Skip to main content
SpringerLink
Log in

Disease development and mycotoxin production by the Fusarium graminearum species complex associated with South African maize and wheat

  • Published:
European Journal of Plant Pathology Aims and scope Submit manuscript

Abstract

Fungal species comprising the Fusarium graminearum species complex (FGSC) may cause disease in maize and wheat. Host preference within the FGSC has been suggested, in particular F. boothii towards maize ears. Therefore, the disease development and mycotoxin production of five FGSC species in maize and wheat grain was determined. Eighteen isolates representing F. acaciae-mearnsii, F. boothii, F. cortaderiae, F. graminearum and F. meridionale were used. Each isolate was inoculated on maize ears and wheat heads to determine host preferences. Disease severity and disease incidence was measured for maize and wheat, respectively. Fungal colonisation and mycotoxins, deoxynivalenol (DON), nivalenol and zearalenone, was also quantified. Isolates differed significantly (P < 0.05) in their ability to produce symptoms on maize ears, however, no significant differences between FGSC species were determined. Similarly, significant differences (P < 0.05) between isolates but not between FGSC species in disease incidence on wheat were determined. The isolates also differed significantly (P < 0.05) in their ability to colonise maize and wheat grain. No significant differences in fungal colonisation, among the five FGSC species, were determined in field grown maize. However, under greenhouse conditions, F. boothii was the most successful coloniser of maize grain (P < 0.05). In wheat, F. graminearum colonised the grain more successfully and produced significantly more (P < 0.05) DON than the other species. Fusarium boothii isolates were the best colonisers and mycotoxin producers in maize, and F. graminearum isolates in wheat. The selective advantage of F. boothii to cause disease on maize was supported in this study.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Alexander, N. J., McCormick, S. P., Waalwijk, C., van der Lee, T., & Proctor, R. H. (2011). The genetic basis for 3-ADON and 15-ADON trichothecene chemotypes in Fusarium. Fungal Genetics and Biology, 48, 485–495.

    Article  CAS  PubMed  Google Scholar 

  • Aoki, T., Ward, T. J., Kistler, H. B., & O’Donnell, K. (2012). Systematics, phylogeny and Trichothecene mycotoxin potential of fusarium head blight cereal pathogens. Mycotoxins, 62(2), 91–102.

    Article  CAS  Google Scholar 

  • Atoui, A., El Khoury, A., Kallassy, M., & Lebrihi, A. (2012). Quantification of Fusarium graminearum and Fusarium culmorum by real-time PCR system and zearalenone assessment in maize. International Journal of Food Microbiology, 154, 59–65.

    Article  CAS  PubMed  Google Scholar 

  • Beukes, I., Rose, L.J., Shephard, G.S., Flett, B.C. & Viljoen, A. (2017). Mycotoxigenic Fusarium species associated with grain crops in South Africa – A review. South African Journal of Science, 113 (3/4), art. #2016-0121, 12 pages.

  • Boutigny, A.-L., Ward, T. J., Van Coller, G. J., Flett, B., Lamprecht, S. C., O’Donnell, K., et al. (2011). Analysis of the Fusarium graminearum species complex from wheat, barley and maize in South Africa provides evidence of specie-specific differences in host preference. Fungal Genetics and Biology, 48(9), 914–920.

    Article  CAS  PubMed  Google Scholar 

  • Boutigny, A.-L., Beukes, I., Small, I., Zuhlke, S., Spiteller, M., Van Rensburg, B. J., Flett, B., & Viljoen, A. (2012). Quantitative detection of Fusarium pathogens and their mycotoxins in south African maize. Plant Pathology, 61(3), 522–531.

    Article  CAS  Google Scholar 

  • Boutigny, A.-L., Ward, T. J., Ballois, N., Iancu, G., & Ioos, R. (2014). Diversity of the Fusarium graminearum species complex on French cereals. European Journal of Plant Pathology, 138, 133–148.

    Article  CAS  Google Scholar 

  • Burlakoti, R. R., Estrada Jr., R., Rivera, V. V., Boddeda, A., Secor, G. A., et al. (2007). Real-time PCR quantification and mycotoxin production of Fusarium graminearum in wheat inoculated with isolates collected from potato, sugar beet, and wheat. Phytopathology, 97(7), 835–841.

    Article  CAS  PubMed  Google Scholar 

  • Burlakoti, P., Rivera, V., Secor, G. A., Qi, A., Del Rio-Mendoza, L. E., & Khan, M. F. R. (2012). Comparative pathogenicity and virulence of Fusarium species on sugar beet. Plant Disease, 96, 1291–1296.

  • Bustin, S. A., Benes, V., Garson, J. A., Hellemans, J., Huggett, J., Kubista, M., et al. (2009). The MIQE guidelines: Minimum information for publication of quantitative real-time PCR experiments. Clinical Chemistry, 55(4), 611–622.

    Article  CAS  PubMed  Google Scholar 

  • Clements, M. J., Maragos, C. A., Pataky, J. K., & White, D. G. (2004). Sources of resistance to fumonisin accumulation in grain and fusarium ear and kernel rot of corn. Phytopathology, 94, 251–260.

    Article  CAS  PubMed  Google Scholar 

  • Corbett Life Science (2006). Rotor-gene™ 6000 operator manual. Corbett Robotics, Queensland, Australia. 152 pp.

  • Covarelli, L., Beccari, G., Prodi, A., Generotti, S., Etruschi, F., Juan, C., et al. (2015). Fusarium species, chemotype characterisation and trichothecene contamination of durum and soft wheat in an area of central Italy. Journal of the Science of Food and Agriculture, 95, 540–551.

    Article  CAS  PubMed  Google Scholar 

  • Del Ponte, E. M., Spolti, P., Ward, T. J., Gomes, L. B., Nicolli, C. P., Kuhnem, P. R., Silva, C. N., & Tessmann, D. J. (2015). Regional and field-specific factors affect the composition of fusarium head blight pathogens in subtropical no-till wheat agroecosystem of Brazil. Phytopathology, 105, 246–254.

    Article  PubMed  Google Scholar 

  • Desjardins, A. E. (2006). Fusarium mycotoxins: chemistry, genetics, and biology. APS press, St. Paul, MN, USA 203 pp.

  • Desjardins, A. E., & Proctor, R. H. (2011). Genetic diversity and trichothecene chemotypes of the Fusarium graminearum clade isolated from maize in Nepal and identification of a putative new lineage. Fungal Biology, 115, 38–48.

    Article  CAS  PubMed  Google Scholar 

  • Engle, J. S., Madden, L. V., & Lipps, P. E. (2003). Evaluation of inoculation methods to determine resistance reactions of wheat to Fusarium graminearum. Plant Disease, 87(12), 1530–1535.

    Article  Google Scholar 

  • European Commission: Institute for Health and Consumer Protection (2008). Report of the verification of the performance of a method for the detection of DAS-59132-8 (event 32) in maize using real-time PCR. CRL-EM-01⁄08. Ispra, Italy: Community Reference Laboratory for GM Food and Feed. http://gmo-crl.jrc.ec.europa.eu/doc/Maize_E32_verification_report.pdf. Accessed 23 Jan 2015.

  • Evans, C. K., Xie, W., Dill-Macky, R., & Mirocha, C. J. (2000). Biosynthesis of deoxynivalenol in spikelets of barley inoculated with macroconidia of Fusarium graminearum. Plant Disease, 84(6), 654–660.

    Article  CAS  Google Scholar 

  • Fredlund, E., Gidlund, A., Olsen, M., Börjesson, T., Spliid, N. H. H., & Simonsson, M. (2008). Method evaluation of Fusarium DNA extraction from mycelia and wheat for down-stream real-time PCR quantification and correlation to mycotoxin levels. Journal of Microbiological Methods, 73, 33–40.

    Article  CAS  PubMed  Google Scholar 

  • Gale, L. R., Ward, T. J., Balmas, V., & Kistler, H. C. (2007). Population subdivision of Fusarium graminearum sensu stricto in the upper midwestern United States. Phytopathology, 97(11), 1434–1439.

    Article  CAS  PubMed  Google Scholar 

  • Gomes, L. B., Ward, T. J., Badiale-Furlong, E., & Del Ponte, E. M. (2015). Species composition, toxigenic potential and pathogenicity of Fusarium graminearum species complex isolates from southern Brazilian rice. Plant Pathology, 64, 980–987.

    Article  CAS  Google Scholar 

  • Goswami, R. S., & Kistler, H. C. (2005). Pathogenicity and in planta mycotoxin accumulation among members of the Fusarium graminearum species complex on wheat and rice. Phytopathology, 95(12), 1397–1404.

    Article  CAS  PubMed  Google Scholar 

  • Hao, J. J., Xie, S. N., Sun, J., Yang, G. Q., Liu, J. Z., Xu, F., Ru, Y. Y., & Song, Y. L. (2017). Analysis of Fusarium graminearum species complex from wheat–maize rotation regions in Henan (China). Plant Disease, 101(5), 720–725.

    Article  Google Scholar 

  • Harris, L. J., Balcerzak, M., Johnston, A., Schneiderman, D., & Ouellet, T. (2016). Host-preferential Fusarium graminearum gene expression during infection of wheat, barley, and maize. Fungal Biology, 120, 111–123.

    Article  CAS  PubMed  Google Scholar 

  • Hilton, A., Jenkinson, P., Hollins, T. W., & Parry, D. W. (1999). Relationship between cultivar height and severity of fusarium ear blight in wheat. Plant Pathology, 48, 202–208.

    Article  Google Scholar 

  • Jansen, C., von Wettstein, D., Schäfer, W., Kogel, K.-H., Felk, A., & Maier, F. J. (2005). Infection patterns in barley and wheat spikes inoculated with wild-type and trichodiene synthase gene disrupted Fusarium graminearum. Proceedings of the National Academy of Sciences of the United States of America, 102(46), 16892–16897.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kazan, K., Gardiner, D. M., & Manners, J. M. (2012). On the trail of a cereal killer: Recent advances in Fusarium graminearum pathogenomics and host resistance. Molecular Plant Pathology, 13(4), 399–413.

    Article  CAS  PubMed  Google Scholar 

  • Kuhnem, P. R., Ward, T. J., Silva, C. N., Spolti, P., Ciliato, M. L., Tessmann, D. J., & Del Ponte, E. M. (2016). Composition and toxigenic potential of the Fusarium graminearum species complex from maize ears, stalks and stubble in Brazil. Plant Pathology, 65, 1185–1191.

    Article  CAS  Google Scholar 

  • Lamprecht, S. C., Tewoldemedhin, Y. T., Botha, W. J., & Calitz, F. J. (2011). Fusarium graminearum species complex associated with maize crowns and roots in the KwaZulu-Natal province of South Africa. Plant Disease, 95, 1153–1158.

    Article  Google Scholar 

  • Lee, J., Chang, I. Y., Kim, H., Yun, S.-H., Leslie, J. F., & Lee, Y. -W. (2009). Genetic diversity and fitness of Fusarium graminearum populations from rice in Korea. Applied and Environmental Microbiology, 75(10), 3289–3295.

  • Lee, J., Kim, H., Jeon, J.-J., Kim, H.-S., Zeller, K. A., Carter, L. L. A., et al. (2012). Population structure of and mycotoxin production by Fusarium graminearum from maize in South Korea. Applied and Environmental Microbiology, 78(7), 2161–2167.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lysøe, E., Seong, K. Y., & Kistler, H. C. (2011). The transcriptome of Fusarium graminearum during the infection of wheat. Molecular Plant-Microbe Interactions, 24(9), 995–1000.

    Article  PubMed  Google Scholar 

  • Maier, F. J., Miedaner, T., Hadeler, B., Felk, A., Salomon, S., Lemmens, M., et al. (2006). Involvement of trichothecenes in fusarioses of wheat, barley and maize evaluated by gene disruption of the trichodiene synthase (Tri5) gene in three field isolates of different chemotype and virulence. Molecular Plant Pathology, 7(6), 449–461.

    Article  CAS  PubMed  Google Scholar 

  • Malbrán, I., Mourelos, C. A., Girotti, J. R., Aulicino, M. B., Balatti, P. A., & Lori, G. A. (2012). Aggressiveness variation of Fusarium graminearum isolates from Argentina following point inoculation of field grown wheat spikes. Crop Protection, 42, 234–243.

    Article  Google Scholar 

  • Malbrán, I., Mourelos, C. A., Girotti, J. R., Balatti, P. A., & Lori, G. A. (2014). Toxigenic capacity and trichothecene production by Fusarium graminearum isolates from Argentina and their relationship with aggressiveness and fungal expansion in the wheat spike. Phytopathology, 104(4), 357–364.

    Article  PubMed  Google Scholar 

  • McLean, M. (1995). The phytotoxicity of selected mycotoxins on mature, germinating Zea mays embryos. Mycopathologia, 132(3), 173–183.

    Article  CAS  PubMed  Google Scholar 

  • Menke, J., Dong, Y., & Kistler, H. C. (2012). Fusarium graminearum Tri12p influences virulence to wheat and Trichothecene accumulation. Molecular Plant-Microbe Interactions, 25(11), 1408–1418.

    Article  CAS  PubMed  Google Scholar 

  • Moradi, M., Oerke, E.-C., Steiner, U., Tesfaye, D., Schellander, K., & Dehne, H. -W. (2010). Microbiological and Sybr® green real-time PCR detection of major fusarium head blight pathogens on wheat ears. Microbiology, 79(5), 646–654.

  • Munkvold, G. P. (2003). Epidemiology of Fusarium diseases and their mycotoxins in maize ears. European Journal of Plant Pathology, 109, 705–713.

    Article  CAS  Google Scholar 

  • Nicolaisen, M., Suproniene, S., Nielsen, L. K., Lazzaro, I., Spliid, N. H., & Justesen, A. F. (2009). Real-time PCR for quantification of eleven individual Fusarium species in cereals. Journal of Microbiological Methods, 76, 234–240.

    Article  CAS  PubMed  Google Scholar 

  • O’Donnell, K., Kistler, H. C., Tacke, B. K., & Casper, H. H. (2000). Gene genealogies reveal global phylogeographic structure and reproductive isolation among lineages of Fusarium graminearum, the fungus causing wheat scab. Proceedings of the National Academy of Sciences of the United States of America, 97(14), 7905–7910.

    Article  PubMed  PubMed Central  Google Scholar 

  • O’Donnell, K., Ward, T. J., Geiser, D. M., Kistler, H. C., & Aoki, T. (2004). Genealogical concordance between the mating type locus and seven other nuclear genes supports formal recognition of nine phylogenetically distinct species within the Fusarium graminearum clade. Fungal Genetics and Biology, 41, 600–623.

    Article  PubMed  Google Scholar 

  • O’Donnell, K., Ward, T. J., Aberra, D., Kistler, H. C., Aoki, T., Orwig, N., et al. (2008). Multilocus genotyping and molecular phylogenetics resolve a novel head blight pathogen within the Fusarium graminearum species complex from Ethiopia. Fungal Genetics and Biology, 45, 1514–1522.

    Article  PubMed  Google Scholar 

  • Ott, R. L. (1998). An introduction to statistical methods and data analysis (p. 837). Belmont: Duxbury Press.

    Google Scholar 

  • Picot, A., Hourcade-Marcolla, D., Barreau, C., Pinson-Gadais, L., Caron, D., Richard-Forget, F., & Lannou, C. (2012). Interactions between Fusarium verticillioides and Fusarium graminearum in maize ears and consequences for fungal development and mycotoxin accumulation. Plant Pathology, 61, 140–151.

    Article  CAS  Google Scholar 

  • Proctor, R. H., Hohn, T. M., & McCormick, S. P. (1995). Reduced virulence of Gibberella zeae caused by disruption of a trichothecene toxin biosynthetic gene. Molecular Plant-Microbe Interactions, 8(4), 593–601.

    Article  CAS  PubMed  Google Scholar 

  • Proctor, R. H., Desjardins, A. E., McCormick, S. P., Plattner, R. D., Alexander, N. J., & Brown, D. W. (2002). Genetic analysis of the role of trichothecene and fumonisin mycotoxins in the virulence of Fusarium. European Journal of Plant Pathology, 108, 691–698.

    Article  CAS  Google Scholar 

  • Purahong, W., Nipoti, P., Pisi, A., Lemmens, M., & Prodi, A. (2014). Aggressiveness of different Fusarium graminearum chemotypes within a population from northern-Central Italy. Mycoscience, 55(1), 63–69.

    Article  Google Scholar 

  • Qiu, J., & Shi, J. (2014). Genetic relationships, Carbendazim sensitivity and mycotoxin production of the Fusarium graminearum populations from maize, wheat and Rice in eastern China. Toxins, 6, 2291–2309.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Qu, B., Li, H. P., Zhang, J. B., Huang, T., Carter, J., Liao, Y. C., et al. (2008). Comparison of genetic diversity and pathogenicity of fusarium head blight pathogens from china and Europe by SSCP and seedling assays on wheat. Plant Pathology, 57, 642–651.

    Article  CAS  Google Scholar 

  • Quinnipiac University (2015). http://faculty.quinnipiac.edu/libarts/polsci/Statistics.html . Accessed on 14 June 2015.

  • Reid, L. M., Woldemariam, T., Zhu, X., Stewart, D. W., & Schaafsma, A. W. (2002). Effect of inoculation time and point of entry on disease severity in Fusarium graminearum, Fusarium verticillioides, or Fusarium subglutinans inoculated maize ears. Canadian Journal of Plant Pathology, 24, 162–167.

    Article  Google Scholar 

  • Rose, L. J., Mouton, M., Beukes, I., Flett, B. C., van der Vyver, C., & Viljoen, A. (2016). Multi-environment evaluation of maize inbred lines for resistance to fusarium ear rot and fumonisins. Plant Disease, 100, 2134–2144.

    Article  CAS  Google Scholar 

  • Sarlin, T., Yli-Mattila, T., Jestoi, M., Rizzo, A., Paavanen-Huhtala, S., & Haikara, A. (2006). Real-time PCR for quantification of toxigenic Fusarium species in barley and malt. European Journal of Plant Pathology, 114, 371–380.

    Article  CAS  Google Scholar 

  • Sarver, B. A., Ward, T. J., Gale, L. R., Broz, K., Kistler, H. C., Aoki, T., et al. (2011). Novel fusarium head blight pathogens from Nepal and Louisiana revealed by multilocus genealogical concordance. Fungal Genetics and Biology, 48, 1096–1107.

    Article  PubMed  Google Scholar 

  • Shapiro, S. S., & Wilk, M. B. (1965). An analysis of variance test for normality (complete samples). Biometrika, 52(3–4), 591–611.

    Article  Google Scholar 

  • Small, I. M., Flett, B. C., Marasas, W. F. O., McLeod, A., Stander, M. A., & Viljoen, A. (2012). Resistance in maize inbred lines to Fusarium verticillioides and fumonisin accumulation in South Africa. Plant Disease, 96(6), 881–888.

    Article  Google Scholar 

  • Snedecor, G. W., & Cochran, W. G. (1980). Statistical methods (7th ed.p. 478). Ames: The Iowa State University Press.

    Google Scholar 

  • Starkey, D. E., Ward, T. J., Aoki, T., Gale, L. H., Kistler, H. C., Geiser, D. M., et al. (2007). Global molecular surveillance reveals novel Fusarium head blight species and trichothecene toxin diversity. Fungal Genetics and Biology, 44, 1191–1204.

    Article  CAS  PubMed  Google Scholar 

  • Suga, H., Karugia, G. W., Ward, T., Gale, L. R., Tomimura, K., Nakajima, T., et al. (2008). Molecular characterization of the Fusarium graminearum species complex in Japan. Phytopathology, 98(2), 159–166.

    Article  CAS  PubMed  Google Scholar 

  • Taylor, J. W., Jacobson, D. J., Kroken, S., Kasuga, T., Geiser, D. M., Hibbett, D. S., et al. (2000). Phylogenetic species recognition and species concepts in fungi. Fungal Genetics and Biology, 31, 21–32.

    Article  CAS  PubMed  Google Scholar 

  • Teich, A. H., & Michelutti, R. (1993). Determining resistance to wheat scab by covering field inoculated heads with plastic bags. Cereal Research Communications, 21(1), 69–73.

    Google Scholar 

  • van der Lee, T., Zhang, H., van Diepeningen, A., & Waalwijk, C. (2015). Biogeography of Fusarium graminearum species complex and chemotypes: A review. Food Additives & Contaminants: Part A, 32(4), 453–460.

    Article  Google Scholar 

  • Ward, T. J., Bielawski, J. P., Kistler, H. C., Sullivan, E., & O'Donnell, K. (2002). Ancestral polymorphism and adaptive evolution in the trichothecene mycotoxin gene cluster of phytopathogenic Fusarium. Proceedings of the National Academy of Sciences of the United States of America, 99(14), 9278–9283.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wegulo, S. N., Bockus, W. W., Hernandez Nopsa, J., De Wolf, E. D., Eskridge, K. M., Peiris, K. H. S., et al. (2011). Effects of integrating cultivar resistance and fungicide application on fusarium head blight and deoxynivalenol in winter wheat. Plant Disease, 95(5), 554–560.

    Article  Google Scholar 

  • Windels, C. E. (2000). Economic and social impacts of fusarium head blight: Changing farms and rural communities in the northern Great Plains. Phytopathology, 90(1), 17–21.

    Article  CAS  PubMed  Google Scholar 

  • Yli-Mattila, T., Gagkaeva, T., Ward, T. J., Aoki, T., Kistler, H. C., & O'Donnell, K. (2009). A novel Asian clade within the Fusarium graminearum species complex includes a newly discovered cereal head blight pathogen from the Russian far east. Mycologia, 101(6), 841–852.

    Article  PubMed  Google Scholar 

  • Zhang, H., van der Lee, T., Waalwijk, C., Chen, W., Xu, J., Xu, J., Zhang, Y., & Feng, J. (2012). Population analysis of the Fusarium graminearum species complex from wheat in China show a shift to more aggressive isolates. PloS One, 7, e31722.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang, H., Brankovics, B., Luo, W., Xu, J., Xu, J. S., Guo, C., et al. (2016). Crops are a main driver for species diversity and the toxigenic potential of Fusarium isolates in maize ears in China. World Mycotoxin Journal, 9(5), 701–715.

    Article  Google Scholar 

Download references

Acknowledgements

This research was financially supported by the South African Winter Cereal Trust and the National Research Foundation: Technology and Human Resources for Industry Programme (THRIP) of South Africa. We are grateful to Dr. Emmanuel Terrasson, Karlien van Zyl, Ilana Visser and Dewald Gouws for excellent technical assistance. Thank you to Ms. M. van der Rijst for statistical analyses and Mr. D. Lesch for management of the wheat field trials. The mention of trade names or commercial products in this publication is solely for the purpose of providing specific information and does not imply recommendation or endorsement by Stellenbosch University.

Author information

Authors and Affiliations

  1. Department of Plant Pathology, Stellenbosch University, Matieland, 7602, South Africa

    Ilze Beukes, Lindy Joy Rose, Gerhardus Johannes van Coller & Altus Viljoen

  2. Western Cape Department of Agriculture, Elsenburg, 7607, South Africa

    Gerhardus Johannes van Coller

Authors
  1. Ilze Beukes
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lindy Joy Rose
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Gerhardus Johannes van Coller
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Altus Viljoen
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Lindy Joy Rose or Altus Viljoen.

Ethics declarations

Conflict of interest

The authors hereby declare that they have no financial or non-financial conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Beukes, I., Rose, L.J., van Coller, G.J. et al. Disease development and mycotoxin production by the Fusarium graminearum species complex associated with South African maize and wheat. Eur J Plant Pathol 150, 893–910 (2018). https://doi.org/10.1007/s10658-017-1331-5

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10658-017-1331-5

Keywords

Search

Navigation