the flavonoid content of Bupleuruin scorzonerifolium Willd. J Shanxi Agric Sci 4:53–54Google Scholar
  150. Torelli A, Trotta A, Acerbi L, Arcidiacono G, Berta G, Branca C (2000) IAA and ZR content in leek (Allium porrum L.), as influenced by P nutrition and arbuscular mycorrhizae, in relation to plant development. Plant Soil 226(1):29–35CrossRefGoogle Scholar
  151. Toussaint JP (2007) Investigating physiological changes in the aeria parts of AM plants: what do we know and where should we be heading? Mycorrhiza 17:349–353PubMedCrossRefPubMedCentralGoogle Scholar
  152. Toussaint JP, St-Arnaud M, Charest C (2004) Nitrogen transfer and assimilation between the arbuscular mycorrhizal fungus Glomus intraradices Schenck & Smith and Ri T-DNA roots of Daucus carota L. in an in vitro compartmented system. Can J Microbiol 50:251–260PubMedCrossRefPubMedCentralGoogle Scholar
  153. Toussaint JP, Smith FA, Smith SE (2007) Arbuscular mycorrhizal fungi can induce the production of phytochemicals in sweet basil irrespective of phosphorus nutrition. Mycorrhiza 17:291–297CrossRefGoogle Scholar
  154. Verpoorte R (1999) Secondary metabolism. In: Verpoorte R, Alfermann AW (eds) Metabolic engineering of plant secondary metabolism. Klumer Academic Publishers, Dordrecht, pp 1–29Google Scholar
  155. Volpin H, Elkind Y, Okon Y, Kapulnik Y (1994) A vesicular arbuscular mycorrhizal fungus (Glomus intraradices) induces a defense response in alfalfa roots. Plant Physiol 104:683–689PubMedPubMedCentralCrossRefGoogle Scholar
  156. Wang LY, He XL (2009) The resource and spatio-temporal distribution of AM fungi from Salvia miltiorrhiza in Anguo. J Agric Univ Hebei 32(6):73–79Google Scholar
  157. Wang Q, Li HQ, Du YR, Li Y, Li HW (1998) Isolation and identification of VA mycorrhizal fungi on Radix gentianae. Biotechnology 8(2):19–22Google Scholar
  158. Wang Q, He XL, Chen TS, Dou WF (2006) Ecological research of arbuscular mycorrhizal fungi in rhizosphere of Puerraria lobata. J Hebei Univ 26(4):420–425Google Scholar
  159. Wang DX, Lu YQ, He XL (2010) Effects of AM fungi on growth and physiological characters of Atractylodes macrocephala under different P-applied levels. Acta Bot Bor Occi Sin 30(1):136–142Google Scholar
  160. Warrier PK, Nambiar VPK, Ramankutti C (1996) (eds), In Indian medicinal plants: a compendium of 500 species, Orient Longmann, Hyderabad, vol 4. p 409Google Scholar
  161. Wei GT, Wang HG (1989) Effects of VA mycorrhizal fungi on growth, nutrient uptake and effective compounds in Chinese medicinal herb Datura stramonium L. Sci Agric Sin 22(5):56–61Google Scholar
  162. Wei GT, Wang HG (1991) Effect of vesicular-arbuscular mycorrhizal fungi on growth, nutrient uptake and synthesis of volatile oil in Schizonepeta tenuifolia Briq. Chin J Chin Mater Med 16(3):139–142Google Scholar
  163. Wiermann R (1981) Secondary plant products and cell and tissue differentiation. In: The biochemistry of plants, vol. 7. Academic, New York, pp 85–116Google Scholar
  164. Wink M (1997) Compartmentation of secondary metabolites and xenobiotics in plant vacuoles. Adv Bot Res 25:141–169CrossRefGoogle Scholar
  165. Wink M (1999) Introduction: biochemistry, role and biotechnology of secondary metabolites. In: Wink M (ed) Biochemistry of plant secondary metabolism. Sheffield Academic Press Ltd, Sheffield, pp 1–16Google Scholar
  166. Wu QC, Wei QA (2008) Arbuscular mycorrhizae of Ginkgo biloba and its correlation with soil available phosphorus. J Yangtze Univ 5(3):49–52Google Scholar
  167. Wu QS, Liu W, Zhai HF, Ye XF, Zhao LJ (2010) Influences of AM fungi on growth and root antioxidative enzymes of Trifoliate orange seedlings under salt stress. Acta Agric Univ Jiangxiensis 32(4):759–762Google Scholar
  168. Xing XK, Li Y, Yolande D (2000) Ten species of vAM fungi in five ginseng fields of Jilin province. J Jilin Agric Univ 22(2):41–46Google Scholar
  169. Xing XK, Li Y, Wang Y, Zhang MP (2003) Foundation of dual cultural system of ginseng VA mycorrhiza fungi. J Jilin Agric Univ 25(2):154–157Google Scholar
  170. Xiao WJ, Yang G, Chen ML, Guo LP, Wang M (2011) AM and its application in plant disease prevention of Chinese medicinal herbs cultivation. Chin J Chin Med 36(3):252–257Google Scholar
  171. Yang G, Guo LP, Huang LQ, Chen M (2008) Inoculation methods of AM fungi in medicinal plant. Resour Sci 30(5):778–785Google Scholar
  172. Yang Y, Ou X, Yang G, Xia Y, Chen M, Guo L, Liu D (2017) Arbuscular mycorrhizal fungi regulate the growth and phyto-active compound of Salvia miltiorrhiza seedlings. Appl Sci 7(1):68CrossRefGoogle Scholar
  173. Yadav K, Aggarwal A, Singh N (2013) Arbuscular mycorrhizal fungi (AMF) induced acclimatization, growth enhancement and colchicine content of micropropagated Gloriosa superba L. plantlets. Ind Crop Prod 45:88–93CrossRefGoogle Scholar
  174. Yu Y, Yu T, Wang Y, Yan XF (2010) Effect of inoculation time on camptothecin content in arbuscular mycorrhizal Camptotheca acuminate seedlings. Chin J Plant Ecol 34(6):687–694Google Scholar
  175. Zeng Y, Guo LP, Hang LQ, Zhou J, Sun YZ (2007) AM and its application in TCM cultivation. World Sci Technol/Moder TCM Mater Med 9(6):83–87Google Scholar
  176. Zhang MC, Jing YJ, Ma J (1990) The changing of microbial ecological types after the improvement of ginseng soil. J Jilin Agric Univ 12(4):42–46Google Scholar
  177. Zhang Y, Xie LY, Xiong BQ, Zeng M, Yu D (2004) Correlation between the growth of arbuscular mycorrhizal fungi in the rhizosphere and the flavonoid content in the root of Ginkgo biloba. Mycosystema 23(1):133–138Google Scholar
  178. Zhang J, Liu DH, Guo LP, Jin H, Zhou J, Yang G (2010) Effects of four AM fungi on growth and essential oil composition in rhizome of Atractylodes lancea. World Sci Technol/Moder TCM Mater Med 12(5):779–782Google Scholar
  179. Zhang J, Liu DH, Guo LP, Jin H, Yang G, Zhou J (2011) Effects of arbuscular mycorrhizae fungi on biomass and essential oil in rhizome of Atractylodes lancea in different temperatures. Chin Tradit Herb Drugs 42(2):372–375Google Scholar
  180. Zhao JL, He XL (2011) Effects of AM fungi on drought resistance and content of chemical components in Angelica dahurica. Acta Agric Bor Occi Sin 20(3):184–189Google Scholar
  181. Zhao X, Wang BW, Yan XF (2006) Effect of arbuscular mycorrhiza on camptothecin content in Camptotheca acuminate seedlings. Acta Ecol Sin 26(4):1057–1062Google Scholar
  182. Zhao PJ, An F, Tang M (2007) Effects of arbuscular mycorrhiza fungi on drought resistance of Forsythia suspense. Acta Bot Bor Occi Sin 27(2):396–399Google Scholar
  183. Zhao JL, Deng HY, He XL (2009) Effects of AM fungi on the quality of trueborn Angelica dahurica from Hebei province. Acta Agric Boreali-Sin 24:299–302Google Scholar
  184. Zhou JH, Fan JH (2007) Effects of AM fungi on the berberine content in Phellodendron chinense seedings. North Hortic 12:25–27Google Scholar
  185. Zhou N, Xia CL, Jiang B, Bai ZC, Liu GN, Ma XK (2009) Arbuscular mycorrhiza in Paris polyphylla var. yunnanensis. Chin J Chin Med 34(14):1768–1772Google Scholar
  186. Zhou N, Zou L, Wang GZ, Jiang B (2010) Primary explore to relation of arbuscular mycorrhizae and its secondary metabolite steroidal saponin in Paris polyphylla. Chin J Exp Tradit Med Formulae 16(16):85–88Google Scholar
  187. Zubek S, Stojakowska A, Anielska T, Turnau K (2010) Arbuscular mycorrhizal fungi alter thymol derivative contents of Inula ensifolia L. Mycorrhiza 20:497–504PubMedCrossRefGoogle Scholar
  188. Zubek S, Mielcarek S, Turnau K (2012) Hypericin and pseudohypericin concentrations of a valuable medicinal plant Hypericum perforatum L. are enhanced by arbuscular mycorrhizal fungi. Mycorrhiza 22:149–156PubMedCrossRefGoogle Scholar
  189. Zubek S, Błaszkowski J, Seidler-Łożykowska K, Bąba W, Mleczko P (2013) Arbuscular mycorrhizal fungi abundance, species richness and composition under the monocultures of five medicinal plants. Acta Sci Pol-Hortoru 12:127–141Google Scholar
  190. Zubek S, Rola K, Szewczyk A, Majewska ML, Turnau K (2015) Enhanced concentrations of elements and secondary metabolites in Viola tricolor L. induced by arbuscular mycorrhizal fungi. Plant Soil 390(1–2):129–142CrossRefGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2018

Authors and Affiliations

  • Devendra K. Pandey
    • 1
  • Prabhjot Kaur
    • 1
  • Abhijit Dey
    • 2
  1. 1.Department of Biotechnology, Lovely Faculty of Technology and SciencesLovely Professional UniversityPhagwaraIndia
  2. 2.Department of Life SciencesPresidency UniversityKolkataIndia

Personalised recommendations