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A comparative study of phosphate solubilization and the host plant growth promotion ability of Fusarium verticillioides RK01 and Humicola sp. KNU01 under salt stress

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Abstract

The aim of the present study was to compare the benefit to soybean in terms of phosphate solubilization and host plant growth under salt stress of the endophytic fungi Fusarium verticillioides RK01 and Humicola sp. KNU01. Endophyte F. verticillioides RK01 increased phosphate solubilization significantly more than Humicola sp. KNU01, as confirmed by increasing activities of acid phosphatase (1.0 U−1 g fwt), alkaline phosphatase (2.1 U−1 g fwt ) and fungal biomass (4.6 g), with a concurrent decrease in tri-calcium phosphate concentration in the culture medium. In a plant growth evaluation study, 0.1 M NaCl was added to pots containing soybean plants pre-treated with fungi. The salt-affected plants exhibited stunted growth due to a lower concentration of protein and higher level of lipid peroxidation than their controls. F. verticillioides RK01 and Humicola sp. KNU01 isolates significantly increased shoot length (7.3 % and 2.5 %) and protein content (59.1 % and 65.1 %), while inhibiting the lipid peroxidation level in salt stressed plants. Moreover, carotenoids, the activities of superoxide dismutase (SOD) and catalase were lower in plants affected by salinity than in non-stressed plants, whereas Humicola sp. KNU01 fungal association significantly mitigated oxidative stress by enhancing carotenoids (24.1 %) and SOD activity (61.2 %). F. verticillioides RK01 also triggered SOD activity to prevent oxidative damage. In addition, salt stress caused an increase of absicsic acid (ABA) in soybean plants, and F. verticillioides RK01 colonization effectively reduced ABA content in stressed plants. Salicylic acid (SA) is another plant hormone that was present in lower amounts in stressed plants, but the endophytic (F. verticillioides RK01 and Humicola sp. KNU01) fungal association increased SA content in salt-affected plants. The results of the present study indicate that the efficient phosphate solubilizing endophytic fungi F. verticillioides RK01 was more favorable to protect soybean plants against oxidative damage than Humicola sp. KNU01.

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References

  • Aebi H (1983) Catalase. In: Bergmeyer HU (ed) Methods of enzymatic analysis. 3rd edn. Verlag Chemie, Weinheim, pp 273–286

  • Alonso-Ramirez A, Rodriguez D, Reyes D, Jimenez JA, Nicolas G, Lopez-Climent M, Gomez-Cadenas A, Nicolas C (2009) Evidence for a role of gibberellins in salicylic acid-modulated early plant responses to abiotic stress in Arabidopsis seeds. Plant Physiol 150:1335–1344

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Alvarez M, Huygens D, Olivares E, Saavedra I, Alberdi M, Valenzuela E (2009) Ectomycorrhizal fungi enhance nitrogen and phosphorus nutrition of Nothofagus dombeyi under drought conditions by regulating assimilative enzyme activities. Physiol Plant 136(4):426–436

    Article  CAS  PubMed  Google Scholar 

  • Auge RM (2001) Water relations, drought and vesicular arbuscular mycorrhizal symbiosis. Mycorrhiza 11:3–42

    Article  Google Scholar 

  • Borde M, Dudhane M, Jite P (2011) Growth photosynthetic activity and antioxidant responses of mycorrhizal and non-mycorrhizal bajra (Pennisetum glaucum) crop under salinity stress condition. Crop Prot 30:265–271

    Article  CAS  Google Scholar 

  • Bradford MM (1976) Rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248–254

  • Dodd IC, Perez-Alfocea F (2012) Microbial amelioration of crop salinity stress. J Exp Bot 63:3415–3428

    Article  CAS  PubMed  Google Scholar 

  • Enyedi AJ, Yalpani N, Silverman P, Raskin I (1992)Localization, conjugation, and function of salicylic acid in tobacco during the hypersensitive reaction to tobacco mosaic virus.Proc Natl Acad Sci USA 89:2480–2484

  • Evelin H, Kapoor R, Giri B (2009) Arbuscular mycorrhizal fungi in alleviation of salt stress: a review. Ann Bot 104:1263–1280

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Fateh SH, Fagan WF (2002) Fungal endophytes: common host plant symbionts but uncommon mutualists. Integ Comp Biol 42:360–368

    Article  Google Scholar 

  • Fenice M, Selbman L, Federici F, Vassilev N (2000) Application of encapsulated Penicillium variabile P16 in solubilization of rock phosphate. Bioresour Technol 73:157–162

    Article  CAS  Google Scholar 

  • Ghorbanli M, Ebrahimzadeh H, Sharifi M (2004) Effects of NaCl and mycorrhizal fungi on antioxidative enzymes in soybean. Biol Plant 48:575–581

    Article  CAS  Google Scholar 

  • Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930

  • Giri B, Kapoor R, Mukerji KG (2003) Influence of arbuscular mycorrhizal fungi and salinity on growth, biomass and mineral nutrition of Acacia auriculiformis. Biol Fertil Soils 38:170–175

    Article  Google Scholar 

  • Hajiboland R, Aliasgharzadeh N, Laiegh SF, Poschenrieder C (2010) Colonization with arbuscular mycorrhizal fungi improves salinity tolerance of tomato (Solanum lycopersicum L.) plants. Plant Soil 331:313–327

    Article  CAS  Google Scholar 

  • Hariprasad P, Niranjana SR (2009) Isolation and characterization of phosphate solubilizing rhizobacteria to improve plant health of tomato. Plant Soil 316:13–24

    Article  CAS  Google Scholar 

  • Ikawa T, Nisizawa K, Miwa T (1964) Specificities of several acid phosphatases from plant sources. Nature 203:939–940

    Article  CAS  Google Scholar 

  • Imlay JA, Linn S (1988) DNA damage and oxygen radical toxicity. Science 240:1302–1309

    Article  CAS  PubMed  Google Scholar 

  • Jahromi F, Aroca R, Porcel R, Ruiz-Lozano JM (2008) Influence of salinity on the in vitro development of Glomus intraradices and on the in vivo physiological and molecular esponses of mycorrhizal lettuce plants. Microb Ecol 55:45–53

    Article  PubMed  Google Scholar 

  • Jha BK, Pragash MG, Cletus J, Raman G, Sakthivel N (2009) Simultaneous phosphate solubilization potential and antifungal activity of new fluorescent pseudomonad strains, Pseudomonas aeruginosa, P. plecoglossicida and P. mosselii. World J Microbiol Biotechnol 25:573–581

    Article  CAS  Google Scholar 

  • Jiang M, Zhang J (2001) Effect of abscisic acid on active oxygen species, antioxidative defence system and oxidative damage in leaves of maize seedlings. Plant Cell Pysiol 42:1265–1273

    Article  CAS  Google Scholar 

  • Kang SC, Hat CG, Lee TG, Maheshwari DK (2002) Solubilization of insoluble inorganic phosphates by a soil-inhabiting fungus Fomitopsis sp. PS 102. Curr Sci 82:439–442

  • Khan AL, Hamayun M, Kim YH, Kang SM, Lee IJ (2011a) Ameliorative symbiosis of endophyte (Penicillium funiculosum LHL06) under salt stress elevated plant growth of Glycine max L. Plant Physiol Biochem 49:852–861

    Article  CAS  PubMed  Google Scholar 

  • Khan AL, Hamayun M, Ahmad N, Hussain J, Kang SM, Kim YH, Adnan M, Tang DS, Waqas M, Radhakrishnan R, Hwang YH, Lee IJ (2011b) Salinity stress resistance offered by endophytic fungal interaction between Penicillium minioluteum LHL09 and Glycine max L. J Microbiol Biotechnol 21:893–902

    Article  CAS  PubMed  Google Scholar 

  • Khan AL, Hamayun M, Ahmad N, Waqas M, Kang SM, Kim YH, Lee IJ (2011c) Exophiala sp. LHL08 reprograms Cucumis sativus to higher growth under abiotic stresses. Physiol Plant 143:329–343

    Article  CAS  PubMed  Google Scholar 

  • Khan AL, Hamayun M, Waqas M, Kang SM, Kim YH, Kim DH, Lee IJ (2012) Exophiala sp.LHL08 association gives heat stress tolerance by avoiding oxidative damage to cucumber plants. Biol Fertil Soils 48:519–529

    Article  CAS  Google Scholar 

  • Khan MS, Zaidi A, Wani PA (2007) Role of phosphate-solubilizing microorganisms in sustainable agriculture—a review. Agron Sustain Dev 27:29–43

    Article  Google Scholar 

  • King JE (1936) The colorimetric determination of phosphorus. Biochem J 26:292–297

    Google Scholar 

  • Kohler J, Hernandez JA, Caravaca F, Roldan A (2009) Induction of antioxidant enzymes is involved in the greater effectiveness of a PGPR versus AM fungi with respect to increasing the tolerance of lettuce to severe salt stress. Environ Exp Bot 65:245–252

    Article  CAS  Google Scholar 

  • Marklund S, Marklund G (1974) Involvement of the superoxide anion radical in the autoxidation of pyrogallol and a convenient assay for superoxide dismutase. Eur J Biochem 47:469–474

  • Ohkawa H, Ohishi N, Yagi K (1979) Assay for lipid peroxidation in animal tissues by thiobarbituric acid reaction. Ann Biochem 95:351–358

  • Pandey A, Das N, Kumar B, Rinu K, Trivedi P (2008) Phosphate solubilization by Penicillium spp. isolated from soil samples of Indian Himalayan region. World J Microbiol Biotechnol 24:97–102

    Article  CAS  Google Scholar 

  • Pradhan N, Sukla LB (2005) Solubilization of inorganic phosphates by fungi isolated from agriculture soil. Afr J Biotechnol 5(10):850–854

    Google Scholar 

  • Porcel R, Aroca R, Ruiz-Lozano JM (2012) Salinity stress alleviation using arbuscular mycorrhizal fungi. A review. Agron Sustain Dev 32:181–200

    Article  CAS  Google Scholar 

  • Poss JA, Pond E, Menge JA, Harrell WM (1985) Effect of salinity on mycorrhizal onion and tomato in soil with and without additional phosphate. Plant Soil 88:307–319

    Article  CAS  Google Scholar 

  • Qi Q, Rose PA, Abrams GD, Taylor DC, Abrams SR, Cutler AJ (1998) (+)-Abscisic acid metabolism, 3-ketoacyl-coenzyme A synthase gene expression, and very long-chain monounstaurated fatty acid biosynthesis in Brassica napus embryos. Plant Physiol 117:979–987

  • Radhakrishnan R, Leelapriya T, Ranjithakumari BD (2012) Effects of pulsed magnetic field treatment of soybean seeds on calli growth, cell damage, and biochemical changes under salt stress. Bioelectromagnetics 33:670–681

    Article  CAS  PubMed  Google Scholar 

  • Radhakrishnan R, Lee IJ (2013) Spermine promotes acclimation to osmotic stress by modifying antioxidant, abscisic acid, and jasmonic acid signals in soybean. J Plant Growth Regul 32:22–30

    Article  CAS  Google Scholar 

  • Reyes I, Bernier L, Simard RR, Tanguay P, Antoun H (1999) Characteristics of phosphate solubilization by an isolate of a tropical Penicillium rugulosum and two UV-induced mutants. FEMS Microb Ecol 28:291–295

    Article  CAS  Google Scholar 

  • Richardson AE (2001) Prospects for using soil microorganism to improve the acquisition of phosphate by plant. Aust J Plant Physiol 28:897–906

    Google Scholar 

  • Seskar M, Shulaev V, Raskin I (1998)Endogenous methyl salicylate in pathogen-inoculated tobacco plants.Plant Physiol 116:387–392

  • Sharma P, Dubey RS (2005) Drought induces oxidative stress and enhances the activities of antioxidant enzymes in growing rice seedlings. Plant Growth Regul 46:209–221

    Article  CAS  Google Scholar 

  • Sharma YK, Leon J, Raskin I, Davis KR (1996) Ozoneinduced responses in Arabidopsis thaliana: the role of salicylic acid in the accumulation of defense-related transcripts and induced resistance. Proc Natl Acad Sci USA 93:5099–5104

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sheng M, Tang M, Chen H, Yang B, Zhang F, Huang Y (2009) Influence of arbuscular mycorrhizae on the root system of maize plants under salt stress. Can J Microbiol 55:879–886

  • Siefermann-Harms D (1987) The light-harvesting and protective functions of carotenoids in photosynthetic membranes. Physiol Plant 69:561–568

    Article  CAS  Google Scholar 

  • Sohrabi Y, Heidari G, Weisany W, Ghasemi-Golezani K, Mohammadi K (2012a) Changes of antioxidative enzymes, lipid peroxidation and chlorophyll content in chickpea types colonized by different Glomus species under drought stress. Symbiosis 56:5–18

    Article  CAS  Google Scholar 

  • Sohrabi Y, Heidari G, Weisany W, Ghasemi-Golezani K, Mohammadi K (2012b) Some physiological responses of chickpea cultivars to arbuscular mycorrhiza under drought stress. Russ J Plant Physiol 59:708–716

    Article  CAS  Google Scholar 

  • Vassilev N, Vassileva M, Fenice M, Federici F (2001) Immobilized cell technology applied in solubilization of insoluble inorganic (rock) phosphates and P plant acquisition. Bioresour Technol 79:263–271

    Article  CAS  PubMed  Google Scholar 

  • Vassilev N, Vassileva M, Nikolaeva I (2006) Simultaneous P-solubilizing and biocontrol activity of microorganisms: potentials and future trends. Appl Microbiol Biotechnol 71:137–144

    Article  CAS  PubMed  Google Scholar 

  • Wu QS, Zon YN, Liu W, Ye XE, Zai HE, Zhao LJ (2010) Alleviation of salt stress in citrus seedlings inoculated with mycorrhiza: changes in leaf antioxidant defense systems. Plant Soil Environ 56:470–475

    CAS  Google Scholar 

  • Wu QS, Zou YN, Huang YM (2013) The arbuscular mycorrhizal fungus Diversispora spurca ameliorates effects of waterlogging on growth, root system architecture and antioxidant enzyme activities of citrus seedlings. Fungal Ecol 6:37–43

    Article  Google Scholar 

  • Yates IE, Widstrom NW, Bacon CW, Glenn A, Hinton DM, Sparks D, Jaworski AJ (2005) Field performance of maize grown from Fusarium verticillioides-inoculated seed. Mycopathologia 159:65–73

    Article  CAS  PubMed  Google Scholar 

  • Zhang J, Jia W, Yang J, Ismail AM (2006) Role of ABA in integrating plant responses to drought and salt stresses. Field Crop Res 97:111–119

    Article  Google Scholar 

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Acknowledgment

This research work was supported financially by the Eco-Innovation Project, Korea Ministry of the Environment.

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Correspondence to In-Jung Lee.

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Radhakrishnan, R., Khan, A.L., Kang, S.M. et al. A comparative study of phosphate solubilization and the host plant growth promotion ability of Fusarium verticillioides RK01 and Humicola sp. KNU01 under salt stress. Ann Microbiol 65, 585–593 (2015). https://doi.org/10.1007/s13213-014-0894-z

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