Skip to main content

Advertisement

SpringerLink
Log in

Arbuscular mycorrhizae induce a global metabolic change and improve the nutritional and health benefits of pennyroyal and parsley

  • Original Article
  • Published:
Acta Physiologiae Plantarum Aims and scope Submit manuscript

Abstract

This study was conducted to investigate the potential use of arbuscular mycorrhizal fungi (AMF), Rhizophagus irregularis, as an innovative cultivation procedure to improve the production and quality of two medicinal plants, pennyroyal (Mentha pulegium), and parsley (Petroselinum hortense). We elucidated the impact of AMF on soil properties and growth and metabolic profiling of pennyroyal and parsley. AMF treatment improved the availability of essential elements and phenols in the rhizospheric soil. Plant biomass production and photosynthetic rate were improved. We also recorded improved primary and secondary metabolism, where the levels of most of the detected soluble and insoluble sugars, organic acids, essential (isoleucine and valine), and non-essential (glutamine, alanine, and cysteine) amino acids, fatty acids (especially unsaturated fatty acids), phenolic acids, and flavonoids were increased. Overall, this study supports the use of AMF in the artificial cultivation, as an alternative to the chemical fertilizers, for the production of high-quality medicinal plants with enhanced levels of bioactive compounds.

Graphic abstract

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Abdelgawad H, Saleh AM, Al S et al (2019) Utilization of actinobacteria to enhance the production and quality of date palm (Phoenix dactylifera L.) fruits in a semi-arid environment. Sci Total Environ 665:690–697

    Article  CAS  PubMed  Google Scholar 

  • Agusa T, Kunito T, Yasunaga G et al (2005) Concentrations of trace elements in marine fish and its risk assessment in Malaysia. Mar Pollut Bull 51:896–911

    Article  CAS  PubMed  Google Scholar 

  • Akhtar MS, Siddiqui ZA (2008) Arbuscular mycorrhizal fungi as potential bioprotectants against plant pathogens. In: Mycorrhizae: Sustainable agriculture and forestry. Springer, pp 61–97

  • Al Jaouni S, Saleh AM, Wadaan MAM et al (2018) Elevated CO2 induces a global metabolic change in basil (Ocimum basilicum L.) and peppermint (Mentha piperita L.) and improves their biological activity. J Plant Physiol 224–225:121–131

    Article  PubMed  CAS  Google Scholar 

  • Aljanaby AAJJ (2013) Antibacterial activity of an aqueous extract of Petroselinum crispum leaves against pathogenic bacteria isolated from patients with burns infections in Al-najaf Governorate, Iraq. Res Chem Intermed 39:3709–3714

    Article  CAS  Google Scholar 

  • Behtash N, Kargarzadeh F, Shafaroudi H (2008) Analgesic effects of seed extract from Petroselinum crispum (Tagetes minuta) in animal models. Toxic Lett 180:S127–S128

    Article  Google Scholar 

  • Brahmi F, Adjaoud A, Marongiu B et al (2016) Chemical and biological profiles of essential oils from Mentha spicata L. leaf from Bejaia in Algeria. J Essent oil Res 28:211–220

    Article  CAS  Google Scholar 

  • Bücking H, Liepold E, Ambilwade P (2012) The role of the mycorrhizal symbiosis in nutrient uptake of plants and the regulatory mechanisms underlying these transport processes. In: Plant science. IntechOpen

  • Cardoso IM, Kuyper TW (2006) Mycorrhizas and tropical soil fertility. Agric Ecosyst Environ 116:72–84

    Article  Google Scholar 

  • Ceccarelli N, Curadi M, Martelloni L et al (2010) Mycorrhizal colonization impacts on phenolic content and antioxidant properties of artichoke leaves and flower heads two years after field transplant. Plant Soil 335:311–323

    Article  CAS  Google Scholar 

  • Chandra KK, Kumar N, Chand G (2010) Studies on mycorrhizal inoculation on dry matter yield and root colonization of some medicinal plants grown in stress and forest soils. J Environ Biol 31:975

    CAS  PubMed  Google Scholar 

  • Chen X-H, Zhao B (2009) Arbuscular mycorrhizal fungi mediated uptake of nutrient elements by Chinese milk vetch (Astragalus sinicus L.) grown in lanthanum spiked soil. Biol Fertil Soils 45:675

    Article  CAS  Google Scholar 

  • Darwish HY, Ahmed SM (2020) Elicitors enhancing phenolics content and related gene expression variation in petal-derived calli of Rosa damascena mill. Egypt J Bot 60:71–79

    Google Scholar 

  • Duke JA (2001) Mentha pulegium L. (Lamiaceae)—Pennyroyal. In: Duke JA (ed) Handb Med herbs. CRC Press, Boca Raton, pp 307–308

    Google Scholar 

  • Evans JR (1989) Photosynthesis and nitrogen relationships in leaves of C3 plants. Oecologia 78:9–19

    Article  PubMed  Google Scholar 

  • Farshori NN, Al-Sheddi ES, Al-Oqail MM et al (2013) Anticancer activity of Petroselinum sativum seed extracts on MCF-7 human breast cancer cells. Asian Pac J Cancer Prev 14:5719–5723

    Article  PubMed  Google Scholar 

  • French LG (2002) Isolation of (R)-(+)-Pulegone from the European Pennyroyal Mint, Mentha Pulegium. Chem Educ 7:270–277

    Article  CAS  Google Scholar 

  • Giovannetti M, Sbrana C, Avio L, Strani P (2004) Patterns of below-ground plant interconnections established by means of arbuscular mycorrhizal networks. New Phytol 164:175–181

    Article  PubMed  Google Scholar 

  • Gupta ML, Janardhanan KK (1991) Mycorrhizal association of Glomus aggregatum with palmarosa enhances growth and biomass. Plant Soil 131:261–263

    Article  Google Scholar 

  • Hamad I, Abdelgawad H, Al Jaouni S et al (2015) Metabolic analysis of various date palm fruit (Phoenix dactylifera L.) cultivars from Saudi Arabia to assess their nutritional quality. Molecules 20:13620–13641

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Helal NM, Ibrahim N, Khattab H (2019) Phytochemical analysis and antifungal bioactivity of Pulicaria undulata (L.) methanolic extract and essential oil. Egypt J Bot 59:827–844

    Google Scholar 

  • Hosamani PA, Lakshman HC, Sandeepkumar K et al (2011) Role of arbuscular mycorrhizae in conservation of Withania somnifera. Biosci Discov 2:201–206

    Google Scholar 

  • Ibrahim MA, Campbell WF, Rupp LA, Allen EB (1990) Effects of mycorrhizae on sorghum growth, photosynthesis, and stomatal conductance under drought conditions. Arid L Res Manag 4:99–107

    Google Scholar 

  • Johansen A, Finlay RD, Påla O (1996) Nitrogen metabolism of external hyphae of the arbuscular mycorrhizal fungus Glornus intraradices. New Phytol 133:705–712

    Article  CAS  Google Scholar 

  • Jones JB Jr (2001) Laboratory guide for conducting soil tests and plant analysis. CRC Press, Boca Raton

    Book  Google Scholar 

  • Kapoor R, Giri B, Mukerji KG (2002a) Mycorrhization of coriander (Coriandrum sativum L) to enhance the concentration and quality of essential oil. J Sci Food Agric 82:339–342

    Article  CAS  Google Scholar 

  • Kapoor R, Giri B, Mukerji KG (2002b) 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 18:459–463

    Article  CAS  Google Scholar 

  • Karagiannidis N, Thomidis T, Lazari D et al (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 (Amsterdam) 129:329–334

    Article  CAS  Google Scholar 

  • Karthikeyan B, Joe MM, Cheruth AJ (2009) Response of some medicinal plants to vesicular arbuscular mycorrhizal inoculations. J Sci Res 1:381–386

    Article  Google Scholar 

  • Kim O-M, Kim M-K, Lee S-O et al (1998) Antimicrobial effect of ethanol extracts from spices against Lactobacillus plantarum and Leuconostoc mesenteroides isolated from kimchi. J Korean Soc Food Sci Nutr 27:455–460

    Google Scholar 

  • Kurian A (2012) Health benefits of herbs and spices. In: Handbook of herbs and spices (2nd edn), vol 2. Elsevier, pp 72–88

  • Livingstone KM, Lovegrove JA, Givens DI (2012) The impact of substituting SFA in dairy products with MUFA or PUFA on CVD risk: evidence from human intervention studies. Nutr Res Rev 25:193–206

    Article  CAS  PubMed  Google Scholar 

  • Lohse S, Schliemann W, Ammer C et al (2005) Organization and metabolism of plastids and mitochondria in arbuscular mycorrhizal roots of Medicago truncatula. Plant Physiol 139:329–340

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Malundo TMM, Shewfelt RL, Ware GO, Baldwin EA (2001) Sugars and acids influence flavor properties of mango (Mangifera indica). J Am Soc Hort Sci 126:115–121

    Article  CAS  Google Scholar 

  • Meng JJ, He XL (2011) Effects of AM fungi on growth and nutritional contents of Salvia miltiorrhiza Bge. under drought stress. J Agr Univ Hebei 34(1):51–61

    CAS  Google Scholar 

  • Mikkelsen BL, Rosendahl S, Jakobsen I (2008) Underground resource allocation between individual networks of mycorrhizal fungi. New Phytol 180:890–898

    Article  PubMed  Google Scholar 

  • Nema R, Khare S, Jain P et al (2013) Natural products potential and scope for modern cancer research. Am J Plant Sci 4:1270

    Article  Google Scholar 

  • Petersen M, Simmonds MSJ (2003) Rosmarinic acid. Phytochemistry 62:121–125

    Article  CAS  PubMed  Google Scholar 

  • Phillips JM, Hayman DS (1970) Improved procedures for clearing roots and staining parasitic and vesicular–arbuscular mycorrhizal fungi for rapid assessment of infection. Trans Br Mycol Soc 55:158–161

    Article  Google Scholar 

  • Rillig MC (2004) Arbuscular mycorrhizae, glomalin, and soil aggregation. Can J Soil Sci 84:355–363

    Article  Google Scholar 

  • Saleh AM, Selim S, Al JS, AbdElgawad H (2018) CO2 enrichment can enhance the nutritional and health benefits of parsley (Petroselinum crispum L.) and dill ( Anethum graveolens L.). Food Chem 269:519–526

    Article  CAS  PubMed  Google Scholar 

  • Saleh AM, Abdel-Mawgoud M, Hassan AR et al (2020) Global metabolic changes induced by arbuscular mycorrhizal fungi in oregano plants grown under ambient and elevated levels of atmospheric CO2. Plant Physiol Biochem 151:255–263

    Article  CAS  PubMed  Google Scholar 

  • Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic (Elsevier), London

    Google Scholar 

  • Smith AM, Zeeman SC (2006) Quantification of starch in plant tissues. Nat Protoc 1:1342

    Article  CAS  PubMed  Google Scholar 

  • 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 4:53–54

    Google Scholar 

  • Toussaint J-P, Smith FA, Smith SE (2007) Arbuscular mycorrhizal fungi can induce the production of phytochemicals in sweet basil irrespective of phosphorus nutrition. Mycorrhiza 17:291–297

    Article  CAS  Google Scholar 

  • Toussaint J, Kraml M, Nell M et al (2008) Effect of Glomus mosseae on concentrations of rosmarinic and caffeic acids and essential oil compounds in basil inoculated with Fusarium oxysporum f. sp. basilici. Plant Pathol 57:1109–1116

    Article  Google Scholar 

  • Ufaz S, Galili G (2008) Improving the content of essential amino acids in crop plants: goals and opportunities 1. Plant Physiol 147:954–961

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang B, Qiu Y-L (2006) Phylogenetic distribution and evolution of mycorrhizas in land plants. Mycorrhiza 16:299–363

    Article  CAS  PubMed  Google Scholar 

  • Wang P, He XL, Zhao LL et al (2012) Effects of AM fungi on the growth and microelement of Scuteliaria baiealensis Georgi under different N-applied levels. Acta Agric Bor Sin 27:259–263

    Google Scholar 

  • Wong PYY, Kitts DD (2006) Studies on the dual antioxidant and antibacterial properties of parsley (Petroselinum crispum) and cilantro (Coriandrum sativum) extracts. Food Chem 97:505–515

    Article  CAS  Google Scholar 

  • Wu Q-S, Xia R-X (2006) Arbuscular mycorrhizal fungi influence growth, osmotic adjustment and photosynthesis of citrus under well-watered and water stress conditions. J Plant Physiol 163:417–425

    Article  CAS  PubMed  Google Scholar 

  • Xu H, Lu Y, Tong S (2018) Effects of arbuscular mycorrhizal fungi on photosynthesis and chlorophyll fluorescence of maize seedlings under salt stress. Emirates J Food Agric 30:199–204

    Google Scholar 

  • Yanardağ R, Bolkent Ş, Tabakoğlu-Oğuz A, Özsoy-Saçan Ö (2003) Effects of Petroselinum crispum extract on pancreatic B cells and blood glucose of streptozotocin-induced diabetic rats. Biol Pharm Bull 26:1206–1210

    Article  PubMed  Google Scholar 

  • Yeasmin T, Zaman P, Rahman A et al (2007) Arbuscular mycorrhizal fungus inoculum production in rice plants. Afr J Agric Res 2:463–467

    Google Scholar 

  • Yehia RS, Osman GH, Assaggaf H et al (2020) Isolation of potential antimicrobial metabolites from endophytic fungus Cladosporium cladosporioides from endemic plant Zygophyllum mandavillei. S Afr J Bot. https://doi.org/10.1016/j.sajb.2020.02.033

    Article  Google Scholar 

  • Zhang Y, Xie L, Xiong B et al (2004) Correlation between the growth of arbuscular mycorrhizal fungi in the rhizosphere and the flavonoid content in the root of Ginkgo biloba. Mycosystema 23:133–138

    CAS  Google Scholar 

Download references

Acknowledgements

This project was funded by the Deanship of Scientific Research (DSR), King Abdulaziz University, Jeddah, Saudi Arabia, under grant no. (G:15-363-1439). The authors, therefore, acknowledge with thanks DSR technical and financial support.

Author information

Authors and Affiliations

  1. Department of Biological Sciences, College of Science, King Abdulaziz University, Jeddah, Saudi Arabia

    Rukaia Gashgari

  2. Department of Biological Sciences, Faculty of Science, University of Jeddah, Jeddah, Saudi Arabia

    Rukaia Gashgari

  3. Department of Clinical Laboratory Sciences, College of Applied Medical Sciences, Jouf University, PO 2014, Sakaka, Saudi Arabia

    Samy Selim

  4. Microbiology and Botany Department, Faculty of Science, Suez Canal University, PO 41522, Ismailia, Egypt

    Samy Selim

  5. Department of Medicinal and Aromatic Plants, Desert Research Centre, Cairo, Egypt

    Mohamed Abdel-Mawgoud

  6. Department of Clinical Laboratory Sciences, College of Applied Medical Sciences at Al-Quriat, Jouf University, Al-Quriat, Saudi Arabia

    Mona Warrad

  7. Biology Department, Faculty of Science at Yanbu, Taibah University, King Khalid Rd., Al Amoedi, Yanbu El-Bahr, 46423, Saudi Arabia

    Talaat H. Habeeb

  8. Department of Botany and Microbiology, Faculty of Science, Cairo University, Giza, 12613, Egypt

    Ahmed M. Saleh

  9. Botany and Microbiology Department, Faculty of Science, Beni-Suef University, Beni-Suef, Egypt

    Hamada AbdElgawad

Authors
  1. Rukaia Gashgari
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Samy Selim
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mohamed Abdel-Mawgoud
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Mona Warrad
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Talaat H. Habeeb
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Ahmed M. Saleh
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Hamada AbdElgawad
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ahmed M. Saleh.

Additional information

Communicated by R. Baczek-Kwinta.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 1615 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gashgari, R., Selim, S., Abdel-Mawgoud, M. et al. Arbuscular mycorrhizae induce a global metabolic change and improve the nutritional and health benefits of pennyroyal and parsley. Acta Physiol Plant 42, 102 (2020). https://doi.org/10.1007/s11738-020-03091-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11738-020-03091-3

Keywords

Search

Navigation