Population Biology

Genetic Diversity of the Fusarium oxysporum Complex Isolated from the Grassland Biome of South Africa

Department of Botany and Plant Biotechnology, University of Johannesburg, Auckland Park, Johannesburg 2006, South Africa

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Grace T. Kwinda

Biosystematics Unit, Plant Health and Protection, Agricultural Research Council, Pretoria 0001, South Africa

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Brett A. Summerell

Australian Institute of Botanical Science, Royal Botanic Gardens and Domain Trust, Sydney NSW 2000, Australia

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Eduard Venter

https://orcid.org/0000-0002-1838-6453

Department of Botany and Plant Biotechnology, University of Johannesburg, Auckland Park, Johannesburg 2006, South Africa

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, and

Adriaana Jacobs

^†Corresponding author: A. Jacobs;

E-mail Address: JacobsR@arc.agric.za

https://orcid.org/0000-0002-6318-6514

Biosystematics Unit, Plant Health and Protection, Agricultural Research Council, Pretoria 0001, South Africa

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Affiliations

Authors and Affiliations

Mudzuli Nephalela-Mavhunga¹
Grace T. Kwinda²
Brett A. Summerell³
Eduard Venter¹
Adriaana Jacobs²^†

¹Department of Botany and Plant Biotechnology, University of Johannesburg, Auckland Park, Johannesburg 2006, South Africa
²Biosystematics Unit, Plant Health and Protection, Agricultural Research Council, Pretoria 0001, South Africa
³Australian Institute of Botanical Science, Royal Botanic Gardens and Domain Trust, Sydney NSW 2000, Australia

Published Online:22 Sep 2021https://doi.org/10.1094/PHYTO-09-20-0377-R

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Abstract

The genetic diversity of pathogenic members of the Fusarium oxysporum species complex (FOSC) has been intensively studied worldwide, yet strains occurring in native soils with low anthropogenic disturbance remain poorly understood. This study focused on 355 F. oxysporum isolates from soils with low anthropogenic activity obtained from the grassland biome of South Africa. Analysis of the translation elongation factor 1-alpha (tef-1α) gene revealed high levels of sequence type diversity within the soil population in comparison with the global dataset. Phylogenetic relationships of the South African isolates revealed that four nested within FOSC clade 1. This is the first report of members of the basal clade recovered from ecosystems with low anthropogenic disturbance from Sub-Saharan Africa. The remaining strains nested within clades 2 to 5. This study contributes significantly to our understanding of the distribution of the FOSC in natural systems as we show that FOSC populations in the South African grassland biome are genetically diverse. This fills in our knowledge gap because previous studies reported only on the occurrence and diversity of the FOSC isolated from plant debris in South Africa. This is the first comprehensive survey of fusaria from grassland soils with low anthropogenic disturbance in South Africa.

LITERATURE CITED

Achari, S. R., Kaur, J., Dinh, Q., Mann, R., Sawbridge, T., Summerell, B. A., and Edwards, J. 2020. Phylogenetic relationship between Australian Fusarium oxysporum isolates and resolving the species complex using the multispecies coalescent model. BMC Genomics 21:248. https://doi.org/10.1186/s12864-020-6640-y Crossref, Medline, ISI, Google Scholar
Appel, D. J., and Gordon, T. R. 1996. Relationships among pathogenic and nonpathogenic isolates of Fusarium oxysporum based on the partial sequence of the intergenic spacer region of the ribosomal DNA. Mol. Plant-Microbe Interact. 9:125-138. https://doi.org/10.1094/MPMI-9-0125 Crossref, Medline, ISI, Google Scholar
Baayen, R. P., O’Donnell, K., Bonants, P. J. M., Cigelnik, E., Kroon, L. P. N. M., Roebroeck, E. J. A., and Waalwijk, C. 2000. Gene genealogies and AFLP analyses in the Fusarium oxysporum complex identify monophyletic and nonmonophyletic formae speciales causing wilt and rot disease. Phytopathol 90:891-900. https://doi.org/10.1094/PHYTO.2000.90.8.891 Link, ISI, Google Scholar
Baayen, R. P., O’Donnell, K., Breeuwsma, S., Geiser, D. M., and Waalwijk, C. 2001. Molecular relationships of fungi within the Fusarium redolens–F. hostae clade. Phytopathology 91:1037-1044. Google Scholar
Balmas, V., Migheli, Q., Scherm, B., Garau, P., O’Donnell, K., Ceccherelli, G., Kang, S., and Geiser, D. M. 2010. Multilocus phylogenetics show high levels of endemic fusaria inhabiting Sardinian soils (Tyrrhenian Islands). Mycologia 102:803-812. https://doi.org/10.3852/09-201 Crossref, Medline, ISI, Google Scholar
Bao, J. R., Fravel, D. R., O’Neill, N. R., Lazarovits, G., and van Berkum, P. 2002. Genetic analysis of pathogenic and nonpathogenic Fusarium oxysporum from tomato plants. Can. J. Bot. 80:271-279. https://doi.org/10.1139/b02-004 Crossref, ISI, Google Scholar
Bogale, M., Wingfield, B. D., Wingfield, M. J., and Steenkamp, T. 2007. Species-specific primers for Fusarium redolens and a PCR-RFLP technique to distinguish among three clades of Fusarium oxysporum. FEMS Microbiol. Lett. 271:27-32. https://doi.org/10.1111/j.1574-6968.2007.00687.x Crossref, Medline, ISI, Google Scholar
Brankovics, B., van Dam, P., Rep, M., de Hoog, G. S., van der Lee, T. A. J., Waalwijk, C., and van Diepeningen, A. D. 2017. Mitochondrial genomes reveal recombination in the presumed asexual Fusarium oxysporum species complex. BMC Genomics 18:1-14. https://doi.org/10.1186/s12864-017-4116-5 Crossref, Medline, ISI, Google Scholar
Bushula, V. S. 2008 Native Fusarium species from indigenous fynbos soils of the Western Cape. Dissertation, University of Stellenbosch. Google Scholar
Chang, D. C., Grant, G. B., O’Donnell, K., Wannemuehler, K. A., Noble-Wang, J., Rao, C. Y., Jacobson, L. M., Crowell, C. S., Sneed, R. S., Lewis, F. M. T., Schaffzin, J. K., Kainer, M. A., Genese, C. A., Alfonso, E. C., Jones, D. B., Srinivasan, A., Fridkin, S. K., and Park, B. J. 2006. Multistate outbreak of Fusarium keratitis associated with use of a contact lens solution. J. Am. Med. Assoc. 296:953-963. https://doi.org/10.1001/jama.296.8.953 Crossref, Medline, ISI, Google Scholar
Crous, P., Phillips, A. J., and Baxter, A. 2000. Phytopathogenic Fungi From South Africa. University of Stellenbosch, Department of Plant Pathology Press, Stellenbosch, South Africa. Google Scholar
Crous, P. W., Rong, I. H., Wood, A., Lee, S., Glen, H., Botha, W., Slippers, B., de Beer, W. Z., Wingfield, M. J., and Hawksworth, D. L. 2006. How many species of fungi are there at the tip of Africa? Stud. Mycol. 55:13-33. https://doi.org/10.3114/sim.55.1.13 Crossref, Medline, Google Scholar
Deltour, P., França, S. C., Heyman, L., Pereira, O. L., and Höfte, M. 2018. Comparative analysis of pathogenic and nonpathogenic Fusarium oxysporum populations associated with banana on a farm in Minas Gerais, Brazil. Plant Pathol. 67:707-718. https://doi.org/10.1111/ppa.12757 Crossref, ISI, Google Scholar
Demers, J. E., Gugino, B. K., and Jiménez-Gasco, M. M. 2014. Highly diverse endophytic and soil Fusarium oxysporum populations associated with field-grown tomato plants. Appl. Environ. Microbiol. 81:81-90. https://doi.org/10.1128/AEM.02590-14 Crossref, Medline, ISI, Google Scholar
Doidge, E. M. 1950. The South African fungi and lichens to the end of 1945. Bothalia 5:1-1094. Google Scholar
Edel, V., Steinberg, C., Gautheron, N., and Alabouvette, C. 1997. Populations of nonpathogenic Fusarium oxysporum associated with roots of four plant species compared to soilborne populations. Phytopathol 87:693-697. https://doi.org/10.1094/PHYTO.1997.87.7.693 Link, ISI, Google Scholar
Edel, V., Steinberg, C., Gautheron, N., Recorbet, G., and Alabouvette, C. 2001. Genetic diversity of Fusarium oxysporum populations isolated from different soils in France. FEMS Microbiol. Ecol. 36:61-71. https://doi.org/10.1111/j.1574-6941.2001.tb00826.x Crossref, Medline, ISI, Google Scholar
Edel-Hermann, V., and Lecomte, C. 2019. Current Status of Fusarium oxysporum formae speciales and Races. Phytopathol 109:512-530. https://doi.org/10.1094/PHYTO-08-18-0320-RVW Link, ISI, Google Scholar
Felsenstein, J. 1985. Confidence limits on phylogenies: An approach using the bootstrap. Evolution 39:783-791. https://doi.org/10.1111/j.1558-5646.1985.tb00420.x Crossref, Medline, ISI, Google Scholar
Fourie, G., Steenkamp, E. T., Gordon, T. R., and Viljoen, A. 2009. Evolutionary relationships among the Fusarium oxysporum f. sp. cubense vegetative compatibility groups. Appl. Environ. Microbiol. 75:4770-4781. https://doi.org/10.1128/AEM.00370-09 Crossref, Medline, ISI, Google Scholar
Geiser, D. M., Jiménez-Gasco, M. M., Kang, S., Makalowska, I., Veeraraghavan, N., Ward, T. J., Zhang, N., Kuldau, G. A., and O’Donnell, K. 2004. FUSARIUM-ID v. 1.0: A DNA sequence database for identifying Fusarium. Eur. J. Plant Pathol. 110:473-479. https://doi.org/10.1023/B:EJPP.0000032386.75915.a0 Crossref, ISI, Google Scholar
Golan, J. J., and Pringle, A. 2017. Long-distance dispersal of fungi. Microbiol Spectrum 5. https://doi.org/10.1128/9781555819583.ch14 Crossref, Google Scholar
Hall, T. A. 1999. BioEdit: A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl. Acids. Symp. Ser. 41:95-98. Google Scholar
Hall, T. A. 2011. BioEdit: An important software for molecular biology. GERF Bull. Biosci. 2:60-61. https://www.researchgate.net/publication/258565830_BioEdit_An_important_software_for_molecular_biology Google Scholar
Hillis, D. M., and Bull, J. J. 1993. An empirical test of bootstrapping as a method for assessing confidence in phylogenetic analysis. Syst. Biol. 42:182-192. https://doi.org/10.1093/sysbio/42.2.182 Crossref, ISI, Google Scholar
Jeschke, N., Nelson, P. E., and Marasas, W. F. O. 1990. Fusarium species isolated from soil samples collected at different altitudes in the Transkei, southern Africa. Mycologia 82:727-733. https://doi.org/10.1080/00275514.1990.12025953 Crossref, ISI, Google Scholar
Katoh, K., and Standley, D. M. 2013. MAFFT multiple sequence alignment software version 7: Improvements in performance and usability. Mol. Biol. Evol. 30:772-780. https://doi.org/10.1093/molbev/mst010 Crossref, Medline, ISI, Google Scholar
Kumar, S., Stecher, G., and Tamura, K. 2016. MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for bigger datasets. Mol. Biol. Evol. 33:1870-1874. Google Scholar
Laurence, M. H., Burgess, L. W., Summerell, B. A., and Liew, E. C. Y. 2012. High levels of diversity in Fusarium oxysporum from non-cultivated ecosystems in Australia. Fungal Biol. 116:289-297. https://doi.org/10.1016/j.funbio.2011.11.011 Crossref, Medline, ISI, Google Scholar
Laurence, M. H., Summerell, B. A., Burgess, L. W., and Liew, E. C. Y. 2014. Genealogical concordance phylogenetic species recognition in the Fusarium oxysporum species complex. Fungal Biol. 118:374-384. https://doi.org/10.1016/j.funbio.2014.02.002 Crossref, Medline, ISI, Google Scholar
Leslie, J. F., and Summerell, B. (eds.) 2006. The Fusarium Laboratory Manual. Blackwell Publishing, Ames, Iowa. https://doi.org/10.1002/9780470278376 Crossref, Google Scholar
Lombard, L., Sandoval-Denis, M., Lamprecht, S. C., and Crous, P. W. 2019. Epitypification of Fusarium oxysporum: clearing the taxonomic chaos. Persoonia Mol Phylogeny Evol Fungi 43:1-47. https://doi.org/10.3767/persoonia.2019.43.01 Crossref, Google Scholar
Mandeel, Q. A. 2006. Biodiversity of the genus Fusarium in saline soil habitats. J. Basic Microbiol. 46:480-494. https://doi.org/10.1002/jobm.200510128 Crossref, Medline, ISI, Google Scholar
Marasas, W. F. O., Burgess, L. W., Anelich, R. Y., Lamprecht, S. C., and van Schalkwyk, D. J. 1988. Survey of Fusarium species associated with plant debris in South African soils. S. Afr. J. Bot. 54:63-71. https://doi.org/10.1016/S0254-6299(16)31363-1 Crossref, ISI, Google Scholar
Marasas, W. F. O., Lamprecht, S. C., Van Wyk, P. S., and Anelich, R. Y. 1987. Bibliography of Fusarium (Fungi: Hyphomycetes) in South Africa, 1945-1985. Bothalia 17:97-104. https://doi.org/10.4102/abc.v17i1.1019 Crossref, ISI, Google Scholar
Maryani, N., Lombard, L., Poerba, Y. S., Subandiyah, S., Crous, P. W., and Kema, G. H. J. 2019. Phylogeny and genetic diversity of the banana Fusarium wilt pathogen Fusarium oxysporum f. sp. cubense in the Indonesian centre of origin. Stud. Mycol. 92:155-194. https://doi.org/10.1016/j.simyco.2018.06.003 Crossref, Medline, ISI, Google Scholar
Michielse, C. B., and Rep, M. 2009. Pathogen profile update: Fusarium oxysporum. Mol. Plant Pathol. 10:311-324. https://doi.org/10.1111/j.1364-3703.2009.00538.x Crossref, Medline, ISI, Google Scholar
Miller, M. A., Pfeiffer, W., and Schwartz, T. 2010. Creating the CIPRES Science Gateway for inference of large phylogenetic trees. 2010 Gateway Computing Environments Workshop. IEEE, Piscataway, NJ. https://doi.org/10.1109/GCE.2010.5676129 Google Scholar
Nelson, P. E., Tousson, T. A., and Marasas, W. F. O. 1983. Fusarium Species: An Illustrated Manual for Identification. Pennsylvania State University Press, University Park, PA. Google Scholar
O’Donnell, K., Gueidan, C., Sink, S., Johnston, P. R., Crous, P. W., Glenn, A., Riley, R., Zitomer, N. C., Colyer, P., Waalwijk, C., van der Lee, T., Moretti, A., Kang, S., Kim, H.-S., Geiser, D. M., Juba, J. H., Baayen, R. P., Cromey, M. G., Bithell, S., Sutton, D. A., Skovgaard, K., Ploetz, R., Kistler, H. C., Elliott, M., Davis, M., and Sarver, B. A. J. 2009a. A two-locus DNA sequence database for typing plant and human pathogens within the Fusarium oxysporum species complex. Fungal Genet. Biol. 46:936-948. https://doi.org/10.1016/j.fgb.2009.08.006 Crossref, Medline, ISI, Google Scholar
O’Donnell, K., Kistler, H. C., Cigelnik, E., and Ploetz, R. C. 1998. Multiple evolutionary origins of the fungus causing panama disease of banana: Concordant evidence from nuclear and mitochondrial gene genealogies. Proc. Natl. Acad. Sci. USA 95:2044-2049. https://doi.org/10.1073/pnas.95.5.2044 Crossref, Medline, ISI, Google Scholar
O’Donnell, K., Sutton, D. A., Fothergill, A., McCarthy, D., Rinaldi, M. G., Brandt, M. E., Zhang, N., and Geiser, D. M. 2008. Molecular phylogenetic diversity, multilocus haplotype nomenclature, and in vitro antifungal resistance within the Fusarium solani species complex. J. Clin. Microbiol. 46:2477-2490. https://doi.org/10.1128/JCM.02371-07 Crossref, Medline, ISI, Google Scholar
O’Donnell, K., Sutton, D. A., Rinaldi, M. G., Gueidan, C., Crous, P. W., and Geiser, D. M. 2009b. Novel multilocus sequence typing scheme reveals high genetic diversity of human pathogenic members of the Fusarium incarnatum-F. equiseti and F. chlamydosporum species complexes within the United States. J. Clin. Microbiol. 47:3851-3861. https://doi.org/10.1128/JCM.01616-09 Crossref, Medline, ISI, Google Scholar
O’Donnell, K., Sutton, D. A., Rinaldi, M. G., Johnston, P. R., Crous, P. W., Glenn, A., Riley, R., Zitomer, N. C., Colyer, P., Waalwijk, C., van der Lee, T., Moretti, A., Kang, A., Kim, K.-S., Geiser, D. M., Juba, J. H., Baayen, R. P., Cromey, M. G., Bithell, S., Sutton, D. A., Skovgaard, K., Ploetz, R., Kistler, H. C., Elliott, M., Davis, M., and Sarver, B. A. J. 2010. Internet-accessible DNA sequence database for identifying fusaria from human and animal infections. J. Clin. Microbiol. 48:3708-3718. https://doi.org/10.1128/JCM.00989-10 Crossref, Medline, ISI, Google Scholar
O’Donnell, K., Sutton, D. A., Rinaldi, M. G., Magnon, K. C., Cox, P. A., Revankar, S. G., Sanche, S., Geiser, D. M., Juba, J. H., van Burik, J.-A. H., Padhye, A. A., Anaissie, E. J., Francesconi, A., Walsh, T. J., and Robinson, J. S. 2004. Genetic diversity of human pathogenic members of the Fusarium oxysporum complex inferred from multilocus DNA sequence data and amplified fragment length polymorphism analyses: Evidence for the recent dispersion of a geographically widespread clonal lineage and nosocomial origin. J. Clin. Microbiol. 42:5109-5120. https://doi.org/10.1128/JCM.42.11.5109-5120.2004 Crossref, Medline, ISI, Google Scholar
Ploetz, R., and Pegg, K. 1997. Fusarium wilt of banana and Wallace’s line: was the disease originally restricted to his Indo-Malayan region? Australas. Plant Pathol. 26:239-249. https://doi.org/10.1071/AP97039 Crossref, ISI, Google Scholar
Posada, D. 2008. jModelTest: phylogenetic model averaging. Mol. Biol. Evol. 25:1253-1256. https://doi.org/10.1093/molbev/msn083 Crossref, Medline, ISI, Google Scholar
Rambaut, A. 2018. FigTree v. 1.4.4. http://tree.bio.ed.ac.uk/software/figtree/ Google Scholar
Rheeder, J. P., and Marasas, W. F. O. 1998. Fusarium species from plant debris associated with soils from maize production areas in the Transkei region of South Africa. Mycopathologia 143:113-119. https://doi.org/10.1023/A:1006975825586 Crossref, Medline, ISI, Google Scholar
Ronquist, F., and Huelsenbeck, J. P. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinf 19:1572-1574. https://doi.org/10.1093/bioinformatics/btg180 Crossref, Medline, ISI, Google Scholar
Ronquist, F., Teslenko, M., Van Der Mark, P., Ayres, D. L., Darling, A., Höhna, S., Larget, B., Liu, L., Suchard, M. A., and Huelsenbeck, J. P. 2012. Mrbayes 3.2: Efficient Bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 61:539-542. https://doi.org/10.1093/sysbio/sys029 Crossref, Medline, ISI, Google Scholar
Stamatakis, A. 2014. RAxML version 8: A tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinf 30:1312-1313. https://doi.org/10.1093/bioinformatics/btu033 Crossref, Medline, ISI, Google Scholar
Summerell, B. A., Laurence, M. H., Liew, E. C. Y., and Leslie, J. F. 2010. Biogeography and phylogeography of Fusarium: A review. Fungal Divers. 44:3-13. https://doi.org/10.1007/s13225-010-0060-2 Crossref, ISI, Google Scholar
Swofford, D. L. 2002. Phylogenetic Analysis Using Parsimony * (and Other Methods). Version 4. Sinauer Associates, Cary, NC. Google Scholar
Taylor, A., Vágány, V., Jackson, A. C., Harrison, R. J., Rainoni, A., and Clarkson, J. P. 2016. Identification of pathogenicity-related genes in Fusarium oxysporum f. sp. cepae. Mol. Plant Pathol. 17:1032-1047. https://doi.org/10.1111/mpp.12346 Crossref, Medline, ISI, Google Scholar
van Diepeningen, A. D., and de Hoog, G. S. 2016. Challenges in Fusarium, a trans-kingdom pathogen. Mycopathologia 181:161-163. https://doi.org/10.1007/s11046-016-9993-7 Crossref, Medline, ISI, Google Scholar
Visser M., Gordon T., Fourie G., and Viljoen A. 2010. Characterisation of South African isolates of Fusarium oxysporum f. sp. cubense from Cavendish bananas. S. Afr. J. Sci. 106:154. doi:https://doi.org/10.4102/sajs.v106i3/4.154 Crossref, ISI, Google Scholar
Wang, B., Brubaker, C. L., and Burdon, J. J. 2004. Fusarium species and Fusarium wilt pathogens associated with native Gossypium populations in Australia. Mycol. Res. 108:35-44. https://doi.org/10.1017/S0953756203008803 Crossref, Medline, ISI, Google Scholar
Wang, B., Brubaker, C. L., Tate, W., Woods, J. M., Matheson, B. A., and Burdon, J. J. 2006. Genetic variation and population structure of Fusarium oxysporum f. sp. vasinfectum in Australia. Plant Pathol. 55:746-755. https://doi.org/10.1111/j.1365-3059.2006.01445.x Crossref, ISI, Google Scholar

Vol. 111, No. 8
August 2021

ISSN:0031-949X
e-ISSN:1943-7684

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Strawberry plant showing wilting symptoms due to crown rot disease (top); crown rots caused by Macrophomina phaseolina (bottom left), Colletotrichum gloeosporioides (bottom center), and Phytophthora cactorum (bottom right) (Wang et al.). Photo credit: Natalia Peres

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Article History

Issue Date: 10 Nov 2021
Published: 22 Sep 2021
First Look: 23 Nov 2020
Accepted: 18 Nov 2020

Pages: 1459-1469

Information

Funding

National Research Foundation
Grant/Award Number: FBIS150520118174
Grant/Award Number: SFH160723181425
Grant/Award Number: TTK13070120147

Keywords

The author(s) declare no conflict of interest.