Abstract
Since the early 2000s, over 5000 hectares of guava orchards have been decimated in Brazil by guava decline. The disease has caused tens of millions of dollars in yield losses, the loss of thousands of jobs, and the closing of many fruit pulp-processing plants. Guava decline has been described as a synergistic interaction between the nematode Meloidogyne enterolobii and the fungus Fusarium solani. Nonetheless, the etiology of the disease has had to be reappraised because recent molecular studies have reassigned the whole ‘F. solani species complex’ to the genus Neocosmospora, with several plant-parasitic species being reclassified or synonymized. Hence, from a collection of ‘F. solani’ isolates associated with guava decline, we chose four of the most aggressive isolates, from which we sequenced RNA polymerase II subunit 1 (RPB1), RNA polymerase II subunit 2 (RPB2), and translation elongation factor 1-alpha (TEF1) genes. A GenBank® BLASTn search showed that the isolates belonged to Neocosmospora sp. Phylogenetic analyses using the maximum likelihood (ML) and Bayesian inference (BI) methods, with individual and combined datasets for TEF1, RPB1 and RPB2 genes, clustered all isolates within the N. falciformis clade, with maximum support in the ML and BI multilocus analyses. This and previous studies show that N. falciformis is the causal agent of guava decline and soybean sudden death syndrome, as well as of crown and root rots in other annual and perennial crops.
Data availability
All data generated during this study are included in the article and its supplementary information files.
References
Ayala-Armenta, Q. A., Tovar-Pedraza, J. M., Apodaca-Sánchez, M. A., Correia, K. C., Sauceda-Acosta, C. P., Camacho-Tapia, M., & Beltrán-Peña, H. (2020). Phylogeny and pathogenicity of soilborne fungi associated with wilt disease complex of tomatillo (Physalis ixocarpa) in northern Sinaloa, Mexico. European Journal of Plant Pathology. https://doi.org/10.1007/s10658-020-02030-9.
Costa, S. S., Matos, K. S., Tessmann, D. J., Seixas, C. D. S., & Pfenning, L. H. (2016). Fusarium paranaense sp. nov., a member of the Fusarium solani species complex causes root rot on soybean in Brazil. Fungal Biology, 120, 51–60. https://doi.org/10.1016/j.funbio.2015.09.005.
Crespo, M., Lawrence, D. P., Nouri, M. T., Doll, D. A., & Trouillas, F. P. (2019). Characterization of Fusarium and Neocosmospora species associated with crown rot and stem canker of pistachio rootstocks in California. Plant Disease. https://doi.org/10.1094/PDIS-11-18-2012-RE.
Dettman, J. R., Jacobson, D. J., & Taylor, J. W. (2003). A multilocus genealogical approach to phylogenetic species recognition in the model eukaryote Neurospora. Evolution. https://doi.org/10.1111/j.0014-3820.2003.tb01514.x.
Díaz-Nájera, J. F., Ayvar-Serna, S., Mena-Bahena, A., Baranda-Cruz, E., Vargas-Hernández, M., Alvarado-Gómez, O. G., & Fuentes-Aragón, D. (2020). First report of Fusarium falciforme (FSSC 3 + 4) causing wilt disease of Phaseolus vulgaris in Mexico. Plant Disease. https://doi.org/10.1094/PDIS-06-20-1160-PDN.
Didwania, N., Sadana, D., & Katyal, N. (2013). A review on current research advancement on wilt disease of Psidium guajava L. with special reference to management. International Journal of Science and Advanced Technology, 3, 8–13.
Douriet-Angulo, A., López-Orona, C. A., López-Urquídez, G. A., Vega-Gutiérrez, T. A., Tirado-Ramírez, M. A., Estrada-Acosta, M. D., Ayala-Tafoya, F., & Yáñez-Juárez, M. G. (2019). Maize stalk rot caused by Fusarium falciforme (FSSC 3 + 4) in Mexico. Plant Disease. https://doi.org/10.1094/PDIS-05-19-1055-PDN.
Doyle, J. J., & Doyle, J. L. (1990). Isolation of plant DNA from fresh tissue. Focus 12. https://doi.org/10.1007/978-3-642-83962-7_18.
Doyle, V. P., Oudemans, P. V., Rehner, S. A., & Litt, A. (2013). Habitat and host indicate lineage identity in Colletotrichum gloeosporioides s.l. from wild and agricultural landscapes in North America. PLoS One. https://doi.org/10.1371/journal.pone.0062394.
Geiser, D. M., Aoki, T., Bacon, C. W., Baker, S. E., Bhattacharyya, M. K., & Brandt, M. E. (2013). One fungus, one name: defining the genus Fusarium in a scientifically robust way that preserves longstanding use. Phytopathology. https://doi.org/10.1094/PHYTO-07-12-0150-LE.
Gomes, V. M., Ribeiro, R. M., Viana, A. P., Souza, R. M., & Santos, E. A. (2017). Inheritance of resistance to Meloidogyne enterolobii and individual selection in segregating populations of Psidium spp. European Journal of Plant Pathology. https://doi.org/10.1007/s10658-016-1128-y.
Gomes, V. M., Souza, R. M., Almeida, A. M., & Dolinski, C. M. (2014). Relationships between M. enterolobii and F. solani: spatial and temporal dynamics in the occurrence of guava decline. Nematoda, 1. https://doi.org/10.4322/nematoda.02015.
Gomes, V. M., Souza, R. M., Midorikawa, G., Miller, R., & Almeida, A. M. (2012). Guava decline: evidence of nationwide incidence in Brazil. Nematropica, 42, 153–162.
Gomes, V. M., Souza, R. M., Mussi-Dias, V., Silveira, S. F., & Dolinski, C. M. (2011). Guava decline: a complex disease involving Meloidogyne mayaguensis and Fusarium solani. Journal of Phytopathology. https://doi.org/10.1111/j.1439-0434.2010.01711.x.
Gomes, V. M., Souza, R. M., Silveira, S. F., & Almeida, A. M. (2013). Guava decline: effect of root exudates from Meloidogyne enterolobii-parasitized plants on Fusarium solani in vitro and on growth and development of guava seedlings under controlled conditions. European Journal of Plant Pathology. https://doi.org/10.1007/s10658-013-0251-2.
González, V., García-Martínez, S., Ruiz, J. J., Flores-León, A., Picó, B., & Garcés-Claver, A. (2020). First Report of Neocosmospora falciformis causing wilt and root rot of muskmelon in Spain. Plant Disease. https://doi.org/10.1094/PDIS-09-19-2013-PDN.
Guarro, J. (2013). Fusariosis, a complex infection caused by a high diversity of fungal species refractory to treatment. European Journal of Clinical Microbiology & Infectious Diseases. https://doi.org/10.1007/s10096-013-1924-7.
Herron, D. A., Wingfield, M. J., Wingfield, B. D., Rodas, C. A., Marincowitz, S., & Steenkamp, E. T. (2015). Novel taxa in the Fusarium fujikuroi species complex from Pinus spp. Studies in Mycology. https://doi.org/10.1016/j.simyco.2014.12.001.
Katoh, K., Rozewicki, J., & Yamada, K. D. (2017). MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Briefings in Bioinformatics. https://doi.org/10.1093/bib/bbx108.
Katoh, K., & Standley, D. M. (2013). MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution. https://doi.org/10.1093/molbev/mst010.
Lombard, L., van der Merwe, N. A., Groenewald, J. Z., & Crous, P. W. (2015). Generic concepts in Nectriaceae. Studies in Mycology, 80, 189–245. https://doi.org/10.1016/j.simyco.2014.12.002.
Nylander, J. A. A. (2004). MrModeltest v2 - Program distributed by the author. Uppsala: Evolutionary Biology Centre, Uppsala University.
Pereira, F. O. M., Souza, R. M., Souza, P. M., Dolinski, C., & Santos, G. K. (2009). Estimativa do impacto econômico e social direto de Meloidogyne mayaguensis na cultura da goiaba no Brasil. Nematologia Brasileira, 33, 176–181.
Rambaut, A., & Drummond, A. (2010). Tracer v. 1.4. http://beast.bio.ed.ac.uk/Tracer. Accessed 15 Mar 2019.
Ribeiro, R. M., Gomes, V. M., Viana, A. P., Souza, R. M., & Santos, P. R. (2019). Selection of interspecific Psidium spp. hybrids resistant to Meloidogyne enterolobii. Acta Scientiarum – Agronomy. https://doi.org/10.4025/actasciagron.v41i1.42702.
Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D. L., Darling, A., Hohna, 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. https://doi.org/10.1093/sysbio/sys029.
Sandoval-Denis, M., & Crous, P. W. (2018). Removing chaos from confusion: assigning names to common human and animal pathogens in Neocosmospora. Persoonia. https://doi.org/10.3767/persoonia.2018.41.06.
Sandoval-Denis, M., Guarnaccia1, V., Polizzi, G., & Crous, P. W. (2018). Symptomatic citrus trees reveal a new pathogenic lineage in Fusarium and two new Neocosmospora species. Persoonia. https://doi.org/10.3767/persoonia.2018.40.01.
Sandoval-Denis, M., Lombard, L., & Crous, P. W. (2019). Back to the roots: a reappraisal of Neocosmospora. Persoonia. https://doi.org/10.3767/persoonia.2019.43.04.
Schoeman, M. H., Labuschagne, N., & Calitz, F. J. (2017). Efficacy of fungicides, plant resistance activators and biological control agents against guava wilt disease caused by Nalanthamala psidii. South African Journal of Plant and Soil. https://doi.org/10.1080/02571862.2016.1231348.
Shukla, P. K., Fatima, T., & Rajan, S. (2019). Research on Fusarium wilt disease of guava. Indian Phytopathology. https://doi.org/10.1007/s42360-019-00167-0.
Sousa, E. S., Melo, M. P., Mota, J. M., Sousa, E. M. J., Beserra, J. E. A. Jr., & Matos, K. S. (2017). First report of Fusarium falciforme (FSSC 3 + 4) causing root rot in lima bean (Phaseolus lunatus L.) in Brazil. Plant Disease. https://doi.org/10.1094/PDIS-05-17-0657-PDN.
Souza, R. R. C., Santos, C. A. F., & Costa, S. R. (2018). Field resistance to Meloidogyne enterolobii in a Psidium guajava × P. guineense hybrid and its compatibility as guava rootstock. Fruits. https://doi.org/10.17660/th2018/73.2.4.
Stamatakis, A. (2014). RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics. https://doi.org/10.1093/bioinformatics/btu033.
Summerell, B. A. (2019). Resolving Fusarium: current status of the genus. Annual Review of Phytopathology. https://doi.org/10.1146/annurev-phyto-082718-100204.
Tamura, K., Stecher, G., Peterson, D., Filipski, A., & Kumar, S. (2013). MEGA6: Molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution. https://doi.org/10.1093/molbev/mst197.
Taylor, J. W., Jacobson, D. J., Kroken, S., Kasuga, T., Geiser, D. M., Hibbett, D. S., & Fisher, M. C. (2000). Phylogenetic species recognition and species concepts in fungi. Fungal Genetics and Biology. https://doi.org/10.1006/fgbi.2000.1228.
Tirado-Ramírez, M. A., López-Orona, C. A., Velázquez-Alcaraz, T. J., Díaz-Valdés, T., Velarde-Féliz, S., Martínez-Campos, A. R., & Manjarrez-Retes, J. E. (2018). First report of onion basal rot caused by Fusarium falciforme in Mexico. Plant Disease. https://doi.org/10.1094/PDIS-05-18-0757-PDN.
Vega-Gutiérrez, T. A., López-Orona, C. A., López-Urquídez, G. A., Velarde-Félix, V., Amarillas-Bueno, L. A., Martínez-Campos, A. R., & Allende-Molar, R. (2018). Foot rot and wilt in tomato caused by Fusarium falciforme (FSSC 3 + 4) in Mexico. Plant Disease. https://doi.org/10.1094/PDIS-06-18-1001-PDN.
Vega-Gutiérrez, T. A., Tirado-Ramírez, M. A., López-Urquídez, G. A., Angulo-Castro, A., Martínez-Gallardo, J. A., & López-Orona, C. A. (2019). Fusarium falciforme (FSSC 3 + 4) causing root and stem rot in papaya (Carica papaya) in Mexico. Plant Disease. https://doi.org/10.1094/PDIS-05-19-0917-PDN.
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The authors thank Dr. Willie A. S. Vieira for capturing the images on the morphological and cultural characteristics of the fungal isolates.
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Veloso, J.S., Câmara, M.P.S. & Souza, R.M. Guava decline: updating its etiology from ‘Fusarium solani’ to Neocosmospora falciformis. Eur J Plant Pathol 159, 455–460 (2021). https://doi.org/10.1007/s10658-020-02161-z
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DOI: https://doi.org/10.1007/s10658-020-02161-z