Abstract
Nowadays, using arbuscular mycorrhizal fungi (AMF) is an important environment-friendly management technique for improving crop productivity. The current study was conformed to evaluate the inoculation effect by different AM fungi on morpho-physiological and biochemical characteristics as well as nutrient uptake of Calendula officinalis L. A pot experiment was carried out based on a completely randomized design with three replications. Treatments were inoculation with nine Glomus species included Glomus mosseae, Glomus intraradices, Glomus fasciculatum, Glomus caledonium, Glomus claroideum, Glomus versiform, Glomus geosporum, Glomus etanicatum, Glomus gigaspora, and non-inoculated treatment. Results of the present investigation showed that the C. officinalis plants benefit more from the AMF colonization with regard to growth, biomass, and biochemical accumulation. According to obtained results, the effect and outcome of colonization depend on the AMF species. Among the studied Glomus species, G. mosseae, G. etanicatum, and G. geosporum showed a considerable effect on increasing both growth and antioxidant metabolites in C. officinalis. The inoculation by these species with a high colonization rate increased the growth and yield of C. officinalis by providing essential nutrients and increasing relative water content and photosynthesis pigments. Also, the highest antioxidant capacity of leaves and flowers of C. officinalis in terms of total phenol, flavonoids, and carotenoids content as well as antioxidant enzymes activity was observed in the inoculated plants by these species. So that G. mosseae, G. etanicatum, and G. geosporum can be suggested as suitable AM fungi for use in the cultivation of the C. officinalis plant.
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Abbreviations
- AMF:
-
Arbuscular mycorrhizal fungi
- GPX:
-
Guaiacol peroxidase
- PPO:
-
Polyphenol oxidase
- RWC:
-
Relative water content
- SOD:
-
Superoxide dismutase
References
Abdel Latef AA, Chaoxing H (2014) Does the inoculation with Glomus mosseae improve salt tolerance in pepper plants. J Plant Growth Regul 33:644–653. https://doi.org/10.1007/s00344-014-9414-4
Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 44:276–287. https://doi.org/10.1016/0003-2697(71)90370-8
Blainski A, Lopes GC, de Mello JCP (2013) Application and analysis of the Folin Ciocalteu method for the determination of the total phenolic content from Limonium Brasiliense L. Molecules 18:6852–6865. https://doi.org/10.3390/molecules18066852
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254. https://doi.org/10.1006/abio.1976.9999
Bulgarelli RG, Marcos FCC, Ribeiro RV, de Andrade SAL (2017) Mycorrhizae enhance nitrogen fixation and photosynthesis in phosphorus-starved soybean (Glycine max L. Merrill). Environ Exp Bot 140:26–33. https://doi.org/10.1016/j.envexpbot.2017.05.015
Dalpe Y (1993) Vesicular-arbuscular mycorrhiza. In: Carter MR (ed) Soil sampling and methods of analysis, 3rd edn. Canadian Society of Soil Science, Lewis, Boca Raton, Fla, pp 287–301
Dolatabadi H, Mohammadi Goltapeh E, Moieni A, Varma A (2012) Evaluation of different densities of auxin and endophytic fungi (Piriformospora indica and Sebacina vermifera) on Mentha piperita and Thymus vulgaris growth. J Biotechnol 11:1644–1650. https://doi.org/10.5897/AJB10.1336
Engel R, Szabo K, Abranko L, Rendes K, Fuzy A, Takacs T (2016) Effect of arbuscular mycorrhizal fungi on the growth and the polyphenol profile of marjoram, lemon balm and marigold. J Agric Food Chem 64:3733–3742. https://doi.org/10.1021/acs.jafc.6b00408
Ferrol N, Azċon-Aguilar C, Pérez-Tienda J (2019) Review: Arbuscular mycorrhizas as key players in sustainable plant phosphorus acquisition: an overview on the mechanisms involved. Plant Sci 280:441–447. https://doi.org/10.1016/j.plantsci.2018.11.011
Foster CE, Martin TM, Pauly M (2010) Comprehensive compositional analysis of plant cell walls (Lignocellulosic biomass) part II: Carbohydrates. J vis Exp 12:1837. https://doi.org/10.3791/1837
Ganjeali A, Ashiani E, Zare M, Tabasi E (2018) Influences of the arbuscular mycorrhizal fungus Glomus mosseae on morphophysiological traits and biochemical compounds of common bean (Phaseolus vulgaris) under drought stress. S Afr J Plant Soil 35:121–127. https://doi.org/10.1080/02571862.2017.1340982
Genre A, Chabaud M, Balzergue C, Puech-Pagès V, Novero M, Rey T, Fournier J, Rochange S, Bécard G, Bonfante P, Barker DG (2013) Short- chain chitin oligomers from arbuscular mycorrhizal fungi trigger nuclear Ca2+ spiking in Medicago truncatula roots and their production is enhanced by strigolactone. New Phytol 198:190–202. https://doi.org/10.1111/nph.12146
Gheisari Zardak S, Movahhedi Dehnavi M, Salehi A, Gholamhoseini M (2017) Responses of field grown fennel (Foeniculum vulgare Mill.) to different mycorrhiza species under varying intensities of drought stress. J Appl Res Med Aroma 5:16–25. https://doi.org/10.1016/j.jarmap.2016.09.004
HeitorMarta LC, FreitasVanessa SM, BritoAlmy N, CarvalhoMarco JC, Martins A (2016) Growth and yield of marigold flowers in response to mycorrhizal inoculation and phosphorus. Hortic Bras 34:26–30. https://doi.org/10.1590/S0102-053620160000100004
Hristozkova M, Geneva M, Stancheva I, Boychinova M, Djonova E (2015) Aspects of mycorrhizal colonization in adaptation of sweet marjoram (Origanum majorana L.) grown on industrially polluted soil. Turk J Biol 39:461–468. https://doi.org/10.3906/biy-1408-47
Hristozkova M, Geneva M, Stancheva I, Boychinova M, Djonova E (2016) Contribution of arbuscular mycorrhizal fungi in attenuation of heavy metal impact on Calendula officinalis development. Appl Soil Ecol 101:57–63. https://doi.org/10.1016/j.apsoil.2016.01.008
Johny L, Cahill DM, Adholeya A (2021) AMF enhance secondary metabolite production in ashwagandha, licorice, and marigold in a fungi-host specific manner. Rhizosphere 17:100314. https://doi.org/10.1016/j.rhisph.2021.100314
Kar M, Mishra D (1976) Catalase, peroxidase, and polyphenoloxidase activities during rice leaf senescence. Plant Physiol 57:315–319. https://doi.org/10.1104/pp.57.2.315
Ak G, Zengin G, Ceylan R, Mahomoodally MF, Jugreet S, Mollica A, Stefanucci A (2020) Chemical composition and biological activities of essential oils from Calendula officinalis L. flowers and leaves. Flavour Fragr J 36:554–563. https://doi.org/10.1002/ffj.3661
Lim TK (2014) Calendula officinalis. In: Lim TK (ed) Edible medicinal and non-medicinal plants, flowers. Springer International Publishing AG, Cham, 7, p 213–244
Maillet F, Poinsot V, André O, Puech-Pagès V, Haouy A, Gueunier M, Cromer L, Giraudet D, Formey D, Niebel A, Martinez EA, Driguez H, Bécard G, Dénarié J (2011) Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza. Nature 469:58–63. https://doi.org/10.1038/nature09622
Mendis HC, Thomas VP, Schwientek P, Salamzade R, Chien JT, Waidyarathne P, Kloepper J, De La Fuente L (2018) Strain-specific quantification of root colonization by plant growth promoting rhizobacteria Bacillus firmus I-1582 and Bacillus amyloliquefaciens QST713 in non-sterile soil and field conditions. PLoS ONE 13:e0193119. https://doi.org/10.1371/journal.pone.0193119
Motsara MR, Roy RN (2008) Guide to laboratory establishment for plant nutrient analysis. FAO Fertilizer and Plant Nutrition Bulletin, 19, Food and Agriculture Organization of the United Nations, Rome
Pękal A, Pyrzynska K (2014) Evaluation of aluminium complexation reaction for flavonoid content assay. Food Anal Methods 7:1776–1782. https://doi.org/10.1007/s12161-014-9814-x
Pellegrino E, Bedini S (2014) Enhancing ecosystem services in sustainable agriculture: biofertilization and biofortification of chickpea (Cicer arietinum L.) by arbuscular mycorrhizal fungi. Soil Biol Biochem 68:429–439. https://doi.org/10.1016/j.soilbio.2013.09.030
Pieczynski M, Marczewski W, Hennig J, Dolata J, Bielewicz D, Piontek P, Wyrzykowska A, Krusiewicz D, Strzelczyk-Zyta D, Konopka-Postupolska D (2013) Down-regulation of CBP80 gene expression as a strategy to engineer a drought-tolerant potato. Plant Biotechnol J 11:459–469. https://doi.org/10.1111/pbi.12032
Plewa MJ, Smith SR, Wagner ED (1991) Diethyldithiocarbamate suppresses the plant activation of aromatic amines into mutagens by inhibiting tobacco cell peroxidase. Mutat Res 247:57–64. https://doi.org/10.1016/0027-5107(91)90033-k
Pocock T, Król M, Huner NPA (2004) The determination and quantification of photosynthetic pigments by reverse phase high-performance liquid chromatography, thin-layer chromatography, and spectrophotometry. Methods Mol Biol 274:137–148. https://doi.org/10.1385/1-59259-799-8:137
Rouphael Y, Colla G, Graziani G, Ritieni A, Cardarelli M, De Pascale S (2017) Phenolic composition, antioxidant activity and mineral profile in two seed-propagated artichoke cultivars as affected by microbial inoculants and planting time. Food Chem 234:10–19. https://doi.org/10.1016/j.foodchem.2017.04.175
Salvioli di Fossalunga A, Novero M (2019) To trade in the field: the molecular determinants of arbuscular mycorrhiza nutrient exchange. Chem Biol Technol Agric 6:1–12. https://doi.org/10.1186/s40538-019-0150-7
Selvaraj A, Thangavel K, Uthandi S (2020) Arbuscular mycorrhizal fungi (Glomus intraradices) and diazotrophic bacterium (Rhizobium BMBS) primed defense in blackgram against herbivorous insect (Spodoptera litura) infestation. Microbiol Res 231:126355. https://doi.org/10.1016/j.micres.2019.126355
Tabrizi L, Mohammadi S, Delshad M, Moteshare Zadeh M (2015) Effect of arbuscular mycorrhizal fungi on yield and phytoremediation performance of pot marigold (Calendula officinalis L.) under heavy metals stress. Int J Phytoremediation 17:1244–1252. https://doi.org/10.1080/15226514.2015.1045131
Thokchom SD, Gupta S, Kapoor R (2020) Arbuscular mycorrhiza augments essential oil composition and antioxidant properties of Ocimum tenuiflorum L.—a popular green tea additive. Ind Crops Prod 153:112418. https://doi.org/10.1016/j.indcrop.2020.112418
Tian L, Shi S, Ma L, Zhou X, Luo S, Zhang J, Lu B, Tian C (2019) The effect of Glomus intraradices on the physiological properties of Panax ginseng and on rhizospheric microbial diversity. J Ginseng Res 43:77–85. https://doi.org/10.1016/j.jgr.2017.08.005
Vora J, Srivastava A, Modi H (2018) Antibacterial and antioxidant strategies for acne treatment through plant extracts. Inform Med Unlocked 13:128–132. https://doi.org/10.1016/j.imu.2017.10.005
Xie J, Schaich KM (2014) Re-evaluation of the 2,2-diphenyl-1-picrylhydrazyl free radical (DPPH) assay for antioxidant activity. J Agric Food Chem 62:4251–4260. https://doi.org/10.1021/jf500180u
Zaller JG, Saccani F, Frank T (2011) Effects of earthworms and mycorrhizal fungi on the growth of the medicinal herb Calendula officinalis (Asteraceae). Plant Soil Environ 57:499–504. https://doi.org/10.17221/189/2011-PSE
Zeng Y, Guo LP, Chen BD, Hao Z, Wang JY, Huang LQ, Yang G, Cui XM, Yang L, Wu ZX, Chen ML, Zhang Y (2013) Arbuscular mycorrhizal symbiosis and active ingredients of medicinal plants: current research status and prospectives. Mycorrhiza 23:253–265. https://doi.org/10.1007/s00572-013-0484-0
Zhang T, Hu Y, Zhang K, Tian C, Guo J (2018) Arbuscular mycorrhizal fungi improve plant growth of Ricinus communis by altering photosynthetic properties and increasing pigments under drought and salt stress. Ind Crops Prod 117:13–19. https://doi.org/10.1016/j.indcrop.2018.02.087
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Kheyri, Z., Moghaddam, M. & Farhadi, N. Inoculation Efficiency of Different Mycorrhizal Species on Growth, Nutrient Uptake, and Antioxidant Capacity of Calendula officinalis L.: a Comparative Study. J Soil Sci Plant Nutr 22, 1160–1172 (2022). https://doi.org/10.1007/s42729-021-00721-8
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DOI: https://doi.org/10.1007/s42729-021-00721-8