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

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

doi:10.3114/sim.2024.107.04

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

Stud Mycol. 2024 Mar:107:251-388. doi: 10.3114/sim.2024.107.04. Epub 2024 Feb 27.

Authors

T Jung^{1

2}, I Milenković^{1

3}, Y Balci⁴, J Janoušek¹, T Kudláček^{1

5}, Z Á Nagy¹, B Baharuddin⁶, J Bakonyi⁷, K D Broders^{8

9}, S O Cacciola¹⁰, T-T Chang¹¹, N M Chi¹², T Corcobado¹, A Cravador¹³, B Đorđević¹, A Durán¹⁴, M Ferreira¹⁵, C-H Fu¹¹, L Garcia¹⁶, A Hieno¹⁷, H-H Ho¹⁸, C Hong¹⁹, M Junaid⁶, K Kageyama¹⁷, T Kuswinanti⁶, C Maia²⁰, T Májek¹, H Masuya²¹, G Magnano di San Lio²², B Mendieta-Araica¹⁶, N Nasri²³, L S S Oliveira²⁴, A Pane¹⁰, A Pérez-Sierra²⁵, A Rosmana⁶, E Sanfuentes von Stowasser²⁶, B Scanu²⁷, R Singh¹⁵, Z Stanivuković²⁸, M Tarigan¹⁴, P Q Thu¹², Z Tomić²⁹, M Tomšovský¹, S Uematsu³⁰, J F Webber²⁵, H-C Zeng³¹, F-C Zheng³², C M Brasier²⁵, M Horta Jung^{1

2}

Affiliations

¹ Mendel University in Brno, Faculty of Forestry and Wood Technology, Department of Forest Protection and Wildlife Management, Phytophthora Research Centre, 613 00 Brno, Czech Republic.
² Phytophthora Research and Consultancy, 83131 Nussdorf, Germany.
³ University of Belgrade, Faculty of Forestry, 11030 Belgrade, Serbia.
⁴ USDA-APHIS Plant Protection and Quarantine, 4700 River Road, Riverdale, Maryland, 20737 USA.
⁵ University of Greifswald, Institute for Mathematics and Computer Science & Center for Functional Genomics of Microbes, 17489 Greifswald, Germany.
⁶ Departement of Plant Pest and Disease, Faculty of Agriculture, Hasanuddin University, Makassar, 90245, South Sulawesi, Indonesia.
⁷ HUN-REN Centre for Agricultural Research, Plant Protection Institute, ELKH, 1022 Budapest, Hungary.
⁸ Smithsonian Tropical Research Institute, Apartado Panamá, República de Panamá.
⁹ USDA, Agricultural Research Service, National Center for Agricultural Utilization Research, Mycotoxin Prevention and Applied Microbiology Research Unit, Peoria, IL, 61604, USA.
¹⁰ Department of Agriculture, Food and Environment, University of Catania, 95123 Catania, Italy.
¹¹ Forest Protection Division, Taiwan Forestry Research Institute, Taipei, Taiwan.
¹² Forest Protection Research Centre, Vietnamese Academy of Forest Sciences, 10000 Hanoi, Vietnam.
¹³ MED-Mediterranean Institute for Agriculture, Environment and Development & CHANGE-Global Change and Sustainability Institute, University of Algarve, 8005-130 Faro, Portugal.
¹⁴ Fiber Research and Development, Asia Pacific Resources International Limited (APRIL), 28300 Pangkalan Kerinci, Riau, Indonesia.
¹⁵ Plant Diagnostic Center, Department of Plant Pathology and Crop Physiology, Louisiana State University Agricultural Center, Baton Rouge, Louisiana, USA.
¹⁶ Universidad Nacional Agraria, Carretera Norte, Managua 11065, Nicaragua.
¹⁷ River Basin Research Center, Gifu University, Gifu, 501-1193, Japan.
¹⁸ Department of Biology, State University of New York, New Paltz, New York 12561, USA.
¹⁹ Hampton Roads Agricultural Research and Extension Center, Virginia Tech, Virginia Beach, VA 23455, USA.
²⁰ Centre of Marine Sciences (CCMAR), University of Algarve, 8005-139 Faro, Portugal.
²¹ Forestry and Forest Products Research Institute (FFPRI), Tsukuba, Ibaraki, 305-8687, Japan.
²² University Mediterranea of Reggio Calabria, Department of Agriculture, 89124 Reggio Calabria, Italy.
²³ The United Graduate School of Agricultural Science, Ehime University, Matsuyama, 790-8566, Japan.
²⁴ Research and Development, Bracell, Alagoinhas, Bahia 48030-300, Brazil.
²⁵ Forest Research, Alice Holt Lodge, Farnham, Surrey GU10 4LH, UK.
²⁶ Laboratorio de Patología Forestal, Facultad Ciencias Forestales y Centro de Biotecnología, Universidad de Concepción, 4030000 Concepción, Chile.
²⁷ Department of Agricultural Sciences, University of Sassari, Viale Italia 39A, 07100 Sassari, Italy.
²⁸ University of Banja Luka, Faculty of Forestry, 78000 Banja Luka, Bosnia and Herzegovina.
²⁹ Center for Plant Protection, Croatian Agency for Agriculture and Food, 10000 Zagreb, Croatia.
³⁰ Laboratory of Molecular and Cellular Biology, Dept. of Bioregulation and Bio-interaction, Tokyo University of Agriculture and Technology, Fuchu, Tokyo, 183-8509, Japan.
³¹ The Institute of Bioscience and Biotechnology, Chinese Academy of Tropical Agricultural Sciences, Haikou 571101, Hainan, China.
³² College of Environment and Plant Protection, Hainan University, Baodoa Xincun, Danzhou City, Hainan 571737, China.

Abstract

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.

Keywords: Gondwana; Laurasia; allopatric speciation; biodiversity; breeding systems; lifestyle; new taxa; phylogeny; sympatric species radiation.