Phytophthora : taxonomic and phylogenetic revision of the genus

Abstract

Many members of the Oomycota genus Phytophthora cause economic and environmental impact diseases in nurseries, horticulture, forest, and natural ecosystems and many are of regulatory concern around the world. At present, there are 223 described species, including eight unculturable and three lost species. Twenty-eight species need to be redescribed or validated. A lectotype, epitype or neotype was selected for 20 species, and a redescription based on the morphological/molecular characters and phylogenetic placement is provided. In addition, the names of five species are validated: P. cajani, P. honggalleglyana (Synonym: P. hydropathica), P. megakarya, P. pisi and P. pseudopolonica for which morphology and phylogeny are given. Two species, P. ×multiformis and P. uniformis are presented as new combinations. Phytophthora palmivora is treated with a representative strain as both lecto- and epitypification are pending. This manuscript provides the updated multigene phylogeny and molecular toolbox with seven genes (ITS rDNA, β-tub, COI, EF1α, HSP90, L10, and YPT1) generated from the type specimens of 212 validly published, and culturable species (including nine hybrid taxa). The genome information of 23 types published to date is also included. Several aspects of the taxonomic revision and phylogenetic re-evaluation of the genus including species concepts, concept and position of the phylogenetic clades recognized within Phytophthora are discussed. Some of the contents of this manuscript, including factsheets for the 212 species, are associated with the "IDphy: molecular and morphological identification of Phytophthora based on the types" online resource (https://idtools.org/tools/1056/index.cfm). The first version of the IDphy online resource released to the public in September 2019 contained 161 species. In conjunction with this publication, we are updating the IDphy online resource to version 2 to include the 51 species recently described. The current status of the 223 described species is provided along with information on type specimens with details of the host (substrate), location, year of collection and publications. Additional information is provided regarding the ex-type culture(s) for the 212 valid culturable species and the diagnostic molecular toolbox with seven genes that includes the two metabarcoding genes (ITS and COI) that are important for Sanger sequencing and also very valuable Molecular Operational Taxonomic Units (MOTU) for second and third generation metabarcoding High-throughput sequencing (HTS) technologies. The IDphy online resource will continue to be updated annually to include new descriptions. This manuscript in conjunction with IDphy represents a monographic study and the most updated revision of the taxonomy and phylogeny of Phytophthora, widely considered one of the most important genera of plant pathogens. Taxonomic novelties: New species: Phytophthora cajani K.S. Amin, Baldev & F.J. Williams ex Abad, Phytophthora honggalleglyana Abad, Phytophthora megakarya Brasier & M.J. Griffin ex Abad, Phytophthora pisi Heyman ex Abad, Phytophthora pseudopolonica W.W. Li, W.X. Huai & W.X. Zhao ex Abad & Kasiborski; New combinations: Phytophthora ×multiformis (Brasier & S.A. Kirk) Abad, Phytophthora uniformis (Brasier & S.A. Kirk) Abad; Epitypifications (basionyms): Peronospora cactorum Lebert & Cohn, Pythiacystis citrophthora R.E. Sm. & E.H. Sm., Phytophthora colocasiae Racib., Phytophthora drechsleri Tucker, Phytophthora erythroseptica Pethybr., Phytophthora fragariae Hickman, Phytophthora hibernalis Carne, Phytophthora ilicis Buddenh. & Roy A. Young, Phytophthora inundata Brasier et al., Phytophthora megasperma Drechsler, Phytophthora mexicana Hotson & Hartge, Phytophthora nicotianae Breda de Haan, Phytophthora phaseoli Thaxt., Phytophthora porri Foister, Phytophthora primulae J.A. Toml., Phytophthora sojae Kaufm. & Gerd., Phytophthora vignae Purss, Pythiomorpha gonapodyides H.E. Petersen; Lectotypifications (basionym): Peronospora cactorum Lebert & Cohn, Pythiacystis citrophthora R.E. Sm. & E.H. Sm., Phytophthora colocasiae Racib., Phytophthora drechsleri Tucker, Phytophthora erythroseptica Pethybr., Phytophthora fragariae Hickman, Phytophthora hibernalis Carne, Phytophthora ilicis Buddenh. & Roy A. Young, Phytophthora megasperma Drechsler, Phytophthora mexicana Hotson & Hartge, Phytophthora nicotianae Breda de Haan, Phytophthora phaseoli Thaxt., Phytophthora porri Foister, Phytophthora primulae J.A. Toml., Phytophthora sojae Kaufm. & Gerd., Phytophthora vignae Purss, Pythiomorpha gonapodyides H.E. Petersen; Neotypifications (basionym): Phloeophthora syringae Kleb., Phytophthora meadii McRae Citation: Abad ZG, Burgess TI, Bourret T, Bensch K, Cacciola S, Scanu B, Mathew R, Kasiborski B, Srivastava S, Kageyama K, Bienapfl JC, Verkleij G, Broders K, Schena L, Redford AJ (2023). Phytophthora: taxonomic and phylogenetic revision of the genus. Studies in Mycology 106: 259-348. doi: 10.3114/sim.2023.106.05.

Keywords: IDphy; Phytophthora; identification; molecular toolbox; multilocus phylogeny; new taxa; online resource; redescription; revision; taxonomy; typification; validation.

Fig. 1

Order Peronosporales. Maximum likelihood tree inferred with IQ-TREE v. 2 from a three-loci (ITS, COI and β-tub) alignment (Supplementary Table S1). Ultrafast bootstrap support values ≤ 50 % are not shown. The strains employed as outgroups for the remainder of the phylogenetic inference are shown in bold. The uncollapsed version of this tree is available as Supplementary Fig. S1.

Fig. 2

Numbered clades of Phytophthora, and obligate biotrophic taxa including downy mildews. Maximum likelihood tree inferred with IQ-TREE v. 2 from a five-loci (COI, β-tub, EF1α, L10 and HSP90) alignment (Supplementary Table S1). The original ten clades (Clades 1–10) were collapsed for display purposes. The numbering of Bourret et al. (2018) was followed for Clades 14–16 despite topological differences. The uncollapsed version of this tree is available as Supplementary Fig. S2.

Fig. 3

Seven-loci Phytophthora phylogeny featuring 212 described species. Maximum likelihood best-tree inferred with IQ-TREE v. 2. Ultrafast ML bootstrap approximation support values > 50 % are shown, and bipartitions receiving a 1.0 posterior probability in a Bayesian analysis are thickened. Taxa in bold were re-described or newly described in the present manuscript. Clades and subclades are indicated with bold numerals and letters. The length of the Phytopythium outgroup branch was halved for display purposes. ET = ex-type; EEpT = ex-epitype; ENT = ex-neotype; SE = selected specimen. Sequence accessions are listed in Table 2.

Fig. 3

Seven-loci Phytophthora phylogeny featuring 212 described species. Maximum likelihood best-tree inferred with IQ-TREE v. 2. Ultrafast ML bootstrap approximation support values > 50 % are shown, and bipartitions receiving a 1.0 posterior probability in a Bayesian analysis are thickened. Taxa in bold were re-described or newly described in the present manuscript. Clades and subclades are indicated with bold numerals and letters. The length of the Phytopythium outgroup branch was halved for display purposes. ET = ex-type; EEpT = ex-epitype; ENT = ex-neotype; SE = selected specimen. Sequence accessions are listed in Table 2.

Fig. 4

Phytophthora cajani ex-type culture ATCC 44388. A–C. Colony morphology after 7 d growth at 20 °C. A. V8-Agar. B. Potato-Dextrose Agar. C. Malt Extract Agar. D. Empty sporangia with internal and extended proliferations. E. Ovoid sporangium originated in an unbranched sporangiophore. F. Globose sporangium originated in a sporangiophore showing hyphal swellings. G–I. Smooth-walled oogonia with amphigynous antheridia. I. Oogonium with highly aplerotic oospore. Scale bars = 20 μm; D applies to D–F; I applies to G–I.

Fig. 5

Phytophthora megakarya ex-type culture CBS 238.83 (IMI 202077). A–C. Colony morphology after 7 d growth at 20 °C. A. V8-Agar. B. Potato-Dextrose Agar. C. Malt Extract Agar. D, I. Ovoid, globose to limoniform sporangia originated in sympodial sporangiophores. E–G. Papillate sporangia with well-rounded bases. H. Caducous sporangium with medium and lateral attached pedicel. J–M. Gametangia with smooth-walled oogonia and amphigynous antheridia. K, L. Oogonia with thick-walled oospores. L. Oogonium with slightly aplerotic oospore and tapered base. Scale bars = 20 μm; J applies to E–M.

Fig. 6

Phytophthora pisi ex-type culture CBS 130350. A–C. Colony morphology after 7 d growth at 20 °C. A. V8-Agar. B. Potato-Dextrose Agar. C. Malt Extract Agar. D–F. Ovoid to ellipsoid persistent sporangia. D. Sporangium with globose catenulated hyphal swellings in the sporangiophore. G. Empty sporangium with direct germination from the apex. H–K. Gametangia showing smooth-walled oogonia; amphigynous antheridia and aplerotic oospores. Scale bars = 20 μm; K applies to D–K.

Fig. 7

Phytophthora pseudopolonica ex-type culture CBS 142610. A–C. Colony morphology after 7 d growth at 20 °C. A. V8-Agar. B. Potato-Dextrose Agar. C. Malt Extract Agar. D. Catenulate, globose to subglobose and irregular hyphal swellings. E–G. Ellipsoid to ovoid sporangia. H, I. Thin-walled chlamydospores. J. Germinating chlamydospores. K–N. Gametangia with smooth wall oogonia and paragynous antheridia. M. Comma-shaped oogonium with slightly aplerotic oospores containing a big ooplast. Scale bars = 20 μm; K applies to E–N.

Fig. 8

Phytophthora cactorum ex-epitype CBS 231.30. A–C. Colony morphology after 7 d growth at 20 °C. A. V8-Agar. B. Potato-Dextrose Agar. C. Malt Extract Agar. D. Sporangia originated in lax sympodial sporangiophore. E–H. Limoniform to obpyriform papillate sporangia with short pedicels. H. Detached sporangium with direct germination through the apex. I. Persistent sporangium with an external proliferation. J. Terminal globose chlamydospore. K–N. Globose oogonia, with plerotic oospores and paragynous antheridia nearly spherical to club-shaped. M. A paragynous antheridium with finger-like projection. Scale bars = 20 μm; K applies to E–N.

Fig. 9

Phytophthora citrophthora ex-epitype CBS 950.87. A–C. Colony morphology after 7 d growth at 20 °C. A. V8-Agar. B. Potato-Dextrose Agar. C. Malt Extract Agar. D. Persistent semipapillate sporangia originated in simple sympodial, individually or in irregularly branched sporangiophores. E. Sporangia originated in clusters. F. Sporangium originating individually in a log sporangiophore. G–I. Different shapes of sporangia. J. Sporangium with two papillae. G, K. Sporangia with caducous medium pedicels (rarely observed). L. Terminal globose chlamydospore. M. Clustered distorted shapes hyphal swellings. Scale bars = 20 μm; E applies to D–F; K applies to G–M.

Fig. 10

Lectotype of Phytophthora colocasiae preserved in FH.

Fig. 11

Phytophthora colocasiae ex-epitype culture CBS 149404. A–C. Colony morphology after 7 d growth at 20 °C. A. V8-Agar. B. Potato-Dextrose Agar. C. Malt Extract Agar. D. Sporangia originated in a simple branched sporangiophore with globose catenulated hyphal swellings. E–I. Limoniform to ellipsoid sporangia with medium pedicels. H, I. Semipapillate sporangia with folded and comma-shaped pedicels. J. Sporangium with unreleased zoospores inside. K–N. Globose and smooth-walled oogonia with plerotic oospore and amphigynous antheridia. Scale bars = 20 μm; K applies to E–N.

Fig. 12

Phytophthora drechsleri ex-epitype culture CBS 292.35 (A2). A–C. Colony morphology after 7 d growth at 20 °C. A. V8-Agar. B. Potato-Dextrose Agar. C. Malt Extract Agar. D. Globose, catenulate and rosary shape hyphal swellings. E–H. Ovoid to ellipsoid persisted sporangia. G. Empty sporangium with external extended proliferation. H. Internal nested proliferation and direct germination. I, J. Globose oogonia with amphigynous antheridia. Scale bars = 20 μm; J applies to E–J.

Fig. 13

Phytophthora erythroseptica ex-epitype culture CBS 148925. A–C. Colony morphology after 7 d growth at 20 °C. A. V8-Agar. B. Potato-Dextrose Agar. C. Malt Extract Agar. D–H. Nonpapillate, persistent, rounded bases sporangia originated in unbranched sporangiophores. H. Sporangium with distorted shape. I. Globose, subglobose and catenulate hyphal swellings. J–M. Gametangia showing typical smooth-walled oogonia, amphigynous antheridia and aplerotic oospores. Scale bar = 20 μm; J applies to D–M.

Fig. 14

Phytophthora fragariae ex-epitype culture CBS 309.62. A–C. Colony morphology after 7 d growth at 20 °C. A. V8-Agar. B. Potato-Dextrose Agar. C. Malt Extract Agar. D. Mycelium with hairy and coralloid hyphal swellings. E–J. Ovoid to ellipsoid, nonpapillate and persistent sporangia. J. Empty sporangium with external proliferation from the base. K–N. Smooth-walled golden brown oogonia with amphigynous antheridia, plerotic oospores and big ooplasts. Scale bar = 20 μm; K applies to D–N.

Fig. 15

Phytophthora gonapodyides ex-epitype culture CBS 554.67. A–C. Colony morphology after 7 d growth at 20 °C. A. V8-Agar. B. Potato-Dextrose Agar. C. Malt Extract Agar. D–H. Ellipsoid to elongated sporangia, nonpapillate, persistent originated in unbranched sporangiophores. D, H. Internal extended sporangial proliferation. E. Sporangium germinating directly with hyphae. I. Sporangium on a sporangiophore with hyphal swellings. J, K. Globose and irregular hyphal swellings. Scale bars = 20 μm; D applies to D–I; J applies to J, K.

Fig. 16

Phytophthora hibernalis ex-epitype culture CBS 114104 (IMI 134760). A–C. Colony morphology after 7 d growth at 20 °C. A. V8-Agar. B. Potato-Dextrose Agar. C. Malt Extract Agar. D. Sporangia originated in lax sympodial branching sporangiophores. E–I. Semipapillate caducous sporangia with medium to long pedicels. J–M. Oogonia with thick-walled, plerotic oospores and paragynous antheridia. Scale bars = 20 μm; E applies to E–I; J applies to J–M.

Fig. 17

Phytophthora ilicis ex-epitype culture NRRL 64374. A–C. Colony morphology after 7 d growth at 20 °C. A. V8-Agar. B. Potato-Dextrose Agar. C. Malt Extract Agar. D–F. Globose to sub-globose hyphal swellings. G–I. Semipapillate ovoid empty sporangia with short pedicels. J–M. Oogonia with amphigynous antheridia. J. Thick-walled plerotic oospore with a lipid globule. K. Smooth-walled oogonium with a plerotic oospore and a long unicellular amphigynous antheridium. Scale bars = 20 μm; J applies to E–M.

Fig. 18

Phytophthora inundata ex-epitype culture CBS 216.85 (IMI 389751). A–C. Colony morphology after 7 d growth at 20 °C. A. V8-Agar. B. Potato-Dextrose Agar. C. Malt Extract Agar. D, E, G–I. Globose to subglobose and irregular hyphal swellings. F. Typical coiled hyphae. J–L. Sporangia originated in unbranched sporangiophores. H, I. Internal nested sporangial proliferation. Scale bars = 20 μm; D applies to D, E, G; I applies to F, H–L.

Fig. 19

Phytophthora meadii ex-neotype culture CBS 148927. A–C. Colony morphology after 7 d growth at 20 °C. A. V8-Agar. B. Potato-Dextrose Agar. C. Malt Extract Agar. D. New forming sporangia in a sympodium sporangiophore. E–G. Ovoid to limoniform papillate sporangia. E. Caducous sporangium with medium pedicel. H. Irregular hyphal swellings. I. Intercalar hyphal swelling. J. Terminal chlamydospore. K–N. Smooth-walled oogonia with plerotic oospores and elongated amphigynous antheridia. Scale bar = 20 μm; K applies to K–N.

Fig. 20

Phytophthora megasperma ex-epitype culture CBS 402.72 (IMI 32035). A–C. Colony morphology after 7 d growth at 20 °C. A. V8-Agar. B. Potato-Dextrose Agar. C. Malt Extract Agar. D. Empty sporangia with internal extended proliferations. E–G. Ovoid to elongated persistent sporangia. H. Sporangium with internal extended proliferations and, on the right side, an intercalary hyphal swelling. I. External proliferation from the sporangium base. J. Internal nested sporangial proliferation. K–N. Oogonia with slightly aplerotic and thick-walled oospores and paragynous antheridia. Scale bar = 20 μm; K applies to D–N.

Fig. 21

Phytophthora mexicana ex-epitype culture CBS 149405. A–C. Colony morphology after 7 d growth at 20 °C. A. V8-Agar. B. Potato-Dextrose Agar. C. Malt Extract Agar. D–G. Ovoid to limoniform papillate and caducous sporangia. D. Long pedicel. E, F. Short pedicels. G. Medium pedicel. H, I. Knobby irregular hyphal swellings. J. Terminal globose chlamydospore. K–N. Globose to slightly wavy oogonia with aplerotic oospores and short amphigynous antheridia. Scale bar = 20 μm; D applies to D–N.

Fig. 22

Phytophthora nicotianae ex-epitype culture NRRL 64371. A–C. Colony morphology after 7 d growth at 20 °C. A. V8-Agar. B. Potato-Dextrose Agar. C. Malt Extract Agar. D. Globose chlamydospores. E–I. Globose to ovoid papillate sporangia. E. Lateral attached sporangium. H. Intercalary sporangium. J–M. Smooth-walled oogonia with oospores and amphigynous antheridia. J. Aborted oogonium. L. A slightly aplerotic oospore containing a lipid globule. Scale bar = 20 μm; J applies to D–M.

Fig. 23

Phytophthora palmivora representative strain culture CBS 305.62 (IMI 348384). A–C. Colony morphology after 7 d growth at 20 °C. A. V8-Agar. B. Potato-Dextrose Agar. C. Malt Extract Agar. D. Sporangia originated in simple sympodial sporangiophore. E–I. Ovoid to obpyriform papillate sporangia. E, F, I. Sporangia showing a short, preformed pedicel. J. Terminal globose chlamydospore. K–M. Oogonia with golden-brown wall and unicellular amphigynous antheridia. L. Aplerotic oospore. N. Oogonium with two antheridia. Scale bars = 20 μm; K applies to E–N.

Fig. 24

Lectotype of Phytophthora phaseoli preserved in FH.

Fig. 25

Phytophthora phaseoli ex-epitype culture CBS 114105. A–C. Colony morphology after 7 d growth at 20 °C. A. V8-Agar. B. Potato-Dextrose Agar. C. Corn Meal Agar. D. Sporangia originated in simple and simple sympodial sporangiophores. E–I. Obpyriform, limoniform, ovoid and globose semi-papillate and papillate (G) sporangia. F–I. Caducous sporangia with short to medium pedicels. Scale bars = 20 μm; I applies to E–I.

Fig. 26

Phytophthora porri ex-epitype culture CBS 116662. A–C. Colony morphology after 7 d growth at 20 °C. A. V8-Agar. B. Potato-Dextrose Agar. C. Malt Extract Agar. D–F. Sporangia originated in simple sympodial sporangiophores. G, H. Limoniform to elongated, semipapillate, persistent sporangia. I. Irregular hyphal swellings. J–M. Oogonia with golden-brown and slight wavy wall, and paragynous antheridia. J, K. Thick-walled and aplerotic oospores. Scale bars = 20 μm; D applies to D–I; J applies to J–M.

Fig. 27

Phytophthora primulae ex-epitype culture CBS 620.97. A–C. Colony morphology after 7 d growth at 20 °C. A. V8-Agar. B. Potato-Dextrose Agar. C. Malt Extract Agar. D, E. Catenulate, globose to subglobose and irregular hyphal swellings. F–J. Ovoid, obpyriform and elongated persistent sporangia. F, G. Sporangia showing direct germination from the apex and close to the base. K–N. Slight wavy walled oogonia with aplerotic oospores. K, M, N. Oogonia with paragynous antheridia. L. Oogonium with thick-walled oospore and amphigynous antheridium. Scale bars = 20 μm; D applies to D–J; K applies to K–N.

Fig. 28

Phytophthora sojae ex-epitype culture CBS 149406. A–C. Colony morphology after 7 d growth at 20 °C. A. V8-Agar. B. Potato-Dextrose Agar. C. Malt Extract Agar. D. Catenulate, globose to subglobose and irregular hyphal swellings. E–G. Nonpapillate and permanent sporangia. H. Oogonium and sporangium produced at the same time on solid medium. I. Terminal globose chlamydospore. J–L. Smooth-walled oogonia with paragynous antheridia nearly spherical to club-shaped and aplerotic oospores with big ooplasts. Scale bar = 20 μm; I applies to D–L.

Fig. 29

Phytophthora syringae ex-epitype culture CBS 110161. A–C. Colony morphology after 7 d growth at 20 °C. A. V8-Agar. B. Potato-Dextrose Agar. C. Malt Extract Agar. D. Catenulate, globose to subglobose and irregular hyphal swellings. E–H. Sporangia originated in simple sympodial sporangiophores. E. Empty, primary transitional sporangium with a secondary mature sporangium originated from through the apex. E, F, H. Nonpapillate and persistent sporangia. I. Terminal globose chlamydospore. J–M. Globose oogonia showing golden-brown wall, slightly aplerotic oospore and paragynous antheridia with digital projections. M. Elongated oogonium with a slightly aplerotic oospore. Scale bars = 20 μm; J applies to E–M.

Fig. 30

Phytophthora vignae ex-epitype culture WPC P3019. A–C. Non-papillate persistent sporangia produced in unbranched sporangiophores. C. Ovoid sporangium with a hyphal swelling in the sporangiophore. Scale bar = 20 μm.