AR TICLE an Expanded Phylogeny for the Genus Phytophthora

ARTICLE 355

, P. et ?< et al. et al.

(Hong et al. 2012), P. drechsleri P. Phytophthora 3*4 oomycetes systematics taxonomy evolution plant pathology et al. 2011, Villa et al. 2011), P. multivesiculata P. that they are distinct P. irrigata P. *E[[O=X@W EL GL@BX >GL@BX observation of ?=F?@BL@EBX these @DBELELZ features BLV requires GMGD@E?G important morphological data can impair accurate species EVGL@E[OB@E<@HBXXE?> antheridia. However, plasticity in morphological characters B>

et al. 2010, 1 et al. 2016), et al. 2010, P. infestans, P. Phytophthora et al. 2002, Rizzo P. ramorum, P. that has species has continued P. sojae, P. can also cause et al. 2003a, 2004, Hansen @DBL?[

P. nicotianae, P. and Phytophthora et al. 2014a, b). The total number of formally , Brett M. Tyler , Brett M. here for this rapidly expanding genus. This phylogeny features signature sequences of 114 ex-types and 1 et al. 2011), streams (Bezuidenhout A comprehensive A phylogeny representing 142 described and 43 provisionally named Phytophthora stricta was placed basal to other clade 8 species, 7<=>=?@B@@DEF=@G@HGIBLLGD?MGOE[GVFW@HGB=@HBWL<@BX@GD 7<=>BWL<@=?G@HE?I>GDOEBXM=DM

sequences from P. sojae, P. ramorum (Tyler et al. 2006) and that were designated as representative isolates by the P. infestans (Haas et al GLBFXGV@HGEVGL@E[OB@E

ARTICLE phylogeny for the genus by analyzing sequences of the The Netherlands. internal transcribed spacer region (ITS) of 51 species. Kroon et al. (2004) constructed a phylogeny based on sequences =8# of four nuclear and mitochondrial genes of 48 species, and To extract genomic DNA (gDNA), an approximately 5 × 5 Blair et al. (2008) produced a sophisticated phylogeny based mm culture plug of each isolate was taken from the actively on sequences of seven nuclear genetic markers. That multi- growing area of a fresh culture. This was then grown in 20 % locus phylogeny divided 82 Phytophthora species into 10 OXBDE[GVFD<@HXE>BFGBLFD<@H[MXE[OB@EBX MD<@GEL between molecular phylogenies and individual morphological FG@B@=F=XEL$@=FGXMXE[OB@EMXE[OB@EM@ ?=OOG??[=X B>MXE[OB@EEELZ BLLGBXELZ tested and the exact evolutionary history of the genus temperature using gradient PCR (typically with lower Phytophthora warranted more investigation. annealing temperatures) or using the GoTaq® Flexi DNA In this study, an expanded phylogeny, including more Polymerase (Promega, Madison, WI) PCR mixture system. than 180 Phytophthora taxa, many not included in any Prior to sequencing, excess primer and dNTPs were previous phylogeny, was constructed. Sequences of seven removed from successful PCR products with shrimp alkaline nuclear genetic markers were used for construction of phosphatase and exonuclease I (USB Catalog # 70092Y the phylogeny. In light of this phylogeny, ancestral state and 70073Z). One unit of each enzyme was added to 15 μL reconstructions were conducted on the sporangial papillation PCR product, incubated at 37 °C for 30 min, followed by heat of Phytophthora species. Important evolutionary divergence inactivation at 65 °C for 15 min. Sequencing was performed events and associated changes in the sporangial morphology with both amplifying primers as well as internal primers, if any, of Phytophthora species are discussed. for individual genetic markers at the University of Kentucky Advanced Genetic Technologies Center (Lexington, KY). *GDEGV ?G=GLOELZ [XG? IGDG E?=BXEGV IE@H ELOH ;<=<;59= version 1.4.0 (Geospiza, Seattle, WA). Sequences of each isolate with all primers for individual genetic markers were $#$ aligned with Clustal W (Larkin et al. 2007) and edited manually A total of 376 Phytophthora isolates representing 142 to correct obvious sequencing errors and code ambiguous described and 43 provisionally named species, plus one sites according to the International Union of Pure and Applied isolate of each Elongisporangium undulatum (basionym: Chemistry (IUPAC) nucleotide ambiguity codes to produce a Pythium undulatum), , and consensus sequence. All sequences produced in this study Phytopythium vexans (basionym: Pythium vexans) as have been deposited in GenBank (Supplementary Table 1). outgroup taxa were included (Table 1). These included 114 Among 379 isolates (including three isolates of the ex-types (Table 2). Also included were 164 authentic isolates outgroup taxa) in the following phylogenetic analyses,

356 IMA FUNGUS 2'*$"*1Phytophthora ARTICLE 1 (Schröter 1886) 1993) 1985) 1985) Lévesque 2004) Duncan 1995) 1983) f 1969 (Ershad 1971) n.a. & Hohl (Galindo-A n.a. n.a. 1992 (De Bary 1876) 1999 n.a. (Flier et al. 2002) n.a. Germany n.a. (Kröber & Marwitz Ecuador 2001 AustraliaAustraliaAustralia 1985Iran et al. (Taylor 1985 n.a. Oregon, USA Oregon, USA 1975 n.a. Zimbabwe n.a. Mexico Mexico Mexico Mexico The Netherlands 2004 GermanyEcuadorEcuador 2004 n.a. n.a. (Oliva et al. 2010) Scotland, UK 1987 (Kennedy & Delaware, USA 2000 (Thaxter 1889) Mexico Mexico Mexico Scotland, UK Oregon, USA 1985 n.a. (Hamm & Hansen Delaware, USADelaware, USA n.a. n.a. $#" sp. Minnesota, USA 2003 n.a. sp. Ohio, USA n.a. sp. Minnesota, USA 2002 (de Cock & sp. Delaware, USA 2000 sp. The Netherlands 2001 sp. Chrysanthemum leucanthemum Solanum brevifolium Trifolium subterraneum Trifolium subterranea Trifolium n.a. Solanum melongena Psendotsuga menziesii Malus sp. Mirabilis jalapa Mirabilis jalapa Ipomoea longipedunculata Solanum tuberosum Bacopa Argyranthemum frutescens Solanum betaceum Solanum betaceum Rhododendron Rhododendron Rhododendron Viburnum Rubus idaeus Phaseolus lunatus Ipomoea longipedunculata Ipomoea longipedunculata Solanum tuberosum Irrigation water USA Virginia, Rubus idaeus Psendotsuga menziesii 2006 Phaseolus Phaseolus lunatus Phaseolus lunatus e A T ;*( A T A p304 p215 A p106 p460p461 A A P13365 P8497 P3007 p153 A P3006 p145 A P10227 P10650 P10150 P10145 P10225 P10226 d 158964 P3882 p218 T $## MYA-3655 MYA-4064 287317 64070, MYA-4063 64069, MYA-4062 38D4 CH ., ATCC IMI WPC MG 5)# Location ?# 22E722E8 16693 16694, MYA-3653 50470 P10193 p7 21168 P0715 p6 n.a. UK n.a. 30D5 30G8 33D8 30C2 31B6 60A3 38C2 62A5 11172562A1 968.95 P19523 T A 35B6 31B5 109229 c 2#($$# SP 27A8 PP 61J4 29F2 374.72 552.96 60237 P 32G1 347.86 58713, 60438 278933 P3943 p200 T PP 33F4 29B3 p226 p185 A P 22E6 P10194 p25 P 33F3 MYA-4165 p225 SP 23B4 SP 30C1 SP 60A2 P 34D4 971.95 MYA-4065 313728 P6767 p220 T SP 31B4 P 52938 331662 P10339 T ) #11L'### #11L("# P. infestans P. P. iranica P. tentaculata P. P. clandestina P. ( P. P. P. cactorum P. P. hedraiandra P. P. phaseoli P. P. mirabilis P. P. andina P. P. idaei P. P. ipomoeae P. P. pseudotsugae P. a 1b Information regarding isolates used in this study. GenBank accession numbers are listed in Table S1. Table GenBank accession numbers are listed in Information regarding isolates used in this study. ;#)$L )$# 1a 1c

VOLUME 8 · NO. 2 357 ?#" et al. 1 1923) 1896) 1906) 2011) al. 2015) al. 2015) ARTICLE 1948 (Leonian 1922) n.a. (Breda de Haan n.a. n.a. 1992 (Raciborski 1900) 2005 et al. (Vettraino 2005 1992 (McRae 1918) 1987 New Mexico, USA MexicoMichigan, USABrazil 1997 Brazil 1964 California, USACalifornia, USA n.a. n.a. n.a. (Hong et al. 2009) 1995 (Abad et al. 2011) MalaysiaIndiaIndonesia n.a. n.a. n.a. n.a. n.a. n.a. Argentina n.a. (Hotson & Hartge North Carolina, USA Malaysia 1966 North Carolina, USA California, USACalifornia, USA 2002 n.a. Malaysia 1986 ThailandThailand n.a. n.a. (Chee 1969) n.a. n.a. Hawaii, USA 2005 Nepal Nepal India India The Netherlands 1998 et (Man In’t Veld The Netherlands 2010 et (Man In’t Veld $#" sp. Nepal 2005 n.a. sp. sp. England, UK 1990 Capsicum annum Theobroma cacao Cucumis sativus Nicotiana tabacum Nicotiana tabacum Persea americana Persea americana Syringa Hevea brasiliensis Hevea brasiliensis Theobroma cacao Solanum lycopersicum Castanopsis Nicotiana tabacum Hevea brasiliensis Nicotiana tabacum Metrosideros excelsa Citrus sp. Hevea brasiliensis Heavae Hevea brasiliensis Irrigation water USA Virginia, 2000 (Smith & Smith n.a. Colocasia esculenta Colocasia esculenta Quercus leucotricophora Quercus leucotricophora Citrus sp. Hevea brasiliensis Buxus sempervirens Pachysandra terminalis e ;*( T T A T T p341 A p44 p132 p384 A p31 p47 p276 p75 P10116 P1452 d 92550 P0646 p355 342898 P10341 A 136915 P3425 130422 P6945 129185 $## 46012 P0253 MYA-4555 MYA-4059 26481 MYA-4159 MYA-4043 121656 P10386 CH ., ATCC IMI WPC MG 5)# Location ?# 62B4 12196942B3 P11685 T 22G1 15409, MYA-4036 p22 62C6 581.69 46C2 26H3 35D3 61G3 128753 61J9 219.88 c 2#($$# SPSP 31E5P 42B2 45G4 554.88 MYA-4554 46731 p340 p167 T A P 22F4 15399, MYA-4034 p8 A PP 26H4n.a.n.a. 61G4n.a. 46C3 128754 66767 P6713 p385 A p32 P6262 A P6310 A n.a. A A n.a. n.a. n.a. P 22F9 15410, MYA-4037 p23 P 22H8 P 03E5 SP 22F8 P 61G2 128767 P 22G5 SP 65B9 101557 SP 65B8 133865 ) #11L(''# #11L'%#$$&# (LMW.P (L2WW (L2WP $%&#'# ( P. glovera P. mengei P. P. capsici P. P. P. P. P. P. P. nicotianae P. P. botryosa P. P. citrophthora P. P. colocasiae P. P. himalsilva P. P. meadii P. P. occultans P. P. terminalis P. a (Continued). ;#)$L )$# 2b 1 2a

358 IMA FUNGUS 2'*$"*1Phytophthora et et ARTICLE 1 2007) Coffey 1991) Coffey 2014) al. 2010) 2001) al. 2010) 2014) 2009) n.a. n.a. 2011 n.a. 1929 n.a. (Aragaki & Uchida 2007 (Scott et al. 2009) 2010 2006 (Henricot et al. 2008 2009 1987 (Hong et al. 2011) 1998 (Jung & Burgess New York, USAYork, New n.a. New York, USAYork, New n.a. n.a. Brazil 1969 (Oudemans & North Carolina, USA Pennsylvania, USA Oregon, USA Oregon, USA 2003 Italy 2010 (Ginetti et al. AfricaSouth TaiwanJapan 1986 1987 (Sawada 1927) AfricaSouth 2005 (Bezuidenhout Tahiti Hawaii, USA n.a. South AfricaSouth n.a. (Bezuidenhout Australia, Australia Italy UK UK UK USA Minnesota, USA 1925 Western Western Australia, Australia New York, USAYork, New n.a. $#" sp. Virginia, West sp. cv. sp. cv. sp. Germany 1958 sp. Fagus sylvatica Fagus sylvatica Theobroma cacao Nicotiana tabacum sp. Taxus Acer pseudoplatanus Olea campensis Citrus sinensis Citrus sp. Agathosma betulina Vanila Macadamia integrifolia Curtisia dentata Acuba japonica Rhododendron Pinus resinosa Kalmia latifolia Rhododendron “Olga Mezitt” Rhododendron e ;*( A Soil A T A Soil T A Soil A Soil p27 p272 T p53 A p343p101 T p52 P1819 d 502404 $## MYA-3656 64532 MYA-3657 CH ., ATCC IMI WPC MG 5)# Location ?# 28D3 p121 A 41B8 62C3 12832133J2 295.29 P1823 A p375 A 61H2 35C8 434.91 76651, MYA-4218 61H8 62C2 128320 P1822 A Stream water Africa South n.a. 45F1 61H7 22F2 33H9 379.61 c 2#($$# P 22F5 15427, MYA-4035 p9 SPSP 22F3SP 28D1SP 27D9 56G1 p33 p119 A A n.a. A A ÒLEVGL@E[GVXGB[ Ohio, USA Hainan, China n.a. n.a. n.a. n.a. SP 41B7 122779 MYA-4187 P15122 T Stream water Oregon, USA 2003 (Reeser et al. SP 61H1 133931 T n.a. 46705 P0630 A SP 61F2 P 22H5 SPSP 33H8 221.88 55C5 60440 124094 21173 P0716 p396 T T Soil Western SP 61H6 SP 62C1 128319 SP 22F1 SP 22E9 ) (L$#E #11L#( (LP (L= (L(>$6 (L)#$ #8%/# ( P. P. P. P. P. P. siskiyouensis P. P. acerina P. P. P. P. tropicalis P. P. citricola P. multivora P. P. pachypleura P. P. capensis P. P. pini P. plurivora P. a (Continued). ;#)$L )$# 2c

VOLUME 8 · NO. 2 359 ?#" et al. et al. 1 2007) Young 1957) Young 2003) 2013) 2007) $ DB?EGD DE[[L 1979) ARTICLE 1999 n.a. 2004 1996 2009 (Rea et al. 2011) 2009 n.a. South AfricaSouth 2005 North Carolina, USA USA Wisconsin, USA 1989 (Abad et al. 2008) Australia 1995 (Rea et al. 2010) Australia Western Australia, Australia 1995 South AfricaSouth n.a. (Maseko et al. South AfricaSouth AfricaSouth n.a. 2001 Virginia, USAVirginia, 2006 (Hong et al. 2012) Canada n.a. (Buddenhagen & GermanyThe Netherlands n.a. 1999 California, USA n.a. California, USA n.a. (Hansen Oregon, USA Oregon, USA 2008Germany (Reeser et al. Germany 1997 (Jung et al. 2003) 1997 South AfricaSouth n.a. (Maseko et al. France Germany 1995 (Jung et al. 2002) Western Western Australia, Australia Western Western Australia, Australia Africa $#" sp. North Carolina, cv. cv. sp. The Netherlands n.a. (Ilieva et al. 1998) sp. The Netherlands n.a. Agathosma betulina Fragaria ×ananassa Rhododendron Rubus idaeus Canby Eucalyptus smithi Cymbidium Eucalyptus smithi Eucalyptus smithi Cymbidium Ilex sp. Quercus sp. Ilex aquifolium Umbellularia californica Quercus robur Quercus robur Eucalyptus dunnii Quercus ilex Quercus robur Theobroma cacao e ;*( T A n.a. T Soil A n.a. A T A T A A Stream water T T Rainwater A A T T Soil A Soil p141 p320 T p284Pp285 T A p288 p42 P1620 P10117 P10410 P3939 p113 P16948 d $## MYA-4577 56615, MYA-3897 MYA-4061 MYA-4930 MYA-2948 MYA-4083 MYA-4040 CH ., ATCC IMI WPC MG 5)# Location ?# 61F3 A 31E6 122081 55C4 125799 33J4 47G7 47G8 30D4 34D6 62A7 114348 41C4 30B1 29J6 62B7 125800 c 2#($$# SP 29D2 SP 33J3 P 47G6 SP to NPSP 29E3 545.96 SP 38J5 SP 23A7 SP 28J3 SP 60B3 SPSP 30A8 111772 29J5 MYA-4222 803.95 P 55C2 127950 P 47G5 121939 P 22H7 ) #8#@#$ ( P. bisheria P. P. elongata P. P. frigida P. P. multivesiculata P. P. P. ilicis P. P. nemorosa P. P. pluvialis P. P. pseudosyringae P. psychrophila P. P. arenaria P. P. alticola P. P. megakarya P. a (Continued). ;#)$L )$# 2d 2e 3 4

360 IMA FUNGUS 2'*$"*1Phytophthora ARTICLE et al. 1 2003a) 2012) al. 2011) 2003b) 2009) n.a. n.a. 1997 (Balci et al. 2008) 1997 2009 (Crous et al. 2003 n.a. n.a. (Katsura 1976) n.a. 1996 (Brasier et al. 1972 n.a. 1976Ann 1985) (Ko & Nigeria n.a. CameroonFlorida, USA n.a. n.a. (Butler 1910) North Carolina, USA Costa Rica n.a. South Carolina, USA South Carolina, USA Australia, Australia Germany 1995 (Jung et al. 1999) Ohio, USA 2006 n.a. GermanySerbia 1995 New Zealand 2006 et al. 2015) (Weir Taiwan Japan Hawaii, USAMalaysia 1990 et al. 2015) (Weir n.a. (Thompson 1929) Hainan, China n.a. Tennessee, USATennessee, 1964 The Netherlands 1999 et (Man in’t Veld California, USACalifornia, USA n.a. n.a. Taiwan Spain UK Iran California, USA 1987 (Hansen The Netherlands 1999 Taiwan $#" sp. sp. sp. Theobroma cacao Theobroma cacao Citrus sp. Nicotiana tabacum Theobroma cacao Soil Soil Quercus robur Quercus robur Quercus sp. Agathis australis Castanea Cocos nucifera Heavae Soil soil Zostera marina Malus domestica Phaseolus vulgaris Olea sp. Salix matsudana Pistacia vera Prunus sp. Prunus Zostera marina e ;*( A A Soil T T T Soil T A T A A p26 p45 p28p17 T p291 T p298 T p82 A p321 P16050 P8619 P3826P6702 p198 p199 T A Soil d 325914 180616 390121 389751 $## MYA-4038 MYA-4060 16701, MYA-3895 MYA-4456 MYA-3662 CH ., ATCC IMI WPC MG 5)# Location ?# 61J6 239.83 42099 106327 A 22G9 61J5 238.83 42100 202077 T 43G1 A Irrigation water USA Virginia, 2007 15C8 30A7 30A5 784.95 MYA-4084 61J7 587.85 36818 30E7 22J2 47J1 46H2 123383 30J4 41C1 32F9 c 2#($$# P 22G8 MYA-4039 P10213 p65 NPNP 48H2 62C9 A A Stream water Stream water USA Virginia, Taiwan 2008 n.a. 2013 n.a. NP 40A7 A Irrigation water USA Virginia, 2006 (Brasier et al. n.a. P11555 A P 15C7 NP 61G6 131652 T Stream water Western P 30A4 783.95 P 67D5 n.a. P 22H6 P 67D6 P 22J1 NP 46H1 123382 NP 30J3 NP 22J9 NP 32F8 200.81 52179, MYA-4080 ) (LM5 (LW.+ #84#$ (L( (L' ( P. palmivora P. P. P. P. P. P. quercetorum P. P. amnicola P. P. quercina P. P. agathidicida P. P. P. castaneae P. P. cocois P. P. heveae P. P. gemini P. P. inundata P. rosacearum P. P. humicola P. a (Continued). ;#)$L )$# 6b 5 6a

VOLUME 8 · NO. 2 361 ?#" et al. et al. et al. et al. 1 2012) 2012) 2015) 2011) Petersen 1910) 2013) 2015) ARTICLE 2010 (Aghighi 2012 (Scanu et al. 2011 2009 (Crous et al. 2009 (Jung et al. 2011) 2009 1967 2009 (Jung et al. 2011) 2009 1931 (Drechsler 1931) 2008 (Jung et al. 2011) 2012 (Scanu et al. Australia, Australia Alaska, USA 2008 (Hansen Italy Italy Western Western Australia, Australia Western Western Australia, Australia Western Western Australia, Australia England, UK n.a. (Buisman 1927, Western Western Australia, Australia Western Western Australia, Australia Germany 2003 (Nechwatal Germany 2003 England, UK 1972 Germany 2006 Washington DC, Washington USA Western Western Australia, Australia Italy $#" sp. The Netherlands n.a. Pachysandra Picea abies Water Reservoir water n.a. Salix matsudana Althaea rosea e ;*( T Stream water A T Soil T Stream water A Soil T Soil A Soil T Soil A Soil A Soil T A Soil T T Soil A Irrigation water Mississippi, USA 2012 et al. 2013) (Yang ATA Irrigation water Irrigation water Irrigation water Mississippi, USA 2012 Mississippi, USA 2012 Mississippi, USA 2012 T Soil p117 P6872 d 389725 P10337 32035 P3599 $## 46726 MYA-4946 CH ., ATCC IMI WPC MG 5)# Location ?# 62C5 133867 66D1 140357 62B8 127951 34A8 554.67 60351 62B9 127952 61D8 57J2 57J3 57J4 c 2#($$# NP 61G8 131653 T Soil Western NP 60B2 132023 MYA-4881 NP 66C9 NP 55B6 129424 NP to SPNP 55B7 NP 21J5 NP 55B8 NP 61D6 NP 61E1 NP 55B9 127953 NP to SPNP 57J1 NP 62C7 402.72 58817 NP 66D2 140647 ) (%#)%" ( P. bilorbang P. P. borealis P. P. crassamura P. P. gibbosa P. P. gonapodyides P. P. gregata P. P. lacustris P. P. litoralis P. P. mississippiae P. P. megasperma P. P. ornamentata P. a (Continued). ;#)$L )$#

362 IMA FUNGUS 2'*$"*1Phytophthora ARTICLE et al. 1 2012) 2008) 2012) 2014c) 2007) 2013 (Jung et al. 2017) 1998 (Jung et al. 2002) 1998 2013 (Jung et al. 2017) 2004 (Jung et al. 2011) 2013 (Jung et al. 2017) 1998 (Jung et al. 2002) 2013 (Jung et al. 2017) 2005 California, USANew Zealand 1987 1980 (Crous et al. New York, USAYork, New n.a. n.a. California, USA n.a. n.a. Indonesia 1989 n.a. Michigan, USA 2006 Taiwan Chile 2007 (Duran et al. France Chile 2007 France Germany 1999 Taiwan Australia, Australia Taiwan England, UK n.a. Maryland, USA n.a. (Hickman 1940) Poland Taiwan AustraliaScotland, UK n.a. (Man in ‘t Veld n.a. Virginia, USAVirginia, n.a. Norway $#" cv. "Glen cv. sp. sp. Actinidia chinensis Malus domestica Prunus sp. Syzygium aromaticum Pinus radiata Quercus sp. Pinus radiata Quercus sp. Fragaria ×ananassa Fragaria ×ananassa Rubus Rubus idaeus Clova" Fragaria ×ananassa Rubus e ;*( A T T Soil T Soil T Soil T Soil A Irrigation water USA Virginia, 2006 et al. (Yang T ATA Irrigation water Irrigation water Irrigation water USA Virginia, USA Virginia, 2006 USA Virginia, 2007 2007 T Soil T Soil p186 A p389 T P6306 P3570 p114 P10413 d 181417 P6231 $## 11374 MYA-4926 90442 CH ., ATCC IMI WPC MG 5)# Location ?# 62C4 132095 MYA-4826 23A3 MYA-3660 p79 A 66D3 A Soil Italy 2012 63H7 A Pond water Delaware, USA 2014 47H2 122922 A 34C2 62A2 109049 43F3 44F9 36J7 30C5 61J3 209.46 41D5 46C7 c 2#($$# NP 33D7 384046 A n.a. P10456 A Canal water California, USA 2002 n.a. NPNP 26E1NP 63H4NP 22J5 23A1 16698 p116 A p16 A A p81 n.a. A Pond water Delaware, USA 2014 n.a. n.a. n.a. n.a. NP 67C5 n.a. NP 47H1 122924 T NP 30A3 NP 60B1 132024 MYA-4882 T Stream water Oregon, USA 2006 (Hansen NP 67C3 NP 55C1 127954 T Soil Western NP 67C4 NP 36H8 NP 22G6 NP 67B9 NP 30D7 NP 62A3 109054 ) (L##$ (LW< (L$#4# (L""##>$6 (L%"#(%#>$6 (L$#4 !"# ( P. asparagi P. P. P. P. P. P. P. attenuata P. P. P. pinifolia P. P. europaea P. P. riparia P. P. thermophila P. P. formosa P. P. ×stagnum P. P. fragariae P. P. intricata P. P. rubi P. uliginosa P. a (Continued). ;#)$L )$# 6 7a

VOLUME 8 · NO. 2 363 ?#" et al. et et et al. 1 2013) 2014a) Jung et al. 2017) 2004, Husson al. 2015) al. 2001) Gerdemann 1958) Gerdemann ARTICLE 2001 1994 n.a. n.a. n.a. n.a.n.a. (Katsura 1976) 2005 2005 n.a. 1996 n.a. 1986 (Mirabolfathy n.a.n.a. (Amin et al. 1978) 2013 (Jung et al. 2017) n.a. (Purss 1957) 2013 (Jung et al. 2017) n.a. n.a. (Rands 1922) North Carolina, USA The Netherlands n.a. UK Sweden 2009 (Heyman et al. Japan India China Iran Japan Jiangsu, China n.a.Jiangsu, China (Rahman n.a. USA Oregon, USA Oregon, USA n.a. (Buisman 1927, FranceAustria 1996 (Brasier et al. Iran SwedenIran 2009 India India New York, USAYork, New n.a. Ontario, Canada 1959 (Kaufmann & Taiwan Mississippi, USA 1970 n.a. Taiwan Sri Lankan.a. n.a. South Carolina, USA $#" Thuja occidentalis Alnus sp. Alnus sp. Cucumis sativus Cajanus cajani Cucumis sativus Cucumis sativus Pueraria lobata Robinia pseudoacacia Robinia pseudoacacia Abies sp. Alnus glutinosa Alnus sp. Pistacia vera Pistacia vera Cajanus cajani Cajanus cajani n.a. Glycine max Glycine max Glycine max Vigna unguiculata Vigna sinensis Vigna Camellia japonica e ;*( A T Pea T T A Pea T Stream water T Stream water p64 p312p57 A A Irrigation water Unknown ornamental Israel USA Virginia, 2000 (Abad et al. 2014) p318 A p214 p388 A p38 p19 p314 A p216 T p348 A p236 p380 p357 A p10 P10617 p169 A P1371 p196 A P3105 p349 T d 316196 P3420 p379 $## 46719, MYA-4076 MYA-4163 MYA-4079 44388 56194 MYA-4075 MYA-4082 386658 44389 46735 64832 15400, MYA-4057 CH ., ATCC IMI WPC MG 5)# Location ?# 47A8 31E7 45F3 582.69 52854 61H3 133347 47A7 392314 T 60A5 23J6 41B4 45F7 46C6 26F8 62A4 10905532J7 392318 P10328 A Soil p206 A Germany 1998 41A9 45F6 28F9 46C1 112.76 64129 45G9 c 2#($$# NP 60A4 NP 22F6 NP 01D5 NP 32F6 NP 33D9 NP 45G1 90455 p352 A NP 33F7 p229 A Soil Virginia, West NP 32J6 392317 MYA-4081 p205 A NP 22D8 312.62 16705, MYA-3899 131375 NP 33D6 NP 67C1 NP 67C2 NP 45G6 NP 23B1 ) (L(##F ( P. pisi P. P. ×cambivora P. P. niederhauserii P. P. melonis P. P. cajani P. P. asiatica P. P. P. ×alni P. P. sojae P. P. pistaciae P. P. ×heterohybrida P. P. ×incrassata P. P. vignae P. P. cinnamomi P. a (Continued). ;#)$L )$# 7b 7c

364 IMA FUNGUS 2'*$"*1Phytophthora et et al. et al. ARTICLE et al. 1 2014) 2014b) 2014b) 1919) Lafferty 1913) Maxwell 1991) al. 2015) 2009) Maxwell 1991) 1968 (Rahman n.a. (Pethybridge & n.a. (Pethybridge 1997 1931) (Tucker 2003 1998 1989 (Buisman 1927) n.a. 1989 Indonesia 1922 Virginia, USAVirginia, 2008 n.a. California, USA n.a. n.a. Puerto Rico 1960 ItalyItaly 2008 2011 Japan 2005 (Rahman Japan Ireland Ireland South Carolina, USA California, USA n.a. New Hampshire, USA Ohio, USA n.a. (Hansen & South Carolina, USA California, USA 1975 Ecuador n.a. (Safaiefarahani USA Japan Indiana, USA n.a. (Hansen Indiana, USAIndiana, USA n.a. Mississippi, USA 1978 n.a. (Hansen & Mississippi, USA n.a. $#" sp. Japan var. var. sp. Germany 1991 (Scanu et al. sp. Germany 1992 cv. cv. Cinnamomum burmannii Beaucarnea Ilex glabra “Shamrock” Aster sp. Persea americana Beaucarnea Arbutus unedo Arbutus unedo Fragaria ×ananassa Rosa sp. Solanum lycopersicum Solanum tuberosum Soil Beta vulgaris altissima Gerbera jamesonii Medicago sativa Soil Medicago sativa Solanum marginatum Zantedeschia Zantedeschia aethiopica Zantedeschia aethiopica Glycine sp. Glycine sp. Glycine sp. vesiculosum Trifolium Trifolium sp. Trifolium e ;*( T T T T A A T p37 p347 T p142 A P10331 P1087 p41 T P1057 p124 P3103 P10811 P10355 p170 d 180615 P1738 34684 P1693 $## MYA-3900 44390 52402 MYA-4455 MYA-3901 CH ., ATCC IMI WPC MG 5)# Location ?# 23B261J1 144.22 46671 15401, MYA-405846F666C766C8 132771 22938 132772 P2110 p11 T A T A 15E6 23J5 292.35 46724 28F1 45F5 240.30 60353, 46734 325930 47H5 47H4 62A9 117687 c 2#($$# NP 46H5 A NP 22G2 308.62 15402, MYA-4161 325907 p12 NP 30G9 MYA-4078 p178 A NP 61H4 135747 T NP 61H5 133248 NPNP 61H9 113.19 15E5 NP 23A4 NP 61J2 129.23 NP NP 31E8 NP 47H3 NP 29B2 ) #11L*("# (L#8 ( P. P. P. parvispora P. P. fragariaefolia P. P. nagaii P. P. drechsleri P. P. cryptogea P. P. medicaginis P. P. erythroseptica P. P. pseudocryptogea P. P. richardiae P. P. sansomeana P. P. trifolii P. a (Continued). ;#)$L )$# 7d 8a

VOLUME 8 · NO. 2 365 ?#" et al. et al. 1 2013) al. 2002) 2013) 2006) 2013) 2013) 1942) 2013) 2001) ARTICLE 1998 n.a. 2002 1958 n.a. et al. (Werres UKThe Netherlands n.a. n.a. 1999 n.a. Maine, USA Virginia, West USA 2004 North Carolina, USA Sweden 1995 (Bertier et al. The Netherlands 1995 et (Man in’t Veld The Netherlands 1986 Greece 2006 (Bertier et al. The Netherlands 2004 (Bertier et al. Portugal 1931 (Carne 1925) France 2009 (Bertier et al. Western Australia, Australia Oregon, USA n.a.Milbrath & (Tucker FranceFranceFrance 2004 2004 2004 California, USA 1997 Greece 2001 (Bertier et al. South Carolina, USA GreeceGreece 2002 2003 Germany 1997 1952) (Tomlinson Switzerland n.a. n.a. var. var. var. var. $#" sp. USA Tennessee, 2004 (Donahoo sp. The Netherlands 1998 Cichorium intybus foliosum Allium porrum Solanum tuberosum Abies concolor Abes fraseri Fragaria ×ananassa Brassica oleracea Brassica oleracea Petroselinum crispum Rhododendron Cichorium intybus foliosum Citrus sinensis Daucus carota Citrus sinensis Chamaecyparis lawsoniana Duscus carota Duscus carota Duscus carota Chamaecyparis lawsoniana Lactuca sativa Camellia japonica Lactuca sativa Lactuca sativa Primula acaulis Primula Allium cepa e ;*( T p51 A p128 P19521 d 36906 P6871 p115 $## MYA-3898 201856 CH ., ATCC IMI WPC MG 5)# Location ?# 33A1 p207 31E4 P10613 p166 A 61J8 179.87 P7517, 32F7 114104 56353, MYA-3896 134760 P3822 p197 32E5 32E632E7 P10728 p194 29A9 61F761F8 A A 29F1 p287 c 2#($$# NP 22J4 MYA-4041 p50 n.a.SPSP 61E3 133815 29E7 Ohio, USA n.a. n.a. A A SP 61E7 131246 A NP 24A7SP 29D8 MYA-4162 686.95 p102 A A SP 61G1 A SP 62A8 115029SP T SP 49J8 121655 22H1 MYA-3638 270.31 60352 P10974 T SP 61E5 127102 T NP to SPNP 22H9 SP 61F4SP T 32G2 SP 29E9 620.97 p286 n.a. 112968 P6207 A ) (L6$%## #11L*'(# #11L' (L+ ( P. P. P. P. P. P. P. brassicae P. P. cichorii P. hibernalis P. P. foliorum P. P. dauci P. P. lateralis P. P. lactucae P. ramorum P. P. primulae P. P. a (Continued). ;#)$L )$# 8b 8c

366 IMA FUNGUS 2'*$"*1Phytophthora et al. et al. ARTICLE 1 2007) 2012) 2014a) 2011) 2014b) 2014a)

VOLUME 8 · NO. 2 367 ?#" et al. et al. 1 2013) 2006) ARTICLE n.a. (Irwin 1991) n.a. (Irwin 1991) 1994 Iran 1992 Iran 1992 n.a. Queensland, Australia Iran n.a.Iran n.a. Taiwan n.a.Hainan, China n.a. n.a. n.a. n.a. n.a. New South Australia Wales, IranIran n.a. Iran 1992 Iran n.a. n.a. New South Australia Wales, The Netherlands 1927 PeruPeru n.a. n.a. (Crandall 1947) New ZealandNew Zealand 1992 2000 New Zealand 1999 (Dick et al. 2006) $#" Pistacia vera Pistacia vera Glycine max Pistacia vera Pistacia vera Dianthus caryophyllus seawater Glycine max Pistacia vera Pistacia vera Pistacia vera Pistacia vera Glycine max Zantedeschia aethiopica Irrigation water USA Virginia, 2006 (Belbahri Eucalyptus saligna Eucalyptus saligna Irrigation waterEucalyptus saligna USA Virginia, 2007 e ;*( T A P8223P10264 A n.a. Ecuador 1993 P10267 P6703 A Soil Taiwan n.a. P10719 d 351473 P8017 p171 395328 P8618 A $## CH ., ATCC IMI WPC MG 5)# Location ?# 47C6 395331 A 33D5 240.30 60353 340618 47E1 A 47C847D860B5 A A P8217 T n.a. Ecuador n.a. 44G646A2 MYA-4927 T A Irrigation water Irrigation water USA Virginia, 2007 USA Virginia, 2007 46C4 407.48 46733 p386 T 38E1 691.79 38789 28880546H8 T Soil Taiwan 1980 43F9 49J9 P15005 A Soil Poland 2006 46H7 c 2#($$# NP 47C7NPNP 47C5 47D5NPNPNP 35G4 38D9 40J5SP 395330 33E1 SP 31E9 A A A A A A Irrigation water Unknown leaf in USA Virginia, 2005 n.a. NP 40A9 A Irrigation water USA Virginia, 2006 & Hong (Yang n.a.NP 60B4 P8220 P8213 A A n.a. n.a. Ecuador Ecuador n.a. 1993 n.a. n.a. NPNP 45F2 406.48 327E1 56964NP 40G9 MYA-4077 p344 A p123 water Waterfall Hainan, China n.a. (Ann & Ko 1980) NP 46H6 A ) #11L(### (LMQS (L$#"### #11L(### #11L(###P (LPSM (LP=+ (L*#) ( P. P. P. P. P. P. macrochlamydospora > P. macrochlamydospora > P. P. virginiana P. P. P. P. quininea P. polonica P. P. insolita P. P. captiosa P. a (Continued). ;#)$L )$# 9a (cluster 9a2) 9a (cluster 9a3) 9b

368 IMA FUNGUS 2'*$"*1Phytophthora et al. et al. ARTICLE 1 2015) 2010) 2015) Nechwatal 2008) 2014) 2015) 2005) 2010) n.a. (de Cock et al. 2006 (Rea et al. 2011) $ E$6 *#))# ( P. lilii P. P. P. constricta P. :#)!/+,-!/+-+!;# (%#-%)%" +,-!/,-+%$ (#'" Elongisporangium undulatum P. gallica P. gondwanensis P. P. boehmeriae P. P. intercalaris P. P. kernoviae P. P. morindae P. a Sporangial papillation: NP = non-papillate, P = papillate, and SP = semi-papillate. = papillate, and SP = non-papillate, P Sporangial papillation: NP Molecular (sub)clade as designated in Fig. 1 B>G?<[@BBEL[BXXWVG?EZLB@GV[GEL@HE??@=VWBDG=LVGDXELGV ?

VOLUME 8 · NO. 2 369 ?#" et al.

;#)$L Numbers of species and ex-types included in phylogenies ?=OH B? @HG ) ZGLG <[ Phytophthora bilorbang (61G8), for the genus Phytophthora in previous studies and this study. the Enl gene of P. macrochlamydospora (33E1, 31E9, and %)1( 33D5), and P. quininea (45F2), and TigA of P. megasperma 2'*$"* %#$ 2&#$ %)18>*( (62C7) (Supplementary Table 1). These failures were set as Cooke et al. (2000) 49 2 9 missing data in the alignment. After trimming, each isolate

ARTICLE Kroon et al. (2004) 46 2 18 was represented by an 8435-bp concatenated sequence in Blair et al. (2008) 72 10 16 the alignment including gaps and missing data. This included Martin et al. (2014) 90 17 31 FM [ 95 % bootstrap values in ML Clustal X version 2.1 (Larkin et al. 2007). The alignment was analysis and 100 % posterior probability (PP) in BA analysis edited in BioEdit version 7.2.5 (Hall 1999) to trim aligned (Fig. 1). Clades 1–3, 5, 7, and 10 were also highly supported concatenated sequences to an equal size and set missing data by > 95 % bootstrap values in the MP analysis (Fig. 1). to question marks. The edited alignment was then analyzed However, clades 6, 8, and 9, were only moderately supported in jModelTest version 2.1.7 (Posada 2008) to select the most with bootstrap numbers of 68, 61, and 52 in the MP analysis, appropriate model for the following phylogenetic analyses. respectively (Fig. 1). Maximum likelihood (ML) analysis was performed using As nearly half of all taxa included in this phylogeny were RAxML version 8.2.0 (Stamatakis 2014) with the selected recently described, all clades in this phylogeny are expanded model and 1000 bootstrap replicates. Maximum parsimony here to various extents compared to previously published (MP) analysis was conducted using PAUP version 4.0a147 phylogenies. The general structure of clades 1, 3, 5, 8 and (Swofford 2002) with 1000 bootstrap replicates. Bayesian 10 remained as previously assigned by Blair et al. (2008) analysis (BA) was performed using MrBayes version 3.2.6 and Martin et al. (2014) with additions of new species. For (Ronquist et al. 2012) for two million generations with the example, clade 1 was divided into three well-supported selected model. Phylogenetic trees were viewed and edited in subclades and P. nicotianae was placed basal to subclades FigTree version 1.4.2. Alignment and phylogenetic trees from 1b and 1c (Fig. 1). Clade 8 was divided into four generally all methods have been deposited in TreeBASE (S19303). well-supported subclades, except P. stricta, which was placed basal to all clade 8 species (Fig. 1). New subclades #$ '## # 1 were assigned to clade 2 (Fig. 2), clade 6 (Fig. 3), clade 7 (#"#$(#($$# (Fig. 4) and clade 9 (Fig. 5). Information on the sporangial papillation of individual species Several species were placed basal to other species in was compiled from the literature (Erwin & Ribeiro 1996, their respective clades. First, the cluster of P. quercina and Gallegly & Hong 2008, Kroon et al. 2012, Martin et al. 2012) P. sp. ohioensis was placed basal to other species of clade 4 with emphasis given to their respective original descriptions in all three analyses. The bootstrap supports of the ML and (Table 1). Both likelihood and parsimony ancestral state MP analyses, and PP (percentage) for the separation of this reconstructions were performed on the ML tree from cluster from that of P. alticola, P. arenaria, P. megakarya, P. the phylogenetic analyses using Mesquite version 3.03 palmivora, and P. quercetorum in clade 4 were only 48, 78, (Maddison & Maddison 2017). and 84, respectively (Fig. 1). Second, P. lilii was excluded from all known clades; it was placed basal to clades 1–5 and 7 (Fig. 1). Third, in clade 6, bootstrap support for the ML <; and MP analyses, and PP for all species except P. asparagi and P. sp. sulawesiensis were 100/100/100 (Fig. 3). This @0#$"%0#('*$" set of support numbers decreased to 99/92/100 when P. sp. %$ sulawesiensis was included, and to 100/68/100 when further (©B>MXE[OB@E

370 IMA FUNGUS 2'*$"*1Phytophthora ARTICLE

"LLA phylogeny for the genus Phytophthora based on concatenated sequences of seven nuclear genetic markers. Topology and branch lengths of maximum likelihood analysis are shown. Bootstrap values for maximum likelihood and maximum parsimony, and Bayesian posterior probabilities (percentages) are indicated on individual nodes and separated by a forward slash. An asterisk is used in place of nodes with unambiguous (100 %) support in all three analyses. A dash is used in place of a topology from an analysis ambiguous to the other two analyses and these sets of numbers with ambiguity in one analysis are also highlighted in red. Detailed structures of clades 2, 6, 7, and 9 are shown in Figs 2–5, respectively. Species represented by ex-types and authentic isolates are written in brown and blue, respectively. Branches indicating three hypothesized evolutionary paths with all species producing papillate or semi-papillate sporangia are drawn in red or orange, respectively. Scale bar indicates number of substitutions per site.

VOLUME 8 · NO. 2 371 ?#" et al. ARTICLE

"LL Structure of Phytophthora clade 2 in a genus-wide phylogeny for the genus Phytophthora based on concatenated sequences of seven nuclear genetic markers. Topology and branch lengths of maximum likelihood analysis are shown. Bootstrap values for maximum likelihood and maximum parsimony, and Bayesian posterior probabilities (percentages) are indicated on individual nodes and separated by a forward slash. An asterisk is used in place of nodes with unambiguous (100 %) support in all three analyses. A dash is used in place of a topology from an analysis ambiguous to the other two analyses and these sets of numbers with ambiguity in one analysis are also highlighted in red. Species represented by ex-types and authentic isolates are written in brown and blue, respectively. Scale bar indicates number of substitutions per site.

all papillate species in clade 10 (Table 1) formed a well- VG[LGVBLGI?=FOXBVGOEZ=D@HGD>

372 IMA FUNGUS 2'*$"*1Phytophthora ARTICLE

"LPL Structure of Phytophthora clade 6 in a genus-wide phylogeny for the genus Phytophthora based on concatenated sequences of seven nuclear genetic markers. Topology and branch lengths of maximum likelihood analysis are shown. Bootstrap values for maximum likelihood and maximum parsimony, and Bayesian posterior probabilities (percentages) are indicated on individual nodes and separated by a forward slash. An asterisk is used in place of nodes with unambiguous (100 %) support in all three analyses. A dash is used in place of a topology from an analysis ambiguous to the other two analyses and these sets of numbers with ambiguity in one analysis are also highlighted in red. Species represented by ex-types and authentic isolates are written in brown and blue, respectively. Scale bar indicates number of substitutions per site.

(82/61/100) (Fig. 3). Isolates 62C9 and 48H2, belonging to considering that the support value of MP analysis was only two new species, had ambiguous placements within subclade moderate (68 %) when this single taxon was included (Fig. 6a among the three analyses (Fig. 3). With approximately 3), this previous assignation as a subclade was not adopted 20 species newly included in the present phylogeny, the here. In addition, in order to be consistent with subclade previously recognized “P. megasperma-P. gonapodyides names in other clades, subclades 6a and 6b were used here complex” (Brasier et al. 2003a), subclade II of clade 6 (Jung instead of subclades I and II by Jung et al. (2011). et al. 2011), or subclade 6b (Kroon et al. 2012) expanded and its separation from subclade 6a was well-supported by (c) Clade 7 100/100/100 values (Fig. 3). Within subclade 6b, separation Four subclades were distinguished in clade 7. Separation of the cluster of P. bilorbang, P. lacustris, and P. riparia from of the previously assigned subclades 7a and 7b was only the other subclade 6b species was highly supported by moderately supported by values 71/56/100 (Fig. 4). The 97/94/100 (Fig. 3), indicating that these three species may general structure of subclade 7a remained the same even VG[LGBLGI?=FOXBVGBX@H<=ZH@HE?E?L<@V

VOLUME 8 · NO. 2 373 ?#" et al. ARTICLE

"LML Structure of Phytophthora clade 7 in a genus-wide phylogeny for the genus Phytophthora based on concatenated sequences of seven nuclear genetic markers. Topology and branch lengths of maximum likelihood analysis are shown. Bootstrap values for maximum likelihood and maximum parsimony, and Bayesian posterior probabilities (percentages) are indicated on individual nodes and separated by a forward slash. An asterisk is used in place of nodes with unambiguous (100 %) support in all three analyses. A dash is used in place of a topology from an analysis ambiguous to the other two analyses and these sets of numbers with ambiguity in one analysis are also highlighted in red. Species represented by ex-types and authentic isolates are written in brown and blue, respectively. Scale bar indicates number of substitutions per site.

along with a provisional species, P. sp. ax from Virginia, USA recently described high-temperature tolerant species, such (Table 1), formed a distinct new subclade 7c (Fig. 4). The new as P. aquimorbida, P. chrysanthemi, P. hydropathica, P. subclade 7d, including two recently described species from macilentosa, P. parsiana, and P. virginiana). The cluster of Japan (Rahman et al. 2014b), P. fragariaefolia and P. nagaii, P. macrochlamydospora (two lineages with two isolates in was placed basal to other subclades in clade 7 (Fig. 4). each lineage, Table 1) and P. quininea constituted 9a2 (Fig. 5). The cluster of two other high-temperature tolerant species (d) Clade 9 P. insolita and P. polonica constituted 9a3 (Fig. 5). The well- The split of clade 9 into two subclades 9a and 9b was highly supported cluster of P. captiosa, P. constricta, and P. fallax supported in ML (98 %) and BA (100 %) analyses and was assigned as subclade 9b (Fig. 5). moderately supported in the MP (52 %) analysis (Fig. 5). However, monophyly was highly supported for subclade 9b <&$#*'*1(#"#$(#($$# (100/100/100) but not for subclade 9a (44/-/95) (Fig. 5). Within 11%##$'### subclade 9a, three monophyletic clusters were formed: 9a1, 9a2, and 9a3. However, support for the separation of these Sporangial papillation of individual species is indicated in three clusters was moderate or ambiguous. In particular, Table 1 and Fig. 6. Due to the size of the cladograms, clusters the MP results did not produce any consistent separation including species with the same sporangial papillation of the three clusters (Fig. 5). Cluster 9a1 included many within each (sub)clade were compressed in Mesquite. Both

374 IMA FUNGUS 2'*$"*1Phytophthora ARTICLE

"LSLStructure of Phytophthora clade 9 in a genus-wide phylogeny for the genus Phytophthora based on concatenated sequences of seven nuclear genetic markers. Topology and branch lengths of maximum likelihood analysis are shown. Bootstrap values for maximum likelihood and maximum parsimony, and Bayesian posterior probabilities (percentages) are indicated on individual nodes and separated by a forward slash. An asterisk is used in place of nodes with unambiguous (100 %) support in all three analyses. A dash is used in place of a topology from an analysis ambiguous to the other two analyses and these sets of numbers with ambiguity in one analysis are also highlighted in red. Species represented by ex-types and authentic isolates are written in brown and blue, respectively. Scale bar indicates number of substitutions per site. likelihood and parsimony methods suggested that non- =.9 papillate is the progenitor state of Phytophthora species, and that semi-papillate and papillate types were derived Here we presented an expanded phylogeny for the genus from the non-papillate. The analyses indicated three major Phytophthora, encompassing 142 formally named and 43 clusters of semi-papillate and (or) papillate species diverged provisionally recognized species (Table 2). In addition to from the non-papillate ancestors. First, species in clades 1 this comprehensive coverage, this expanded phylogeny to 5 (semi-papillate or papillate) diverged from non-papillate features over 1500 signature sequences generated from species in clade 7 and P. lilii (Fig. 6). Second, species in 278 ex-type and authentic isolates of 162 Phytophthora taxa subclades 8b to 8d (semi-papillate) diverged from non- (Supplementary Table 1). Furthermore, this study provided papillate subclade 8a species (Fig. 6). Third, papillate clade new insights into the evolutionary history of sporangial 10 species including P. boehmeriae, P. gondwanensis, P. papillation in Phytophthora. kernoviae, and P. morindae diverged from the non-papillate The expanded phylogeny provides a sound taxonomic P. gallica and P. intercalaris (Fig. 6). Several species such framework for this agriculturally and ecologically important as P. macrochlamydospora, P. mississippiae, P. gibbosa, genus. One hundred and fourteen ex-types were included, and P. constricta also evolved to produce partially semi- representing 80 % of the 142 formally named species in this papillate sporangia (Fig. 6). phylogeny. The majority of the 29 species not represented by ex-types, such as P. gonapodyides, P. infestans, P. meadii, P. mexicana, and P. nicotianae, were described long ago without

VOLUME 8 · NO. 2 375 ?#" et al. ARTICLE

"LWL Ancestral state reconstructions of sporangial papillation for the genus Phytophthora based on likelihood (left cladogram) and parsimony (right cladogram). Trace character history analyses were performed on the maximum likelihood phylogeny in Mesquite. Clusters including species of uniform sporangial papillation within individual (sub)clades were compressed in Mesquite.

designation of an ex-type culture. Likewise, almost all the 43 2015), P. uniformis (basionym: P. alni subsp. uniformis) and P. provisional species in this phylogeny were represented by ×multiformis (basionym: P. alni subsp. multiformis) in subclade authentic isolates from the originators of the respective species 7a (Brasier et al. 2004, Husson et al. 2015), P. pseudolactucae (Table 1 and Supplementary Table 1). This new framework in subclade 8b (Rahman et al. 2015), and P. prodigiosa (Puglisi IEXX [BOEXE@B@G EVGL@E[OB@E

376 IMA FUNGUS 2'*$"*1Phytophthora

The generation of over 1500 signature sequences ARTICLE from ex-types and authentic isolates in this study will aid DG?GBDOHGD? BLV [D?@ DG?MB@OHG? @< GDDGL@BDWBFXG G ?G>EMBMEXXB@G ?MGOEG? GG>MXE[GV FW P. a subject that has fascinated generations of mycologists and primulae in the group III of Waterhouse (1963), are primitive and plant pathologists. There have been three major hypotheses evolved to be non-papillate and papillate through two evolutionary regarding the development of papillation, as illustrated in paths, by Brasier (1983); (c) papillate species evolved from non- Fig. 7a, b, and c, respectively. First, papillate species were papillate ancestors. Semi-papillate species have been considered considered as descendants of Pythium-like, non-papillate as morphological variants of papillate or non-papillate species, by ancestors and semi-papillation has been considered as Cooke et al. (2000); (d) a new hypothesis developed in this study that intermediate between non-papillation and papillation non-papillate ancestors evolved directly to either papillate or semi- (Blackwell 1949, Cooke et al. 2000, Erwin & Ribeiro papillate species. Some semi-papillate species further evolved to be GOG ?G>EMBMEXXB@G ?MGOEG? GG>MXE[GV papillate, or vice versa. by P. primulae in the group III of Waterhouse (1963) are

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primitive; they were suggested to have evolved to papillate respective clades and the current 10-clade system. First, P. and non-papillate species through two distinct evolutionary stricta was initially placed close to other species in subclade lines (Brasier 1983). Third, semi-papillate sporangia are 8a based on sequences of the cytochrome c oxidase 1 morphological variants of papillate and non-papillate types (cox1) gene, but was not grouped in any ITS clade (Yang (Cooke et al. 2000). Here we suggest that the non-papillate et al. 2014a). This species was grouped in clade 8 in our

ARTICLE type is ancestral, and that non-papillate species could expanded phylogeny by ML and BA analyses (Fig. 1); the have evolved directly into either semi-papillate or papillate monophyly of this clade was only moderately supported (61 species (Fig. 7d). The evolution to semi-papillate species %) in the MP analysis (Fig. 1). Second, the monophyly of E? GG>MXE[GV FW @HGV@HG[LVELZFW©BH>BLet al. papillate ancestor of clade 7 species (Figs 1, 6). Second, (2015) that P. lilii was not grouped in any clade of the current the common ancestor of species in subclades 8b–d 10-clade system (Fig. 1). This species was not assigned as diverged from that of subclade 8a species while acquiring a distinct clade in our study, due to the relatively low clade- semi-papillation (Figs 1, 6). Third, the common ancestor to-clade resolutions (Fig. 1). Further analyses are warranted <[ [G OXBVG ?MGOEG? EL @HG >BEL OX=?@GD ELOX=VELZ P. to determine whether this unique species should be assigned boehmeriae, P. gondwanensis, P. kernoviae, P. morindae, as a new clade. and P. sp. boehmeriae-like, acquired papillate sporangia Although many branches in the expanded phylogeny while diverging from two non-papillate clade 10 species, P. have consistent maximum support in all three methods, gallica and P. intercalaris (Figs 1, 6). Besides these three some have only moderate to low or inconsistent support. major groups of papillate or semi-papillate species, a few These results highlight the challenges of correctly inferring species may have evolved to acquire semi-papillation the evolutionary separation of many closely related independently, such as P. macrochlamydospora in clade Phytophthora species, even when concatenated sequences 9 (Fig. 6). This evolutionary process may be underway for from seven phylogenetic markers were used. It can be some other species including P. constricta, P. gibbosa, and expected that as the cost of gene sequencing drops further, P. mississippiae, which all produce both semi-papillate and it will become possible to increase phylogenetic resolution non-papillate sporangia (Fig. 6). Furthermore, evolutionary among Phytophthora species by using concatenations reversion to partial production of non-papillate sporangia of much larger numbers of genes. For example, Ye et al. may have occurred in P. multivesiculata and P. lateralis in (2016) used 293 concatenated housekeeping proteins two semi-papillate subclades 2e and 8c, respectively (Fig. to infer a robust phylogeny of seven fully sequenced 6). However, that conclusion is uncertain due to limited Phytophthora ?MGOEG? BLV OGV @HB@ VEXVGI? and ambiguous data from species in these two subclades. (represented by three genome sequences) are nested MGOE[OBXXWP. lateralis was ambiguously reported as non- within the genus Phytophthora, close to Phytophthora papillate (Erwin & Ribeiro 1996, Gallegly & Hong 2008, clade 4 (Ye et al. 2016). However, even with full genome Martin et al. 2012, Tucker & Milbrath 1942) or non- to sequences, ambiguity may not be completely resolved in semi-papillate (Kroon et al. 2012) in different studies. In cases where speciation has involved large populations of subclade 2e, the only sister taxon of P. multivesiculata, sexually reproducing individuals, for example, as a result P. taxon aquatilis, was provisionally described as semi- of geographic separation. In these cases, there may be papillate, but only based on a single isolate (Hong et al. many sequence polymorphisms shared among separated 2012). Evolutionary reversion in the sporangial papillation species and these may confound the inference of a reliable of these two species requires validation in the future. phylogeny. Resolution of this level of ambiguity may require Also, more studies are warranted to analyze additional sequencing the whole genome of many isolates from the characters based on phylogenies with better clade-to-clade species of interest as well as using improved phylogenetic resolutions and provide a more comprehensive picture on and coalescent methods. the evolutionary history of Phytophthora species. With the number of described Phytophthora species That a number of species were placed basal to other increasing, recent studies have raised an important concern species in their respective clades in this expanded phylogeny in the accurate detection of species boundaries using MDG?GL@? B ?EZLE[OBL@ OHBXXGLZG @< @HG >

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Safaiefarahani et al. 2015). One example is the status of P. .39F<=<; ARTICLE hedraiandra as a distinct species in subclade 1a (Pánek et al &? GEVGLOGV FW @HG B>MXE[GV [DBZ>GL@ XGLZ@H This research was supported in part by grants from the USDA-NIFA- polymorphism (AFLP) and phylogenetic analysis based Specialty Crop Research Initiative (Agreement no. 2010-51181- on sequences of ITS, phenolic acid decarboxylase, and 21140). We would like to thank all authorities and species originators cox1 genes, a recent study concluded that P. hedraiandra who provided Phytophthora isolates to our study, including Yilmaz was just one lineage of P. cactorum, while morphological Balci, Zia Banihashemi, Lien Bertier, Karien Bezuidenhout, Clive data provided only limited information to delimitate these Brasier, Treena Burgess, Mike Coffey, Mannon Gallegly, Beatrice two species (Pánek et al. 2016). Also, phylogenetic Ginetti, Niklaus Grünwald, Everett Hansen, Beatrice Henricot, Fredrik analyses in this study indicated that P. cactorum and P. Heyman, Hon Ho, Maria Holeva, Steven Jeffers, Thomas Jung, Koji hedraiandra cluster with strong support (98/100/100), and Kageyama, Willem Man in ‘t Veld, Jan Nechwatal, Bruno Scanu, P. B[[HGVDBEBLVDBE?MXE[GVFWP. ×alni (Brasier et nov. from Amaranth in Taiwan. Journal of Phytopathology WM: al. 2004, Husson et al. 2015), many hybrid species have been 94–101. EVGL@E[GVB>GDZELZMXBL@MB@HBWFGB>FEZ=<=?MGOE[OBXXWEL?=FOXBVG quercetorum sp. nov., a novel species isolated from eastern and 6b, support values for the placement of P. ×stagnum and its north-central USA oak forest soils. Mycological Research : closely related species, P. mississippiae, P. borealis, and 906–916. P. sp. delaware were moderate in the ML and BA analyses Belbahri L, Moralejo E, Calmin G, Oszako T, Garcia JA, et al. (2006) and ambiguous in the MP analysis (Fig. 3). Similarly, in Phytophthora polonica, a new species isolated from declining subclade 7a, the placement of P. ×alni, P. ×cambivora, P. Alnus glutinosa stands in Poland. FEMS Microbiology Letters ×heterohybrida, and P. ×incrassata’ cluster was not well W: 165–174. resolved due to ambiguous placement in the MP analysis Bertier L, Brouwer H, De Cock A, Cooke DEL, Olsson CHB, et al. and moderate support values in the other two analyses (Fig. (2013) The expansion of Phytophthora clade 8b: three new 4). Adding mitochondrial sequences into the phylogenetic species associated with winter grown vegetable crops. Persoonia analyses may be a solution to this problem. However, due P: 63–76. to the uniparental inheritance of mitochondria, the hybrids Bezuidenhout CM, Denman S, Kirk SA, Botha WJ, Mostert L, et al. and their maternal parents are inseparable by mitochondrial (2010) Phytophthora taxa associated with cultivated Agathosma, ?G=GLOG?BLV@HGEDMXBOG>GL@?O<=XVO

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