Skip to main content
SpringerLink
Log in

Alternaria species associated with cladode brown spot in cactus prickly pear (Nopalea cochenillifera)

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

Abstract

Brown spot is the most important disease for the culture of cactus prickly pear (Nopalea cochenillifera (L) Salm-Dyck; Cactaceae family), and in many countries, Alternaria spp. are commonly associated with the disease. In Brazil, only three species of Alternaria are associated with brown spot: A. alternata, A. tenuissima, and A. longipes. However, other Alternaria spp. may be involved in the etiology of the disease. This study aimed to identify Alternaria species associated with prickly pear brown spot in Northeast Brazil. Cladodes presenting symptoms of brown spot were collected from three counties in the state of Alagoas and three in the state of Pernambuco. Isolation, obtaining monosporic cultures, and pathogenicity tests were performed. For correct taxonomic positioning of the isolates, morphological and molecular analyses were performed using the internal transcribed spacer (ITS) region and the translation elongation factor 1-alpha (tef1), Alternaria major allergen (Alt a1), glyceraldehyde-3-phosphate dehydrogenase (gapdh), and second largest subunit of RNA polymerase (rpb2). Fourteen pathogenic isolates were obtained, and according to the morphological and molecular analyses, three species of Alternaria were identified: A. gossypina, A. jacinthicola, and A. tomato, all belonging to the Alternata section. A. gossypina, A. jacinthicola, and A. tomato are described for the first time in Nopalea cochenillifera worldwide.

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

  • Andrew, M., Peever, T. L., & Pryor, B. M. (2009). An expanded multilocus phylogeny does not resolve morphological species within the small-spored Alternaria species complex. Mycologia, 101(1), 95–109.

    Article  CAS  PubMed  Google Scholar 

  • Altschul, S. F., Gish, W., Miller, W., & Myers, E. W. (1990). & Lipman, D.J. (1990). Basic local alignment search tool. Journal of Molecular Biology, 215, 403–410.

    Article  CAS  PubMed  Google Scholar 

  • Baldauf, S. L., & Palmer, J. D. (1993). Animals and fungi are each other's closest relatives: Congruent evidence from multiple proteins. Proceedings of the National Academy of Sciences, 90(24), 11558–11562.

    Article  CAS  Google Scholar 

  • Barbosa, R. S., Calvalcanti, V. A. L., Lopes, E. B, & Araújo, E. (2012). Doenças da Palma forrageira. In E. B. Lopes (Ed.), Palma forrageira: Cultivo, uso atual e perspectivas de utilização no semiárido nordestino (pp. 81–98). João Pessoa: EMEPA/FAEPA.

  • Berbee, M. L., Pirseyedi, M., & Hubbard, S. (1999). Cochliobolus phylogenetics and the origin of known, highly virulent pathogens, inferred from ITS and glyceraldehyde-3-phosphate dehydrogenase gene sequences. Mycologia, 91, 964–977.

    Article  CAS  Google Scholar 

  • Castellani, A. (1960). A brief note on the viability of some pathogenic fungi in sterile distilled water. Imprensa Medica Lisbon., 24, 270–272.

    Google Scholar 

  • Cheney, S. A., Lafranchi-Tristem, N. J., Bourges, D., & Canning, E. U. (2001). Relationships of microsporidian genera, with emphasis on the polysporous genera, revealed by sequences of the largest subunit of RNA polymerase II (RPB1). Journal of Eukaryotic Microbiology, 48(1), 111–117.

    Article  CAS  Google Scholar 

  • Conforto, C., Lima, N. B., Garcete-Gómez, J. M., Câmara, M. P., & Michereff, S. J. (2019). Characterization of fungal species associated with cladode brown spot on Nopalea cochenillifera in Brazil. European Journal of Plant Pathology, 155(4), 1179–1194.

    Article  CAS  Google Scholar 

  • Ding, S., Meinholz, K., Cleveland, K., Jordan, S. A., & Gevens, A. J. (2019). Diversity and virulence of Alternaria spp. causing potato early blight and Brown spot in Wisconsin. Phytopathology, 109(3), 436–445.

    Article  CAS  PubMed  Google Scholar 

  • Doyle, J., & Doyle, J. L. (1987). A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Bull. Bot. Soc. am. 19: 11–15. Hemphill J, basal H and Wayne C. 2006. Screening method for salt tolerance in cotton. American Journal of Plant Physiology., 1, 107–112.

    Google Scholar 

  • Edgar, R. C. (2004). MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic acids research, 32(5), 1792–1797.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Farr, D. F., & Rossman, A. Y. (2019). Fungal database: Fungus-host distributions. http://nt.ars-grin.gov/fungaldatabases/fungushost/fungushost.cfm. Accessed23 Mar 2019.

  • Feijó, F. M., Silva, M. J., Nascimento, A. D., Infante, N. B., Ramos-Sobrinho, R., Assunção, I. P., & Lima, G. S. A. (2019). Espécies de Botryosphaeriaceae associada ao cacto pickly pickly pear, Nopalea cochenillifera. Tropical Plant Pathology, 44(5), 452–459.

    Article  Google Scholar 

  • Flores-Flores, R., Velázquez-del Valle, M. G., León-Rodriguez, R., Flores-Moctezuma, H. E., & Hernández-Lauzardo, N. A. (2013). Identification of fungal species associated with cladode spot of prickly pear and their sensitivity to chitosan. Journal of phytopathology, 161(7-8), 544–552.

    Article  CAS  Google Scholar 

  • Gabriel, M. F., Uriel, N., Teifoori, F., Postigo, I., Suñén, E., & Martínez, J. (2017). The major Alternaria alternata allergen, alt a 1: A reliable and specific marker of fungal contamination in citrus fruits. International Journal of Food Microbiology, 257(18), 26–30.

    Article  CAS  PubMed  Google Scholar 

  • Grum-Grzhimaylo, A. A., Grum-Grzhimaylo, A. A., Georgieva, M. L., Bondarenko, S. A., Debets, A. J., & Bilanenko, E. N. (2016). On the diversity of fungi from soda soils. FungalDdiversity, 76(1), 27–74.

    Google Scholar 

  • Hong, S. G., Cramer, R. A., Lawrence, C. B., & Pryor, B. M. (2005). Alt a 1 allergen homologs from Alternaria and related taxa: Analysis of phylogenetic content and secondary structure. Fungal Genetics and Biology, 42(2), 119–129.

    Article  CAS  PubMed  Google Scholar 

  • Hopkins, J. C. F. (1931). "Alternaria gossypina (Thüm.) comb. nov. causing a leaf spot and boll rot of cotton." Transactions of the British Mycological Society 16.2-3: 136-IN4.

  • Hyde, K. D., Nilsson, R. H., Alias, S. A., Ariyawansa, H. A., Blair, J. E., Cai, L., De Cock, A. W. A. M., Dissanayake, A. J., Glockling, S. L., Goonasekara, I. D., Gorczak, M., Hahn, M., Jayawardena, R. S., Al Van Kan, J. A. L., Laurence, M. H., Lévesque, C. A., Li, X., Liu, J. K., Maharachchikumbura, S. S. N., Manamgoda, D. S., Martin, F. N., Mckenzie, E. H. C., Mctaggart, A. R., Mortimer, P. E., Nair, P. V. R., Pawłowska, J., Rintoul, T. L., Shivas, R. G., Spies, C. F. J., Summerell, B. A., Taylor, P. W. J., Terhem, R. B., Udayanga, D., Vaghefi, N., Walther, G., Wilk, M., Wrzosek, M., Xu, J.-C., Yan, J.-Y., & Zhou, N. (2014). One stop shop: Backbones trees for important pytopathogenic genera: I. Fungal Diversity., 67, 21–125.

    Article  Google Scholar 

  • Lanfear, R., Frandsen, P. B., Wright, A. M., Senfeld, T., & Calcott, B. (2016). PartitionFinder 2: New methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Molecular biology and evolution, 34(3), 772–773.

    Google Scholar 

  • Lawrence, D. P., Park, M. S., & Pryor, B. M. (2012). Nimbya and Embellisia revisited, with nov. comb for Alternaria celosiae and A. perpunctulata. Mycological progress, 11(3), 799–815.

    Article  Google Scholar 

  • Lawrence, D. P., Gannibal, P. B., Peever, T. L., & Pryor, B. M. (2013). The sections of Alternaria: Formalizing species-group concepts. Mycologia, 105(3), 530–546.

    Article  PubMed  Google Scholar 

  • Lawrence, D. P., Gannibal, P. B., Dugan, F. M., & Pryor, B. M. (2014). Characterization of Alternaria isolates from the infectoria species-group and a new taxon from Arrhenatherum, Pseudoalternaria arrhenatheria sp. nov. Mycological progress, 13(2), 257–276.

    Article  Google Scholar 

  • Lawrence, D. P., Travadon, R., & Baumgartner, K. (2015). Diversity of Diaporthe species associated with wood cankers of fruit and nut crops in northern California. Mycologia, 107(5), 926–940.

    Article  CAS  PubMed  Google Scholar 

  • Lawrence, D. P., Rotondo, F., & Gannibal, P. B. (2016). Biodiversity and taxonomy of the pleomorphic genus Alternaria. Mycological Progress, 15, 3.

    Article  Google Scholar 

  • Lima, G. S. A., Assunção, I. P., Martins, R. B., Santos, H. V., & Michereff, S. J. (2011). Development and validation of a standard area diagram set for assessment of Alternaria spot on the cladodes of the prickly pear cactus. Journal of Plant Pathology., 93, 691–695.

    Google Scholar 

  • Luo, H., Ma, D. F., Sun, Z. X., & Deng, J. X. (2018). First report of leaf spot disease caused by Alternaria jacinthicola on Tagetes erecta in China. Plant disease, 102(11), 2375.

    Article  Google Scholar 

  • Miller, M.A., Pfeiffer, W., Schwartz T. (2010). Creating the CIPRES science gateway for inference of large phylogenetic trees. In 2010 gateway computing environments workshop (GCE). Nov 14:1–8.

  • Oliveira, L. F., Feijó, F. M., Mendes, A. L., Neto, J. D., Netto, M. S., Assunção, I. P., & Lima, G. S. (2018). Identification of Colletotrichum species associated with brown spot of cactus prickly pear in Brazil. Tropical Plant Pathology, 43(3), 247–253.

    Article  Google Scholar 

  • Poudel, B., Velázquez-del Valle, M. G., Hernández-Lauzardo, A. N., & Zhang, S. (2019). First report of Alternaria tomato causing leaf spot on sunflower in Mexico. Plant Disease, 103(5), 1029.

    Article  Google Scholar 

  • Pryor, B. M., & Gilbertson, R. L. (2000). Molecular phylogenetic relationships amongst Alternaria species and related fungi based upon analysis of nuclear ITS and mt SSU rDNA sequences. Mycological Research, 104(11), 1312–1321.

    Article  CAS  Google Scholar 

  • Pryor, B. M., Creamer, R., Shoemaker, R. A., McLain-Romero, J., & Hambleton, S. (2009). Undifilum, a new genus for endophytic Embellisia oxytropis and parasitic Helminthosporium bornmuelleri on legumes. Botany, 87(2), 178–194.

    Article  CAS  Google Scholar 

  • Rannala, B., & Yang, Z. (1996). Probability distribution of molecular evolutionary trees: A new method of phylogenetic inference. Journal of molecular evolution, 43(3), 304–311.

    Article  CAS  PubMed  Google Scholar 

  • Reeb, V., Lutzoni, F., & Roux, C. (2004). Contribution of RPB2 to multilocus phylogenetic studies of the euascomycetes (Pezizomycotina, Fungi) with special emphasis on the lichen-forming Acarosporaceae and evolution of polyspory. Molecular Phylogenetics and Evolution, 32(3), 1036–1060.

    Article  CAS  PubMed  Google Scholar 

  • Rehner, S. (2001). Primers for elongation factor 1-α (EF1-α). Available form: http://ocid.NACSE.ORG/research/deephyphae/EF1primer.pdf (https://www2.clarku.edu/faculty/dhibbett/Protocols_Folder/Primers/Primers.pdf).

  • Rokas, A., & Carroll, S. B. (2005). More genes or more taxa? The relative contribution of gene number and taxon number to phylogenetic accuracy. Molecular Biology and Evolution, 22(5), 1337–1344.

    Article  CAS  PubMed  Google Scholar 

  • Ronquist, F., Teslenko, M., Van Der Mark, P., Ayres, D. L., Darling, A., Höhna, S., Larget, B., Liu, L., Suchard, M. A., & Huelsenbeck, J. P. (2012). MrBayes 3.2: Efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic biology, 61(3), 539–542.

    Article  PubMed  PubMed Central  Google Scholar 

  • Santos, D. C., Santos, M. V., Farias, I., Dias, F. M., & Lira, M. D. (2001). Desempenho produtivo de vacas 5/8 holando/zebu alimentadas com diferentes cultivares de palma forrageira (Opuntia e Nopalea). Revista Brasileira de Zootecnia., 30(1), 12–17.

    Article  Google Scholar 

  • Siciliano, I., Ortega, S. F., Gilardi, G., Bosio, P., Garibaldi, A., & Gullino, M. L. (2018). Molecular phylogeny and characterization of secondary metabolite profile of plant pathogenic Alternaria species isolated from basil. Food Microbiology, 73, 264–274.

    Article  CAS  PubMed  Google Scholar 

  • Silva, L. M., Silva, L. M., Fagundes, J. L., Viegas, P. A., Muniz, E. N., Rangel, J. H., Moreira, A. L., & Backes, A. A. (2014). Produtividade da Palma Forrageira cultivada em diferentes densidades de plantio. Ciência Rural, 44(11), 2064–2071.

    Article  Google Scholar 

  • Simmons, E. G. (1967). Typification of Alternaria, Stemphylium, and Ulocladium. Mycologia, 59(1), 67–92.

    Article  CAS  PubMed  Google Scholar 

  • Simmons, E. G. (1971). Helminthosporium allii as type of a new genus. Mycologia, 63(2), 380–386.

    Article  Google Scholar 

  • Simmons, E. G. (1989). Macrospora Fuckel (Pleosporales) and related anamorphs. Sydowia., 41, 314–329.

    Google Scholar 

  • Simmons, EG. (1992). Alternaria taxonomy: Current status, viewpoint, challenge. Alternaria biology. Plant diseases and metabolites.:1-35.

  • Simmons, E. G. (2007). Alternaria. An identification manual. In: CBS biodiversity series 6. CBS Fungal Biodiversity Centre, Utrecht, The Netherlands.

  • Shinha, K.K., & Bhatnagar, D. (1998). Mycotoxins in agriculture and food safety. CRC Press, 1998.

  • Souza, A. E. F., Nascimento, L. C., Araújo, E., Lopes, E. B., & Souto, F. M. (2010). Ocorrência e identificação dos agentes etiológicos de doenças em palma forrageira (Opuntia fícus-indica Mill.) no semiárido paraibano. Revista Biotemas., 23(3), 11–20.

    Google Scholar 

  • Stiller, J. W., & Hall, B. D. (1997). The origin of red algae: Implications for plastid evolution. Proceedings of the National Academy of Sciences, 94(9), 4520–4525.

    Article  CAS  Google Scholar 

  • Tamura, K., Stecher, G., Peterson, D., Filipski, A., & Kumar, S. (2013). MEGA6: Molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution. (30):2725–2729.

  • White, T. J., Bruns, T., Lee, S., & Taylor, J. (1990). Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In M. A. Innis, D. H. Gelfand, J. J. Snisky, & T. J. White (Eds.), PCR, Guia de métodos e aplicações (pp. 315–322). San Diego: Academic Press.

    Google Scholar 

  • Woudenberg, J. H., Groenewald, J. Z., Binder, M., & Crous, P. W. (2013). Alternaria redefined. Studies in mycology, 75, 171–212.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Woudenberg, J. H., Seidl, M. F., Groenewald, J. Z., De Vries, M., Stielow, J. B., Thomma, B. P., & Crous, P. W. (2015). Alternaria section Alternaria: Species, formae speciales or pathotypes. Studies in Mycology., 82, 1–21.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

This work was supported by Fundação de Amparo à Pesquisa de Alagoas – FAPEAL. We also thank the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior – CAPES for a masters fellowiship.

Author information

Authors and Affiliations

  1. Centro de Ciências Agrárias, Universidade Federal de Alagoas, Br 104, km 85 Norte, Rio Largo, AL, 57100-000, Brazil

    Nayana Bruschi Infante, Gilberlan Costa Santos da Silva, Frederico Monteiro Feijó, Sarah Jacqueline Cavalcanti da Silva, Iraildes Pereira Assunção & Gaus Silvestre de Andrade Lima

Authors
  1. Nayana Bruschi Infante
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Gilberlan Costa Santos da Silva
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Frederico Monteiro Feijó
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Sarah Jacqueline Cavalcanti da Silva
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Iraildes Pereira Assunção
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Gaus Silvestre de Andrade Lima
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Frederico Monteiro Feijó.

Ethics declarations

This research article is not submitted elsewhere for publication and this manuscript complies with the Ethical Rules applicable for this journal.

Ethical statement

This article does not contain any studies with human participants or animals performed by any of the authors.

Conflict of interest

The authors declare that they have no competing interest.

Supplementary Information

ESM 1

(PDF 418 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Infante, N.B., da Silva, G.C.S., Feijó, F.M. et al. Alternaria species associated with cladode brown spot in cactus prickly pear (Nopalea cochenillifera). Eur J Plant Pathol 160, 215–226 (2021). https://doi.org/10.1007/s10658-021-02236-5

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10658-021-02236-5

Keywords

Search

Navigation