Using Plant Growth-promoting Fungi (PGPF), as a Biofertilizer and Biocontrol Agents against Tetranychus cucurbitacearum on Nubian Watermelon (Citrullus lanatus L.)

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Rabab Hammad
Mohssen Elbagory


Plant growth-promoting fungi (PGPF) have attracted considerable interest as biofertilizers and biocontrol due to their multiple beneficial effects on plant quantity and quality as well as their positive relationship with the ecological environment. The objective of this study was to determine the efficacy of different concentrations 25, 50, 75 and 100% from cultural filtrate of Trichoderma viride and T. harzianum to induce the two-spotted spider mite, Tetranychus cucurbitacearum (In vitro), and their ability to improve the growth dynamics of Nubian watermelon plants in field experiment during two growing summer seasons of 2017 and 2018.

In general the effect of tested concentrations of T. viride were non effective on egg deposition by adult females after five days from treatment, while in T. harzianum, the concentration 75% was the most effect than the other concentrations. Also, egg hatchability % decreased with increased of two egg age (1 – 2 day old) at treatment by concentrations 25 and 50% of both fungal. In field experiment, the test compound (vertimec) was the more effective against egg stage of spider mite T. cucurbitacearum than motile stages of both T. viride and T. harzianum treatments. Also, plants inoculated with T. harzianum showed increases in vegetative growth parameters included numbers of leaves, Leaf dry weight, stem length and numbers of branches and biochemical analysis of leaves included chlorophyll content and percentages of NPK at 30 and 60 days from sowing during both seasons compared to uninoculated control plants. Also, enzymes activities, treatment T2 (inoculated with T. viride) recorded the highest values at all growth stages, which recorded 155.77, 257.29 and 114.62 mg TPF g-1 soil day-1 for dehydrogenase and 113.79, 201.03 and 115.24 mg NH4+- N g-1 soil d-1 for urease at 30, 60 and harvest during 2017 growing season, respectively. The same trend was observed in total count of fungi during both seasons.

For fruit yield, T. viride (T2) had significantly the highest number of fruits per plant, number of seeds per fruit, fruit weight (g) and dry weight of 100 seeds (g) which recorded 1.92, 273.07, 1126 g and 16.29 g as compared to untreated control treatment, which attained 1.21, 185.08, 526.66 g and 14.41 g at 2017 season, respectively. Therefore, these results reflected to increase fruit yield (Kg/m2), seed yield (g/m2) and weight of yield (ton fed.-1) during both seasons.

PGPF, Trichoderma viride, Trichoderma harzianum, Tetranychus cucurbitacearum, Nubian watermelon, yield

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Hammad, R., & Elbagory, M. (2019). Using Plant Growth-promoting Fungi (PGPF), as a Biofertilizer and Biocontrol Agents against Tetranychus cucurbitacearum on Nubian Watermelon (Citrullus lanatus L.). Journal of Advances in Microbiology, 16(2), 1-15.
Original Research Article


Neethu KB, Priji P, Unni KN, Sajiths S, Anithak N, Rosana B, Benkamins MB. New Bacillus thuringiensis strain isolated from the gut of Malabari goat ie effective against Tetranychus macfarlanie. Journal of applied entomology. 2015;140(3):187– 198 Dol : https : / doi . org / 10.1111/jen.12235.

Park YL, Lee JH. Deaf cell and tissue damage of cucumber caused by two spotted spider mite (Acari: Tetranychidae) . Journal of Economic Entomology. 2002; 95(5):952 – 957 .

Van Leeuwen T, Vontas J, Tsagkarakou A, Dermauw W, Tirry L. Acaricide resistance mechanisms in the two spotted spider mite Tetranychus urticae and other important Acari: A review. Insect Biochemistry and Molecular Biology. 2010;40(8):563–572. DOI:

Fiedler Ż. Interaction between beneficial organisms in control of spider mite Tetranychus urticae (Koch.). Journal of Plant Protection Research. 2012;52(2): 226–229.
DOI: https://

Arzanlou M, Mousavi S, Bakhshi M, Khakvar R, Bandehagh A. Inhibitory effects of antagonistic bacteria inhabiting the rhizosphere of the sugarbeet plants, on Cercospora beticolasacc, the Sacc. The causal agent of cerospora leaf spot disease on sugarbeet. Journal of plant; protection Research. 2016;56(1):6 – 14 . DoI : https : // .doi-org/10-1515/jppr – 2016 – 0002

Hamza A, Mohamed A, Derbalah A. Unconventional alertnatives for control of tomato root caused by Rhizoctonia solani under greenhouse conditions . Journal of plant protection research. 2016;56(3):298 -305.
DoI :

Chandanie WA, Kubota M, Hyakamachi M. Interaction between arbuscular mycorrhizal fungus Glomus mosseae and plant growth promoting fungus Phoma sp. on their root colonization and growth promotion of cucumber (Cucumis sativus). Mycoscience. 2006;46:201-204.

Cheplick GP. Recovery from drought stress in Lolium perenne (Poaceae): are fungal endophytes detrimental? American J. f Bot. 2004;91:1960-1968.

Harrison MJ. Signalling in the arbuscular mycorrhizal symbiosis. Anu. Rev. Microbiol. 2005;59:19-42.

Deshmukh S, Ckelhoven RH, Schafer P, Imani J, Sharma M, Weiss M, Waller F, Kogel KH. The root endophytic fungus Piriformospora indica requires host cell death for proliferation during mutualistic symbiosis with barley. PNAS. 2006; 103(49):18450-18457.

Murali M, Amruthesh KN, Sudisha J, Niranjana SR, Shetty HS. Screening for plant growth promoting fungi and their ability for growth promotion and induction of resistance in pearl millet against downy mildew disease. J. of Phytology. 2012; 4(5):30-36.

Hajek AE, Leger RJ. Interactions between fungal pathogens and insects hosts. Annu. Rev. Entomol. 1994;39:293-322. doi:10.1146/annurev.en.39.010194.001453

Manniche L. An ancient Egyptian herbel. Third university of Texas press printing. Great Britain. 1989;92.

FAO. The state of food insecurity in the world; 2008.

Mariod AA, Ahmed YM, Matthaus B, Khaled G, siddig A, Gaber AM, Abdelwahab SI. A comparative study of the properties of six Sudanese cucurbit seeds and seed oils. An oil chem. Soc. 2009;86(12):1181 – 1181.

Ibrahim MO, Ahmed FA, sulieman YR. The Nutritive value of Gurum seed cakes (Citrullus lanatus var. colocynthoid) as feed for ruminants . Sudan Ancient production. 2002;15:71 – 78 .

Ziyada AK, Elhussin SA. Physical and chemicals .characteristics of citrullus lanatus var. colocynthoide seed oil. physical. Sci. 2008;19(2):69 – 75 .

Masunaka A, Hyakumachi M, Takenaka S. (2011). Plant Growth–Promoting Fungus, Trichoderma koningi Suppresses Isoflavonoid Phytoalexin Vestitol Production for Colonization on/in the Roots of Lotus japonicas. Microbes Environ. 2011;26(2):128–134. DOI:10.1264/jsme2.ME10176

Pappas ML, Liapoura M, Papantoniou D, Avramidou M, Kavroulakis N, Weinhold A, Broufas GD, Papadopoulou KK. The Beneficial Endophytic Fungus Fusarium solani Strain K Alters Tomato Responses Against Spider Mites to the Benefit of the Plant. Front. Plant Sci. 2018;9:1603.
DOI: 10.3389/fpls.2018.01603

El-Bogdady MME. Integrated Postharvest Diseases Management of Certain Pome Fruits. Ph.D. thesis Fac. Agric., Al-Azhar Univ. 1993;55.

Siegler EH. Leaf dis technique for laboratory tests of acaricidesj. Econ. Entomod. 1947;40:441– 442 .

Henderson CF, Titton EW. Test with acaricides against the brown wheat mite .J .Econ. Entomol. 1955;48:157 – 161 .

Yadva UL. A rapid and non-destructive method to determine chlorophyll in intact leaves. Hort. Sci. 1986;21:1449.

Allen SG, Girmshaw HM, Parkinson JA, Quarmby C. Chemical analysis of ecological materials. Black Well Sci. Publ. Oxford, London. 1974;565.

Pregl F. Quantitative organic microanalysis 4th Edit. J. A. Churchill Ltd. London; 1945.

Trough E, Mager AH. Improvement in deiness colorimetric method for phosphorus and arsenic. Ind. En. Chemical Anal. Ed. 1939;1:136-139.

Brown JD, Lilliland O. Rapid determination of potassium and sodium in plant material and soils extracts by flam-photometry. Proc. Amer. Soc. Hort. Sci. 1946;48:341- 346.

Allen ON. Experiments in Soil Bacteriology. Burgess pub. Co., Ninn, Minnesota; 1959.

Casida LE, Klein DA and Snatoro T. Soil dehydrogenase activity. Soil Sci. 1964;98: 371-376.

Pancholy SK, Rice EL. Soil enzymes in relation to old succession: Amylase, invertase, cellulose, dehydrogenase and urease. Soil Sci. Soc. American Proc. 1973;37:47-50.

Duncan BD. Multiple range and multiple test. Biometrics. 1955;11:1 – 42 .

Exen C, Hayat R. Preliminary evaluation of Cladosporium cladosporioides (fresen) de vries in laboratory conditions, as a potential candidate for biocontrol of Tetranychus urticae (Koch) department of plant . World J. Microbiol. Biotechnal. 2009;25:489 – 492.

Amer SAA, Dimetry NZ, Mahran GH, Saleh MM, El-sherei MM, Motawe HM, M . H Grace MH. A caricid al and Biological properties of Brown marine Alga Petalomia fascia (Muller Kuntze) against the two – spotted spider mite Tetranychus urticae (koch) – Bull .zool, soc. Egypt. 1994;42:91 -101.

Magouz R. Integrated spider mite management. Ph.D. Agric. (pesticides). Tanta Univ. 2003;253 .

Benitez T, Rincón AMM, Limón C, Codón AC. Biocontrol mechanisms of Trichoderma strains. Int. Microbiol. 2004; 7:249–260

Harman GE, Howell CR, Vitrebo A, Chet I, Lorito M. Trichoderma species opportunistic, arivulent plant symbionts. Nat. Rev. Microbiol. 2004;2:43–56.

Harman GE. Overview of mechanisms and uses of Trichoderma spp. Phytopathol. 2006;96:190–194.

Dawar S, Hayat S, Anis M, Zaki MJ. Effect of seed coating material in the efficacy of microbial antagonistic for the control of root rot fungi on okra and sunflower. Pak. J. Bot. 2008;40(3):1269–1278.

Hoyos-Carvajal L, Ordua S, Bissett J. Growth stimulation in bean (Phaseolus vulgaris L.) by Trichoderma. Biol. Cont. 2009;51:409–416.

Shanmugaiah V, Balasubramanian N, Gomathinayagam S, Monoharan PT, Rajendran A. Effect of single application of Trichoderma viride and Pseudomonas fluorences on growth promotion in cotton plants. Afr J Agric Res. 2009;4(11):1220-1225

Azarmi R, Hajieghrari B, Gigloul A. Effect of Trichoderma isolates on tomato seedling growth response and nutrient uptake. Afr. J. Biotech. 2011;10:5850–5855.

Islam MS, Rahman MA, Bulbul SH, Alam MF. Effect of Trichoderma on seed germination and seeling parameters in chilli. Int. J. Expt. Agric. 2011;2(1):21–26.

Nagaraju A, Sudisha J, Mahadeva MS, Shin-ichi I. Seed priming with Trichoderma harzianum isolates enhances plant growth and induces resistance against Plasmopara halstedii, An incitant of sunflower downy mildew disease. Australasian Plant Pathol. 2012;41(6):609–620.
DOI: 10.1007/s13313-012-0165-z

Ruiz JM, Belakbir A, Lopez-Cantarero A, Romero L. Leaf macronutrient content and yield in grafted melon plants: a model to evaluate the influence of rootstock genotype. Sci. Hort. 1997;71:227-234.

Omara A, Hauka F, Afify A, Nour El-Din M, Kassem M. The Role of Some PGPR Strains to Biocontrol Rhizoctonia Solani in Soybean and Enhancement The Growth Dynamics and Seed Yield. Environ. Biodiv. & Soil Security. 2017;1:47 – 59.

El-Nahrawy S, Omara A. Effectiveness of Co-inoculation with Pseudomonas koreensis and Rhizobia on Growth, Nodulation and Yield of Common Bean (Phaseolus vulgaris L.). Microbiology Research Journal International. 2017; 21(6):1-15
Article no.MRJI.37422

Omara A, El-Gaafarey T. Alleviation of Salinity Stress Effects in Forage Cowpea (Vigna unguiculata L.) by Bradyrhizobium sp. Inoculation. Microbiology Research Journal International. 2018;23(3):1-16, Article no.MRJI.40727

Omara A, Azza AG, El-Akhdar IA. Isolation and Identification of Zinc Dissolving Bacteria and Their Potential on Growth of Zea mays. Egypt. J. Microbiol. 2016;51: 29 – 43.

Nour El-Din M, Omara A, Elbagory MH. Effect of Bulking Agent Levels (Rice Straw) on Compost Quality and Net Return. International Journal of Plant & Soil Science. 2016;19(3):1-12.

Article no.IJPSS.36518

Chendrayan K, Adhya JK, Sethunathan N. Dehydrogenase and invertase activities of flooded soils. Soil Biol. Biochem. 1980;12: 271-273.

Nagaraja MS, Ramakrishna VR, Siddaramappa R. Effect of atrazine urea-N-mineralization and activity of some soil enzymes. Indian J. Agron.1998;46:189-192.

El-Akhdar I, Omara A, Abdel-Rahman MA. Intergradation of different fertilizers for sustainable agriculture enhanced growth and yield of wheat (Triticum aestivum L.). Env. Biodiv. Soil Security. 2018;2:11- 24.

Das AC, Debnath A. Effect of systemic herbicides on N2-fixing and phosphate solubilizing microorganisms in relation to availability of nitrogen and phosphorus in paddy soils of West Bengal. Chemosphere. 2006;65:1082–1086.

DOI: 10.1016/j.chemosphere.2006.02.063

Chen Z, Chen H, Zou Y, Qiu J, Wen Y, Xu D. Are nutrient stresses associated with enantioselectivity of the chiral herbicide imazethapyr in Arabidopsis thaliana? J. Agric. Food Chem. 2015;63:10209–10217. DOI: 10.1021/acs.jafc.5b04495

Omara A, El-Ghandor A. Effect of thiobencarb and penoxsulam herbicides on soil microbial population and weed control in transplanted rice. Global Advanced Research Journal of Microbiology. 2018; 7(5):084-094.

Echebarria PH, Castro R, Vivaracho SM, Vallejo AD. Influence of rootstock and soil treatments on the yield and quality of greenhouse-grown cucumber in Spain. Acta. Hort. 2002;633:403-408.

El-Nemr M. Effect of mulch types on soil environmental conditions and their effect on the growth and yield of cucumber plants. App. Sci. Res. 2006;22:67-73.

Huh YC, Lee JM, Lee SG. The current situation and prospect of cucurbits grafting in Korea. Turkiye Ulusal V. Bah. Bit. Kong. 2007;37-39. Erzurum, Turkey.

Leoni S, Gruidina R, Cadinu M, Madeddu B, Carlett MG. The influence of four rootstocks on some melon hybrids and a cultivar in greenhouse. Acta. Hort. 1990; 287:127-134.

Lee JM (1994). Cultivation vegetable I. Current status, grafting methods, and benefits. Hort. 1994;29(4):235-239.

Kabeel SMAM. Effect of some Cucurbits root stocks on growth, yield and resistance to some soil pests of cucumber under plastic houses. Ph. D. Thesis. Zagazig Univ. Moshtohor. Egypt; 1999.

Abd Alla AM. Effect of soil solarization, fertilizer sort and grafting on growth and productivity of cucumber crop (Cucumis sativus, L.) Ph. D. Thesis. Fac. Agric., Kafr El-Sheikh.Tanta Univ, Egypt; 2002.

Hamed ESM. Effect of grafting on growth and yield of watermelon plants under low plastic tunnels in Baltiem district. Ph. D. Thesis. Fac. Agric. Kafr El-Sheikh.Tanta Univ., Egypt; 2005.

Yetisir H, Sari N. Effect of different rootstock on plant growth, yield and quality of watermelon. Aust. Exper. Agri. 2003; 43(10):1269 – 1274.

El-Tanbashawy H. Increase the Productivity of Nubian Watermelon Plant by Grafting Technique., Thesis, Faculty of Science, Tanta University; 2012.