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

Authors: JUNG, THOMAS - Mendel University; MILENKOVIC, IVAN - Mendel University; BALCI, YILMAZ - Animal And Plant Health Inspection Service (APHIS); JANOUSEK, JOSEF - Mendel University; KUDLACEK, TOMAS - Mendel University; NAGY, ZOLTAN - Mendel University; BAHARUDDIN, BAHARUDDIN - Muhammadiyah University Of Makassar; BAKONYI, JOZSEF - Hungarian Academy Of Sciences; Broders, Kirk; CACCIOLA, SANTA - University Of Catania

Submitted to: Studies in Mycology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/15/2024
Publication Date: 2/27/2024
Citation: Jung, T., Milenkovic, I., Balci, Y., Janousek, J., Kudlacek, T., Nagy, Z.A., Baharuddin, B., Bakonyi, J., Broders, K.D., Cacciola, S.O., et al. 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. https://doi.org/10.3114/sim.2024.107.04.
DOI: https://doi.org/10.3114/sim.2024.107.04

Interpretive Summary: Phytophthora are some of the most damaging microbial pathogens of agricultural crops, horticultural plants, and native forests. In the last twenty years over 150 new species of Phytophthora have been described, most of these coming from native forest ecosystems. Many of these species are not native to North American and may represent a biosecurity risk to the U.S. There is a critical lack of information on the scale of unknown pathogen threats and significant gaps in plant bio-security protocols that are based on incomplete or inaccurate lists of named pathogenic organisms. Therefore, it is important to continue documenting and surveying Phytophthora species in natural habitats around the world. An ARS researcher in Peoria, Illinois, collaborated with a global network of scientists led by the Phytophthora Research Centre at Mendel University in the Czech Republic to conduct a global survey of Phytophthora species. The research identified 43 new species of Phytophthora in natural ecosystems in Europe, Southeast and East Asia, and the Americas. This represents a significant expansion of our understanding of the diversity of this important pathogen and will be of interest to plant protection and quarantine officials, plant disease diagnosticians, plant pathologists, and foresters around the world.

Technical Abstract: During surveys of global Phytophthora diversity 43 new species were detected in natural ecosystems and, infrequently, in plantings and nurseries 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 the five known subclades 2a–e of Phytophthora major Clade 2 and the new subclade 2f. The evolutionary history of the Clade appears to have involved the pre-Gondwanan divergence of three extant subclades, 2c, 2d and 2e, 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 2f in Southeast/East Asia and 2b in South America, respectively, from their common ancestor. Species in Clade 2f 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. Evidence suggests the currently 93 described species and informally designated taxa of 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 in the genus Phytophthora 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 demonstrating the anachronism of plant biosecurity protocols based 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.