View More View Less
  • 1 Federal University of Paraná, Brazil
  • 2 Federal University of Paraná, Brazil
  • 3 Federal University of Paraná, Brazil
  • 4 Embrapa Soja, Brazil
Restricted access

Purchase article

USD  $25.00

1 year subscription (Individual Only)

USD  $784.00

The objective of this study was to conduct a survey about fungi associated with leaves from two different maize plant lineages and to analyze their microbiota diversity. Isolated fungi were identified by morphological analysis and molecular taxonomy was performed using ITS1-5.8S-ITS2 rDNA. About 27 fungi morphotypes were obtained, 15 of them were from the first maize lineage. About 86.7% of the individuals belonged to the Dothideomycetes class (Phoma sorghina, Epicocum nigrum, Cladosporium sp., Bipolaris zeicola, and Alternaria alternata complex) and 13.3% to the Sordariomycetes class (Diaporthe/Phomopsis sp. and Nigrospora sp.). This ratio was opposite in the other maize lineage with 25.0% of Dothideomycetes (E. nigrum and Pleosporales) and 75.0% of Sordariomycetes (Gibberella fujikuroi complex, Fusarium graminearum complex, Diaporthe/Phomopsis sp., and Nigrospora sp.). By concerning the analyses of morphological characteristics and molecular phylogeny, this study intended to identify the groups of saprophytic, phytopathogenic, and mycotoxin fungi, which differently co-inhabit leaf tissue of maize plants in both tested lineages.

  • 1.

    Bono, J., Rodrigues, A., Mauad, M., Albuquerque, J., Yamamoto, C., Chermouth, K., Freitas, M.: Modo de aplicação de fertilizantes nitrogenados na qualidade fisiológica de sementes de milho [Application of nitrogen fertilizers and physiological quality of corn seeds]. Rev Agrarian 1, 91102 (2008).

    • Search Google Scholar
    • Export Citation
  • 2.

    Juniper, B. E.: The leaf from the inside and the outside: A microbe’s perspective. In Andrews, J. H, Hirano S. S. (eds): Microbial Ecology of Leaves. Springer-Verlag, New York, 1991, pp. 2142.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 3.

    Gomes, R. R., Glienke, C., Videira, S. I. R., Lombard, L., Groenewald, J. Z., Crous, P. W.: Diaporthe: A genus of endophytic, saprobic and plant pathogenic fungi. Persoonia 31, 141 (2013).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 4.

    Promputtha, I., Lumyong, S., Dhanasekaran, V., Mckenzie, E. H. C., Hyde, K. D., Jeewon, R.: A phylogenetic evaluation of whether endophytes become saprotrophs at host senescence. Microb Ecol 53, 579590 (2007).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 5.

    Zabalgogeazcoa, I.: Fungal endophytes and their interaction with plant pathogens. Span J Agric Res 6, 138146 (2008).

  • 6.

    Hyde, K. D., Soytong, K.: The fungal endophyte dilemma? Fungal Divers 33, 63173 (2008).

  • 7.

    Shurtleff, M. C.: Compendium of Corn Diseases. American Phytopathological Society, St. Paul, USA, 1980.

  • 8.

    Reis, E. M., Casa, R. T., Bresolim, A. C. R.: Manual de Diagnose e Controle de Doenças de Milho [Diagnosis Manual and Corn Diseases Control]. Graphel, Lages, 2004.

    • Search Google Scholar
    • Export Citation
  • 9.

    Tanaka, M. A. S., Maeda, J. A., Ihde, A., Plazas, Z.: Fungi associated to corn seeds under storage conditions. Sci Agri 58, 501508 (2001).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 10.

    Scott, P. M.: Analysis of agricultural commodities and foods for Alternaria mycotoxins. J AOAC Int 84, 18091817 (2001).

  • 11.

    Herre, E. A., Knowlton, N., Mueller, U. G., Rehner, S. A.: The evolution of mutualisms: Exploring the paths between conflict and cooperation. Trends Ecol Evolut 14, 4953 (1999).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 12.

    Bensch, K., Groenewald, J. Z., Dijksterhuis, J., Starink-Willemse, M., Andersen, B., Summerell, B. A., Shin, H.-D., Dugan, F. M., Schroers, H.-J., Braun, U., Crous, P. W.: Species and ecological diversity within the Cladosporium cladosporioides complex (Davidiellaceae Capnodiales). Stud Mycol 67, 194 (2010).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 13.

    De Hoog, G. S., Gerrits Van Den Ende, A. H. G.: Molecular diagnostics of clinical strains of filamentous Basidiomycetes. Mycoses 41, 183189 (1998).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 14.

    White, T. J., Bruns, T., Lee, S., Taylor, J.: Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In Innis, M. A., Gelfand, D. H., Sninsky, J. J., White, T. J. (eds): PC Protocols: A Guide to Methods and Applications. Academic, San Diego, 1990, pp. 315322.

    • Search Google Scholar
    • Export Citation
  • 15.

    Menna, P., Hungria, M., Barcellosa, F. G., Bangele, E. V., Hessf, P. N., Martinez-Romero, E.: Molecular phylogeny based on the 16S rRNA gene of elite rhizobial strains used in Brazilian commercial inoculants. Syst Appl Microbiol 29, 315332 (2006).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 16.

    Szilagyi-Zecchin, V. J., Ikeda, A. C., Hungria, M., Adamoski, D., Kava-Cordeiro, V., Glienke, C., Galli-Terasawa, L. V.: Identification and characterization of endophytic bacteria from corn (Zea mays L.) roots with biotechnological potential in agriculture. AMB Express 4, 19 (2014).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 17.

    Ewing, B., Hillier, L., Wendl, M. C., Green, P.: Basecalling of automated sequencer traces using phred I accuracy assessment. Gen Res 8, 175185 (1998).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 18.

    Löytynoja, A., Goldman, D.: webPRANK: A phylogenyaware multiple sequence aligner with interactive alignment browser. BMC Bioinformatics 11, 579 (2010).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 19.

    Zwickl, D. J.: Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion. PhD dissertation, The University of Texas at Austin, 2006.

    • Export Citation
  • 20.

    Sukumaran, J., Holder, M. T.: DendroPy: A Python library for phylogenetic computing. Bioinformatics 26, 15691571 (2010).

  • 21.

    Shannon, C. E., Weaver, W.: The Mathematical Theory of Communication. University of Illinois Press, Urban, 1949.

  • 22.

    Simpson, E. H.: Measurement of species diversity. Nature 163, 688 (1949).

  • 23.

    Hammer, Ø., Harper, D. A. T., Ryan, P. D.: Past: Paleontological statistics software package for education and data analysis. Paleontol Electron 4, 49 (2001).

    • Search Google Scholar
    • Export Citation
  • 24.

    Bernardi-Wenzel, J., García, A., Filho-Celso, J. R., Prioli, A. J., Pamphile, J. A.: Evaluation of foliar fungal endophyte diversity and colonization of medicinal plant Luehea divaricata (Martius et Zuccarini). Biol Res 43, 375384 (2010).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 25.

    Sun, X., Guo, L. D., Hyde, K. D.: Community composition of endophytic fungi in Acer truncatum and their role in decomposition. Fungal Divers 47, 8595 (2011).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 26.

    Arnold, A. E.: Understanding the diversity of foliar fungal endophytes: Progress challenges and frontiers. Fungal Biol Rev 21, 5166 (2007).

  • 27.

    Mims, C. W., Richardson, E. A.: Ultrastructure of sporodochium and conidium development in the anamorphic fungus Epicoccum nigrum. Can J Bot 83, 13541363 (2005).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 28.

    de Cal, M. A., Larena, I., Liñán, M., Torres, R., Lamarca, N., Usall, J., Domenichini, P., Bellini, A., de Eribe, X. O., Melgarejo, P.: Population dynamics of Epicoccum nigrum a biocontrol agent against brown rot in stone fruit. J Appl Microbiol 106, 592605 (2009).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 29.

    Hashem, M., Ali, E. H.: Epicoccum nigrum as biocontrol agent of Pythium damping-off and root rot of cotton seedlings. Arch Phytopathol Plant Prot 37, 283297 (2004).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 30.

    Schubert, K., Greslebin, A., Groenewald, J. Z., Crous, P. W.: New foliicolous species of Cladosporium from South America. Persoonia 22, 111122 (2009).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 31.

    Aveskamp, M. M., De Gruyter, J., Woudenberg, J. H. C., Verkley, G. J. M., Crous, P. W.: Highlights of the Didymellaceae: A polyphasic approach to characterise Phoma and related pleosporalean genera. Stud Mycol 65, 160 (2010).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 32.

    Amaral, A. L., Carli, M. L., Barbosa Neto, J. F., Dal Soglio, F. K.: Phoma sorghina a new pathogen associated with Phaeosphaeria leaf spot on maize in Brazil. New Dis Rep 8, 26 (2003).

    • Search Google Scholar
    • Export Citation
  • 33.

    Costa, R. V., Casela, C. R., Cota, L. V.: Embrapa Milho e Sorgo Sistemas de Produção 1, Cultivo do Milho – Doenças [Embrapa Maize and Sorghum, Production Systems 1, Growing Corn – Diseases], 6th Edition, 2010. Available from http://www.cnpms.embrapabr/publicacoes/milho_6_ed/doencas.htm. Accessed 15 January 2011.

    • Search Google Scholar
    • Export Citation
  • 34.

    Berbee, M. L.: Loculoascomycete origins and evolution of filamentous Ascomycete morphology based on 18S gene sequence data. Mol Biol Evol 13, 462470 (1996).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 35.

    Andrew, M., Peever, T. L., Pryor, B. M.: An expanded multilocus phylogeny does not resolve morphological species within the small spored Alternaria species complex. Mycologia 101, 95109 (2009).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 36.

    Peever, T. L., Su, G., Carpenter-Boggs, L., Timmer, L. W.: Molecular systematics of citrus-associated Alternaria species. Mycologia 96, 119134 (2004).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 37.

    Leslie, J. F., Summerell, B. A.: The Fusarium Laboratory Manual. Blackwell Publishing Ltd., Iowa, 2006.

  • 38.

    Pinto, L. S. R. C., Azevedo, J. L., Pereira, J. O., Vierira, M. L. C., Labate, C. A.: Symptomless infection of banana and maize by endophytic fungi impairs photosynthetic efficiency. New Phytol 147, 609615 (2000).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 39.

    O’Donnell, K., Ward, T. J., Aberra, D., Kistler, H. C., Aoki, T., Orwig, N., Kimura, M., Bjornstad, A., Klemsda, L. S. S.: Multilocus genotyping and molecular phylogenetics resolve a novel head blight pathogen within the Fusarium graminearum species complex from Ethiopia. Fungal Gen Biol 45, 15141522 (2008).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 40.

    Sampietro, D. A., Díaz, C. G., Gonzalez, V., Vattuone, M. A., Ploper, L. D., Catalan, C. A. N., Ward, T. J.: Species diversity and toxigenic potential of Fusarium graminearum complex isolates from maize fields in northwest Argentina. Int J Food Microbiol 145, 359364 (2011).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 41.

    Pronczuk, M., Pronczuk, S., Messyasz, M.: Pathogenicity of Fusarium spp. contributing to the stalk rot of maize in Poland. Mycotoxin Res 7, 97101 (1991).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 42.

    IARC Monographs on the Evaluation of Carcinogenic risks to Humans: Some naturally occurring substances: Food items and constituents heterocyclic aromatic amines and mycotoxins. International Agency for Research on Cancer, Lyon, 1993.

    • Export Citation
  • 43.

    Arnold, A. E., Miadlikowska, J., Higgins, K. L., Sarvate, S. D., Gugger, P., Way, A., Hofstetter, V., Kauff, F., Lutzoni, F.: A phylogenetic estimation of trophic transition networks for ascomycetous fungi: Are lichens cradles of symbiotrophic fungal diversification? Syst Biol 58, 283297 (2009).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 44.

    Arnold, A. E., Lutzoni, F.: Diversity and host range of foliar fungal endophytes: Are tropical leaves biodiversity hotspots? Ecology 88, 541549 (2007).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 45.

    Pan, J. H., Jones, E. B. G., She, Z. G., Pang, J. Y., Lin, Y. C.: Review of bioactive compounds from fungi in the South China. Sea Bot Mar 51, 179190 (2008).

    • Search Google Scholar
    • Export Citation
  • 46.

    Niaz, I., Dawar, S.: Detection of seed borne mycoflora in maize (Zea mays L.). Pakistan J Bot 41, 443451 (2009).

  • 47.

    Watson, S. A., Ramstad, P. E.: Corn: Chemistry and Technology. American Association of Cereal Chemist, St. Paul, 1987.

  • 48.

    Chassy, B. M.: Food safety risks and consumer health. New Biotechnol 27, 534544 (2010).

  • 49.

    Crous, P. W., Groenewald, J. Z.: Hosts, species and genotypes: Opinions versus data. Australas Plant Path 34, 463470 (2005).

  • 50.

    Arnold, A. E., Herre, E. A.: Canopy cover and leaf age affect colonization by tropical fungal endophytes: Ecological pattern and process in Theobroma cacao (Malvaceae). Mycologia 95, 388398 (2003).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 51.

    Arnold, A. E., Engelbrecht, B. M. J.: Fungal endophytes double minimum leaf conductance in seedlings of a tropical tree. J Trop Ecol 23, 369372 (2007).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 52.

    Rodrigues, A. A. C., Menezes, M.: Identification and pathogenic characterization of endophytic Fusarium species from cowpea seeds. Mycopathol 159, 7985 (2005).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 53.

    Ahlholm, J. U., Helander, M., Henriksson, J., Metzler, M., Saikkonen, K.: Environmental conditions and host genotype direct genetic diversity of Venturia ditricha a fungal endophyte of birch trees. Evolution 56, 15661573 (2002).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 54.

    Agrios, G. N.: Plant Pathology, 5th Edition. Elsevier Academic Press, London, 2005.

  • 55.

    Korkama-Rajala, T., Müeller, M. M., Pennanen, T.: Decomposition and fungi of needle litter from slow- and fast-growing Norway spruce (Picea abies) clones. Microbial Ecol 56, 7689 (2008).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 56.

    Bacon, C. W., Hinton, D. M.: Symptomless endophytic colonization of maize by Fusarium moniliforme. Can J Bot 74, 11951202 (1996).

  • 57.

    Bottalico, A., Logrieco, A., Visconti, A.: Fusarium species and their mycotoxins in infected corn in Italy. Mycopathol 107, 8592 (1989).

  • 58.

    Azevedo, J. L., Júnior, W. M., Pereira, J. O., Araújo, W. L.: Endophytic microorganisms: A review on insect control and recent advances on tropical plants. Environ Biotechnol 3, 4065 (2000).

    • Search Google Scholar
    • Export Citation

Monthly Content Usage

Abstract Views Full Text Views PDF Downloads
May 2020 0 4 2
Jun 2020 0 8 4
Jul 2020 2 1 1
Aug 2020 19 0 0
Sep 2020 16 0 0
Oct 2020 33 0 0
Nov 2020 0 0 0