Abstract
The microbial diversity associated with natural vegetation in the Greater Cape Floristic Region of South Africa is largely unexplored. As part of the Cape Citizen Science programme and independent research, surveys were conducted between 2015 and 2019 to catalogue the diversity of Phytophthora species associated with many plant species endemic to this region. Using soil and water baiting techniques, six isolates of the provisionally described Phytophthora taxon emzansi were recovered, together with three isolates of an undescribed Phytophthora species. In this study, we used both molecular and morphological data to describe these Phytophthora species. Isolates of P. emzansi sp. nov. and P. afrocarpa sp. nov. formed monophyletic lineages within Phytophthora Clades 2 and 10, respectively. Phytophthora emzansi sp. nov. and P. capensis are sister species residing in the P. citricola species complex, and both are homothallic. Phytophthora afrocarpa sp. nov. is a sister species to P. gallica, and both these taxa are sexually sterile. The present study augments our knowledge of the unique Phytophthora species associated with the native vegetation of southern Africa.
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Data availability
Phytophthora species described in this study are available at recognized microbial culture repositories. All sequence data generated in this study (Table 1) are available at NCBI GenBank (https://www.ncbi.nlm.nih.gov/genbank/). Alignment files can be accessed via TreeBASE (http://www.treebase.org).
References
Abad ZG, Burgess TI, Bienapfl JC, Redford AJ, Coffey M, Knight L (2019) IDphy: molecular and morphological identification of Phytophthora based on the types. USDA APHIS PPQ S&T Beltsville Lab, USDA APHIS PPQ S&T ITP, and Centre for Phytophthora Science and Management. . http://idtools.org/id/phytophthora/index.php. Accessed 15 February 2020
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410
Barker NP, Muller EM, Mill RR (2004) A yellowwood by any other name: molecular systematics and the taxonomy of Podocarpus and the Podocarpaceae in southern Africa. S Afr J Sci 100:629–632
Bezuidenhout CM, Denman S, Kirk SA, Botha WJ, Mostert L, McLeod A (2010) Phytophthora taxa associated with cultivated Agathosma, with emphasis on the P. citricola complex and P. capensis sp. nov. Persoonia 25:32–49
Blair JE, Coffey MD, Park S-Y, Geiser DM, Kang S (2008) A multi-locus phylogeny for Phytophthora utilizing markers derived from complete genome sequences. Fungal Genet Biol 45:266–277
Born J, Linder HP, Desmet P (2007) The greater cape floristic region. J Biogeogr 34:147–162
Burgess TI, Scott JK, Mcdougall KL, Stukely MJ, Crane C, Dunstan WA, Brigg F, Andjic V, White D, Rudman T (2017) Current and projected global distribution of Phytophthora cinnamomi, one of the world’s worst plant pathogens. Glob Chang Biol 23:1661–1674
Burgess TI, McDougall KL, Scott PM, Hardy GESJ, Garnas J (2019) Predictors of Phytophthora diversity and community composition in natural areas across diverse Australian ecoregions. Ecography 42:565–577
Cooke DEL, Drenth A, Duncan JM, Wagels G, Brasier CM (2000) A molecular phylogeny of Phytophthora and related oomycetes. Fungal Genet Biol 30:17–32
Crous PW, Rong IH, Wood A, Lee S, Glen H, Botha W, Slippers B, de Beer WZ, Wingfield MJ, Hawksworth DL (2006) How many species of fungi are there at the tip of Africa? Stud Mycol 55:13–33
Dick MW (1990) Keys to Pythium. University of Reading Reading, UK
Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797
Erwin DC, Ribeiro OK (1996) Phytophthora diseases worldwide. American Phytopathological Society, St. Paul, Minnesota
Goldblatt P, Manning JC (2002) Diversity of the cape region of southern Africa. Ann Mo Bot Gard 89:281–302
Grünwald NJ, LeBoldus JM, Hamelin RC (2019) Ecology and evolution of the sudden oak death pathogen Phytophthora ramorum. Annu Rev Phytopathol 57:301–321
Hüberli D, Tommerup IC, Hardy GESJ (2000) False-negative isolations or absence of lesions may cause mis-diagnosis of diseased plants infected with Phytophthora cinnamomi. Australas Plant Pathol 29:164–169
Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755
Hulbert JM, Paap T, Burgess TI, Roets F, Wingfield MJ (2019) Botanical gardens provide valuable baseline Phytophthora diversity data. Urban For Urban Green 46:126461
Kroon LPNM, Bakker FT, Van Den Bosch GBM, Bonants PJM, Flier WG (2004) Phylogenetic analysis of Phytophthora species based on mitochondrial and nuclear DNA sequences. Fungal Genet Biol 41:766–782
Lee S, Crous PW, Wingfield MJ (2006) Pestalotioid fungi from Restionaceae in the Cape floral kingdom. Stud Mycol 55:175–187
Lübbe WA, Mostert GP (1991) Rate of Ocotea bullata decline in association with Phytophtora cinnamomi at three study sites in the southern Cape indigenous forests. South African Forestry Journal 159:17–24
Maddison WP, Maddison DR (2019) Mesquite: a modular system for evolutionary analysis. Version 3.61 http://www.mesquiteproject.org.
Martin FN, Tooley PW (2003) Phylogenetic relationships among Phytophthora species inferred from sequence analysis of mitochondrially encoded cytochrome oxidase I and II genes. Mycologia 95:269–284
Myers N, Mittermeier RA, Mittermeier CG, da Fonseca GAB, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858
Nguyen L-T, Schmidt HA, Von Haeseler A, Minh BQ (2015) IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol 32:268–274
Oh E, Gryzenhout M, Wingfield BD, Wingfield MJ, Burgess TI (2013) Surveys of soil and water reveal a goldmine of Phytophthora diversity in South African natural ecosystems. IMA Fungus 4:123–131
Oudemans P, Förster H, Coffey MD (1994) Evidence for distinct isozyme subgroups within Phytophthora citricola and close relationships with P. capsici and P. citrophthora. Mycol Res 98:189–199
Roets F, Wingfield MJ, Crous PW, Dreyer LL (2009) Fungal radiation in the Cape Floristic Region: an analysis based on Gondwanamyces and Ophiostoma. Mol Phylogenet Evol 51:111–119
Roets F, Wingfield MJ, Crous PW, Dreyer LL (2014) Discovery of fungus-mite mutualism in a unique niche. Environ Entomol 36:1226–1237
Snijman DA (2013) Plants of the Greater Cape Floristic Region volume 2: the extra cape flora. Strelitzia 30. South African National Biodiversity Institute, Pretoria, South Africa
van Wyk PS (1973) Root and crown rot of silver trees. Journal of South African Botany 39:255–260
von Broembsen SL (1984) Occurrence of Phytophthora cinnamomi on indigenous and exotic hosts in South Africa, with special reference to the South-Western Cape Province. Phytophylactica 16:221–225
von Broembsen SL, Kruger FJ (1985) Phytophthora cinnamomi associated with mortality of native vegetation in South Africa. Plant Dis 69:715–717
von Broembsen SL, Lübbe WA, Geldenhuys CJ (1986) Phytophthora cinnamomi associated with decline of stinkwood (Ocotea bullata) in southern Cape indigenous forests. Phytophylactica 18:44
White TJ, Bruns T, Lee SJWT, Taylor JW (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. PCR protocols: A Guide to Methods and Applications 18:315–322
Acknowledgements
The staff of the SANBI Botanical Gardens are acknowledged for their support for the collections made by Trudy Paap and we are especially grateful to all of the participants of the Cape Citizen Science programme (https://citsci.co.za/). We appreciate permission to collect samples provided by SANParks (HULJ/AGR/006–2016/V3) and Cape Nature (0056-AAA041-00134). We thank Prof Noelani van den Berg and Juanita Engelbrecht of the Avocado Research Programme (ARP) at FABI for kindly sharing the mating type isolates of Phytophthora cinnamomi with us. We thank Dr Janneke Aylward (FABI and Stellenbosch University), Prof Adéle McLeod (Stellenbosch University) and members of the microbial culture collection of the Department of Plant Pathology, Stellenbosch University, for allowing us to retrieve their isolates of P. taxon emzansi.
Funding
This study was partially funded through the crowd-funding initiative of Joseph M. Hulbert (DOI:10.18258/2066). We also acknowledge additional funding from the University of Pretoria, members of the Tree Protection Cooperative Programme (TPCP), DSI/NRF Centre of Excellence in Plant Health Biotechnology (CPHB) South Africa and the Department of Forestry, Fisheries and the Environment (DFFE), South Africa, noting that this publication does not necessarily represent the views or opinions of DFFE or its employees.
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All authors contributed equally to the conception, writing and preparation of this manuscript. Primary isolations and preliminary identification of Phytophthora species were completed by JMH and TP. Morphological characteristics were measured and documented by TB and JMH. Molecular and phylogenetic analyses were completed by TB and JMH. Culture deposition and sequence submission were completed by TB. The first draft of the manuscript was written by TB and all authors commented on previous versions of the manuscript. This study was supervised by MJW, TIB and FR. All authors read and approved the final manuscript.
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Bose, T., Hulbert, J.M., Burgess, T.I. et al. Two novel Phytophthora species from the southern tip of Africa. Mycol Progress 20, 755–767 (2021). https://doi.org/10.1007/s11557-021-01702-y
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DOI: https://doi.org/10.1007/s11557-021-01702-y