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Diversity of Phytophthora species in natural ecosystems of Taiwan and association with disease symptoms

Publication . Jung, Thomas; Chang, T. T.; Bakonyi, J.; Seress, D.; Perez-Sierra, A.; Yang, X.; Hong, C.; Scanu, B.; Fu, C. H.; Hsueh, K. L.; Maia, Cristiana; Abad-Campos, P.; Leon, M.; Horta Jung, Marília

In 2013 a survey of Phytophthora diversity was performed in 25 natural and seminatural forest stands and 25 rivers in temperate montane and subtropical lowland regions of Taiwan. Using baiting assays, 10 described species and 17 previously unknown taxa of Phytophthora were isolated from 71.5% of the 144 rhizosphere soil samples from 33 of 40 tree species sampled in 24 forest stands, and from 19 rivers: P. capensis, P. citrophthora, P. plurivora, P. tropicalis, P. citricola VII, P. sp. x botryosa-like, P. sp. x meadii-like and P. sp. occultans-like from Clade 2; P. palmivora from Clade 4; P. castaneae and P. heveae from Clade 5; P. chlamydospora and P. sp. forestsoil-like from Clade 6; P. cinnamomi (Pc), P. parvispora, P. attenuata nom. prov., P. flexuosa nom. prov., P. formosa nom. prov., P. intricata nom. prov., P. x incrassata nom. prov. and P. x heterohybrida nom. prov. from Clade 7; P. sp. palustris and five new hybrid species from Clade 9. The A1 mating type of Pc was widespread in both montane and lowland forests and rarely associated with disease, whereas the A2 mating type was limited to lowland forests and in some cases causing severe dieback. Most other Phytophthora species were not associated with obvious disease symptoms. It is concluded that (i) Taiwan is within the centre of origin of most Phytophthora taxa found, (ii) Pc A2 is an introduced invasive pathogen, and (iii) interspecific hybridizations play a major role in speciation and species radiations in diverse natural ecosystems.

2017-02Journal article

Open Access

Six new Phytophthora species from ITS Clade 7a including two sexually functional heterothallic hybrid species detected in natural ecosystems in Taiwan

Publication . Jung, Thomas; Horta, Marília; Scanu, B.; Seress, D.; Kovacs, G. M.; Maia, Cristiana; Perez-Sierra, A.; Chang, T. -T.; Chandelier, A.; Heungens, K.; van Poucke, K.; Abad-Campos, P.; Leon, M.; Cacciola, S. O.; Bakonyi, J.

During a survey of Phytophthora diversity in natural ecosystems in Taiwan six new species were detected. Multigene phylogeny based on the nuclear ITS, beta-tubulin and HSP90 and the mitochondrial cox1 and NADH1 gene sequences demonstrated that they belong to ITS Clade 7a with P. europaea, P. uniformis, P. rubi and P. cambivora being their closest relatives. All six new species differed from each other and from related species by a unique combination of morphological characters, the breeding system, cardinal temperatures and growth rates. Four homothallic species, P. attenuata, P. flexuosa, P. formosa and P. intricata, were isolated from rhizosphere soil of healthy forests of Fagus hayatae, Quercus glandulifera, Q. tarokoensis, Castanopsis carlesii, Chamaecyparis formosensis and Araucaria cunninghamii. Two heterothallic species, P. xheterohybrida and P. xincrassata, were exclusively detected in three forest streams. All P. xincrassata isolates belonged to the A2 mating type while isolates of P. xheterohybrida represented both mating types with oospore abortion rates according to Mendelian ratios (4-33 %). Multiple heterozygous positions in their ITS, beta-tubulin and HSP90 gene sequences indicate that P. xheterohybrida, P. xincrassata and P. cambivora are interspecific hybrids. Consequently, P. cambivora is re-described as P. xcambivora without nomenclatural act. Pathogenicity trials on seedlings of Castanea sativa, Fagus sylvatica and Q. suber indicate that all six new species might pose a potential threat to European forests.

2017-06Journal article

Restricted

Worldwide forest surveys reveal forty-three new species in Phytophthora major Clade 2 with fundamental implications for the evolution and biogeography of the genus and global plant biosecurity

Publication . Jung, T.; Milenković, I.; Balci, Y.; Janoušek, J.; Kudláček, T.; Nagy, Z. Á.; Baharuddin, B.; Bakonyi, J.; Broders, K. D.; Cacciola, S. O.; Chang, T.-T.; Chi, N. M.; Corcobado, T.; Cravador, Alfredo; Đorđević, B.; Durán, A.; Ferreira, M.; Fu, C.- H.; Garcia, L.; Hieno, A.; Ho, H.- H.; Hong, C.; Junaid, M.; Kageyama, K.; Kuswinanti, T.; Maia, Cristiana; Májek, T.; Masuya, H.; Magnano di San Lio, G.; Mendieta-Araica, B.; Nasri, N.; Oliveira, L. S. S.; Pane, A.; Pérez-Sierra, A.; Rosmana, A.; Sanfuentes von Stowasser, E.; Scanu, B.; Singh, R.; Stanivuković, Z.; Tarigan, M.; Thu, P. Q.; Tomić, Z.; Tomšovský, M.; Uematsu, S.; Webber, J. F.; Zheng, H.- C.; Zheng, F.- C.; Brasier, C. M.; Horta Jung, M.

During 25 surveys of global Phytophthora diversity, conducted between 1998 and 2020, 43 new species were detected in natural ecosystems and, occasionally, in nurseries and outplantings in Europe, Southeast and East Asia and the Americas. Based on a multigene phylogeny of nine nuclear and four mitochondrial gene regions they were assigned to five of the six known subclades, 2a-c, e and f, of Phytophthora major Clade 2 and the new subclade 2g. The evolutionary history of the Clade appears to have involved the pre-Gondwanan divergence of three extant subclades, 2c, 2e and 2f, all having disjunct natural distributions on separate continents and comprising species with a soilborne and aquatic lifestyle and, in addition, a few partially aerial species in Clade 2c; and the post-Gondwanan evolution of subclades 2a and 2g in Southeast/East Asia and 2b in South America, respectively, from their common ancestor. Species in Clade 2g are soilborne whereas Clade 2b comprises both soil-inhabiting and aerial species. Clade 2a has evolved further towards an aerial lifestyle comprising only species which are predominantly or partially airborne. Based on high nuclear heterozygosity levels ca. 38 % of the taxa in Clades 2a and 2b could be some form of hybrid, and the hybridity may be favoured by an A1/A2 breeding system and an aerial life style. Circumstantial evidence suggests the now 93 described species and informally designated taxa in Clade 2 result from both allopatric non-adaptive and sympatric adaptive radiations. They represent most morphological and physiological characters, breeding systems, lifestyles and forms of host specialism found across the Phytophthora clades as a whole, demonstrating the strong biological cohesiveness of the genus. The finding of 43 previously unknown species from a single Phytophthora clade highlight a critical lack of information on the scale of the unknown pathogen threats to forests and natural ecosystems, underlining the risk of basing plant biosecurity protocols mainly on lists of named organisms. More surveys in natural ecosystems of yet unsurveyed regions in Africa, Asia, Central and South America are needed to unveil the full diversity of the clade and the factors driving diversity, speciation and adaptation in Phytophthora.

2024-03Journal article

Open Access