AI Chat Paper
Note: Please note that the following content is generated by AMiner AI. SciOpen does not take any responsibility related to this content.
{{lang === 'zh_CN' ? '文章概述' : 'Summary'}}
{{lang === 'en_US' ? '中' : 'Eng'}}
Chat more with AI
Powered by AMiner. Clicking this button will take you away from SciOpen.
Home The Crop Journal Article
PDF (499.9 KB)
Cite
EndNote(RIS) BibTeX
Collect
Submit Manuscript AI Chat Paper
Show Outline
Outline
Show full outline
Hide outline
Outline
Show full outline
Hide outline
Research paper | Open Access

Influence of nitrogen sources on growth and mycotoxin production by isolates of Pyrenophora tritici-repentis from wheat

Noureddine Bourasa,b,c( ), Michael D. Holtza,d, Reem Aboukhaddoura, Stephen E. Strelkova( )
Department of Agricultural, Food and Nutritional Science, 410 Agriculture/Forestry Centre, University of Alberta, Edmonton, Alberta T6G 2P5, Canada
Laboratoire de Biologie des Systèmes Microbiens (LBSM), Ecole Normale Supérieure de Kouba, Algiers, Algeria
Département de Biologie, Faculté des Sciences de la Nature et de la Vie et Sciences de la Terre, Université de Ghardaïa, BP 455, Ghardaïa 47000, Algeria
Field Crop Development Centre, Alberta Agriculture and Food, 6000 C&E Trail, Lacombe, AB T4L 1W1, Canada

Peer review under responsibility of Crop Science Society of China and Institute of Crop Science, CAAS.

Show Author Information

Abstract

The fungus Pyrenophora tritici-repentis (Died.) Drechs. infects the leaves and kernels of wheat, causing tan spot and red smudge, respectively. Isolates of P. tritici-repentis have been reported to be both phytopathogenic and mycotoxigenic. This research investigates the influence of nitrogen sources on growth and production of mycotoxins by eight different isolates of P. tritici-repentis. A synthetic agar medium (SAM) was used with different nitrogen sources, both inorganic [(NH4Cl, NH4NO3 and (NH4)2SO4)] and organic (L-alanine, L-histidine, and L-lysine), at a concentration of 37.5 mmol L−1. Individual isolates exhibited different growth rates that varied according to the nitrogen source added to the medium. The choice of nitrogen source also had a major effect on production of the mycotoxins emodin, catenarin and islandicin. The highest concentrations of emodin, 54.40 ± 4.46 μg g−1, 43.07 ± 23.39 μg g−1 and 28.91 ± 4.64 μg g−1 of growth medium, were produced on the complex medium (V8-potato dextrose agar) by the isolates Alg-H2, 331-2 and TS93-71B, respectively. A relatively high concentration of emodin also was produced by isolates Az35-5 (28.29 ± 4.71 μg g−1 of medium) and TS93-71B (27.03 ± 4.09 μg g−1 of medium) on synthetic medium supplemented with L-alanine. The highest concentrations of catenarin (174.54 ± 14.46 μg g−1 and 104.87 ± 6.13 μg g−1 of medium) were recorded for isolates TS93-71B and Alg-H2 on synthetic medium supplemented with L-alanine and NH4Cl, respectively. The highest concentration of islandicin (4.64 ± 0.36 μg g−1 medium) was observed for isolate 331-2 in the presence of L-lysine. There was not a close relationship between mycelial growth and mycotoxin production by the fungal isolates. This is the first report on the influence of nitrogen sources on the production of mycotoxins by P. tritici-repentis.

Keywords

Triticum aestivumCatenarinEmodinIslandicinNitrogen sourceTan spot

References

[1]
R.M. Hosford, Tan spot, in: R.M. Hosford (Ed.), Tan Spot ofWheat and Related Diseases, North Dakota State University, Fargo, ND 1982, pp. 1–24.
[2]

A. Shabber, W.W. Bockus, Tan spot effects on yield and yield components relative to growth stage in winter wheat, Plant Dis. 72 (1988) 599-602.
Crossref Google Scholar
[3]

E.E. Sykes, C.C. Bernier, Qualitative inheritance of tan spot resistance in hexaploid, tetraploid and diploid wheat, Can. J. Plant Pathol. 13 (1991) 38-44.
Crossref Google Scholar
[4]
J. Menzies, J. Gilbert, Diseases of wheat, in: K.L. Bailey, B.D.Gossen, R.K. Gugel, R.A.A. Morrall (Eds.), Diseases of FieldCrops in Canada, Canadian Phytopathological Society, thirded.Canadian Phytopathological Society, Harrow, ON 2003, pp. 94–128.
[5]

M.R. Fernandez, J.M. Clarke, R.M. Depauw, Effect of environmental variables on the development of kernel discoloration by Pyrenophora tritici-repentis in durum wheat, Can. J. Plant Pathol. 20 (1998) 104-110.
Crossref Google Scholar
[6]

W. Wakuliński, P. Kachli cki, P. Sobiczewski, M. Schollenberger, C.Z. Zamorski, B. Łotocka, J. Šarova, Catenarin production by isolates of Pyrenophora tritici-repentis (Died.) Drechsler and its antimicrobial activity, J. Phytopathol. 151 (2003) 74-79.
Crossref Google Scholar
[7]

N. Bouras, S.E. Strelkov, The anthraquinone catenarin is phytotoxic and produced in leaves and kernels of wheat infected by Pyrenophora tritici-repentis, Physiol. Mol. Plant Pathol. 72 (2008) 87-95.
Crossref Google Scholar
[8]

W.B. Turner, Fungal Metabolites, Academic Press, New York,1971.
[9]

C. Moreau, Moulds, Toxins and Food, John Wiley and Sons,New York, 1974.
[10]

J.M. Wells, R.J. Col, J.W. Kirksey, Emodin, a toxic metabolite of Aspergillus wentii isolated from weevil-damaged chestnuts, Appl. Microbiol. 30 (1975) 26-28.
Crossref Google Scholar
[11]

D.F. Liberman, F.L. Schaefer, R.C. Fink, M. Ramgopal, A.C. Ghosh, R. Mulcahy, Mutagenicity of islandicin and chrysophanol in the Salmonella/microsome system, Appl. Environ. Microbiol. 40 (1980) 476-479.
Crossref Google Scholar
[12]

S.O. Müller, I. Eckert, W.K. Lutz, H. Stopper, Genotoxicity of the laxative drug components emodin, aloe-emodin and danthron in mammalian cells: topoisomerase II mediated? Mutat. Res. 371 (1996) 165-173.
Crossref Google Scholar
[13]

B. Franck, Mycotoxins from mold fungi — weapons of uninvited fellow-borders of man and animal: structures, biological activity, biosynthesis and precaution, Angew. Chem. Int. Ed. Engl. 23 (1984) 493-505.
Crossref Google Scholar
[14]

V. Betina, Mycotoxins: Chemical, Biological, and EnvironmentalAspects, Elsevier, New York, 1989.
[15]

J. Vytřasová, P. Přibáňová, L. Marvanová, Occurrence of xerophilic fungi in bakery gingerbread production, Int. J. Food Microbiol. 6 (2002) 91-96.
Crossref Google Scholar
[16]

J.P.F. D'Mello, A.M.C. Macdonald, Mycotoxins, Anim. Feed Sci. Technol. 69 (1997) 155-166.
Crossref Google Scholar
[17]

R. Steiman, F. Seigle-murandi, L. Sage, S. Krivobok, Production of patulin by micromycetes, Mycopathologia 105 (1989) 129-133.
Crossref Google Scholar
[18]

K. Engström, S. Brishammar, C. Svensson, M. Bengtsson, R. Anderson, Anthraquinones from some Drechslera species and Bipolaris sorokiniana, Mycol. Res. 97 (1993) 381-384.
Crossref Google Scholar
[19]

S.P. Abbott, Mycotoxins and indoor molds, Indoor Environ. Connect. 3 (2002) 14-24.
Google Scholar
[20]

C. Tanaka, H. Miyagawa, Y. Kuwahara, M. Tsuda, Accumulation of anthraquinones in the reddish brown-colored polyoxin resistant mutants of Cochliobolus heterostrophus, Mycoscience 43 (2002) 317-320.
Crossref Google Scholar
[21]
D.K. Arora, Fungal Biotechnology in Agricultural, Food, andEnvironmental Applications, Mycology Series, 21, MarcelDekker Inc., New York, 2004.
[22]

B. Prieto-Simón, T. Noguer, M. Campas, Emerging biotools for assessment of mycotoxins in the past decade, Trends Anal. Chem. 26 (2007) 689-702.
Crossref Google Scholar
[23]

P.S. Solomon, Assessing the mycotoxigenic threat of necrotrophic pathogens of wheat, Mycotoxin Res. 27 (2011) 231-237.
Crossref Google Scholar
[24]

E. Mühlencoert, I. Mayer, M.W. Zapf, R.F. Vogel, L. Niessen, Production of ochratoxin A by Aspergillus ochraceus, Eur. J. Plant Pathol. 110 (2004) 651-659.
Crossref Google Scholar
[25]

M. Rosfarizan, A.B. Ariff, Kinetics of kojic acid fermentation by Aspergillus flavus using different types and concentrations of carbon and nitrogen sources, J. Ind. Microbiol. Biotechnol. 25 (2000) 20-24.
Crossref Google Scholar
[26]

K.C. Ehrlich, P.J. Cotty, Variability in nitrogen regulation of aflatoxin production by Aspergillus flavus strains, Appl. Microbiol. Biotechnol. 60 (2002) 174-178.
Crossref Google Scholar
[27]

M. Mihlan, V. Homann, T.W. Liu, B. Tudzynski, AREA directly mediates nitrogen regulation of gibberellin biosynthesis in Gibberella fujikuroi, but its activity is not affected by NMR, Mol. Microbiol. 47 (2003) 975-991.
Crossref Google Scholar
[28]

J.J. Wang, C.L. Lee, T.M. Pan, Improvement of monacolin K, γ-aminobutyric acid and citrinin production ratio as a function of environmental conditions of Monascus purpureus NTU 601, J. Ind. Microbiol. Biotechnol. 30 (2003) 669-676.
Crossref Google Scholar
[29]

R. Geisen, Molecular monitoring of environmental conditions influencing the induction of ochratoxin A biosynthesis genes in Penicillium nordicum, Mol. Nutr. Food Res. 48 (2004) 532-540.
Crossref Google Scholar
[30]

S.E. Strelkov, L. Lamari, R. Sayoud, R.B. Smith, Comparative virulence of chlorosis-inducing races of Pyrenophora tritici-repentis, Can. J. Plant Pathol. 24 (2002) 29-35.
Crossref Google Scholar
[31]

L. Lamari, S.E. Strelkov, A. Yahyaoui, J. Orabi, R.B. Smith, The identification of two new races of Pyrenophora tritici-repentis from the host center of diversity confirms a one-to-one relationship in tan spot of wheat, Phytopathology 93 (2003) 391-396.
Crossref Google Scholar
[32]

L. Lamari, C.C. Bernier, Evaluation of wheat lines and cultivars to tan spot [Pyrenophora tritici-repentis] based on lesion type, Can. J. Plant Pathol. 11 (1989) 49-56.
Crossref Google Scholar
[33]

G. Awad, F. Mathieu, Y. Coppel, A. Lebrihi, Characterization and regulation of new secondary metabolites from Aspergillus ochraceus M18 obtained by UV mutagenesis, Can. J. Microbiol. 51 (2005) 59-67.
Crossref Google Scholar
[34]
J.I. Pitt, A.D. Hocking, Fungi and Food Spoilage, second ed.Blackie Academic and Professional, London, 1997.
Crossref
[35]

M.R. Bragulat, M.L. Abarca, F.J. Cabañes, An easy screening method for fungi producing ochratoxin A in pure culture, Int. J. Food Microbiol. 71 (2001) 139-144.
Crossref Google Scholar
[36]

N. Bouras, S.E. Strelkov, Influence of carbon source on growth and mycotoxin production by isolates of Pyrenophora tritici-repentis from wheat, Can. J. Microbiol. 56 (2010) 874-882.
Crossref Google Scholar
[37]
M.A. Klich, Identification of Common Aspergillus Species, Centraalbureau voor Schimmelcultures, Utrecht, TheNetherlands, 2002.
[38]
J. Lacey, A. Ramakrishna, N. Hamer, N. Magan, I.C. Marfleet, Grain fungi, in: D.K. Arora, K.G. Mukerji, E.H. Marth (Eds.), Handbook of Applied Mycology, Foods and Feeds, 3, MarcelDekker, New York 1991, pp. 121–177.
[39]

H.S. Hussein, J.M. Brasel, Toxicity, metabolism, and impact of mycotoxins on humans and animals, Toxicology 167 (2001) 101-134.
Crossref Google Scholar
[40]

W.T. Shier, D. Mebs, Handbook of Toxicology, Marcel Dekker, New York, 1990.
[41]

H. Anke, I. Kolthoum, H. Zahner, M. Laatsch, The anthraquinones of the Aspergillus glaucus group: I. Occurrence, isolation, identification and antimicrobial activity, Arch. Microbiol. 126 (1980) 223-230.
Crossref Google Scholar
[42]

T. Ubbink-Kok, J.A. Anderson, W.N. Konings, Inhibition of electron transfer and uncoupling effects by emodin and emodinanthrone in Escherichia coli, Antimicrob. Agents Chemother. 30 (1986) 147-151.
Crossref Google Scholar
[43]
A.C. Ghosh, A. Manmade, A.L. Demain, Toxins fromPenicillium islandicum Sopp, in: J.V. Rodricks, C.W. Hesseltine, M.A. Mehlman (Eds.), Proceedings of a Conference onMycotoxins in Human and Animal Health, PathotoxPublishers, Chicago 1977, pp. 625–638.
[44]

U. Sankawa, Y. Ebizuka, S. Shibata, Biosynthetic incorporation of emodin and emodinanthrone into the anthraquinonoids of Penicillium brunneum and P. islandicum, Tetrahedron Lett. 23 (1973) 2125-2128.
Crossref Google Scholar
[45]
M. Weidenbörner, Encyclopedia of Food Mycotoxins, Springer, Berlin, 2001.
Crossref
[46]

I. Kurobane, L.C. Vining, A.G. Mcinnes, Biosynthetic relationships among the secalonic acids: isolation of emodin, endocrocin, and secalonic acids from Pyrenochaeta terrestris and Aspergillus aculeatus, J. Antibiot. 32 (1979) 1256-1266.
Crossref Google Scholar
[47]

J.E. Smith, R.S. Henderson, Mycotoxins and Animal Foods, CRC Press, Boca Raton, Florida, 1991.
[48]

M. Khalesi, N. Khatib, The effects of different ecophysiological factors on ochratoxin A production, Environ. Toxicol. Pharmacol. 32 (2011) 113-121.
Crossref Google Scholar
[49]

Y. Içgen, B. Içgen, G. Özcengiz, Regulation of crystal protein biosynthesis by Bacillus thuringiensis: II. Effects of carbon and nitrogen sources, Res. Microbiol. 153 (2002) 603-609.
Crossref Google Scholar
[50]

C.J.L. Lopez, S.J.A. Perez, F.J.M. Sevilla, A.F.G. Fernandez, M.E. Grima, Y. Chisti, Production of lovastatin by Aspergillus terreus: effects of the C:N ratio and the principal nutrients on growth and metabolite production, Enzym. Microb. Technol. 23 (2003) 270-277.
Crossref Google Scholar
[51]

P. Häggblom, Production of ochratoxin A in barley by Aspergillus ochraceus and Penicillium viridicatum: effect of fungal growth, time, temperature, and inoculum size, Appl. Environ. Microbiol. 43 (1982) 1205-1207.
Crossref Google Scholar
[52]

N. Paster, D. Huppert, R. Barkei-Golan, Production of patulin by different strains of Penicillium expansum in pear and apple cultivars stored at different temperatures and modified atmospheres, Food Addit. Contam. 12 (1995) 51-58.
Crossref Google Scholar
[53]

M. Lai, G. Semeniuk, C.W. Hesseltine, Conditions for production of ochratoxin A by Aspergillus species in a synthetic medium, Appl. Microbiol. 19 (1970) 542-544.
Crossref Google Scholar
[54]

L. Lamari, S.E. Strelkov, A. Yahyaoui, M. Amedov, M. Saidov, M. Djunusova, M. Koichbayev, Virulence of Pyrenophora tritici-repentis in the countries of the Silk Road, Can. J. Microbiol. 27 (2005) 383-388.
Crossref Google Scholar
[55]

S. Fraleigh, H. Bungay, A. Fiechter, Regulation of oxidoreductive yeast metabolism by extracellular factors, J. Biotechnol. 12 (1989) 185-198.
Crossref Google Scholar
[56]

A. Medina, E.M. Mateo, F.M. Valle-Algarra, F. Mateo, R. Mateo, M. Jiménez, Influence of nitrogen and carbon sources on the production of ochratoxin A by ochratoxigenic strains of Aspergillus spp. isolated from grapes, Int. J. Food Microbiol 122 (2008) 93-99.
Crossref Google Scholar
[57]

W. Giordano, J. Avalos, E. Cerdao, C.E. Domenech, Nitrogen availability and production of bikaverin and gibberellins in Gibberella fujikuroi, FEMS Microbiol. Lett. 173 (1999) 389-393.
Crossref Google Scholar
[58]

J. Heim, Y.Q. Shen, S. Wolfe, A.L. Demain, Regulation of isopenicillin N synthetase and deacetoxycephalosporin C synthetase by carbon source of Cephalosporium acremonium, Appl. Microbiol. Biotechnol. 19 (1984) 232-236.
Crossref Google Scholar
[59]

A. Lebrihi, D. Lamsaif, G. Lefebvre, P. Germain, Effect of ammonium ions on spiramycin biosynthesis in Streptomyces ambofaciens, Appl. Microbiol. Biotechnol. 37 (1992) 382-387.
Crossref Google Scholar
[60]

A. Lounès, A. Lebrihi, C. Benslimane, G. Lefebvre, P. Germain, regulation of valine catabolism by ammonium in Streptomyces ambofaciens, producer of spiramycin, Can. J. Microbiol. 41 (1995) 800-808.
Crossref Google Scholar
[61]

L. Tang, Y.X. Zhang, C.R. Hutchinson, Amino acid catabolism and antibiotic synthesis: valine is source for precursors for macrolide biosynthesis in Streptomyces ambofaciens and Streptomyces fradiae, J. Bacteriol. 176 (1994) 6107-6119.
Crossref Google Scholar
[62]

S.H. Lee, Ammonium ion affecting tylosin production by Streptomyces fradiae NRRL 2702 in continuous culture, Lett. Appl. Microbiol. 25 (1997) 349-352.
Crossref Google Scholar
[63]

J. Zhang, S. Wolfe, A.L. Demain, Ammonium ions repress δ-(L-α-aminoadipyl)-L-cysteinyl-D-valine synthetase in Streptomyces clavuligerus NRRL 3585, Can. J. Microbiol. 35 (1989) 399-402.
Crossref Google Scholar
[64]

O. Litzka, K. Thenbergh, J. Van den Brulle, S. Steidl, A.A. Brakhage, Transcriptional control of expression of fungal β-lactam biosynthesis genes, Anton Leeuw. 75 (1999) 95-105.
Crossref Google Scholar
[65]

A.L. Demain, Production of beta-lactam antibiotics and its regulation, Proc. Natl. Sci. Counc. Repub. China B Life Sci. 15 (1991) 251-265.
Google Scholar
[66]

S. Untrau, A. Lebrihi, G. Lefebvre, P. Germain, Nitrogen catabolite regulation of spiramycin production in Streptomyces ambofaciens, Curr. Microbiol. 28 (1994) 111-118.
Crossref Google Scholar
[67]

N. Bouras, F. Mathieu, N. Sabaou, A. Lebrihi, Nutritional requirements for the production of dithiolopyrrolone antibiotics by Saccharothrix algeriensis NRRL B-24137, Enzym. Microb. Technol. 39 (2006) 1423-1429.
Crossref Google Scholar
[68]

P. Giorni, N. Magan, P. Battilani, Environmental factors modify carbon nutritional patterns and niche overlap between Aspergillus flavus and Fusarium verticillioides strains from maize, Int. J. Food Microbiol. 15 (2009) 213-218.
Crossref Google Scholar
[69]

A. Astoreca, C. Magnoli, C. Barberis, S.M. Chiacchiera, M. Combina, A. Dalcero, Ochratoxin A production in relation to ecophysiological factors by Aspergillus section Nigri strains isolated from different substrates in Argentina, Sci. Total Environ. 388 (2007) 16-23.
Crossref Google Scholar
[70]
O. Filtenborg, J.C. Frisvad, U. Thrane, The Significance ofyeast extract composition on metabolite production inPenicillium, in: R.A. Samson, J.I. Pitt (Eds.), Modern Concepts inPenicillium and Aspergillus Classification, NATO ASI Series, 185, Springer, New York 1990, pp. 433–441.
Crossref
[71]

D.P. Overy, K.A. Seifert, M.E. Savard, J.C. Frisvad, Spoilage fungi and their mycotoxins in commercially marketed chestnuts, Int. J. Food Microbiol. 88 (2003) 69-77.
Crossref Google Scholar
[72]

A. Astoreca, C. Magnoli, M.L. Ramirez, M. Combina, A. Dalcero, Water activity and temperature effects on growth of Aspergillus niger, A. awamori and A. carbonarius isolated from different substrates in Argentina, Int. J. Food Microbiol. 119 (2007) 314-318.
Crossref Google Scholar
[73]

N. Bouras, F. Mathieu, Y. Coppel, S.E. Strelkov, A. Lebrihi, Occurrence of naphtho-gamma-pyrones- and ochratoxin A-producing fungi in French grapes and characterization of new naphtho-gamma-pyrone polyketide (aurasperone G) isolated from Aspergillus niger C-433, J. Agric. Food Chem. 55 (2007) 8920-8927.
Crossref Google Scholar
[74]

E. Pardo, S. Marín, V. Sanchis, A.J. Ramos, Impact of relative humidity and temperature on visible fungal growth and OTA production of ochratoxigenic Aspergillus ochraceus isolates on grapes, Food Microbiol. 22 (2005) 383-389.
Crossref Google Scholar
[75]

A. Esteban, K.L. Abarca, M.R. Bragulat, F.J. Cabañes, Effect of water activity on ochratoxin A production by Aspergillus niger aggregate species, Int. J. Food Microbiol. 108 (2006) 188-195.
Crossref Google Scholar
[76]

L.F. Linhares, J.P. Martin, Decomposition in soil of emodin, chrysophanic acid, and a mixture of anthraquinones synthesized by an Aspergillus glaucus isolate, Soil Sci. Soc. Am. J. 43 (1979) 940-945.
Crossref Google Scholar
[77]

R.H. Thomson, Naturally Occurring Quinones, second ed.Academic Press, London, 1971.
[78]

R.F. Curtis, C.H. Hassal, D.R. Perry, The biosynthesis of phenols XXIV: The conversion of the anthraquinone question into the benzophenone, sulochrin, in cultures of Aspergillus terreus, J. Chem. Soc. Perkin Trans. 12 (1972) 240-244.
Crossref Google Scholar
[79]

J. Téren, J. Varga, Z. Hamari, E. Rinyu, F. Kevei, Immunochemical detection of ochratoxin A in black Aspergillus strains, Mycopathologia 134 (1996) 171-176.
Crossref Google Scholar
[80]

J. Varga, K. Rigó, T. Téren, Degradation of ochratoxin A by Aspergillus species, Int. J. Food Microbiol. 59 (2000) 1-7.
Crossref Google Scholar
[81]

N. Bouras, Y.M. Kim, S.E. Strelkov, Influence of water activity and temperature on mycotoxins produced by Pyrenophora tritici-repentis, Int. J. Food Microbiol. 131 (2009) 251-255.
Crossref Google Scholar
The Crop Journal
Volume 4 Issue 2,
April 2016
Pages 119-128
DOI: 10.1016/j.cj.2016.01.005
Cite this article:
Bouras N, Holtz MD, Aboukhaddour R, et al. Influence of nitrogen sources on growth and mycotoxin production by isolates of Pyrenophora tritici-repentis from wheat. The Crop Journal, 2016, 4(2): 119-128. https://doi.org/10.1016/j.cj.2016.01.005

223

Views

1

Downloads

7

Crossref

N/A

Web of Science

8

Scopus

0

CSCD

Altmetrics
Received: 08 September 2015
Revised: 09 January 2016
Accepted: 02 February 2016
Published: 12 February 2016
© 2016 Crop Science Society of China and Institute of Crop Science, CAAS.

This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
Return