ORIGINAL ARTICLE
Mycorrhizal fungi and microalgae modulate antioxidant capacity of basil plants
1
Laboratory “Plant-Soil Interactions”, Institute of Plant Physiology and Genetics, Bulgarian Academy of Sciences, 1113 Sofia, Bulgaria
2
Laboratory “Experimental Algology”, Institute of Plant Physiology and Genetics, Bulgarian Academy of Sciences, 1113 Sofia, Bulgaria
Submission date: 2017-08-17
Acceptance date: 2017-11-27
Corresponding author
Marieta Hristozkova
Laboratory “Plant-Soil Interactions”, Institute of Plant Physiology and Genetics, Bulgarian Academy of Sciences, 1113 Sofia, Bulgaria
Laboratory “Plant-Soil Interactions”, Institute of Plant Physiology and Genetics, Bulgarian Academy of Sciences, 1113 Sofia, Bulgaria
Journal of Plant Protection Research 2017;57(4):417-426
KEYWORDS
TOPICS
ABSTRACT
Mycorrhizal fungi, algae and cyanobacteria are some of the most important soil microorganisms and major components of a sustainable soil-plant system. This study presents for the first time evidence of the impact of green alga and cyanobacterium solely and in combination with arbuscular mycorrhizal fungi (AMF) on plant-antioxidant capacity. In order to provide a better understanding of the impact of AMF and soil microalgae on Ocimum basilicum L. performance, changes in the pattern and activity of the main antioxidant enzymes (AOEs), esterases and non-enzymatic antioxidants including phenols, flavonoids, ascorbate, and α-tocopherols were evaluated. The targeted inoculation of O. basilicum with AMF or algae (alone and in combination) enhanced the antioxidant capacity of the plants and the degree of stimulation varied depending on the treatment. Plants in symbiosis with AMF exhibited the highest antioxidant potential as was indicated by the enhanced functions of all studied leaf AOEs: 1.5-, 2- and more than 10-fold rises of superoxide dismutase (SOD), glutathione-S-transferase (GST) and glutathione reductase (GR), respectively. The greatest increase in the total esterase activity and concentration of phenols, flavonoids and ascorbate was marked in the plants with simultaneous inoculation of mycorrhizal fungi and the green algae. 2,2-diphenyl-1-pycril-hydrazyl (DPPH) free radical scavenging method and ferric reducing antioxidant power (FRAP) assay proved the increased plant antioxidant capacity after co-colonization of green algae and mycorrhizae.
CONFLICT OF INTEREST
The authors have declared that no conflict of interests exist.
REFERENCES (56)
1.
Abdel Latef A.A.H., Chaoxing H. 2011. Effect of arbuscular mycorrhizal fungi on growth, mineral nutrition, antioxidant enzymes activity and fruit yield of tomato grown under salinity stress. Scientia Horticulturae 127 (3): 228–233. DOI: https://doi.org/10.1016/j.scie....
2.
Abdel-Lateif K., Bogusz D., Hocher V. 2012. The role of flavonoids in the establishment of plant roots endosymbioses with arbuscular mycorrhiza fungi, rhizobia and frankia bacteria. Plant Signaling and Behavior 7 (6): 636–641. DOI: https://doi.org/10.4161/psb.20....
3.
Aiba S., Ogawa T. 1977. Assessment of growth yield of a bluegreen alga: Spirulina platensis in axenic and continuous culture. Journal of General Microbiology 102: 179–182.
4.
Anderson M., Prasad T., Stewart C. 1995. Changes in isozyme profiles of catalase, peroxidase, and glutathione reductase during acclimation to chilling in mesocotyls of maize seedlings. Plant Physiology 109 (4): 1247–1257. DOI: https://doi.org/10.1104/pp.109....
5.
Asada K. 1999. The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Annual Review of Plant Physiology and Plant Molecular Biology 50 (1): 601–639. DOI: https://doi.org/10.1146/annure....
6.
Azevedo R., Alas R., Smith R., Lea P. 1998. Response of antioxidant enzymes to transfer from elevated carbon dioxide to air and ozone fumigation, in the leaves and roots of wildtype and catalase-deficient mutant of barley. Physiologia Plantarum 104 (2): 280–92.
7.
Bais H., Walker T., Schweizer H., Vivanco J. 2002. Root specific elicitation and antimicrobial activity of rosmarinic acid in hairy root cultures of Ocimum basilicum. Plant Physiology and Biochemistry 40 (11): 983–995. DOI: https://doi.org/10.1016/s0981-....
8.
Benzie I., Strain J. 1996. The ferric reducing ability of plasma (FRAP) as a measure of “antioxidant power”: The FRAP assay. Analytical Biochemistry 239 (1): 70–76. DOI: https://doi.org/10.1006/abio.1....
9.
Bradford M. 1976. A rapid and sensitive method for the quantification of micrograms quantities of protein utilising the principle of protein-dye binding. Analytical Biochemistry 72 (1–2): 248–254. DOI: https://doi.org/10.1006/abio.1....
10.
Bunning M., Kendall P., Stone M., Stonaker F., Stushnoff C. 2010. Effects of seasonal variation on sensory properties and total phenolic content of 5 lettuce cultivars. Journal of Food Science 75 (3): 156–161. DOI: https://doi.org/10.1111/j.1750....
11.
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 (7): 485–494. DOI: https://doi.org/10.1007/s00572....
12.
Devi M., Reddy M. 2002. Phenolic acid metabolism of groundnut (Arachis hypogaea L.) Plants inoculated with VAM fungus and Rhizobium. Plant Growth Regulation 37 (2): 151–156. DOI: https://doi.org/10.1023/A:1020....
13.
Dogru E., Warzecha H., Seibel F., Haebel S., Lottspeich F., Stockigt J. 2000. The gene encoding polyneuridine aldehyde esterase of monoterpenoid indole alkaloid biosynthesis in plants is an ortholog of the alpha/β hydrolase super family. European Journal of Biochemistry 267 (5): 1397–1406. DOI: https://doi.org/10.1046/j.1432....
14.
Estrada B., Aroca R., Barea J.M., Ruiz-Lozano J.M. 2013. Native arbuscular mycorrhizal fungi isolated from a saline habitat improved maize antioxidant systems and plant tolerance to salinity. Plant Science 201–202: 42–51. DOI: https://doi.org/10.1016/j.plan....
15.
Ganjewala D., Luthra R. 2009. Geranyl acetate esterase controls and regulates the level of geraniol in lemongrass (Cymbopogon flexuosus Nees ex Steud.) mutant cv. GRL-1 leaves. Zeitschrift für Naturforschung 64 (3–4): 251–259. DOI: https://doi.org/10.1515/znc-20....
16.
Gao Z., Qian Q., Liu X., Yan M., Feng Q., Dong G., Liu J., Han B. 2009. Dwarf 88, a novel putative esterase gene affecting architecture of rice plant. Plant Molecular Biology 71 (3): 265–276. DOI: https://doi.org/10.1007/s11103....
17.
Georgiev D., Dilov H., Avramova S. 1978. Millieu nutritif tamponne et méthode de culture intensive des microalgues vertes [Buffered nutrient medium and intensive method of green microalgae cultivation]. Hydrobiology 7: 14–23. (in Bulgarian).
18.
Gigova L., Gacheva G., Ivanova N., Pilarski P. 2012. Effects of temperature on Synechocystis sp. R10 (Cyanoprocaryota) at two irradiance levels. I: Effect on the growth, biochemical composition and defense enzyme activities. Genetics and Plant Physiology 2 (1–2): 24–37.
19.
Hazzoumi Z., Moustakime Y., Elharchli E., Amrani K. 2015. Effect of arbuscular mycorrhizal fungi (AMF) and water stress on growth, phenolic compounds, glandular hairs, and yield of essential oil in basil (Ocimum gratissimum L). Chemical and Biological Technologies in Agriculture 2 (1): 10. DOI: https://doi.org/10.1186/s40538....
20.
Herbinger K., Tausz M., Wonisch A., Soja G., Sorger A., Grill D. 2002. Complex interactive effects of drought and ozone stress on the antioxidant defense systems of two wheat cultivars. Plant Physiology and Biochemistry 40 (6–8): 691–696. DOI: https://doi.org/10.1016/s0981-....
21.
Jackson N., Franklin R., Miller R. 1972. Effects of vesicular-arbuscular mycorrhizae on growth and phosphorus content of three agronomic crops. Soil Science Society of America 36 (1): 64–67. DOI: https://doi.org/10.2136/sssaj1....
22.
Jayasinghe C., Gotoh N., Aoki T., Wada S. 2003. Phenolics composition and antioxidant activity of sweet basil (Ocimum basilicum L.). Journal of Agricultural and Food Chemistry 51 (15): 4442–4449. DOI: https://doi.org/10.1021/jf0342....
23.
Juliani R., Simon J.E. 2002. Antioxidant activity of basil. p. 575–579. In: “Trends in New Crops and New Uses” (J. Janick, A. Whipkey, eds.). ASHS Press, Alexandria, VA.
24.
Jurkiewicz A., Ryszka P., Anielska T., Waligórski P., Białońska D., Góralska K., Tsimilli-Michael M., Turnau K. 2010. Optimization of culture conditions of Arnica montana L.: effects of mycorrhizal fungi and competing plants. Mycorrhiza 20 (5): 293–306. DOI: https://doi.org/10.1007/s00572....
25.
Karthikeyan N., Prasannaa R., Nainb L., Kaushik B.D. 2007. Evaluating the potential of plant growth promoting cyanobacteria as inoculants for wheat. European Journal of Soil Biology 43 (1): 23–30. DOI: https://doi.org/10.1016/j.ejso....
26.
Khaosaad T., Vierheili H., Nell M., Zitterl-Eglseer K., Novak J. 2006. Arbuscular mycorrhiza alters the concentration of essential oils in oregano (Origanum sp., Lamiaceae). Mycorrhiza 16 (6): 443–446. DOI: https://doi.org/10.1007/s00572....
27.
Laemmli U.K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227 (5259): 680–685. DOI: https://doi.org/10.1038/227680....
28.
Matkowski A., Tasarz P., Szypuła E. 2008. Antioxidant activity of herb extracts from five medicinal plants from Lamiaceae, subfamily Lamioideae. Journal of Medicinal Plants Research 2 (11): 321–330.
29.
Mogren L., Olsson M., Gertsson U. 2007. Effects of cultivar, lifting time and nitrogen fertiliser level on quercetin content in onion (Allium cepa L.) at lifting. Journal of the Science of Food and Agriculture 87 (3): 470–476. DOI: https://doi.org/10.1002/jsfa.2....
30.
Mollavali M., Bolandnazar S., Schwarz D., Rohn S., Riehle P., Nahandi F. 2016. Flavonol glucoside and antioxidant enzyme biosynthesis affected by mycorrhizal fungi in various.
31.
cultivars of onion (Allium cepa L.). Journal of Agricultural and Food Chemistry 64 (1): 71−77. DOI: https://doi.org/10.1021/acs.ja....
32.
Mukherjee S., Bhattacharyyab P., Duttagupta A.K. 2004. Heavy metal levels and esterase variations between metal-exposed and unexposed duckweed Lemna minor: Field and laboratory studies. Environment International 30 (6): 811–814. DOI: https://doi.org/10.1016/j.envi....
33.
Murphy R., Sites J., Buth D., Haufler C. 1996. Proteins I: isozyme electrophoresis. p. 45–126. In: “Molecular Systematics” (D.M. Hillis, C. Moritz, B.K. Mable, eds.). 2nd ed. Sinauer Associates, Sunderland Massachusetts, USA, 655 pp.
34.
Odeyemi I., Afolami S, Sosanya O. 2010. Effect of Glomus mosseae (arbuscular mycorrhizal fungus) on host – parasite relationship of Meloidogyne incognita (southern root-knot nematode) on four improved cowpea varieties. Journal of Plant Protection Research 50 (3): 320–325. DOI: https://doi.org/10.2478/v10045....
35.
Petkov G. 1995. Nutrition medium for intensive cultivation of green microalgae in fresh and sea water. Archiv fűr Hydrobiologie 109: 81–85.
36.
Pfeffer H., Dannel F., Römheld V. 1998. Are there connection between phenol metabolism, ascorbate metabolism and membrane integrity in leaves of boron-deficient sunflower plants? Physiologia Plantarum 104 (3): 479–485. DOI: https://doi.org/10.1034/j.1399....
37.
Phippen W., Simon J. 2000. Anthocyanin inheritance and instability in purple basil (Ocimum basilicum L.). Journal of Heredity 91 (4): 289–296. DOI: https://doi.org/10.1093/jhered....
38.
Pozo M.J., Cordier C., Dumas-Gaudot E., Gianinazzi S., Barea J.M., Azcón-Aguilar C. 2002. Localized versus systemic effect of arbuscular mycorrhizal fungi on the defence responses to Phytophthora infection in tomato plants. Journal of Experimental Botany 53 (368): 525–534. DOI: https://doi.org/10.1093/jexbot....
39.
Prieto P., Pineda M., Aguilar M. 1999. Spectrophotometric quantitation of antioxidant capacity through the formation of a phosphomolybdenum complex: specific application to the determination of vitamin E. Analytical Biochemistry 269 (2): 337–341. DOI: https://doi.org/10.1006/abio.1....
40.
Pusztahelyi T., Holb I., Pócsi I. 2015. Secondary metabolites in fungus-plant interactions. Frontiers in Plant Science 6: 573. DOI: https://doi.org/10.3389/fpls.2....
41.
Radić S., Pevalek-Kozlina B. 2010. Differential esterase activity in leaves and roots of Centaurea ragusina L. As a consequence of salinity. Periodicum Biologorum 112 (3): 253–258.
42.
Ricci G., Bello M., Caccuri A., Galiazzo F., Federici G. 1984. Detection of glutathione transferase activity on polyacrylamide gels. Analytical Biochemistry 143 (2): 226–230. DOI: https://doi.org/10.1016/0003-2....
43.
Rozpądek P., Wężowicz K., Stojakowska A., Malarz J., Surówka E., Sobczyk Ł., Anielskaa T., Ważnyd R., Miszalskic Z., Turnau K. 2014. Mycorrhizal fungi modulate phytochemical production and antioxidant activity of Cichorium intybus L. (Asteraceae) under metal toxicity. Chemosphere 112: 217–224. DOI: https://doi.org/10.1016/j.chem....
44.
Sahu D., Priyadarshani I., Rath B. 2012. Cyanobacteria – as potential biofertilizer. CIB Tech Journal of Microbiology 1 (2–3): 20–26.
45.
Sakihama Y., Yamasaki H. 2002. Lipid peroxidation induces by phenolics in conjunction with aluminium ions. Biologia Plantarum 45 (2): 249–254. DOI: https://doi.org/10.1023/A:1015....
46.
Šetlik I. 1967. Contamination of algal cultures by heterotrophic microorganisms and its prevention. Annual Report of the Algology for the Year 1966, Trebon, CSAV, Institute of Microbiology: 89–100.
47.
Stuhlfelder C., Mueller M.J., Warzecha H. 2004. Cloning and expression of a tomato cdna encoding a methyl jasmonate cleaving esterase. European Journal of Biochemistry 271 (14): 2976–2983. DOI: https://doi.org/10.1111/j.1432....
48.
Tepe B., Sokmen M., Akpulat H.A., Sokmen A. 2006. Screening of the antioxidant potentials of six Salvia species from Turkey. Food Chemistry 95 (2): 200–204. DOI: https://doi.org/10.1016/j.food....
49.
Toussaint J., Smith F., Smith S. 2007. Arbuscular mycorrhizal fungi can induce the production of phytochemicals in sweet basil irrespective of phosphorus nutrition. Mycorrhiza 17 (4): 291–297. DOI: https://doi.org/10.1007/s00572....
50.
Toussaint J., 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. Canadian Journal of Microbiology 50 (4): 251–260. DOI: https://doi.org/10.1139/w04-00....
51.
Wang B., Qiu Y-L. 2006. Phylogenetic distribution and evolution of mycorrhizas in land plants. Mycorrhiza 16 (5): 299–363. DOI: https://doi.org/10.1007/s00572....
52.
Yang J., Meyers K.J., Vander H.J., Liu R. 2004. Varietal differences in phenolic content and antioxidant and anti-proliferative activities of onions. Journal of Agriculture and Food Chemistry 52 (22): 6787–6793. DOI: https://doi.org/10.1021/jf0307....
53.
Yao M.K., Desilets H., Charles M.T., Boulanger R., Tweddell R.J. 2003. Effect of mycorrhization on the accumulation of rishitin and solavetivone in potato plantlets challenged with Rhizoctonia solani. Mycorrhiza 13 (6): 333–336. DOI: https://doi.org./10.1007/s0057....
54.
Zhishen J., Mengcheng T., Jianming W. 1999. The determination of flavonoid contents in mulberry and their scavenging effects on superoxide radicals. Food Chemistry 64 (4): 555–559. DOI: https://doi.org/10.1016/s0308-....
55.
Ziedan E-S. H., Elewa I., Mostafa M., Sahab A. 2011. Application of mycorrhizae for controlling root diseases of sesame. Journal of Plant Protection Research 51 (4): 355–361. DOI: https://doi.org/10.2478/v10045....
56.
Zubek S., Rola K., Szewczyk A., Majewska M., Turnau K. 2015. Enhanced concentrations of elements and secondary metabolites in Viola tricolor L. Induced by arbuscular mycorrhizal fungi. Plant and Soil 390 (1–2): 129–142. DOI: https://doi.org./10.1007/s1110....
Share
RELATED ARTICLE
| eISSN: | 1899-007X |
| ISSN: | 1427-4345 |
We process personal data collected when visiting the website. The function of obtaining information about users and their behavior is carried out by voluntarily entered information in forms and saving cookies in end devices. Data, including cookies, are used to provide services, improve the user experience and to analyze the traffic in accordance with the Privacy policy. Data are also collected and processed by Google Analytics tool (more).
You can change cookies settings in your browser. Restricted use of cookies in the browser configuration may affect some functionalities of the website.
You can change cookies settings in your browser. Restricted use of cookies in the browser configuration may affect some functionalities of the website.
