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Herbicidal efficacy of culture filtrates of Alternaria brassicicola and Alternaria gaisen against parthenium weed

Abstract:

Background:

Parthenium hysterophorus L. is one of the top ten worst weeds globally and is recorded in the global database of invasive species.

Objective:

The current study was aimed to evaluate the herbicidal potential of Alternaria brassicicola (Schwein.) Wiltshire and Alternaria gaisen Nagano. culture filtrates against a problematic weed P. hysterophorus.

Methods:

A. brassicicola and A. gaisen culture filtrates were tested in vitro against the test weed. A. gaisen culture filtrates were found most effective against the test weed, and this test fungus was partitioned with various fractions viz. n-hexane, chloroform, ethyl acetate and n-butanol were isolated. In vitro bioactivity of these fractions were tested against P. hysterophorus. The most productive n-hexane fraction was subjected to GC-MS analysis, and thirteen compounds were identified.

Results:

A. gaisen original (100%) and diluted (50%) culture filtrates showed significant herbicidal activity against P. hysterophorus. However, culture filtrates of A. gaisen suppressed the germination, root and shoot growth of the test weed to a greater extent compared with culture filtrates of A. brassicicola . Original culture filtrates of A. gaisen significantly reduced germination of P. hysterophorus by 88% as compared to diluted concentration by 56% in comparison with control. On the other hand, original and diluted culture filtrates of A. brassicicola reduced the germination of P. hysterophorus by 69% and 50%, respectively, over control treatment. The n-hexane fraction was found more effective in suppressing the P. hysterophorus growth as compared to other fractions. Both 0.10% and 0.05% concentrations of n-hexane fraction significantly inhibited P. hysterophorus seedlings germination by 88% and 81%, respectively. The n-hexane fraction was subjected to GC-MS analysis, and thirteen compounds were identified. Among these, ocimene (27.63%); benzene 1-ethyl-3-methyl-(20.30%) and n-hexadecanoic acid (10.27%) were major compounds.

Conclusion:

The present study concludes that A. gaisen culture filtrate has substantial herbicidal potential against P. hysterophorous.

Keywords:
Alternative herbicides; Fungal metabolites; GC-MS analysis; in vitro; Organic fractions

1. Introduction

Parthenium (Parthenium hysterophorus L.), family Asteraceae, is a devastating and dangerous weed of many economically important crops (Ray, Gour, 2012Ray P, Gour H.Integrated management of Parthenium hysterophorus L.(Asteraceae): a weed of worldwide significance. Ind J Mycol Pl Path. 2012;5(1):605-32.). It is among the top ten worst weeds worldwide and is included in the world catalogue of aggressive species (Callaway, Ridenour, 2004Callaway RM, Ridenour MW, Novel weapons: invasive success and the evolution of increased competitive ability. Front Ecol Environ. 2004;2(8):436-43. Available from: https://doi.org/10.1890/1540-9295(2004)002[0436:NWISAT]2.0.CO;2
https://doi.org/10.1890/1540-9295(2004)0...
; Kapoor, 2012Kapoor R. Awareness related survey of an invasive alien weed, Parthenium hysterophorus L. in Gautam Budh Nagar district, Uttar Pradesh, India. J Agric Technol. 2012;8(3):1129-40.; Khan et al., 2020Khan N, Bibi K, Ullah R. Distribution pattern and ecological determinants of an invasive plant Parthenium hysterophorus L., in Malakand division of Pakistan. J Mt Sci. 2020;17:1670-83. Available from: https://doi.org/10.1007/s11629-019-5932-7
https://doi.org/10.1007/s11629-019-5932-...
). In 1955, it was accidentally introduced through imported food grains in the subcontinent (Hassanein et al., 2008Hassanein N, Abou Zeid M, Youssef K, Mahmoud D. Efficacy of leaf extracts of neem (Azadirachta indica ) and chinaberry (Melia azedarach ) against early blight and wilt diseases of tomato. Austr J Basic Appl Sci. 2008;2(3):763-72.). It is also responsible for significant losses in the agricultural and forestry sector (Knox et al. 2006Knox J, Dass A, Thomas M, Paul MS. Management of Parthenium hysterophorus L. through Atrazine with Cassia uniflora extract. Ann Plant Protect Sci. 2006;14(2):459-61.). P.hysterophorus also caused asthma, diarrhea and skin allergy in humans (Natukunda et al., 2020Natukunda MI, Natukunda K, Kyeyune G, Tusiime SM, Agbemafle I, Bisikwa J. Management strategies for the noxious invasive parthenium weed (Parthenium hysterophorus L.) in Uganda. Afr J Agric Res. 2020;15(1):1-9. Available from: https://doi.org/10.5897/AJAR2019.14569
https://doi.org/10.5897/AJAR2019.14569...
).

Use of commercial synthetic herbicides is considered as the most consistent and common technique for managing weeds. Another approach to control the weeds is to isolate natural herbicidal components from fungi culture filtrates (Zhang et al., 2010Zhang LH, Kang ZH, Jiao X, Xu WC, Zhang LJ. Isolation and structural indentification of herbicidal toxin fractions produced by Pythium aphanidermatum . Agric Sci China. 2010;9(7):995-1000. Available from: https://doi.org/10.1016/S1671-2927(09)60182-6
https://doi.org/10.1016/S1671-2927(09)60...
). Fungal metabolites can be used as a convenient biological pesticides tool (Cipriani et al., 2009Cipriani MG, Stea G, Moretti A, Altomare C, Mulè G, Vurro M. Development of a PCR-based assay for the detection of Fusarium oxysporum strain FT2, a potential mycoherbicide of Orobanche ramosa . Biol Control. 2009;50(1):78-84. Available from: https://doi.org/10.1016/j.biocontrol.2009.03.005
https://doi.org/10.1016/j.biocontrol.200...
; Sands, Pilgeram, 2009Sands DC, Pilgeram LA. Methods for selecting hypervirulent biocontrol agents of weeds: why and how. Pest Manag Sci. 2009;65(5):581-7. Available from: https://doi.org/10.1002/ps.1739
https://doi.org/10.1002/ps.1739...
; Javaid et al., 2017Javaid A, Mubeen T, Bashir U, Shoaib A. Management of parthenium weed using metabolites of Alternaria japonica . Planta Daninha. 2017;35:1-6. Available from: https://doi.org/10.1590/S0100-83582017350100016
https://doi.org/10.1590/S0100-8358201735...
; 2022Javaid A, Jabeen T, Khan IH, Jabeen K, Akbar M. Herbicidal potential of Alternaria citri Ellis and Pierce metabolites against Parthenium hysterophorus L. Allelopathy J. 2022;55(1):25-34. Available from: https://doi.org/10.26651/allelo.j/2022-55-1-1368
https://doi.org/10.26651/allelo.j/2022-5...
).

The members of Deuteromycetes (fungi imperfecti), specifically Alternaria spp. have an extensive distribution in nature and act as saprophytes, endophytes, weak facultative parasites, and plant pathogens (Thomma, 2003Thomma BPHJ. Alternaria spp.: from general saprophyte to specific parasite. Mol Plant Pathol. 2003;4(4):225-36. Available from: https://doi.org/10.1046/j.1364-3703.2003.00173.x
https://doi.org/10.1046/j.1364-3703.2003...
). Some metabolites from Alternaria fungus are labelled as phytotoxins and mycotoxins for plants and animals, respectively (Duke, Dayan, 2011Duke SO, Dayan EF. Modes of action of microbially-produced phytotoxins. Toxins. 2011;3(8):1038-64. Available from: https://doi.org/10.3390/toxins3081038
https://doi.org/10.3390/toxins3081038...
). Alternaria spp. metabolites have drawn the attention of many pharmacologists, chemists and plant pathologists in research programs due to the exhibition of various biological activities including herbicidal potential (Bräse et al., 2009Bräse S, Encinas A, Keck J, Nising CF. Chemistry and biology of mycotoxins and related fungal metabolites. Chem Rev. 2009;109(9):3903-90. Available from: https://doi.org/10.1021/cr050001f
https://doi.org/10.1021/cr050001f...
; Tsuge et al., 2013Tsuge T, Harimoto Y, Akimitsu K, Ohtani K, Kodama M, Akagi Y et al. Host-selective toxins produced by the plant pathogenic fungus Alternaria alternata . FEMS Microbiol Rev. 2013;37(1):44-66. Available from: https://doi.org/10.1111/j.1574-6976.2012.00350.x
https://doi.org/10.1111/j.1574-6976.2012...
; Bashir et al., 2018Bashir U, Khan A, Javaid A. Herbicidal activity of Aspergillus niger metabolites against parthenium weed. Planta Daninha. 2018;36:1-9. Available from: https://doi.org/10.1590/S0100-83582018360100025
https://doi.org/10.1590/S0100-8358201836...
). However, studied regarding herbicidal activities of A. brassicicola and A. gaisen against parthenium weed are lacking. Therefore, this study was planned to explore the herbicidal efficacy of culture filtrates of A. brassicicola and A. gaisen for Parthenium weed biocontrol.

2. Materials and methods

2.1 Preparation of fungal culture filterate

For the preparation of fungal culture filtrates, malt extract broth (2%) 200 mL was autoclaved at 121 ºC for 15 minutes in 500 mL flasks and cool at room temperature. Five-millimetre discs of A. brassicicola and A. gaisen were added to these flasks and incubated for 15 days at 25 °C. The fungal cultures were filtered through a sterilised muslin cloth and sterilised Whattman No. 1 filter paper (Javaid et al., 2017Javaid A, Mubeen T, Bashir U, Shoaib A. Management of parthenium weed using metabolites of Alternaria japonica . Planta Daninha. 2017;35:1-6. Available from: https://doi.org/10.1590/S0100-83582017350100016
https://doi.org/10.1590/S0100-8358201735...
). The filtered test fungal metabolites were centrifuged at 600 rpm for 5 minutes and then re-filtered with millipore filter paper.

2.2 In vitro bioassay of fungal culture filterate

In vitro assessment of fungal metabolites herbicidal activity against test, weed species was carried out following the protocol of Javaid and Ali (2011aJavaid A, Ali S. Alternative management of a problematic weed of wheat Avena fatua L. by metabolites of Trichoderma . Chil J Agri Res. 2011a;71(2):205-11. Available from: https://doi.org/10.4067/S0718-58392011000200004
https://doi.org/10.4067/S0718-5839201100...
; 2011bJavaid A, Ali S. Herbicidal activity of culture filtrates of Trichoderma spp. against two problematic weeds of wheat. Nat Prod Res. 2011b;25(7):730-40. Available from: https://doi.org/10.1080/14786419.2010.528757
https://doi.org/10.1080/14786419.2010.52...
). Nine-centimetre pre-sterilized Petri plates were taken and lined with sterilised filter papers. Twenty surface-sterilised seeds of P. hysterophorus were set in all experimental Petri plates. Two millilitres of 100% and 50% concentrations of culture filtrates of A. brassicicola and A. gaisen were transferred to every Petri plate. The diluted concentration was prepared using sterilised distilled water in a suitable amount (Akbar, Javaid, 2013Akbar M, Javaid A. Prospects of using fungal metabolites for the management of Rumex dentatus , a problematic weed of wheat. Int J Agric Biol. 2013;15(6):1277-82.). In Petri plates of control treatment, two millilitres of distilled water were added. Each treatment was replicated three times. All the plates were incubated at 25 °C in an incubator with ten h daily light period for seven days. After that, data about germination, shoot and root length and seedling’s fresh weight were noted.

2.3 Fractionation of culture filtrates of A. gaisen

A. gaisen culture filtrates were found very effective in reducing the in vitro growth of P. hysterophorus. Fifty millilitres of this fungal culture filtrate was taken for partitioning (Jabeen et al., 2014Jabeen K, Zubairi T, Iqbal S. Control of Botrytis cinerea (Grey mould disease) by methanolic extract of Pongamia pinnata L. Mitt Klostern. 2014;64(3):105-13.). Bioactive compounds in this filtrate were separated with several organic solvents like n-hexane, chloroform, ethyl acetate and n-butanol using a separating funnel. All the separated fractions were evaporated on a rotary evaporator which resulted in 0.02 g n-hexane, 0.01 g chloroform, 0.12 g ethyl acetate and 0.14 g n-butanol fraction.

2.4 In vitro bioassay with isolated fractions of culture filtrates of A. gaisen

The in vitro bioactivity of these four isolated fractions was studied. Two concentrations (0.10% & 0.05%) of each fraction were tested against P. hysterophorus . The experiment was conducted by the addition of 0.07 mg and 0.03 mg of all crude organic fractions and raised the final volume to 15 mL. Control medium was without any extract. All the treatments were replicated thrice.

2.5 Gas chromatography-mass spectrometry (GC-MS) analysis

A. gaisen culture filtrates n-hexane fraction was analysed on GC-MS chromatograph (GC-MS-QP 2010) to separate bioactive compounds against P. hysterophorous. This n-hexane fraction was filtered through nylon membrane filters of 0.22 µm pore size and 47 mm diameter by using filtration assembly. Chromatograph separated with the DB-5MS capillary column (0.25 µm, 0.25 mm, 30 m) was used to analyse the sample. Helium gas was used as a carrier gas and following program temperatures 40 °C for 5 min, 40-70 °C at 2 °C/min, 70 °C for 2 min, 70-120 °C at 3 °C/min, 120-150 °C at 5 °C/min, 150-220 °C at 10 °C/min and then 220 °C for 2 min were applied. The temperatures of the detector and injector were 250 °C and 200 °C, respectively. The mass detector conditions were: 70 ev ionisation voltage, m/z 29-540 mass scanning range and 230 °C base temperature. GC peak areas were used to compare the percentage configuration of volatile constituents. Qualitative analysis was done on software NIST Library 2010 (Sureshkumar et al., 2012Sureshkumar P, Senthilraja P, Kalavathy S. In-Silico docking analysis of Calotropis gigantea (L.) R. Br. derived compound against anti-cervical cancer activity. World Res J Comput-Aided Drug Des. 2012;1(1):9-12.) based on mass spectra, comparison of indices and retention times with the analogous data in the previous literature.

2.6 Statistical analysis

All the obtained data were statistically analysed at 5% level of significance by ANOVA (analysis of variance) and Duncan’s Multiple Range Test (Steel, Torrie, 1980Steel RGD, Torrie JH. Principles and procedures of statistics: a biometrical approach. 2nd ed. New York: McGraw Hill; 1980.).

3. Results and discussion

In this study, the effect of culture filtrates of Alternaria spp. viz. A. gaisen and A. brassicicola were observed on germination and seedling growth of P. hysterophorus. Herbicidal effect of original (100%) and diluted (50%) culture filtrates of A. gaisen was more pronounced than culture filtrates of A. brassicicola. The original and diluted concentrations of culture filtrates of A. gaisen showed remarkable effect by inhibiting the germination of parthenium by 88% and 56%, respectively, compared with control. Whereas original culture filtrate of A. brassicicola reduced P. hysterophorus germination by 69% and its diluted culture filtrate reduced germination by 50% of the tested weed specie as compared to the control treatment (Figure 1).

Figure 1
Effect of 100% and 50% concentrations of A. gaisen and A. brassicicola metabolites on germination of Parthenium seeds

In case of other growth parameters also both concentrations of A. gaisen showed a significant reduction in shoot length, shoot fresh weight, root length, root fresh weight and the decrease was 84-99%, 65-99%, 81-96% and 59-98% respectively (Figure 2A & B). On the other hand, culture filtrates of A. brassicicola reduced these growth parameters by 63-80%, 25-40%, 62-73%, 52-59%, respectively (Figure 3A & B). The metabolites of A. alternata, Fusarium solani, Drechslera rostrata, Trichoderma viride, T. pseudokoningii and T. harzianum significantly retarded the parthenium and other weed species seed germination (Javaid, Ali 2011aJavaid A, Ali S. Alternative management of a problematic weed of wheat Avena fatua L. by metabolites of Trichoderma . Chil J Agri Res. 2011a;71(2):205-11. Available from: https://doi.org/10.4067/S0718-58392011000200004
https://doi.org/10.4067/S0718-5839201100...
; 2011bJavaid A, Ali S. Herbicidal activity of culture filtrates of Trichoderma spp. against two problematic weeds of wheat. Nat Prod Res. 2011b;25(7):730-40. Available from: https://doi.org/10.1080/14786419.2010.528757
https://doi.org/10.1080/14786419.2010.52...
). Culture filtrates of Cladosporium oxysporum, Macrophomina phaseolina and Fusarium equisetti also significantly inhibited parthenium’s in vitro germination (Idrees, Javaid, 2008Idrees H, Javaid A. Screening of some pathogenic fungi for their herbicidal potential against parthenium weed. Pak J Phytopathol. 2008;20(1):150-5.).

Figure 2 A, B
Effect of 100% and 50% concentrations of A. gaisen and A. brassicicola metabolites on root & shoot length of Parthenium seeds
Figure 3 A, B
Effect of 100% and 50% concentrations of A. gaisen and A. brassicicola metabolites on root & shoot fresh weight of Parthenium seeds

Results regarding the herbicidal activity of n-hexane, chloroform, ethyl acetate and n-butanol fractions of A. gaisen culture filtrates against the test weed species P. hysterophorous are illustrated in (Figure 4). Data obtained after a seven-day incubation period revealed that the n-hexane fraction displayed the best herbicidal activity compared to other tested organic fractions. The applied concentrations of n-hexane fraction viz. 0.10% and 0.05% significantly inhibited the germination of test weed by 88% and 81%, respectively. This variable herbicidal expression of the applied fractions of fungal metabolites might cause the solubility of various compounds in different organic solvents (Zonno et al., 2008Zonno MC, Vurro M, Lucretti S, Andolfi A, Perrone C, Evidente A. Phyllostictine A, a potential natural herbicide produced by Phyllosticta cirsii: in vitro production and toxicity. Plant Sci. 2008;175(6):818-25. Available from: https://doi.org/10.1016/j.plantsci.2008.08.003
https://doi.org/10.1016/j.plantsci.2008....
). The herbicidal efficacy of Alternaria species could be owed to the production of some secondary metabolites, some of which are powerful mycotoxins (Thomma, 2003Thomma BPHJ. Alternaria spp.: from general saprophyte to specific parasite. Mol Plant Pathol. 2003;4(4):225-36. Available from: https://doi.org/10.1046/j.1364-3703.2003.00173.x
https://doi.org/10.1046/j.1364-3703.2003...
). Like A. alternata produced a phytotoxin AAL-toxin which has the potential of suppressing the growth of numerous weeds (Abbas et al., 1995Abbas HK, Tanaka T, Duke S, Boyette C. Susceptibility of various crop and weed species to AAL-toxin, a natural herbicide. Weed Technol. 1995;9(1):125-30. Available from: https://doi.org/10.1017/S0890037X0002306X
https://doi.org/10.1017/S0890037X0002306...
).

Figure 4
Result of various organic fractions concentrations of A. gaisen metabolite’s on in vitro growth of P. hysterophorus

Thirteen compounds were identified in the GC-MS analysis of n-hexane fraction of A. gaisen culture filtrates (Table 1). The compounds ocimene (27.6%), benzene 1-ethyl-3-methyl-(20.3%) and n-hexadecanoic acid (10.22%) were identified as major constituents. Other identified compounds were 3-trifluoroacetoxypentadecane (6.4%), trichloroacetic acid 2-tetradecyl ester (6.40%), Z,Z,Z-,4,6,9-nonadecatriene (4.4%), 2,2,6-trimethyl-bicyclo[4.1.0]hept-1-yl)-methanol (4.1%), 2-nitrohept-2-en-1-on (4.1%), Z,Z,Z-1,4,6,9-nonadecatetraene (4.0%), oleic acid (3.2%), 3-trifluoroacetoxytetradecane (3.2%), nonadecane (3.1%) and 3,7,11,15-tetramethyl-2-hexadecene-1-ol (2.7%). Javaid et al. (2019)Javaid A, Khan IH, Jabeen K, Bashir U. Evaluation of mycochemical profile of Alternaria japonica through GC-MS analysis. Pak J Phytopathol. 2019;31(2):171-5. Available from: https://doi.org/10.33866/phytopathol.031.02.0537
https://doi.org/10.33866/phytopathol.031...
also identified ten bioactive compounds from n-hexane fraction of A. japonica . Ocimene a monoterpene compound is well known for its antimicrobial activity. The antimicrobial effects of ocimene were also tested on economically important microbes, and promising results were found (Pirbalouti et al., 2016Pirbalouti AG, Izadi A, Poor FM, Hamedi B. Chemical composition, antioxidant and antibacterial activities of essential oils from Ferulago angulate . Pharm Biol. 2016;54(11):2515-20. Available from: https://doi.org/10.3109/13880209.2016.1162816
https://doi.org/10.3109/13880209.2016.11...
; Mahdian et al., 2017Mahdian F, Mahboub M, Rahimi E, Shad MM. Chemical composition, antimicrobial and antioxidant activities of Echinophora platyloba essential oil. Infect. 2017;21(3):171-86. Available from: https://doi.org/10.22354/in.v21i3.675
https://doi.org/10.22354/in.v21i3.675...
). The second major isolated compound was benzene 1-ethyl-3-methyl-which is an aromatic hydrocarbon). This compound possesses substantial antifungal and antibacterial property (Vukovic et al., 2007Vukovic N, Milosevic T, Sukdolak S, Solujic S. Antimicrobial activities of essential oil and methanol extract of Teucrium montanum . Evid Based Complement Alternat Med. 2007;4(Suppl.1):17-20. Available from: https://doi.org/10.1093/ecam/nem108
https://doi.org/10.1093/ecam/nem108...
). n-hexadecanoic acid a saturated fatty acid was also found in the GC-MS analysis in the present study. n-hexadecanoic acid was isolated from many plants and hold herbicidal and fungi toxic effects (Kordali et al., 2009Kordali S, Cakir A, Akcin TA, Mete E, Akcin A, Aydin T et al. Antifungal and herbicidal properties of essential oils and n-hexane extracts of Achillea gypsicola Hub-Mor. and Achillea biebersteinii Afan. (Asteraceae). Ind Crops Prod. 2009;29(2/3):562-70. Available from: https://doi.org/10.1016/j.indcrop.2008.11.002
https://doi.org/10.1016/j.indcrop.2008.1...
; Shirani et al., 2017Shirani M, Samimi A, Kalantari H, Madani M, Kord AZ. Chemical composition and antifungal effect of hydroalcoholic extract of Allium tripedale (Tvautv.) against Candida species. Curr Med Mycol. 2017;3(1):6-12. Available from: https://doi.org/10.18869/acadpub.cmm.3.1.6
https://doi.org/10.18869/acadpub.cmm.3.1...
). 3-trifluoroacetoxypentadecane a bioactive compound produced fungi-static effects against Aspergillus terreus. Oleic acid, an unsaturated fatty acid identified in the present study, was found to establish resistance in plants and microorganism and be used as a pesticide (Pohl et al., 2011Pohl CH, Kock JLF, Thibane VS. Antifungal free fatty acids: a review. In: Méndez-Vilas A, editor. Science against microbial pathogens: communicating current research and technological advances. Badajoz: Formatex; 2011. p. 61-71.). The substantial herbicidal effects of 3,7,11,15-tetramethyl-2-hexadecen-1-ol isolated from Mikania micrantha were also deliberated by Ni et al. (2007)Ni G, Li F, Chen B, Song L, Peng S. Allelopathic plants 21: Mikania micrantha H.B.K. Allelopathy J. 2007;19(2):287-95.

Table 1
GC-MS analysis of n-hexane fraction of culture filtrates of A. gaisen

4. Conclusion

This syudy conclude that the herbicidal potential of A. gaisen against P. hysterophorus could be attributed to the presence of many significant compounds present in this tested fungus. Furthermore, A. gaisen can effectively be used as an alternative to chemical herbicides to manage this problematic weed P. hysterophorus .

Acknowledgements

The authors are thankful to the Botany Department, Lahore College for Women University, Lahore, Pakistan, and its support in this study is acknowledged.

References

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    » https://doi.org/10.1017/S0890037X0002306X
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  • Bashir U, Khan A, Javaid A. Herbicidal activity of Aspergillus niger metabolites against parthenium weed. Planta Daninha. 2018;36:1-9. Available from: https://doi.org/10.1590/S0100-83582018360100025
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    » https://doi.org/10.1021/cr050001f
  • Callaway RM, Ridenour MW, Novel weapons: invasive success and the evolution of increased competitive ability. Front Ecol Environ. 2004;2(8):436-43. Available from: https://doi.org/10.1890/1540-9295(2004)002[0436:NWISAT]2.0.CO;2
    » https://doi.org/10.1890/1540-9295(2004)002[0436:NWISAT]2.0.CO;2
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    » https://doi.org/10.1016/j.biocontrol.2009.03.005
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  • Idrees H, Javaid A. Screening of some pathogenic fungi for their herbicidal potential against parthenium weed. Pak J Phytopathol. 2008;20(1):150-5.
  • Jabeen K, Zubairi T, Iqbal S. Control of Botrytis cinerea (Grey mould disease) by methanolic extract of Pongamia pinnata L. Mitt Klostern. 2014;64(3):105-13.
  • Javaid A, Ali S. Alternative management of a problematic weed of wheat Avena fatua L. by metabolites of Trichoderma . Chil J Agri Res. 2011a;71(2):205-11. Available from: https://doi.org/10.4067/S0718-58392011000200004
    » https://doi.org/10.4067/S0718-58392011000200004
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    » https://doi.org/10.1080/14786419.2010.528757
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    » https://doi.org/10.33866/phytopathol.031.02.0537
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    » https://doi.org/10.1590/S0100-83582017350100016
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Edited by

Approved by:
Editor in Chief: Anderson Luis Nunes

Publication Dates

  • Publication in this collection
    09 Mar 2022
  • Date of issue
    2022

History

  • Received
    09 Apr 2019
  • Accepted
    23 May 2020
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