Phytophthora cinnamomi stands out as one of the most devastating plant pathogens worldwide, rapidly expanding its range and impacting a wide range of host species. In this study, we investigated the virome of P. cinnamomi across 222 isolates from Africa, Asia, Europe, Oceania, and the Americas using stranded total RNA sequencing, reverse transcription polymerase chain reaction screening, and Sanger sequencing of selected isolates. Our analysis revealed that virus infections were prevalent across all sampled populations, including RNA viruses associated with the orders Ghabrivirales, Martellivirales, and Tolivirales, and the classes Amabiliviricetes, Bunyaviricetes, and the recently proposed Orpoviricetes. Viruses were mainly found in East and Southeast Asian populations, within the geographic origin of P. cinnamomi but have also spread to new regions where the pathogen has emerged as a clonal destructive pathogen. Among the identified viruses, eight species, including two bunya-like viruses, one narna-like virus, and five ormycoviruses, exhibit a global distribution with some genetic divergence between continents. The interaction between P. cinnamomi and its virome indicates a dynamic coevolution across diverse geographic regions. Indonesia is indicated to be the viral epicentre of P. cinnamomi, with the highest intra- and interspecies diversity of viruses. Viral diversity is significantly enhanced in regions where sexual recombination of P. cinnamomi occurs, while regions with predominantly asexual reproduction harbour fewer viral species. Interestingly, only the partially self-fertile mating type (MAT) A2, associated with the global pandemic, facilitates the spread of viruses across different biogeographic regions, whereas viruses are absent in the self-sterile MAT A1 in its areas of introduction like Australia and South Africa. Intriguingly, the presence of a plant tombusvirus suggests a potential cross-kingdom infection among Chilean isolates and a plant host. This study sheds further light on the geographical origin of P. cinnamomi from a novel virome perspective.
- Klíčová slova
- HTS orphan contigs, forest emerging diseases, mating, oomycetes, virus diversity, virus evolution, virus–host coevolution,
- Publikační typ
- časopisecké články MeSH
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. Taxonomic novelties: New species: Phytophthora amamensis T. Jung, K. Kageyama, H. Masuya & S. Uematsu, Phytophthora angustata T. Jung, L. Garcia, B. Mendieta-Araica, & Y. Balci, Phytophthora balkanensis I. Milenković, Ž. Tomić, T. Jung & M. Horta Jung, Phytophthora borneensis T. Jung, A. Durán, M. Tarigan & M. Horta Jung, Phytophthora calidophila T. Jung, Y. Balci, L. Garcia & B. Mendieta-Araica, Phytophthora catenulata T. Jung, T.-T. Chang, N.M. Chi & M. Horta Jung, Phytophthora celeris T. Jung, L. Oliveira, M. Tarigan & I. Milenković, Phytophthora curvata T. Jung, A. Hieno, H. Masuya & M. Horta Jung, Phytophthora distorta T. Jung, A. Durán, E. Sanfuentes von Stowasser & M. Horta Jung, Phytophthora excentrica T. Jung, S. Uematsu, K. Kageyama & C.M. Brasier, Phytophthora falcata T. Jung, K. Kageyama, S. Uematsu & M. Horta Jung, Phytophthora fansipanensis T. Jung, N.M. Chi, T. Corcobado & C.M. Brasier, Phytophthora frigidophila T. Jung, Y. Balci, K. Broders & I. Milenković, Phytophthora furcata T. Jung, N.M. Chi, I. Milenković & M. Horta Jung, Phytophthora inclinata N.M. Chi, T. Jung, M. Horta Jung & I. Milenković, Phytophthora indonesiensis T. Jung, M. Tarigan, L. Oliveira & I. Milenković, Phytophthora japonensis T. Jung, A. Hieno, H. Masuya & J.F. Webber, Phytophthora limosa T. Corcobado, T. Majek, M. Ferreira & T. Jung, Phytophthora macroglobulosa H.-C. Zeng, H.-H. Ho, F.-C. Zheng & T. Jung, Phytophthora montana T. Jung, Y. Balci, K. Broders & M. Horta Jung, Phytophthora multipapillata T. Jung, M. Tarigan, I. Milenković & M. Horta Jung, Phytophthora multiplex T. Jung, Y. Balci, K. Broders & M. Horta Jung, Phytophthora nimia T. Jung, H. Masuya, A. Hieno & C.M. Brasier, Phytophthora oblonga T. Jung, S. Uematsu, K. Kageyama & C.M. Brasier, Phytophthora obovoidea T. Jung, Y. Balci, L. Garcia & B. Mendieta-Araica, Phytophthora obturata T. Jung, N.M. Chi, I. Milenković & M. Horta Jung, Phytophthora penetrans T. Jung, Y. Balci, K. Broders & I. Milenković, Phytophthora platani T. Jung, A. Pérez-Sierra, S.O. Cacciola & M. Horta Jung, Phytophthora proliferata T. Jung, N.M. Chi, I. Milenković & M. Horta Jung, Phytophthora pseudocapensis T. Jung, T.-T. Chang, I. Milenković & M. Horta Jung, Phytophthora pseudocitrophthora T. Jung, S.O. Cacciola, J. Bakonyi & M. Horta Jung, Phytophthora pseudofrigida T. Jung, A. Durán, M. Tarigan & M. Horta Jung, Phytophthora pseudoccultans T. Jung, T.-T. Chang, I. Milenković & M. Horta Jung, Phytophthora pyriformis T. Jung, Y. Balci, K.D. Boders & M. Horta Jung, Phytophthora sumatera T. Jung, M. Tarigan, M. Junaid & A. Durán, Phytophthora transposita T. Jung, K. Kageyama, C.M. Brasier & H. Masuya, Phytophthora vacuola T. Jung, H. Masuya, K. Kageyama & J.F. Webber, Phytophthora valdiviana T. Jung, E. Sanfuentes von Stowasser, A. Durán & M. Horta Jung, Phytophthora variepedicellata T. Jung, Y. Balci, K. Broders & I. Milenković, Phytophthora vietnamensis T. Jung, N.M. Chi, I. Milenković & M. Horta Jung, Phytophthora ×australasiatica T. Jung, N.M. Chi, M. Tarigan & M. Horta Jung, Phytophthora ×lusitanica T. Jung, M. Horta Jung, C. Maia & I. Milenković, Phytophthora ×taiwanensis T. Jung, T.-T. Chang, H.-S. Fu & M. Horta Jung. Citation: Jung T, Milenković I, Balci Y, Janoušek J, Kudláček T, Nagy ZÁ, Baharuddin B, Bakonyi J, Broders KD, Cacciola SO, Chang T-T, Chi NM, Corcobado T, Cravador A, 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 C, Májek T, Masuya H, Magnano di San Lio G, Mendieta-Araica B, Nasri N, Oliveira LSS, Pane A, Pérez-Sierra A, Rosmana A, Sanfuentes von Stowasser E, Scanu B, Singh R, Stanivuković Z, Tarigan M, Thu PQ, Tomić Z, Tomšovský M, Uematsu S, Webber JF, Zeng H-C, Zheng F-C, Brasier CM, Horta Jung M (2024). 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. Studies in Mycology 107: 251-388. doi: 10.3114/sim.2024.107.04.
- Klíčová slova
- Gondwana, Laurasia, allopatric speciation, biodiversity, breeding systems, lifestyle, new taxa, phylogeny, sympatric species radiation,
- Publikační typ
- časopisecké články MeSH
UNLABELLED: Waterways are ideal pathways for Phytophthora dispersal and potential introduction to terrestrial ecosystems. While many Phytophthora species from phylogenetic clades 6, 9 and 10 are predominant oomycetes in watercourses due to their adaptation to a lifestyle as saprotrophs and opportunistic pathogens of riparian plants, species from clades 2, 7 and 8 are predominantly soil- or airborne using aquatic habitats as temporal niches for spreading and invading terrestrial sites along the watercourses. In contrast to forest ecosystems, knowledge of Phytophthora diversity in watercourses in Central Europe is limited. Between 2014 and 2019 extensive surveys of streams and rivers were undertaken across Austria, in South Moravia, Czech Republic and Žilina province, Slovakia to unveil the diversity and distribution of Phytophthora and related oomycetes. In addition, in Austria riparian forests of black alder (Alnus glutinosa) and grey alder (A. incana) in lowlands and in the Alps were examined. A variety of Phytophthora species from clades 2, 6, 7, 8, 9 and 10 were isolated, with clade 6 species showing the widest distribution and abundance. Furthermore, interspecific clade 6 hybrids and other oomycetes such as Halophytophthora fluviatilis and undescribed Nothophytophthora spp. were also obtained. In riparian alders, symptoms of Phytophthora infections were associated with species from the P. × alni complex and P. plurivora. Phytophthora plurivora was most common in alder stands whereas P. uniformis was the oomycete species occurring at the highest altitude in alpine riparian areas. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1007/s11557-023-01898-1.
- Klíčová slova
- Alpine, Dieback, Hybrids, Oomycetes, Phytophthora plurivora, Water filtration,
- Publikační typ
- časopisecké články MeSH
During a survey of Phytophthora diversity in Panama, fast-growing oomycete isolates were obtained from naturally fallen leaves of an unidentified tree species in a tropical cloud forest. Phylogenetic analyses of sequences from the nuclear ITS, LSU and ßtub loci and the mitochondrial cox1 and cox2 genes revealed that they belong to a new species of a new genus, officially described here as Synchrospora gen. nov., which resided as a basal genus within the Peronosporaceae. The type species S. medusiformis has unique morphological characteristics. The sporangiophores show determinate growth, multifurcating at the end, forming a stunted, candelabra-like apex from which multiple (8 to >100) long, curved pedicels are growing simultaneously in a medusa-like way. The caducous papillate sporangia mature and are shed synchronously. The breeding system is homothallic, hence more inbreeding than outcrossing, with smooth-walled oogonia, plerotic oospores and paragynous antheridia. Optimum and maximum temperatures for growth are 22.5 and 25-27.5 °C, consistent with its natural cloud forest habitat. It is concluded that S. medusiformis as adapted to a lifestyle as a canopy-dwelling leaf pathogen in tropical cloud forests. More oomycete explorations in the canopies of tropical rainforests and cloud forests are needed to elucidate the diversity, host associations and ecological roles of oomycetes and, in particular, S. medusiformis and possibly other Synchrospora taxa in this as yet under-explored habitat.
- Klíčová slova
- adaptation, caducity, canopy, evolution, homothallic, leaf pathogen, oomycete, phylogeny, synchronous sporulation, tropical,
- Publikační typ
- časopisecké články MeSH
Invasive, exotic plant pathogens pose a major threat to native and agricultural ecosystems. Phytophthora × cambivora is an invasive, destructive pathogen of forest and fruit trees causing severe damage worldwide to chestnuts (Castanea), apricots, peaches, plums, almonds and cherries (Prunus), apples (Malus), oaks (Quercus), and beech (Fagus). It was one of the first damaging invasive Phytophthora species to be introduced to Europe and North America, although its origin is unknown. We determined its population genetic history in Europe, North and South America, Australia and East Asia (mainly Japan) using genotyping-by-sequencing. Populations in Europe and Australia appear clonal, those in North America are highly clonal yet show some degree of sexual reproduction, and those in East Asia are partially sexual. Two clonal lineages, each of opposite mating type, and a hybrid lineage derived from these two lineages, dominated the populations in Europe and were predominantly found on fagaceous forest hosts (Castanea, Quercus, Fagus). Isolates from fruit trees (Prunus and Malus) belonged to a separate lineage found in Australia, North America, Europe and East Asia, indicating the disease on fruit trees could be caused by a distinct lineage of P. × cambivora, which may potentially be a separate sister species and has likely been moved with live plants. The highest genetic diversity was found in Japan, suggesting that East Asia is the centre of origin of the pathogen. Further surveys in unsampled, temperate regions of East Asia are needed to more precisely identify the location and range of the centre of diversity.
- Klíčová slova
- Hybridization, Invasive pathogen, Polyploidy, Population genetics,
- Publikační typ
- časopisecké články MeSH
During extensive surveys of global Phytophthora diversity 14 new species detected in natural ecosystems in Chile, Indonesia, USA (Louisiana), Sweden, Ukraine and Vietnam were assigned to Phytophthora major Clade 10 based on a multigene phylogeny of nine nuclear and three mitochondrial gene regions. Clade 10 now comprises three subclades. Subclades 10a and 10b contain species with nonpapillate sporangia, a range of breeding systems and a mainly soil- and waterborne lifestyle. These include the previously described P. afrocarpa, P. gallica and P. intercalaris and eight of the new species: P. ludoviciana, P. procera, P. pseudogallica, P. scandinavica, P. subarctica, P. tenuimura, P. tonkinensis and P. ukrainensis. In contrast, all species in Subclade 10c have papillate sporangia and are self-fertile (or homothallic) with an aerial lifestyle including the known P. boehmeriae, P. gondwanensis, P. kernoviae and P. morindae and the new species P. celebensis, P. chilensis, P. javanensis, P. multiglobulosa, P. pseudochilensis and P. pseudokernoviae. All new Phytophthora species differed from each other and from related species by their unique combinations of morphological characters, breeding systems, cardinal temperatures and growth rates. The biogeography and evolutionary history of Clade 10 are discussed. We propose that the three subclades originated via the early divergence of pre-Gondwanan ancestors > 175 Mya into water- and soilborne and aerially dispersed lineages and subsequently underwent multiple allopatric and sympatric radiations during their global spread. Citation: Jung T, Milenković I, Corcobado T, et al. 2022. Extensive morphological and behavioural diversity among fourteen new and seven described species in Phytophthora Clade 10 and its evolutionary implications. Persoonia 49: 1-57. https://doi.org/10.3767/persoonia.2022.49.01.
- Klíčová slova
- Gondwana, Laurasia, Oomycete, allopatric, biogeography, evolution, phylogeny, radiation, sympatric,
- Publikační typ
- časopisecké články MeSH
The considerable economic and social impact of the oomycete genus Phytophthora is well known. In response to evidence that all downy mildews (DMs) reside phylogenetically within Phytophthora, rendering Phytophthora paraphyletic, a proposal has been made to split the genus into multiple new genera. We have reviewed the status of the genus and its relationship to the DMs. Despite a substantial increase in the number of described species and improvements in molecular phylogeny the Phytophthora clade structure has remained stable since first demonstrated in 2000. Currently some 200 species are distributed across twelve major clades in a relatively tight monophyletic cluster. In our assessment of 196 species for twenty morphological and behavioural criteria the clades show good biological cohesion. Saprotrophy, necrotrophy and hemi-biotrophy of woody and non-woody roots, stems and foliage occurs across the clades. Phylogenetically less related clades often show strong phenotypic and behavioural similarities and no one clade or group of clades shows the synapomorphies that might justify a unique generic status. We propose the clades arose from the migration and worldwide radiation ~ 140 Mya (million years ago) of an ancestral Gondwanan Phytophthora population, resulting in geographic isolation and clade divergence through drift on the diverging continents combined with adaptation to local hosts, climatic zones and habitats. The extraordinary flexibility of the genus may account for its global 'success'. The 20 genera of the obligately biotrophic, angiosperm-foliage specialised DMs evolved from Phytophthora at least twice via convergent evolution, making the DMs as a group polyphyletic and Phytophthora paraphyletic in cladistic terms. The long phylogenetic branches of the DMs indicate this occurred rather rapidly, via paraphyletic evolutionary 'jumps'. Such paraphyly is common in successful organisms. The proposal to divide Phytophthora appears more a device to address the issue of the convergent evolution of the DMs than the structure of Phytophthora per se. We consider it non-Darwinian, putting the emphasis on the emergent groups (the DMs) rather than the progenitor (Phytophthora) and ignoring the evolutionary processes that gave rise to the divergence. Further, the generic concept currently applied to the DMs is narrower than that between some closely related Phytophthora species. Considering the biological and structural cohesion of Phytophthora, its historic and social impacts and its importance in scientific communication and biosecurity protocol, we recommend that the current broad generic concept is retained by the scientific community.
- Klíčová slova
- Biosecurity, Cladism, Downy mildews, Economic impact, Molecular phylogeny, Oomycetes, Paraphyly,
- Publikační typ
- časopisecké články MeSH