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  • Article
  • Open Access

An expanded phylogeny for the genus Phytophthora

IMA Fungus20178:802355

https://doi.org/10.5598/imafungus.2017.08.02.09

  • Received: 8 June 2017
  • Accepted: 31 October 2017
  • Published:

Abstract

A comprehensive phylogeny representing 142 described and 43 provisionally named Phytophthora species is reported here for this rapidly expanding genus. This phylogeny features signature sequences of 114 ex-types and numerous authentic isolates that were designated as representative isolates by the originators of the respective species. Multiple new subclades were assigned in clades 2, 6, 7, and 9. A single species P lilii was placed basal to clades 1 to 5, and 7. Phytophthora stricta was placed basal to other clade 8 species, P asparagi to clade 6 and P intercalaris to clade 10. On the basis of this phylogeny and ancestral state reconstructions, new hypotheses were proposed for the evolutionary history of sporangial papillation of Phytophthora species. Non-papillate ancestral Phytophthora species were inferred to evolve through separate evolutionary paths to either papillate or semi-papillate species.

Key words

  • oomycetes
  • systematics
  • taxonomy
  • evolution
  • plant pathology

Introduction

The genus Phytophthora has had profound impacts on human history by causing agriculturally and ecologically important plant diseases (Erwin & Ribeiro 1996). Among the most notorious Phytophthora species is P. infestans, cause of the late blight disease, which was the primary cause of the Irish potato famine from 1845 to 1852 in which approximately one million people died and 1.5 million emigrated from Ireland (Turner 2005). Another example is the sudden oak death pathogen, P. ramorum, that has killed millions of coast live oak, tanoak and Japanese larch trees, and has permanently altered the forest ecosystems in California and Oregon, USA (Goheen et al. 2002, Rizzo et al. 2002, Rizzo et al. 2005). Other species, such as P. cinnamomi, P. nicotianae, and P. sojae, can also cause highly destructive plant diseases (Erwin & Ribeiro 1996). The impact caused by Phytophthora species has continued to increase with the emergence of new pathogens and diseases. The number of species known in the genus has doubled during the past decade due to extensive surveys in previously unexplored ecosystems such as natural forests (Jung et al. 2011, 2017, Rea et al. 2010, Reeser et al. 2013, Vettraino et al. 2011), streams (Bezuidenhout et al. 2010, Brazee et al. 2017, Reeser et al. 2007, Yang et al. 2016), riparian ecosystems (Brasier et al. 2003a, 2004, Hansen et al. 2012), and irrigation systems (Hong et al. 2010, 2012, Yang et al. 2014a, b). The total number of formally named species in the genus was about 58 in 1996 (Erwin & Ribeiro 1996), but now is more than 150. In addition, some provisionally or informally named species are also expected to be formally described in the near future.

A sound taxonomic system is foundational for correctly identifying Phytophthora species and safeguarding agriculture, forestry, and natural ecosystems. Traditionally, taxonomy of the genus was based on morphological characters. A fundamental morphology-based classification of Phytophthora species was established by Waterhouse (1963) who classified the species into six groups based on the morphology of sporangia, homothallism, and configuration of antheridia. However, plasticity in morphological characters amongst isolates of individual species is significant, so is homology or homoplasy among different species. For example, isolates of P. constricta (Rea et al. 2011), P. gibbosa (Jung et al. 2011), P. lateralis (Kroon et al. 2012), P. mississippiae (Yang et al. 2013), and P. multivesiculata (Ilieva et al. 1998) all produce a mixture of semi-papillate and non-papillate sporangia. Many non-papillate species recovered from irrigation water such as Phytophthora hydropathica (Hong et al. 2010) and P. irrigata (Hong et al. 2008) were morphologically inseparable from P. drechsleri, while sequence analyses demonstrated that they are distinct species. Also, production of many morphological structures and physiological features needs specific environmental conditions, while observation of these features requires substantial training and expertise. Difficulty in obtaining important morphological data can impair accurate species identification.

With the advent of DNA sequencing, the taxonomic concept for the genus has evolved from morphology to molecular phylogeny-based (Blair et al. 2008, Cooke et al. 2000, Kroon et al. 2004, Lara & Belbahri 2011, Martin et al. 2014, Martin & Tooley 2003, Robideau et al. 2011, Villa et al. 2006). In particular, the availability of whole genome sequences from P. sojae, P. ramorum (Tyler et al. 2006) and P. infestans (Haas et al. 2009) enabled the identification of genetic markers useful for multi-locus phytogenies (Blair et al. 2008).

Cooke et al. (2000) developed the first molecular phylogeny for the genus by analyzing sequences of the internal transcribed spacer region (ITS) of 51 species. Kroon et al. (2004) constructed a phylogeny based on sequences of four nuclear and mitochondrial genes of 48 species, and Blair et al. (2008) produced a sophisticated phylogeny based on sequences of seven nuclear genetic markers. That multi-locus phylogeny divided 82 Phytophthora species into 10 phylogenetically well-supported clades. Martin et al. (2014) analyzed sequences of seven nuclear and four mitochondrial genes of 90 formally named and 17 provisional species and provided phylogenies including 10 clades, almost identical to that of Blair et al. (2008), except that P. quercina and P. sp. ohioensis were excluded from clade 4 and grouped into a potentially new clade.

A comprehensive molecular phylogeny is required to understanding the evolution of Phytophthora species. Although discordance has been found between the molecular phylogeny and the morphology-based taxonomy (Cooke et al. 2000, Ersek & Ribeiro 2010), correlations have been observed between molecular phylogenies and individual morphological and physiological traits. Recent studies indicated that species in individual clades or subclades are mostly identical in sporangial papillation, and optimum and maximum growth temperatures (Cooke et al. 2000, Kroon et al. 2012, Martin et al. 2012, Yang 2014). However, there was limited to no correlation between phylogeny and the morphology of sexual organs, such as antheridial configuration (Cooke et al. 2000, Kroon et al. 2012, Martin et al. 2012, Yang 2014). These studies have implied that divergence in sporangial morphology and variation in environmental specialization may be the keys in the evolutionary history of Phytophthora species. Nevertheless, these hypotheses need to be further tested and the exact evolutionary history of the genus Phytophthora warranted more investigation.

In this study, an expanded phylogeny, including more than 180 Phytophthora taxa, many not included in any previous phylogeny, was constructed. Sequences of seven nuclear genetic markers were used for construction of the phylogeny. In light of this phylogeny, ancestral state reconstructions were conducted on the sporangial papillation of Phytophthora species. Important evolutionary divergence events and associated changes in the sporangial morphology of Phytophthora species are discussed.

Materials and Methods

Isolate selection

A total of 376 Phytophthora isolates representing 142 described and 43 provisionally named species, plus one isolate of each Elongisporangium undulatum (basionym: Pythium undulatum), Halophytophthora fluviatilis, and Phytopythium vexans (basionym: Pythium vexans) as outgroup taxa were included (Table 1). These included 114 ex-types (Table 2). Also included were 164 authentic isolates that were designated as representative isolates by the originators of the respective species names (Table 1). The majority of these isolates were provided by the originators of the respective species, while the rest were purchased from the Westerdijk Fungal Biodiversity Institute (CBS), Utrecht, The Netherlands.
Table 1

Information regarding isolates used in this study. GenBank accession numbers are listed in Table S1.

   

Isolate identification d

 

Isolate origins

 

(Sub)clade a

Species b

Papilla c

CH

CBS

ATCC

IMI

WPC

MG

Type e

Host or Substrate

Location

Year

Reference

1a

P. cactorum

P

22E6

   

P10194

p25

 

Rhododendron sp.

Ohio, USA

n.a.f

(Schröter 1886)

   

22E7

 

16693

21168

P0715

p6

 

n.a.

UK

n.a.

 
   

22E8

 

16694, MYA-3653

50470

P10193

p7

 

Malus sp.

Zimbabwe

n.a.

 
 

P. hedraiandra

P

33F3

 

MYA-4165

  

p225

 

Rhododendron sp.

Minnesota, USA

2002

(de Cock & Lévesque 2004)

   

38C2

      

Irrigation water

Virginia, USA

2006

 
   

62A5

111725

  

P19523

 

T

Viburnum sp.

The Netherlands

2001

 
 

P. idaei

P

34D4

971.95

MYA-4065

313728

P6767

p220

T

Rubus idaeus

Scotland, UK

1987

(Kennedy & Duncan 1995)

   

62A1

968.95

    

A

Rubus idaeus

Scotland, UK

1985

 
 

P. pseudotsugae

P

  

52938

331662

P10339

 

T

Psendotsuga menziesii

Oregon, USA

n.a.

(Hamm & Hansen 1983)

 

P. aff. hedraiandra

P

33F4

    

p226

 

Rhododendron sp.

Minnesota, USA

2003

n.a.

 

P. aff. Dseudotsugae

P

29B3

    

p185

A

Psendotsuga menziesii

Oregon, USA

1975

n.a.

1b

P. clandestina

P

32G1

347.86

58713, 60438

278933

P3943

p200

T

Trifolium subterraneum

Australia

1985

(Taylor et al. 1985)

   

33D8

 

MYA-4064

287317

 

p215

A

Trifolium subterranea

Australia

1985

 
   

38D4

    

p304

 

n.a.

Australia

n.a.

 
 

P. iranica

P

61J4

374.72

60237

158964

P3882

p218

T

Solanum melongena

Iran

1969

(Ershad 1971)

 

P. tentaculata

P

29F2

552.96

  

P8497

 

A

Chrysanthemum leucanthemum

Germany

n.a.

(Kröber & Marwitz 1993)

   

30D5

      

Bacopa sp.

The Netherlands

2004

 
   

30G8

 

MYA-3655

    

Argyranthemum frutescens

Germany

2004

 

1c

P. andina

SP

60A2

    

p460

A

Solanum betaceum

Ecuador

n.a.

(Oliva et al. 2010)

   

60A3

    

p461

A

Solanum betaceum

Ecuador

n.a.

 
       

P13365

 

T

Solanum brevifolium

Ecuador

2001

 
 

P. infestans

SP

27A8

      

Solanum tuberosum

Mexico

1992

(De Bary 1876)

       

P10650

  

Solanum tuberosum

Mexico

n.a.

 
 

P. ipomoeae

SP

31B4

   

P10226

 

A

Ipomoea longipedunculata

Mexico

n.a.

(Flier et al. 2002)

   

31B5

109229

  

P10225

 

T

Ipomoea

Mexico

1999

 
   

31B6

   

P10227

 

A

Iongipedunculata Ipomoea

Mexico

n.a.

 
          

Iongipedunculata

   
 

P. mirabilis

SP

30C1

 

64069, MYA-4062

 

P3006

p145

A

Mirabilis jalapa

Mexico

n.a.

(Galindo-A & Hohl 1985)

   

30C2

 

64070, MYA-4063

 

P3007

p153

A

Mirabilis jalapa

Mexico

n.a.

 
 

P. phaseoli

SP

23B4

    

p106

 

Phaseolus lunatus

Delaware, USA

2000

(Thaxter 1889)

   

35B6

      

Phaseolus sp.

Delaware, USA

2000

 
       

P10145

  

Phaseolus lunatus

Delaware, USA

n.a.

 
       

P10150

  

Phaseolus lunatus

Delaware, USA

n.a.

 

1

P. nicotianae

P

22F9

 

15410, MYA-4037

  

p23

 

Nicotiana tabacum

North Carolina, USA

n.a.

(Breda de Haan 1896)

   

22G1

 

15409, MYA-4036

  

p22

 

Nicotiana tabacum

North Carolina, USA

n.a.

 
       

P10116

  

Metrosideros excelsa

California, USA

2002

 
       

P1452

  

Citrus sp.

California, USA

n.a.

 

2a

P. botryosa

P

22H8

 

MYA-4059

  

p44

 

Heavae sp.

Thailand

n.a.

(Chee 1969)

   

46C2

 

26481

  

p384

A

Hevea brasiliensis

Thailand

n.a.

 
   

62C6

581.69

 

136915

P3425

 

T

Hevea brasiliensis

Malaysia

1966

 
      

130422

P6945

  

Hevea brasiliensis

Malaysia

1986

 
 

P. citrophthora

P

03E5

    

p132

 

Irrigation water

Virginia, USA

2000

(Smith & Smith 1906)

   

26H3

    

p31

 

n.a.

n.a.

n.a.

 
 

P. colocasiae

SP

22F8

 

MYA-4159

  

p47

 

Colocasia esculenta

n.a.

1992

(Raciborski 1900)

   

35D3

    

p276

 

Colocasia esculenta

Hawaii, USA

2005

 
 

P. himalsilva

P

61G2

128767

    

T

Quercus leucotricophora

Nepal

2005

(Vettraino et al. 2011)

   

61G3

128753

    

A

Quercus

Nepal

2005

 
 

P. meadii

P

22G5

 

MYA-4043

  

p75

 

leucotricophora Citrus sp.

India

1992

(McRae 1918)

   

61J9

219.88

 

129185

   

Hevea brasiliensis

India

1987

 
 

P. occultans

SP

65B9

101557

    

T

Buxus sempervirens

The Netherlands

1998

(Man In’t Veld et al. 2015)

 

P. terminalis

SP

65B8

133865

    

T

Pachysandra terminalis

The Netherlands

2010

(Man In’t Veld et al. 2015)

 

P. aff. citrophthora

P

26H4

    

p32

A

n.a.

n.a.

n.a.

n.a.

      

342898

P10341

 

A

Syringa sp.

England, UK

1990

 
 

P. aff. himalsilva

P

61G4

128754

    

A

Castanopsis sp.

Nepal

2005

n.a.

 

P. sp. 46C3

n.a.

46C3

 

66767

 

P6713

p385

A

Hevea brasiliensis

Malaysia

n.a.

n.a.

 

P. sp. P6262

n.a.

    

P6262

 

A

Hevea brasiliensis

India

n.a.

n.a.

 

P. sp. P6310

n.a.

    

P6310

 

A

Theobroma cacao

Indonesia

n.a.

n.a.

2b

P. capsici

P

22F4

 

15399, MYA-4034

  

p8

A

Capsicum annum

New Mexico, USA

1948

(Leonian 1922)

    

121656

46012

 

P0253 P10386

  

Theobroma cacao Cucumis sativus

Mexico Michigan, USA

1964 1997

 
 

P. glovera

SP

31E5

    

p167

A

Nicotiana tabacum

Brazil

n.a.

(Abad et al. 2011)

   

62B4

121969

  

P11685

 

T

Nicotiana tabacum

Brazil

1995

 
 

P. mengei

SP

42B2

 

MYA-4554

  

p340

T

Persea americana

California, USA

n.a.

(Hong et al. 2009)

   

42B3

 

MYA-4555

  

p341

A

Persea americana

California, USA

n.a.

 
 

P. mexicana

P

45G4

554.88

46731

92550

P0646

p355

 

Solanum lycopersicum

Argentina

n.a.

(Hotson & Hartge 1923)

 

P. siskiyouensis

SP

41B7

122779

MYA-4187

 

P15122

 

T

Stream water

Oregon, USA

2003

(Reeser et al. 2007)

   

41B8

     

A

Soil

Oregon, USA

2003

 
 

P. tropicalis

P

22H5

    

p27

 

Vanila sp.

Tahiti

n.a.

(Aragaki & Uchida 2001)

   

35C8

434.91

76651, MYA-4218

  

p272

T

Macadamia integrifolia

Hawaii, USA

n.a.

 
 

P. aff. capsici

P

22F5

 

15427, MYA-4035

  

p9

 

Nicotiana tabacum

North Carolina, USA

n.a.

n.a.

 

P. sp. brasiliensis

n.a.

  

46705

 

P0630

 

A

Theobroma cacao

Brazil

1969

(Oudemans & Coffey 1991)

2c

P. acerina

SP

61H1

133931

    

T

Acer pseudoplatanus

Italy

2010

(Ginetti et al. 2014)

   

61H2

     

A

Soil

Italy

2010

 
 

P. capensis

SP

62C1

128319

  

P1819

 

T

Curtisia dentata

South Africa

n.a.

(Bezuidenhout et al. 2010)

   

62C2

128320

  

P1822

 

A

Stream water

South Africa

n.a.

 
   

62C3

128321

  

P1823

 

A

Olea campensis

South Africa

1986

 
 

P. citricola

SP

33H8

221.88

60440

21173

P0716

p396

T

Citrus sinensis

Taiwan

1987

(Sawada 1927)

   

33J2

295.29

   

p375

A

Citrus sp.

Japan

1929

 
 

P. multivora

SP

55C5

124094

    

T

Soil

Western Australia, Australia

2007

(Scott et al. 2009)

 

P. pachypleura

SP

61H6

     

A

Soil

UK

2006

(Henricot et al. 2014)

   

61H7

  

502404

  

T

Acuba japonica

UK

2008

 
   

61H8

     

A

Soil

UK

2009

 
 

P. pini

SP

22F1

 

MYA-3656

  

p53

A

Rhododendron sp.

West Virginia, USA

1987

(Hong et al. 2011)

   

45F1

 

64532

  

p343

T

Pinus resinosa

Minnesota, USA

1925

 
 

P. plurivora

SP

22E9

 

MYA-3657

  

p101

 

Kalmia latifolia

Western Australia, Australia

1998

(Jung & Burgess 2009)

   

22F2

    

p52

 

Rhododendron sp. cv. “Olga Mezitt”

New York, USA

n.a.

 
   

33H9

379.61

     

Rhododendron sp.

Germany

1958

 
 

P. sp. 22F3

SP

22F3

    

p33

A

n.a.

Ohio, USA

n.a.

n.a.

 

P. sp. 28D1

SP

28D1

    

p119

A

Fagus sylvatica

New York, USA

n.a.

n.a.

   

28D3

    

p121

A

Fagus sylvatica

New York, USA

n.a.

 
 

P. sp. citricola VIII

SP

27D9

     

A

Unidentified leaf

Hainan, China

n.a.

n.a.

 

P. sp. pini-like

SP

56G1

     

A

Taxus sp.

Pennsylvania, USA

2011

n.a.

 

P. taxon emzansi

SP

61F2

     

A

Agathosma betulina

South Africa

2005

(Bezuidenhout et al. 2010)

   

61F3

     

A

Agathosma betulina

South Africa

2005

 

2d

P. bisheria

SP

29D2

      

Rubus idaeus cv. Canby

Wisconsin, USA

1989

(Abad et al. 2008)

   

31E6

122081

  

P10117

 

T

Fragaria ×ananassa

North Carolina, USA

1999

 
       

P1620

  

Rhododendron sp.

North Carolina, USA

n.a.

 
 

P. elongata

SP

33J3

     

A

n.a.

Australia

1995

(Rea et al. 2010)

   

33J4

     

A

n.a.

Australia

1995

 
   

55C4

125799

    

T

Soil

Western Australia, Australia

2004

 
 

P. frigida

P

47G6

     

A

Eucalyptus smithi

South Africa

n.a.

(Maseko et al. 2007)

   

47G7

     

A

Eucalyptus smithi

South Africa

n.a.

 
   

47G8

     

T

Eucalyptus smithi

South Africa

2001

 

2e

P. multivesiculata

SP to NP

29E3

545.96

  

P10410

 

T

Cymbidium sp.

The Netherlands

n.a.

(Ilieva et al. 1998)

   

30D4

     

A

Cymbidium sp.

The Netherlands

n.a.

 
 

P. taxon aquatilis

SP

38J5

 

MYA-4577

   

A

Stream water

Virginia, USA

2006

(Hong et al. 2012)

3

P. ilicis

SP

23A7

 

56615, MYA-3897

 

P3939

p113

 

Ilex sp.

Canada

n.a.

(Buddenhagen & Young 1957)

   

34D6

      

Quercus sp.

Germany

1999

 
   

62A7

114348

    

T

Ilex aquifolium

The Netherlands

n.a.

 
 

P. nemorosa

SP

28J3

 

MYA-4061

  

p141

 

Umbellularia californica

California, USA

n.a.

(Hansen et al. 2003)

   

41C4

 

MYA-2948

  

p320

T

Lithocarpus densiflorus

California, USA

n.a.

 
 

P. pluvialis

SP

60B3

 

MYA-4930

   

T

Rainwater

Oregon, USA

2008

(Reeser et al. 2013)

 

P. pseudosyringae

SP

30A8

111772

MYA-4222

  

p284

T

Quercus robur

Germany

1997

(Jung et al. 2003)

   

30B1

    

Pp285

A

Quercus robur

Germany

1997

 
 

P. psychrophila

SP

29J5

803.95

    

T

Quercus robur

Germany

1995

(Jung et al. 2002)

   

29J6

 

MYA-4083

  

p288

A

Quercus ilex

France

1996

 

4

P. alticola

P

47G5

121939

  

P16948

 

A

Eucalyptus dunnii

South Africa

n.a.

(Maseko et al. 2007)

 

P. arenaria

P

55C2

127950

    

T

Soil

Western Australia, Australia

2009

(Rea et al. 2011)

   

62B7

125800

    

A

Soil

Western Australia, Australia

2009

 
 

P. megakarya

P

22H7

 

MYA-4040

  

p42

 

Theobroma cacao

Africa

n.a.

(Brasier & Griffin 1979)

   

61J5

238.83

42100

202077

  

T

Theobroma cacao

Cameroon

n.a.

 
   

61J6

239.83

42099

106327

  

A

Theobroma cacao

Nigeria

n.a.

 
 

P. palmivora

P

22G8

 

MYA-4039

 

P10213

p65

 

Citrus sp.

Florida, USA

n.a.

(Butler 1910)

   

22G9

 

MYA-4038

  

p26

 

Theobroma cacao

Costa Rica

n.a.

 
 

P. quercetorum

P

15C7

      

Soil

South Carolina, USA

1997

(Balci et al. 2008)

   

15C8

      

Soil

South Carolina, USA

1997

 
 

P. quercina

P

30A4

783.95

    

A

Quercus robur

Germany

1995

(Jung et al. 1999)

   

30A5

784.95

MYA-4084

   

T

Quercus robur

Germany

1995

 
   

30A7

      

Quercus sp.

Serbia

2003

 
 

P. sp. ohioensis

n.a.

    

P16050

 

A

Soil

Ohio, USA

2006

n.a.

5

P. agathidicida

P

67D5

     

T

Agathis australis

New Zealand

2006

(Weir et al. 2015)

 

P. castaneae

P

22H6

 

MYA-4060

  

p45

 

Castanea sp.

Japan

n.a.

(Katsura 1976)

   

30E7

      

Soil

Hainan, China

n.a.

 
   

61J7

587.85

36818

325914

  

T

Soil

Taiwan

n.a.

 
 

P. cocois

P

67D6

     

T

Cocos nucifera

Hawaii, USA

1990

(Weir et al. 2015)

 

P. heveae

P

22J1

  

180616

 

p28

T

Heavae sp.

Malaysia

n.a.

(Thompson 1929)

   

22J2

 

16701, MYA-3895

  

p17

 

soil

Tennessee, USA

1964

 

6a

P. gemini

NP

46H1

123382

    

A

Zostera marina

The Netherlands

1999

(Man in’t Veld et al. 2011)

   

46H2

123383

    

A

Zostera marina

The Netherlands

1999

 
 

P. humicola

NP

32F8

200.81

52179, MYA-4080

 

P3826

p198

T

Soil

Taiwan

1976

(Ko & Ann 1985)

   

32F9

   

P6702

p199

A

Phaseolus vulgaris

Taiwan

n.a.

 
 

P. inundata

NP

30J3

  

390121

 

p291

T

Olea sp.

Spain

1996

(Brasier et al. 2003b)

   

30J4

  

389751

 

p298

T

Salix matsudana

UK

1972

 
       

P8619

  

Pistacia vera

Iran

n.a.

 
 

P. rosacearum

NP

22J9

 

MYA-3662

  

p82

A

Prunus sp.

California, USA

1987

(Hansen et al. 2009)

   

41C1

    

p321

A

Prunus sp.

California, USA

n.a.

 
   

47J1

 

MYA-4456

   

T

Malus domestica

California, USA

n.a.

 
 

P. sp. 48H2

NP

48H2

     

A

Stream water

Virginia, USA

2008

n.a.

 

P. sp. 62C9

NP

62C9

     

A

Stream water

Taiwan

2013

n.a.

 

P. sp. personii

n.a.

    

P11555

 

A

Nicotiana tabacum

North Carolina, USA

n.a.

n.a.

 

P. taxon walnut

NP

40A7

     

A

Irrigation water

Virginia, USA

2006

(Brasier et al. 2003a)

   

43G1

     

A

Irrigation water

Virginia, USA

2007

 

6b

P. amnicola

NP

61G6

131652

    

T

Stream water

Western Australia, Australia

2009

(Crous et al. 2012)

   

62C5

133867

     

Pachysandra sp.

The Netherlands

n.a.

]

 

P. bilorbang

NP

61G8

131653

    

T

Soil

Western Australia, Australia

2010

(Aghighi et al. 2012)

 

P. borealis

NP

60B2

132023

MYA-4881

   

T

Stream water

Alaska, USA

2008

(Hansen et al. 2012)

 

P. crassamura

NP

66C9

     

A

Picea abies

Italy

2012

(Scanu et al. 2015)

   

66D1

140357

    

T

Soil

Italy

2011

 
 

P. fluvialis

NP

55B6

129424

    

T

Stream water

Western Australia, Australia

2009

(Crous et al. 2011)

 

P. gibbosa

NP to SP

55B7

     

A

Soil

Western Australia, Australia

2009

(Jung et al. 2011)

   

62B8

127951

    

T

Soil

Western Australia, Australia

2009

 
 

P. gonapodyides

NP

21J5

 

46726

  

p117

 

Water

England, UK

n.a.

(Buisman 1927, Petersen 1910)

   

34A8

554.67

60351

 

P6872

  

Reservoir water

n.a.

1967

 
 

P. gregata

NP

55B8

     

A

Soil

Western Australia, Australia

2009

(Jung et al. 2011)

   

62B9

127952

    

T

Soil

Western Australia, Australia

2009

 
 

P. lacustris

NP

61D6

     

A

Soil

Germany

2003

(Nechwatal et al. 2013)

   

61D8

     

A

Soil

Germany

2003

 
  

NP

61E1

     

A

Soil

Germany

2006

 
      

389725

P10337

 

T

Salix matsudana

England, UK

1972

 
 

P. litoralis

NP

55B9

127953

    

T

Soil

Western Australia, Australia

2008

(Jung et al. 2011)

 

P. megasperma

NP

62C7

402.72

58817

32035

P3599

 

T

Althaea rosea

Washington DC, USA

1931

(Drechsler 1931)

 

P. mississippiae

NP to SP

57J1

     

A

Irrigation water

Mississippi, USA

2012

(Yang et al. 2013)

   

57J2

     

A

Irrigation water

Mississippi, USA

2012

 
   

57J3

 

MYA-4946

   

T

Irrigation water

Mississippi, USA

2012

 
   

57J4

     

A

Irrigation water

Mississippi, USA

2012

 
 

P. ornamentata

NP

66D2

140647

    

T

Soil

Italy

2012

(Scanu et al. 2015)

   

66D3

     

A

Soil

Italy

2012

 
 

P. pinifolia

NP

47H1

122924

    

T

Pinus radiata

Chile

2007

(Duran et al. 2008)

   

47H2

122922

    

A

Pinus radiata

Chile

2007

 
 

P. riparia

NP

60B1

132024

MYA-4882

   

T

Stream water

Oregon, USA

2006

(Hansen et al. 2012)

 

P. thermophila

NP

55C1

127954

    

T

Soil

Western Australia, Australia

2004

(Jung et al. 2011)

 

P. ×stagnum

NP

36H8

     

A

Irrigation water

Virginia, USA

2006

(Yang et al. 2014c)

   

36J7

     

A

Irrigation water

Virginia, USA

2006

 
   

43F3

 

MYA-4926

   

T

Irrigation water

Virginia, USA

2007

 
   

44F9

     

A

Irrigation water

Virginia, USA

2007

 
 

P. sp. 26E1

NP

26E1

    

p116

A

Malus domestica

New York, USA

n.a.

n.a.

 

P. sp. canalensis

n.a.

    

P10456

 

A

Canal water

California, USA

2002

n.a.

 

P. sp. delaware

NP

63H4

     

A

Pond water

Delaware, USA

2014

n.a.

   

63H7

     

A

Pond water

Delaware, USA

2014

 
 

P. sp. gregata-like

NP

22J5

 

16698

  

p16

A

n.a.

n.a.

n.a.

n.a.

 

P. sp. megasperma-like

NP

23A1

    

p81

A

Prunus sp.

California, USA

n.a.

n.a.

   

23A3

 

MYA-3660

  

p79

A

Actinidia chinensis

California, USA

1987

 

6

P. asparagi

NP

33D7

  

384046

  

A

Asparagus officinalis

New Zealand

1980

(Crous et al. 2012)

   

62C4

132095

MYA-4826

   

T

Asparagus officinalis

Michigan, USA

2006

 
 

P. sp. sulawesiensis

n.a.

    

P6306

 

A

Syzygium aromaticum

Indonesia

1989

n.a.

7a

P. attenuata

NP

67C5

     

T

Soil

Taiwan

2013

(Jung et al. 2017)

 

P. europaea

NP

30A3

      

Quercus sp.

France

1998

(Jung et al. 2002)

   

34C2

      

Quercus sp.

Germany

1999

 
   

62A2

109049

    

T

Soil

France

1998

 
 

P. flexuosa

NP

67C3

     

T

Soil

Taiwan

2013

(Jung et al. 2017)

 

P. formosa

NP

67C4

     

T

Soil

Taiwan

2013

(Jung et al. 2017)

 

P. fragariae

NP

22G6

 

11374

 

P3570

p114

 

Fragaria ×ananassa

Maryland, USA

n.a.

(Hickman 1940)

   

30C5

      

Fragaria ×ananassa

Virginia, USA

n.a.

 
   

61J3

209.46

 

181417

P6231

 

T

Fragaria ×ananassa

England, UK

n.a.

 
 

P. intricata

NP

67B9

     

T

Soil

Taiwan

2013

(Jung et al. 2017)

 

P. rubi

NP

30D7

    

p186

A

Rubus sp.

Australia

n.a.

(Man in ‘t Veld 2007)

   

41D5

      

Rubus sp.

Norway

2005

 
   

46C7

 

90442

  

p389

T

Rubus idaeus cv. “Glen Clova”

Scotland, UK

n.a.

 
 

P. uliginosa

NP

62A3

109054

  

P10413

 

T

Soil

Poland

1998

(Jung et al. 2002)

   

62A4

109055

  

P10328

 

A

Soil

Germany

1998

 
 

P. ×alni

NP

32J6

392317

MYA-4081

  

p205

A

Alnus glutinosa

France

1996

(Brasier et al. 2004, Husson et al. 2015)

   

32J7

392318

   

p206

A

Alnus sp.

Austria

1996

 
   

47A7

  

392314

  

T

Alnus sp.

UK

1994

 
   

47A8

     

A

Alnus sp.

The Netherlands

n.a.

 
 

P. ×cambivora

NP

22F6

 

46719, MYA-4076

  

p64

 

Abies sp.

Oregon, USA

n.a.

(Buisman 1927, Jung et al. 2017)

   

26F8

 

MYA-4075

  

p38

 

n.a.

New York, USA

n.a.

 
 

P. ×heterohybrida

NP

67C1

     

T

Stream water

Taiwan

2013

(Jung et al. 2017)

 

P. ×incrassata

NP

67C2

     

T

Stream water

Taiwan

2013

(Jung et al. 2017)

 

P. sp. europaea SW

NP

33F7

    

p229

A

Soil

West Virginia, USA

2005

n.a.

7b

P. asiatica

NP

45G1

 

90455

  

p352

A

Robinia pseudoacacia

Jiangsu, China

n.a.

(Rahman et al. 2014a)

   

46C6

 

56194

  

p388

A

Robinia pseudoacacia

Jiangsu, China

n.a.

 
   

61H3

133347

    

T

Pueraria lobata

Japan

2005

 
 

P. cajani

NP

33D9

    

p214

 

Cajanus cajani

India

n.a.

(Amin et al. 1978)

   

45F6

 

44389

  

p348

A

Cajanus cajani

India

n.a.

 
   

45F7

 

44388

 

P3105

p349

T

Cajanus cajani

India

n.a.

 
 

P. melonis

NP

32F6

 

MYA-4079

 

P1371

p196

A

Cucumis sativus

China

n.a.

(Katsura 1976)

   

41B4

    

p318

A

Cucumis sativus

Iran

n.a.

 
   

45F3

582.69

52854

   

T

Cucumis sativus

Japan

n.a.

 
 

P. niederhauserii

NP

01D5

    

p312

A

Irrigation water

Virginia, USA

2000

(Abad et al. 2014)

   

23J6

 

MYA-4163

  

p57

A

Unknown ornamental

Israel

n.a.

 
   

31E7

   

P10617

p169

A

Thuja occidentalis

North Carolina, USA

2001

 
 

P. pisi

NP

60A4

     

T

Pea

Sweden

2009

(Heyman et al. 2013)

   

60A5

     

A

Pea

Sweden

2009

 
 

P. pistaciae

NP

33D6

 

MYA-4082

386658

 

p216

T

Pistacia vera

Iran

1986

(Mirabolfathy et al. 2001)

   

41A9

    

p314

A

Pistacia vera

Iran

n.a.

 
 

P. sojae

NP

22D8

312.62

16705, MYA-3899

131375

 

p19

 

Glycine max

Ontario, Canada

1959

(Kaufmann & Gerdemann 1958)

   

28F9

    

p236

 

Glycine max

Mississippi, USA

1970

 
 

P. vignae

NP

45G6

 

46735

  

p357

A

Glycine max

n.a.

n.a.

(Purss 1957)

   

45G9

 

64832

316196

P3420

p379

 

Vigna unguiculata

Sri Lanka

n.a.

 
   

46C1

112.76

64129

  

p380

 

Vigna sinensis

n.a.

n.a.

 

7c

P. cinnamomi

NP

23B1

 

15400, MYA-4057

  

p10

 

Camellia japonica

South Carolina, USA

n.a.

(Rands 1922)

   

23B2

 

15401, MYA-4058

  

p11

 

Persea americana

Puerto Rico

1960

 
   

61J1

144.22

46671

22938

P2110

 

T

Cinnamomum burmannii

Indonesia

1922

 
 

P. parvispora

NP

30G9

 

MYA-4078

  

p178

A

Beaucarnea sp.

Germany

1991

(Scanu et al. 2014)

   

46F6

     

A

Beaucarnea sp.

Germany

1992

 
   

66C7

132771

    

A

Arbutus unedo

Italy

2008

 
   

66C8

132772

    

T

Arbutus unedo

Italy

2011

 
 

P. sp. ax

NP

46H5

     

A

Ilex glabra cv. “Shamrock”

Virginia, USA

2008

n.a.

7d

P. fragariaefolia

NP

61H4

135747

    

T

Fragaria ×ananassa

Japan

2005

(Rahman et al. 2014b)

 

P. nagaii

NP

61H5

133248

    

T

Rosa sp.

Japan

1968

(Rahman et al. 2014b)

8a

P. cryptogea

NP

61H9

113.19

 

180615

P1738

 

T

Solanum lycopersicum

Ireland

n.a.

(Pethybridge & Lafferty 1919)

 

P. drechsleri

NP

15E5

      

Soil

South Carolina, USA

1997

(Tucker 1931)

   

15E6

      

Soil

South Carolina, USA

1998

 
   

23J5

292.35

46724

 

P1087

p41

T

Beta vulgaris var. altissima

California, USA

n.a.

 
       

P10331

  

Gerbera jamesonii

New Hampshire, USA

2003

 
 

P. erythroseptica

NP

61J2

129.23

 

34684

P1693

 

T

Solanum tuberosum

Ireland

n.a.

(Pethybridge 1913)

 

P. medicaginis

NP

23A4

 

MYA-3900

  

p37

 

Medicago sativa

Ohio, USA

n.a.

(Hansen & Maxwell 1991)

   

28F1

 

44390

 

P1057

p124

 

Medicago sativa

California, USA

1975

 
 

P. pseudocryptogea

NP

  

52402

 

P3103

  

Solanum marginatum

Ecuador

n.a.

(Safaiefarahani et al. 2015)

 

P. richardiae

NP

31E8

   

P10355

p170

 

Zantedeschia sp.

Japan

1989

(Buisman 1927)

   

45 F5

240.30

60353, 46734

325930

 

p347

T

Zantedeschia aethiopica

USA

n.a.

 
       

P10811

  

Zantedeschia aethiopica

Japan

1989

 
 

P. sansomeana

NP

47H3

 

MYA-4455

   

T

Glycine sp.

Indiana, USA

n.a.

(Hansen et al. 2009)

   

47H4

     

A

Glycine sp.

Indiana, USA

n.a.

 
   

47H5

     

A

Glycine sp.

Indiana, USA

n.a.

 
 

P. trifolii

NP

29B2

 

MYA-3901

  

p142

A

Trifolium vesiculosum

Mississippi, USA

1978

(Hansen & Maxwell 1991)

   

62A9

117687

    

T

Trifolium sp.

Mississippi, USA

n.a.

 
 

P. aff. cryptogea

NP

22G2

308.62

15402, MYA-4161

325907

 

p12

 

Aster sp.

California, USA

n.a.

n.a.

 

P. aff. erythroseptica

NP

22J4

 

MYA-4041

  

p50

 

n.a.

Ohio, USA

n.a.

n.a.

   

33A1

    

p207

 

Solanum tuberosum

Maine, USA

2004

 
 

P. sp. kelmania

NP

24A7

 

MYA-4162

  

p102

A

Abies concolor

West Virginia, USA

1998

n.a.

   

31E4

   

P10613

p166

A

Abes fraseri

North Carolina, USA

2002

 

8b

P. brassicae

SP

29D8

686.95

    

A

Brassica oleracea

The Netherlands

1995

(Man in’t Veld et al. 2002)

   

61J8

179.87

  

P7517, P19521

 

T

Brassica oleracea

The Netherlands

1986

 
 

P. cichorii

SP

62A8

115029

    

T

Cichorium intybus var. foliosum

The Netherlands

2004

(Bertier et al. 2013)

 

P. dauci

SP

61E5

127102

    

T

Daucus carota

France

2009

(Bertier et al. 2013)

   

32E5

      

Duscus carota

France

2004

 
   

32E6

   

P10728

  

Duscus carota

France

2004

 
   

32E7

    

p194

 

Duscus carota

France

2004

 
 

P. lactucae

SP

61F4

     

T

Lactuca sativa

Greece

2001

(Bertier et al. 2013)

   

61F7

     

A

Lactuca sativa

Greece

2002

 
   

61F8

     

A

Lactuca sativa

Greece

2003

 
 

P. primulae

SP

29E9

620.97

   

p286

 

Primula acaulis

Germany

1997

(Tomlinson 1952)

   

29F1

    

p287

 

Primula sp.

The Netherlands

1998

 
 

P. aff. brassicae-2

n.a.

 

112968

  

P6207

 

A

Allium cepa

Switzerland

n.a.

n.a.

 

P. aff. cichorii

SP

61E3

133815

    

A

Cichorium intybus var. foliosum

UK

1999

n.a.

 

P. sp. 29E7

SP

29E7

     

A

Allium porrum

The Netherlands

n.a.

n.a.

 

P. taxon castitis

SP

61E7

131246

    

A

Fragaria ×ananassa

Sweden

1995

(Bertier et al. 2013)

 

P. taxon parsley

SP

61G1

     

A

Petroselinum crispum

Greece

2006

(Bertier et al. 2013)

8c

P. foliorum

SP

49J8

121655

MYA-3638

 

P10974

 

T

Rhododendron sp.

Tennessee, USA

2004

(Donahoo et al. 2006)

 

P. hibernalis

SP

22H1

270.31

60352

36906

P6871

p115

 

Citrus sinensis

Portugal

1931

(Carne 1925)

   

32F7

114104

56353, MYA-3896

134760

P3822

p197

 

Citrus sinensis

Western Australia, Australia

1958

 
 

P. lateralis

NP to SP

22H9

 

MYA-3898

  

p51

A

Chamaecyparis lawsoniana

Oregon, USA

n.a.

(Tucker & Milbrath 1942)

   

29A9

 

201856

  

p128

 

Chamaecyparis lawsoniana

California, USA

1997

 
 

P. ramorum

SP

32G2

      

Camellia japonica

South Carolina, USA

n.a.

(Werres et al. 2001)

   

33F2

     

Quercus agrifolia

California, USA

n.a.

  

8d

P. austrocedrae

SP

41B5

 

MYA-4073

  

A

Austrocedrus chilensis

Argentina

n.a.

(Greslebin et al. 2007)

 
   

41B6

122911

MYA-4074

  

T

Austrocedrus chilensis

Argentina

2005

  
 

P. obscura

SP

60E9

129273

   

T

Soil

Germany

1994

(Grünwald et al. 2012)

 
   

60F1

    

A

Pieris sp.

Oregon, USA

2009

  
   

60F2

    

A

Kalmia latifolia

Oregon, USA

n.a.

  
 

P. syringae

SP

21H9

 

34002

P0649

p187

 

Citrus sp.

California, USA

n.a.

(Klebahn 1905)

 
   

23A6

 

MYA-3659

 

p35

 

n.a.

New York, USA

n.a.

  

8

P. stricta

NP

58A1

 

MYA-4944

  

T

Irrigation water

Mississippi, USA

2012

(Yang et al. 2014a)

 
   

58A2

    

A

Irrigation water

Mississippi, USA

2012

  
   

58A3

    

A

Irrigation water

Mississippi, USA

2012

  
   

58A4

    

A

Irrigation water

Mississippi, USA

2012

  

9a (cluster 9a1)

P. aquimorbida

NP

40A6

 

MYA-4578

  

T

Irrigation water

Virginia, USA

2006

(Hong et al. 2012)

 
   

40E3

    

A

Irrigation water

Virginia, USA

2006

  
   

44G9

    

A

Irrigation water

Virginia, USA

2007

  
 

P. Chrysanthemi

NP

61E9

    

A

Chrysanthemum sp.

Japan

1998

(Naher et al. 2011)

 
   

61F1

123163

   

T

Chrysanthemum ×morifolium

Japan

2000

  
 

P. hydrogena

NP

44G8

    

A

Irrigation water

Virginia, USA

2007

(Yang et al. 2014b)

 
   

46A3

 

MYA-4919

  

T

Irrigation water

Virginia, USA

2007

  
   

46A4

    

A

Irrigation water

Virginia, USA

2007

  
 

P. hydropathica

NP

05D1

 

MYA-4460

 

p366

T

Irrigation water

Virginia, USA

2000

(Hong et al. 2010)

 
   

5C11

 

MYA-4459

 

p365

A

Irrigation water

Virginia, USA

2000

  
 

P. irrigata

NP

04E4

 

MYA-4458

 

p335

A

Irrigation water

Virginia, USA

2000

(Hong et al. 2008)

 
   

23J7

 

MYA-4457

 

p108

T

Irrigation water

Virginia, USA

2000

  
   

44E4

    

A

Stream water

Virginia, USA

2007

  
 

P. macilentosa

NP

58A5

    

A

Irrigation water

Mississippi, USA

2012

(Yang et al. 2014a)

 
   

58A6

    

A

Irrigation water

Mississippi, USA

2012

  
   

58A7

 

MYA-4945

  

T

Irrigation water

Mississippi, USA

2012

  
   

58A8

    

A

Irrigation water

Mississippi, USA

2012

  
 

P. parsiana

NP

47C3

  

395329

 

T

Ficus carica

Iran

1991

(Mostowfizadeh-Ghalamfarsa et al. 2008)

 
 

P. virginiana

NP

40A9

     

A

Irrigation water

Virginia, USA

2006

(Yang & Hong 2013)

   

44G6

     

A

Irrigation water

Virginia, USA

2007

 
   

46A2

 

MYA-4927

   

T

Irrigation water

Virginia, USA

2007

 
 

P. aff. parsiana G1

NP

47C7

     

A

Pistacia vera

Iran

n.a.

n.a.

   

47C8

     

A

Pistacia vera

Iran

n.a.

 
      

395328

P8618

 

A

Pistacia vera

Iran

1992

 
 

P. aff. parsiana G2

NP

47C5

  

395330

  

A

Pistacia vera

Iran

1992

n.a.

   

47C6

  

395331

  

A

Pistacia vera

Iran

1992

 
 

P. aff. parsiana G3

NP

47D5

     

A

Pistacia vera

Iran

n.a.

n.a.

   

47D8

     

A

Pistacia vera

Iran

n.a.

 
   

47E1

     

A

Pistacia vera

Iran

n.a.

 
 

P. sp. 35G4

NP

35G4

     

A

Irrigation water

Virginia, USA

2005

n.a.

 

P. sp. 38D9

NP

38D9

     

A

Dianthus caryophyllus

Taiwan

n.a.

n.a.

 

P. sp. 40J5

NP

40J5

     

A

Unknown leaf in seawater

Hainan, China

n.a.

n.a.

 

P. sp. cuyabensis

n.a.

    

P8213

 

A

n.a.

Ecuador

1993

n.a.

 

P. sp. lagoariana

NP

60B4

   

P8220

 

A

n.a.

Ecuador

n.a.

n.a.

   

60B5

   

P8217

 

T

n.a.

Ecuador

n.a.

 
       

P8223

 

A

n.a.

Ecuador

1993

 

9a (cluster 9a2)

P. macrochlamvdospora-G1

SP

33E1

   

P10264

  

Glycine max

New South Wales, Australia

n.a.

(Irwin 1991)

       

P10267

  

Glycine max

New South Wales, Australia

1994

 
 

P. macrochlamvdospora -G2

SP

31E9

  

351473

P8017

p171

 

Glycine max

Queensland, Australia

n.a.

(Irwin 1991)

   

33D5

240.30

60353

340618

   

Zantedeschia aethiopica

The Netherlands

1927

 
 

P. quininea

NP

45F2

406.48

56964

  

p344

A

Cinchona officinalis

Peru

n.a.

(Crandall 1947)

   

46C4

407.48

46733

  

p386

T

Cinchona officinalis

Peru

n.a.

 

9a (cluster 9a3)

P. insolita

NP

327E1

 

MYA-4077

  

p123

 

Waterfall water

Hainan, China

n.a.

(Ann & Ko 1980)

   

38E1

691.79

38789

288805

  

T

Soil

Taiwan

1980

 
       

P6703

 

A

Soil

Taiwan

n.a.

 
 

P. polonica

NP

40G9

      

Irrigation water

Virginia, USA

2006

(Belbahri et al. 2006)

   

43F9

      

Irrigation water

Virginia, USA

2007

 
   

49J9

   

P15005

 

A

Soil

Poland

2006

 

9b

P. captiosa

NP

46H6

     

A

Eucalyptus saligna

New Zealand

1999

(Dick et al. 2006)

   

46H7

   

P10719

 

T

Eucalyptus saligna

New Zealand

1992

 
   

46H8

     

A

Eucalyptus saligna

New Zealand

2000

 
       

P10721

 

A

Eucalyptus saligna

New Zealand

1998

 
 

P. constricta

NP to SP

55C3

125801

    

T

Soil

Western Australia, Australia

2006

(Rea et al. 2011)

 

P. fallax

NP

46J2

   

P10722

 

T

Eucalyptus delegatensis

New Zealand

1997

(Dick et al. 2006)

   

46J3

     

A

Eucalyptus nitens

New Zealand

2000

 
   

46J5

     

A

Eucalyptus nitens

New Zealand

2000

 
       

P10725

 

A

Eucalyptus fastigata

New Zealand

2004

 

10

P. boehmeriae

P

45F9

291.29

 

180614

P6950

 

T

Boehmeriae nivea

Taiwan

1927

(Sawada 1927)

 

P. gallica

NP

50A1

111474

  

P16826

 

T

Quercus robur

France

1998

(Jung & Nechwatal 2008)

   

61D5

111475

  

P16827

 

A

Phragmites australis

Germany

2004

 
 

P. gondwanensis

P

22G7

 

MYA-3893

    

n.a.

Ohio, USA

n.a.

(Crous et al. 2015)

 

P. intercalaris

NP

45B7

140632

TSD-7

   

T

Stream water

Virginia, USA

2007

(Yang et al. 2016)

   

48A1

     

A

Stream water

Virginia, USA

2008

 
   

49A7

140631

    

A

Stream water

Virginia, USA

2009

 
 

P. kernoviae

P

46C8

   

P10956

p390

 

Rhododendron ponticum

England, UK

2004

(Brasier et al. 2005)

   

46J6

   

P10681

  

Annona cherimola

New Zealand

2002

 
   

46J8

   

P10671

  

Soil

New Zealand

2003

 
 

P. morindae

P

62B5

121982

    

T

Morinda citrifolia var. citrifolia

Hawaii, USA

2005

(Nelson & Abad 2010)

 

P. sp. boehmeriae-like

P

45F8

357.52

60173

32199

P1378

p350

A

Citrus sinensis

Argentina

1939

n.a.

n.a.

P. Iilii

NP

 

135746

    

T

Lilium sp.

Japan

1987

(Rahman et al. 2015)

outgroup

Elongisporangium undulatum

P

 

101728

 

337230

P10342

 

T

Larix sp.

Scotland, UK

1989

(Uzuhashi et al. 2010)

 

Phytopythium vexans

P

 

340.49

12194

 

P3980

 

T

n.a.

n.a.

n.a.

(de Cock et al. 2015)

 

Halophytophthora fluviatilis

P

57A9

 

MYA-4961

   

T

Stream water

Virginia, USA

2011

(Yang & Hong 2014)

a Molecular (sub)clade as designated in Fig. 1

b Names of taxa informally designated for the first time in this study are underlined.

c Sporangial papillation: NP = non-papillate, P = papillate, and SP = semi-papillate.

d Isolate identification abbreviations: CH, Chuanxue Hong laboratory at Virginia Polytechnic Institute and State University, Virginia Beach, VA, USA; CBS, Westerdijk Fungal Biodiversity Institute, Utrecht, The Netherlands; ATCC, American Type Culture Collection, Manassas, VA, USA; IMI, CABI Biosciences, UK; WPC, the World Phytophthora Genetic Resource Collection at University of California, Riverside, USA; MG, Mannon E. Gallegly laboratory at West Virginia University, USA. Local identifications of respective isolates are provided in Table S1.

e Ex-types (T) or authentic (A) isolates (designated as representative isolates by the originators of the respective species).

f n.a.= not available.

Fig. 1
Fig. 1

A 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 25, 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.

Fig. 2
Fig. 2

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.

Fig. 3
Fig. 3

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.

Fig. 4
Fig. 4

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.

Fig. 5
Fig. 5

Structure 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.

Table 2

Numbers of species and ex-types included in phylogenies for the genus Phytophthora in previous studies and this study.

 

Number of species

 

Phylogeny in

Formal

Provisional

Number of ex-types

Cooke et al. (2000)

49

2

9

Kroon et al. (2004)

46

2

18

Blair et al. (2008)

72

10

16

Martin et al. (2014)

90

17

31

This study

142

43

114

DNA extraction

To extract genomic DNA (gDNA), an approximately 5 × 5 mm culture plug of each isolate was taken from the actively growing area of a fresh culture. This was then grown in 20 % clarified V8 broth (lima bean broth for growing a P. infestans isolate 27A8) at room temperature (ca. 23 °C) for 7–14 d to produce a mycelial mass. The mass was then blot-dried using sterile tissue paper and then lysed in liquid nitrogen or using a FastPrep®-24 system (MP Biomedicals, Santa Ana, CA). gDNA was extracted using the DNeasy® Plant Mini kit (Qiagen, Valencia, CA) or the Maxwell® Plant DNA kit in combination with a Maxwell® Rapid Sample Concentrator (Promega, Madison, WI).

DNA amplification and sequencing

A set of primers for seven genetic markers were used for DNA amplification including 60S Ribosomal protein L10 (60S), beta-tubulin (Btub), elongation factor 1 alpha (EF1α), enolase (Enl), heat shock protein 90 (HSP90), 28S ribosomal DNA (28S), and tigA gene fusion protein (TigA) as indicated in Blair et al. (2008). PCR reaction mixtures were prepared with the Takara Taq DNA polymerase (Takara Shuzo, Shiga, Japan) according to the manufacturer’s instructions. The PCR cycling protocol was the same as indicated by Blair et al. (2008), except that the Eppendorf® Mastercycler® Pro thermal cycler (Eppendorf, Hamburg) was used in this study. All PCR products were evaluated for successful amplification using agarose gel electrophoresis. Unsuccessful PCR amplifications were repeated using a modified protocol to attempt successful amplifications by optimizing annealing temperature using gradient PCR (typically with lower annealing temperatures) or using the GoTaq® Flexi DNA Polymerase (Promega, Madison, WI) PCR mixture system.

Prior to sequencing, excess primer and dNTPs were removed from successful PCR products with shrimp alkaline phosphatase and exonuclease I (USB Catalog # 70092Y and 70073Z). One unit of each enzyme was added to 15 µL PCR product, incubated at 37 °C for 30 min, followed by heat inactivation at 65 °C for 15 min. Sequencing was performed with both amplifying primers as well as internal primers, if any, for individual genetic markers at the University of Kentucky Advanced Genetic Technologies Center (Lexington, KY). Derived sequencing files were visualized with FinchTV 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 to correct obvious sequencing errors and code ambiguous sites according to the International Union of Pure and Applied Chemistry (IUPAC) nucleotide ambiguity codes to produce a consensus sequence. All sequences produced in this study have been deposited in GenBank (Supplementary Table 1).

Among 379 isolates (including three isolates of the outgroup taxa) in the following phylogenetic analyses, all seven phylogenetic markers from 321 isolates were sequenced in this study. Sequences of all markers from 49 isolates by Blair et al. (2008) were also included in the analyses. Additionally, for seven isolates, sequences of one or two genes were newly produced in this study while the remaining gene sequences were from Blair et al. (2008). Sequences from P. lilii (CBS 135746) and P. sp. ohioensis (ST18-37) were obtained from Rahman et al. (2015) and from the Phytophthora Database (Park et al. 2013), respectively.

Phylogenetic analyses

Concatenated sequences of all isolates were aligned using Clustal X version 2.1 (Larkin et al. 2007). The alignment was edited in BioEdit version 7.2.5 (Hall 1999) to trim aligned concatenated sequences to an equal size and set missing data to question marks. The edited alignment was then analyzed in jModelTest version 2.1.7 (Posada 2008) to select the most appropriate model for the following phylogenetic analyses. Maximum likelihood (ML) analysis was performed using RAxML version 8.2.0 (Stamatakis 2014) with the selected model and 1000 bootstrap replicates. Maximum parsimony (MP) analysis was conducted using PAUP version 4.0a147 (Swofford 2002) with 1000 bootstrap replicates. Bayesian analysis (BA) was performed using MrBayes version 3.2.6 (Ronquist et al. 2012) for two million generations with the selected model. Phylogenetic trees were viewed and edited in FigTree version 1.4.2. Alignment and phylogenetic trees from all methods have been deposited in TreeBASE (S19303).

Ancestral character state reconstructions of sporangial papillation

Information on the sporangial papillation of individual species was compiled from the literature (Erwin & Ribeiro 1996, Gallegly & Hong 2008, Kroon et al. 2012, Martin et al. 2012) with emphasis given to their respective original descriptions (Table 1). Both likelihood and parsimony ancestral state reconstructions were performed on the ML tree from the phylogenetic analyses using Mesquite version 3.03 (Maddison & Maddison 2017).

Results

Sequences, alignment, and phylogenetic model

PCR amplification and sequencing was successful for almost all isolates and seven genetic markers. Failure to obtain sequences only occurred occasionally for a few isolates, such as the EF1α gene of Phytophthora bilorbang (61G8), the Enl gene of P. macrochlamydospora (33E1, 31E9, and 33D5), and P. quininea (45F2), and TigA of P. megasperma (62C7) (Supplementary Table 1). These failures were set as missing data in the alignment. After trimming, each isolate was represented by an 8435-bp concatenated sequence in the alignment including gaps and missing data. This included 496 bp for 60S, 1136 bp for Btub, 965 bp for EF1α, 1169 bp for Enl, 1758 bp for HSP90, 1270 bp for 28S, and 1641 bp for TigA (TreeBASE S19303). The general time reversible nucleotide substitution model with gamma-distributed rate variation and a proportion of invariable sites (GTR+I+G) was identified by jModelTest as the most appropriate model for the phylogenetic analyses.

An expanded phylogeny including 10 clades and basal taxa

The three phylogenetic analysis methods, including ML, MP, and BA analyses (TreeBASE S19303), resulted in similar tree topologies. The topology and branch lengths of the ML inference are shown in Fig. 1. The monophyly of each of the previously recognized 10 clades was generally well supported with a few exceptions. Specifically, all clades except for clade 4 were highly supported by > 95 % bootstrap values in ML analysis and 100 % posterior probability (PP) in BA analysis (Fig. 1). Clades 1–3, 5, 7, and 10 were also highly supported by > 95 % bootstrap values in the MP analysis (Fig. 1). However, clades 6, 8, and 9, were only moderately supported with bootstrap numbers of 68, 61, and 52 in the MP analysis, respectively (Fig. 1).

As nearly half of all taxa included in this phylogeny were recently described, all clades in this phylogeny are expanded here to various extents compared to previously published phylogenies. The general structure of clades 1, 3, 5, 8 and 10 remained as previously assigned by Blair et al. (2008) and Martin et al. (2014) with additions of new species. For example, clade 1 was divided into three well-supported subclades and P. nicotianae was placed basal to subclades 1b and 1c (Fig. 1). Clade 8 was divided into four generally well-supported subclades, except P. stricta, which was placed basal to all clade 8 species (Fig. 1). New subclades were assigned to clade 2 (Fig. 2), clade 6 (Fig. 3), clade 7 (Fig. 4) and clade 9 (Fig. 5).

Several species were placed basal to other species in their respective clades. First, the cluster of P. quercina and P. sp. ohioensis was placed basal to other species of clade 4 in all three analyses. The bootstrap supports of the ML and MP analyses, and PP (percentage) for the separation of this cluster from that of P. alticola, P. arenaria, P. megakarya, P. palmivora, and P. quercetorum in clade 4 were only 48, 78, 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 set of support numbers decreased to 99/92/100 when P. sp. sulawesiensis was included, and to 100/68/100 when further including P. asparagi (Fig. 3). Fourth, the support numbers for clade 8 species excluding P. stricta was 100/100/100, but 96/61/100 when P. stricta was included (Fig. 1). Fifth, all papillate species in clade 10 (Table 1) formed a well-supported main cluster, while two more recently described non-papillate species, P. gallica and P. intercalaris, were placed basal to the main cluster (Fig. 1).

New subclades in clades 2, 6, 7, and 9

(a) Clade 2

In addition to the previously recognized subclades 2a and 2b, many species, such as P. acerina, P. capensis, P. citricola, P. multivora, P. pachypleura, P. plurivora, and P. pini in the commonly referred to “Phytophthora citricola-complex” defined a new subclade 2c (Fig. 2). Furthermore, P. bisheria, P. frigida, and P. elongata formed new subclade 2d and the cluster of P. multivesiculata and P. taxon aquatilis formed new subclade 2e, with maximum support values in each case (Fig. 2).

(b) Clade 6

Subclade 6a included P. gemini, P. humicola, P. inundata, P. rosacearum, P. sp. personii, P. sp. 48H2, P. sp. 62C9 and P. taxon walnut. The cluster of P. rosacearum and P. taxon walnut could not be separated from that represented by P. gemini with only moderate support values for separation (82/61/100) (Fig. 3). Isolates 62C9 and 48H2, belonging to two new species, had ambiguous placements within subclade 6a among the three analyses (Fig. 3). With approximately 20 species newly included in the present phylogeny, the previously recognized “P. megasperma-P. gonapodyides complex” (Brasier et al. 2003a), subclade II of clade 6 (Jung et al. 2011), or subclade 6b (Kroon et al. 2012) expanded and its separation from subclade 6a was well-supported by 100/100/100 values (Fig. 3). Within subclade 6b, separation of the cluster of P. bilorbang, P. lacustris, and P. riparia from the other subclade 6b species was highly supported by 97/94/100 (Fig. 3), indicating that these three species may define a new subclade, although this is not done in this study. Phytophthora sp. sulawesiensis was placed basal to other clade 6 species except for P. asparagi, while P. asparagi was basal to all other species in clade 6 (Fig. 3). Phytophthora asparagi was previously assigned as subclade 6c (Kroon et al. 2012) and subclade III of clade 6 (Jung et al. 2011); considering that the support value of MP analysis was only moderate (68 %) when this single taxon was included (Fig. 3), this previous assignation as a subclade was not adopted here. In addition, in order to be consistent with subclade names in other clades, subclades 6a and 6b were used here instead of subclades I and II by Jung et al. (2011).

(c) Clade 7

Four subclades were distinguished in clade 7. Separation of the previously assigned subclades 7a and 7b was only moderately supported by values 71/56/100 (Fig. 4). The general structure of subclade 7a remained the same even with the addition of seven new taxa. Six of these new species, including P. attenuata, P. flexuosa, P. formosa, P. intricata, P. ×heterohybrida, and P. ×incrassata were recently recovered from forest soils and streamwater in Taiwan (Jung et al. 2017). On the other hand, P. cinnamomi and P. parvispora were separated from subclade 7b. They, along with a provisional species, P. sp. ax from Virginia, USA (Table 1), formed a distinct new subclade 7c (Fig. 4). The new subclade 7d, including two recently described species from Japan (Rahman et al. 2014b), P. fragariaefolia and P. nagaii, was placed basal to other subclades in clade 7 (Fig. 4).

(d) Clade 9

The split of clade 9 into two subclades 9a and 9b was highly supported in ML (98 %) and BA (100 %) analyses and moderately supported in the MP (52 %) analysis (Fig. 5). However, monophyly was highly supported for subclade 9b (100/100/100) but not for subclade 9a (44/-/95) (Fig. 5). Within subclade 9a, three monophyletic clusters were formed: 9a1, 9a2, and 9a3. However, support for the separation of these three clusters was moderate or ambiguous. In particular, the MP results did not produce any consistent separation of the three clusters (Fig. 5). Cluster 9a1 included many recently described high-temperature tolerant species, such as P. aquimorbida, P. chrysanthemi, P. hydropathica, P. macilentosa, P. parsiana, and P. virginiana). The cluster of P. macrochlamydospora (two lineages with two isolates in each lineage, Table 1) and P. quininea constituted 9a2 (Fig. 5). The cluster of two other high-temperature tolerant species P. insolita and P. polonica constituted 9a3 (Fig. 5). The well-supported cluster of P. captiosa, P. constricta, and P. fallax was assigned as subclade 9b (Fig. 5).

Evolutionary history of sporangial papillation inferred from ancestral character state reconstructions

Sporangial papillation of individual species is indicated in Table 1 and Fig. 6. Due to the size of the cladograms, clusters including species with the same sporangial papillation within each (sub)clade were compressed in Mesquite. Both likelihood and parsimony methods suggested that non-papillate is the progenitor state of Phytophthora species, and that semi-papillate and papillate types were derived from the non-papillate. The analyses indicated three major clusters of semi-papillate and (or) papillate species diverged from the non-papillate ancestors. First, species in clades 1 to 5 (semi-papillate or papillate) diverged from non-papillate species in clade 7 and P. lilii (Fig. 6). Second, species in subclades 8b to 8d (semi-papillate) diverged from non-papillate subclade 8a species (Fig. 6). Third, papillate clade 10 species including P. boehmeriae, P. gondwanensis, P. kernoviae, and P. morindae diverged from the non-papillate P. gallica and P. intercalaris (Fig. 6). Several species such as P. macrochlamydospora, P. mississippiae, P. gibbosa, and P. constricta also evolved to produce partially semi-papillate sporangia (Fig. 6).
Fig. 6
Fig. 6

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.

Discussion

Here we presented an expanded phylogeny for the genus Phytophthora, encompassing 142 formally named and 43 provisionally recognized species (Table 2). In addition to this comprehensive coverage, this expanded phylogeny features over 1500 signature sequences generated from 278 ex-type and authentic isolates of 162 Phytophthora taxa (Supplementary Table 1). Furthermore, this study provided new insights into the evolutionary history of sporangial papillation in Phytophthora.

The expanded phylogeny provides a sound taxonomic framework for this agriculturally and ecologically important genus. One hundred and fourteen ex-types were included, representing 80 % of the 142 formally named species in this 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 designation of an ex-type culture. Likewise, almost all the 43 provisional species in this phylogeny were represented by authentic isolates from the originators of the respective species (Table 1 and Supplementary Table 1). This new framework will facilitate identification of new taxa in the future. As the genus continues to rapidly expand, some recently described species were not included in this study: P. mekongensis in subclade 2a (Puglisi et al. 2017), P. amaranthi in subclade 2b (Ann et al. 2016), P. boodjera in clade 4 (Simamora et al. 2015), P. chlamydospora in subclade 6b (Hansen et al. 2015), P. uniformis (basionym: P. alni subsp. uniformis) and P. ×multiformis (basionym: P. alni subsp. multiformis) in subclade 7a (Brasier et al. 2004, Husson et al. 2015), P. pseudolactucae in subclade 8b (Rahman et al. 2015), and P. prodigiosa (Puglisi et al. 2017) and P. pseudopolonica (Li et al. 2017) in subclade 9a. Likewise, some informally designated species also were not included: such as P. taxon humicola-like, P. taxon kwongan, and P. taxon rosacearum-like in subclade 6a (Jung et al. 2011). These and other emerging species are yet to be incorporated in the overall phylogeny of the genus.

The generation of over 1500 signature sequences from ex-types and authentic isolates in this study will aid researchers and first responders in correctly identifying Phytophthora cultures to the species level. DNA sequencing of selected genetic markers has become common practice in the identification of Phytophthora cultures (Kang et al. 2010). However, it is recognized that the accuracy of culture identity determined by this approach depends on the quality of the reference sequences used — and currently many sequence deposits are erroneously identified in public repositories, including GenBank (Kang et al. 2010). These errors originated in sequence deposits of cultures that were identified by morphological characters alone, and compounded by those identified through sequence matches to erroneous reference sequences or by single DNA markers (Kang et al. 2010). In this study, 29 isolates were found associated with an erroneous or modified identity (Supplementary Table 2). For instance, isolate 29B3 in clade 1 was identified as P. pseudotsugae and used as a key isolate for this species by Gallegly & Hong (2008). However, its sequences were distinct from those of the P. pseudotsugae ex-type (ATCC 52938). In the phylogenetic tree, it was basal to the cluster of P. cactorum and P. hedraiandra, thus its species identity was changed to P. aff. pseudotsugae (Fig. 1). In clade 2, isolate 26H4 was identified as P. citrophthora (Gallegly & Hong 2008) but sequences and phylogeny showed that it was close to but distinct from P. citrophthora isolates 03E5 and 26H3. It formed a cluster with isolate IMI 342898 (P10341), which was coded as P. sp. aff. colocasiae-1 by Martin et al. (2014). The identity of both isolates was then changed to P. aff. citrophthora (Fig. 2). Similarly, in clade 8, isolate 22G2 had been identified as P. cryptogea, although it was distinct from the P. cryptogea ex-type 61H9 (CBS 113.19). In the phylogenetic tree, it was basal to the cluster of P. cryptogea and P. erythroseptica, and the species identity was consequently changed to P. aff. cryptogea (Fig. 1). Changes in the identifications of these isolates, including the new and original names used, are indicated in Supplementary Table 2. The changes in the naming of these isolates highlights the importance of using signature sequences from ex-type or authentic isolates as references in future culture identification. In order to facilitate this practice, the signature sequences generated from ex-types or authentic isolates in the present study are marked as ‘(ex-type)’ or ‘(authentic)’, respectively, under the ‘isolate’ section in the ‘feature’ table of GenBank deposits. The research, diagnostic and regulatory communities are encouraged to use these sequences as references in future culture identification.

This study provided new insights into the evolutionary history of sporangial morphology in the genus Phytophthora, a subject that has fascinated generations of mycologists and plant pathologists. There have been three major hypotheses regarding the development of papillation, as illustrated in Fig. 7a, b, and c, respectively. First, papillate species were considered as descendants of Pythium-like, non-papillate ancestors and semi-papillation has been considered as intermediate between non-papillation and papillation (Blackwell 1949, Cooke et al. 2000, Erwin & Ribeiro 1996). Second, some semi-papillate species, exemplified by P. primulae in the group III of Waterhouse (1963) are primitive; they were suggested to have evolved to papillate and non-papillate species through two distinct evolutionary lines (Brasier 1983). Third, semi-papillate sporangia are morphological variants of papillate and non-papillate types (Cooke et al. 2000). Here we suggest that the non-papillate type is ancestral, and that non-papillate species could have evolved directly into either semi-papillate or papillate species (Fig. 7d). The evolution to semi-papillate species is exemplified by those in subclades 8b–d (Fig. 1), while evolution to papillate species is illustrated by P. boehmeriae and other papillate species in clade 10 (Fig. 1). The relationship between semi-papillate and papillate species appears to be more complicated (Fig. 7d). We also hypothesize that some semi-papillate species, such as those in subclade 1c, may have diverged from papillate ancestors, while some papillate species such as P. frigida may have evolved from semi-papillate ancestors of subclade 2d (Fig. 6).
Fig. 7
Fig. 7

Illustration of hypotheses on evolution of Phytophthora and associated changes in sporangial papillation: (a) species producing papillate sporangia evolved from non-papillate ancestors. Semi-papillation is considered as intermediate between non-papillation and papillation (Blackwell 1949, Cooke et al. 2000, Erwin & Ribeiro 1996); (b) some semi-papillate species, exemplified by P. primulae in the group III of Waterhouse (1963), are primitive and evolved to be non-papillate and papillate through two evolutionary paths, by Brasier (1983); (c) papillate species evolved from non-papillate ancestors. Semi-papillate species have been considered as morphological variants of papillate or non-papillate species, by Cooke et al. (2000); (d) a new hypothesis developed in this study that non-papillate ancestors evolved directly to either papillate or semi-papillate species. Some semi-papillate species further evolved to be papillate, or vice versa.

These new hypotheses are supported by the results from phylogeny and ancestral state reconstructions that suggest three major evolutionary paths in sporangial papillation of Phytophthora species (Fig. 1). First, the ancestor of modern species in clades 1–5 evolved to be papillate or semi-papillate (Figs 1, 6) while diverging from the common non-papillate ancestor of clade 7 species (Figs 1, 6). Second, the common ancestor of species in subclades 8b–d diverged from that of subclade 8a species while acquiring semi-papillation (Figs 1, 6). Third, the common ancestor of five clade 10 species in the main cluster including P. boehmeriae, P. gondwanensis, P. kernoviae, P. morindae, and P. sp. boehmeriae-like, acquired papillate sporangia while diverging from two non-papillate clade 10 species, P. gallica and P. intercalaris (Figs 1, 6). Besides these three major groups of papillate or semi-papillate species, a few species may have evolved to acquire semi-papillation independently, such as P. macrochlamydospora in clade 9 (Fig. 6). This evolutionary process may be underway for some other species including P. constricta, P. gibbosa, and P. mississippiae, which all produce both semi-papillate and non-papillate sporangia (Fig. 6). Furthermore, evolutionary reversion to partial production of non-papillate sporangia may have occurred in P. multivesiculata and P. lateralis in two semi-papillate subclades 2e and 8c, respectively (Fig. 6). However, that conclusion is uncertain due to limited and ambiguous data from species in these two subclades. Specifically, P. lateralis was ambiguously reported as non-papillate (Erwin & Ribeiro 1996, Gallegly & Hong 2008, Martin et al. 2012, Tucker & Milbrath 1942) or non- to semi-papillate (Kroon et al. 2012) in different studies. In subclade 2e, the only sister taxon of P. multivesiculata, P. taxon aquatilis, was provisionally described as semi-papillate, but only based on a single isolate (Hong et al. 2012). Evolutionary reversion in the sporangial papillation of these two species requires validation in the future. Also, more studies are warranted to analyze additional characters based on phylogenies with better clade-to-clade resolutions and provide a more comprehensive picture on the evolutionary history of Phytophthora species.

That a number of species were placed basal to other species in their respective clades in this expanded phylogeny presents a significant challenge to the monophyly of their respective clades and the current 10-clade system. First, P. stricta was initially placed close to other species in subclade 8a based on sequences of the cytochrome c oxidase 1 (cox1) gene, but was not grouped in any ITS clade (Yang et al. 2014a). This species was grouped in clade 8 in our expanded phylogeny by ML and BA analyses (Fig. 1); the monophyly of this clade was only moderately supported (61 %) in the MP analysis (Fig. 1). Second, the monophyly of clade 6 including P. asparagi was only moderately supported (68 %) in the MP analysis (Fig. 3). Third, although the inclusion of P. intercalaris in clade 10 was supported with maximum values, the exact positions of this species and P. gallica were still unresolved since the next node was only moderately supported (53 %) in the ML analysis and ambiguous in the MP analysis (Fig. 1). Fourth, similar to the finding of Blair et al. (2008), support for the monophyly of clade 4 including P. quercina and P. sp. ohioensis was only moderate (48/78/84). Also, similar ambiguity in the placement of the ‘P. quercinaP. sp. ohioensis’ cluster was observed among different phylogenetic approaches, and using different datasets including nuclear, mitochondrial, and combined nuclear and mitochondrial sequences (Martin et al. 2014). Fifth, this phylogeny confirmed the finding by Rahman et al. (2015) that P. lilii was not grouped in any clade of the current 10-clade system (Fig. 1). This species was not assigned as a distinct clade in our study, due to the relatively low clade-to-clade resolutions (Fig. 1). Further analyses are warranted to determine whether this unique species should be assigned as a new clade.

Although many branches in the expanded phylogeny have consistent maximum support in all three methods, some have only moderate to low or inconsistent support. These results highlight the challenges of correctly inferring the evolutionary separation of many closely related Phytophthora species, even when concatenated sequences from seven phylogenetic markers were used. It can be expected that as the cost of gene sequencing drops further, it will become possible to increase phylogenetic resolution among Phytophthora species by using concatenations of much larger numbers of genes. For example, Ye et al. (2016) used 293 concatenated housekeeping proteins to infer a robust phylogeny of seven fully sequenced Phytophthora species and confirmed that downy mildews (represented by three genome sequences) are nested within the genus Phytophthora, close to Phytophthora clade 4 (Ye et al. 2016). However, even with full genome sequences, ambiguity may not be completely resolved in cases where speciation has involved large populations of sexually reproducing individuals, for example, as a result of geographic separation. In these cases, there may be many sequence polymorphisms shared among separated species and these may confound the inference of a reliable phylogeny. Resolution of this level of ambiguity may require sequencing the whole genome of many isolates from the species of interest as well as using improved phylogenetic and coalescent methods.

With the number of described Phytophthora species increasing, recent studies have raised an important concern in the accurate detection of species boundaries using phylogenetic data (Jung & Burgess 2009, Pánek et al. 2016, Safaiefarahani et al. 2015). One example is the status of P. hedraiandra as a distinct species in subclade 1a (Pánek et al. 2016). As evidenced by the amplified fragment length polymorphism (AFLP) and phylogenetic analysis based on sequences of ITS, phenolic acid decarboxylase, and cox1 genes, a recent study concluded that P. hedraiandra was just one lineage of P. cactorum, while morphological data provided only limited information to delimitate these two species (Pánek et al. 2016). Also, phylogenetic analyses in this study indicated that P. cactorum and P. hedraiandra cluster with strong support (98/100/100), and P. aff. hedraiandra isolate 33F4 (previously identified as P. hedraiandra Supplementary Table 2), was clustered with P. cactorum (Fig. 1). Phylogenies based on nuclear sequences prior to this study also supported P. hedraiandra as closely related to P. cactorum (Blair et al. 2008, Martin et al. 2014). However, in the phylogenies based on concatenated sequences of four mitochondrial loci, and combined seven nuclear and four mitochondrial loci, P. hedraiandra was basal to the cluster of P. cactorum and P. pseudotsugae, and clustered with P. idaei, respectively (Martin et al. 2014). Phytophthora cactorum and P. hedraiandra also have very distinctive single-strand-conformation polymorphism patterns (Gallegly & Hong 2008). Apparently, more investigations are warranted to resolve the P. cactorum complex. Likewise, indistinct boundaries are present among species in other subclades, such as the ‘P. citricola complex’ or subclade 2c (Brazee et al. 2017, Jung & Burgess 2009), the ‘P. cryptogea complex’ in subclade 8a (Safaiefarahani et al. 2015, 2016) and cluster 9a1 in subclade 9a including P. hydropathica (Hong et al. 2010), P. parsiana (Mostowfizadeh-Ghalamfarsa et al. 2008), P. virginiana (Yang & Hong 2013) and other provisionally designated species. Accurately delimiting these closely related species within the genus remains an important task.

This expanded phylogeny has highlighted the importance and difficulty of accurately interpreting the position of hybrid Phytophthora species. As exemplified by P. xalni (Brasier et al. 2004, Husson et al. 2015), many hybrid species have been identified among emerging plant pathogens (Jung et al. 2017, Man in’t Veld et al. 2012, Nirenberg et al. 2009). Due to the presence of multiple alleles originated from parent species in their nuclear genes, phylogenetic analysis of these hybrids based on nuclear sequences alone may not produce a robust placement. As illustrated in this phylogeny, the placement of hybrid species may be ambiguous. Specifically, in subclade 6b, support values for the placement of P. ×stagnum and its closely related species, P. mississippiae, P. borealis, and P. sp. delaware were moderate in the ML and BA analyses and ambiguous in the MP analysis (Fig. 3). Similarly, in subclade 7a, the placement of P. xalni, P. xcambivora, P. xheterohybrida, and P. ×jncrassata’ cluster was not well resolved due to ambiguous placement in the MP analysis and moderate support values in the other two analyses (Fig. 4). Adding mitochondrial sequences into the phylogenetic analyses may be a solution to this problem. However, due to the uniparental inheritance of mitochondria, the hybrids and their maternal parents are inseparable by mitochondrial sequences and their placements could conflict with nuclear analyses (Martin et al. 2014).

Declarations

Acknowledgments

This research was supported in part by grants from the USDA-NIFA-Specialty Crop Research Initiative (Agreement no. 2010-51181-21140). We would like to thank all authorities and species originators who provided Phytophthora isolates to our study, including Yilmaz Balci, Zia Banihashemi, Lien Bertier, Karien Bezuidenhout, Clive Brasier, Treena Burgess, Mike Coffey, Mannon Gallegly, Beatrice Ginetti, Nikiaus Grünwald, Everett Hansen, Beatrice Henricot, Fredrik Heyman, Hon Ho, Maria Holeva, Steven Jeffers, Thomas Jung, Koji Kageyama, Willem Man in ‘t Veld, Jan Nechwatal, Bruno Scanu, Andrea Vannini, Anna Maria Vettraino, and Irene Vloutoglou. Names of many other contributors are listed in Supplementary Table 1.

This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

Authors’ Affiliations

(1)
Hampton Roads Agricultural Research and Extension Center, Virginia Tech, Virginia Beach, VA 23455, USA
(2)
Center for Genome Research and Biocomputing, and Department of Botany and Plant Pathology, Oregon State University, Corvallis, OR 97331, USA

References

  1. Abad, ZG, Abad, JA, Cacciola, SO, Pane, A, Faedda, R, et al. (2014) Phytophthora niederhauserii sp. nov., a polyphagous species associated with ornamentals, fruit trees and native plants in 13 countries. Mycologia 106: 431–437.PubMedGoogle Scholar
  2. Abad, ZG, Abad, JA, Coffey, MD, Oudemans, PV, Man, WA, et al. (2008) Phytophthora bisheria sp. nov., a new species identified in isolates from the Rosaceous raspberry, rose and strawberry in three continents. Mycologia 100: 99–110.PubMedGoogle Scholar
  3. Abad, ZG, Ivors, KL, Gallup, CA, Abad, JA, Shew, HD (2011) Morphological and molecular characterization of Phytophthora glovera sp. nov. from tobacco in Brazil. Mycologia 103: 341–350.PubMedGoogle Scholar
  4. Aghighi, S, Hardy GESJ, Scott, JK, Burgess, TI (2012) Phytophthora bilorbang sp. nov., a new species associated with the decline of Rubus anglocandicans (European blackberry) in Western Australia. European Journal of Plant Pathology 133: 841–855.Google Scholar
  5. Amin, KS, Baldev, B, Williams, FJ (1978) Phytophthora cajani, a new species causing stem blight on Cajanus cajan. Mycologia 70: 171–176.Google Scholar
  6. Ann, PJ, Huang, JH, Tsai, JN, Ko, WH (2016) Morphological, molecular and pathological characterization of Phytophthora amaranthi sp. nov. from Amaranth in Taiwan. Journal of Phytopathology 164: 94–101.Google Scholar
  7. Ann, PJ, Ko, WH (1980) Phytophthora insolita, a new species from Taiwan. Mycologia 72: 1180–1185.Google Scholar
  8. Aragaki, M, Uchida, JY (2001) Morphological distinctions between Phytophthora capsici and P tropicalis sp. nov. Mycologia 93: 137–145.Google Scholar
  9. Balci, Y, Balci, S, Blair, JE, Park, SY, Kang, S, et al. (2008) Phytophthora quercetorum sp. nov., a novel species isolated from eastern and north-central USA oak forest soils. Mycological Research 112: 906–916.PubMedGoogle Scholar
  10. Belbahri, L, Moralejo, E, Calmin, G, Oszako, T, Garcia, JA, et al. (2006) Phytophthora polonica, a new species isolated from declining Alnus glutinosa stands in Poland. FEMS Microbiology Letters 261: 165–174.PubMedPubMed CentralGoogle Scholar
  11. Bertier, L, Brouwer, H, De Cock, A, Cooke, DEL, Olsson, CHB, et al. (2013) The expansion of Phytophthora clade 8b: three new species associated with winter grown vegetable crops. Persoonia 31: 63–76.PubMedPubMed CentralGoogle Scholar
  12. Bezuidenhout, CM, Denman, S, Kirk, SA, Botha, WJ, Mostert, L, et al. (2010) Phytophthora taxa associated with cultivated Agathosma, with emphasis on the P citricola complex and P capensis sp. nov. Persoonia 25: 32–49.PubMedPubMed CentralGoogle Scholar
  13. Blackwell, E (1949) Terminology in Phytophthora. MycologicalPapers 30: 1–24.Google Scholar
  14. Blair, JE, Coffey, MD, Park S-Y, Geiser, DM, Kang, S (2008) A multilocus phylogeny for Phytophthora utilizing markers derived from complete genome sequences. Fungal Genetics and Biology 45: 266–277.PubMedPubMed CentralGoogle Scholar
  15. Brasier, CM (1983) Problems and prospects in Phytophthora research. In: Phytophthora: its Biology, taxonomy, ecology, and pathology (Erwin, DC, Bartnicki-Garcia, S, Tsao, PH, eds): 351–364. St Paul, MN: American Phytopathological Society Press.Google Scholar
  16. Brasier, CM, Beales, PA, Kirk, SA, Denman, S, Rose, J (2005) Phytophthora kernoviae sp. nov., an invasive pathogen causing bleeding stem lesions on forest trees and foliar necrosis of ornamentals in the UK. Mycological Research 109: 853–859.PubMedPubMed CentralGoogle Scholar
  17. Brasier, CM, Cooke, DEL, Duncan, JM, Hansen, EM (2003a) Multiple new phenotypic taxa from trees and riparian ecosystems in Phytophthora gonapodyides-P. megasperma ITS Clade 6, which tend to be high-temperature tolerant and either inbreeding or sterile. Mycological Research 107: 277–290.PubMedGoogle Scholar
  18. Brasier, CM, Griffin, MJ (1979) Taxonomy of ‘Phytophthora palmivora’ on cocoa. Transactions of the British Mycological Society 72: 111–143.Google Scholar
  19. Brasier, CM, Kirk, SA, Delcan, J, Cooke, DEL, Jung, T, et al. (2004) Phytophthora alni sp. nov. and its variants: designation of emerging heteroploid hybrid pathogens spreading on Alnus trees. Mycological Research 108: 1172–1184.PubMedGoogle Scholar
  20. Brasier, CM, Sanchez-Hernandez, E, Kirk, SA (2003b) Phytophthora inundata sp. nov., a part heterothallic pathogen of trees and shrubs in wet or flooded soils. Mycological Research 107: 477–484.PubMedGoogle Scholar
  21. Brazee, NJ, Yang, X, Hong, C (2017) Phytophthora caryae sp. nov., a new species recovered from streams and rivers in the eastern United States. Plant Pathology 66: 805–817.Google Scholar
  22. Breda De Haan, JV (1896) De bibitziekte in de Deli-tabak veroorzaakt door Phytophthora nicotianae. Mededeelingen uit ‘s Lands Plantentuin Batavia 15: 1–107.Google Scholar
  23. Buddenhagen, IW, Young, RA (1957) A leaf and twig disease of English holly caused by Phytophthora ilicis n. sp. Phytopathology 47: 95–101.Google Scholar
  24. Buisman, CJ (1927) Root rots caused by Phycomycetes. Mededelingen Phytopathologisch Laboratorium “Willie Commelin Scholten” 11:1–51.Google Scholar
  25. Butler, EJ (1910) The bud-rot of palms in India. Memoirs of the Department of Agriculture in India, Botanical Series 3: 221–280.Google Scholar
  26. Carne, WM (1925) A brown rot of citrus in Australia (Phytophthora hibernalis n. sp). Journal of the Royal Society of Western Australia 12: 13–41.Google Scholar
  27. Chee, KH (1969) Variability of Phytophthora species from Hevea brasiliensis. Transactions of the British Mycological Society 52: 425–436.Google Scholar
  28. Cooke, DEL, Drenth, A, Duncan, JM, Wagels, G, Brasier, CM (2000) A molecular phylogeny of Phytophthora and related oomycetes. Fungal Genetics and Biology 30: 17–32.PubMedPubMed CentralGoogle Scholar
  29. Crandall, BS (1947) A new Phytophthora causing root and collar rot of Cinchona in Peru. Mycologia 39: 218–223.PubMedGoogle Scholar
  30. Crous, PW, Groenewald, JZ, Shivas, RG, Edwards, J, Seifert, KA, et al. (2011) Fungal Planet description sheets: 69–91. Persoonia 26: 108–156.PubMedPubMed CentralGoogle Scholar
  31. Crous, PW, Summerell, BA, Shivas, RG, Burgess, TI, Decock, CA, et al. (2012) Fungal Planet description sheets: 107–127. Persoonia 28: 138–182.PubMedPubMed CentralGoogle Scholar
  32. Crous, PW, Wingfield, MJ, Le Roux, JJ, Richardson, DM, Strasberg, D, et al. (2015) Fungal Planet description sheets: 371–399. Persoonia 35: 264–327.PubMedPubMed CentralGoogle Scholar
  33. De Bary, A (1876) Researches into the nature of the potato-fungus, Phytophthora infestans. Journal of the Royal Agricultural Society of England 12: 239–269.Google Scholar
  34. De Cock, AW, Lévesque, CA (2004) New species of Pythium and Phytophthora. Studies in Mycology 50: 481–487.Google Scholar
  35. De Cock AWAM, Lodhi, AM, Rintoul, TL, Bala, K, Robideau, GP, et al. (2015) Phytopythium: molecular phylogeny and systematics. Persoonia 34: 25–39.PubMedGoogle Scholar
  36. Dick, MA, Dobbie, K, Cooke, DEL, Brasier, CM (2006) Phytophthora captiosa sp. nov. and P. fallax sp. nov. causing crown dieback of Eucalyptus in New Zealand. Mycological Research 110: 393–404.PubMedPubMed CentralGoogle Scholar
  37. Donahoo, R, Blomquist, CL, Thomas, SL, Moulton, JK, Cooke, DEL, et al. (2006) Phytophthora foliorum sp. nov., a new species causing leaf blight of azalea. Mycological Research 110: 1309–1322.PubMedGoogle Scholar
  38. Drechsler, C (1931) A crown-rot of hollyhocks caused by Phytophthora megasperma n. sp. Journal of the Washington Academy of Sciences 21: 513–526.Google Scholar
  39. Duran, A, Gryzenhout, M, Slippers, B, Ahumada, R, Rotella, A, et al. (2008) Phytophthora pinifolia sp. nov. associated with a serious needle disease of Pinus radiata in Chile. Plant Pathology 57: 715–727.Google Scholar
  40. Ersek, T, Ribeiro, OK (2010) Mini review article: an annotated list of new Phytophthora species described post 1996. Acta Phytopathologica et Entomologica Hungarica 45: 251–266.Google Scholar
  41. Ershad, D (1971) Beitrag zur Kenntnis der Phytophthora-arten in Iran und Ihrer Phytopathologischen Bedeutung. Berlin-Dahlem: Mitteilungen aus der Biologischen Bundesanstalt fur Land- and Forstwirtschaft.Google Scholar
  42. Erwin, DC, Ribeiro, OK (1996) Phytophthora Diseases Worldwide. St Paul, MN: American Phytopathological Society Press.Google Scholar
  43. Flier, WG, Grünwald, NJ, Kroon, L, Van Den Bosch, TBM, Garay-Serrano, E, et al. (2002) Phytophthora ipomoeae sp. nov., a new homothallic species causing leaf blight on Ipomoea longipedunculata in the Toluca Valley of central Mexico. Mycological Research 106: 848–856.Google Scholar
  44. Galindo-A, J, Hohl, HR (1985) Phytophthora mirabilis, a new species of Phytophthora. Sydowia 38: 87–96.Google Scholar
  45. Gallegly, ME, Hong, C (2008) Phytophthora: identifying species by morphology and DNA fingerprints. St Paul, MN: American Phytopathological Society Press.Google Scholar
  46. Ginetti, B, Moricca, S, Squires, JN, Cooke, DEL, Ragazzi, A, et al. (2014) Phytophthora acerina sp. nov., a new species causing bleeding cankers and dieback of Acer pseudoplatanus trees in planted forests in northern Italy. Plant Pathology 63: 858–876.Google Scholar
  47. Goheen, EM, Hansen, EM, Kanaskie, A, Mcwilliams, MG, Osterbauer, N, et al. (2002) Sudden oak death caused by Phytophthora ramorum in Oregon. Plant Disease 86: 441.PubMedGoogle Scholar
  48. Greslebin, AG, Hansen, EM, Sutton, W (2007) Phytophthora austyocedrae sp. nov., a new species associated with Austyocedrus chilensis mortality in Patagonia (Argentina). Mycological Research 111: 308–316.PubMedGoogle Scholar
  49. Grünwald, NJ, Werres, S, Goss, EM, Taylor, CR, Fieland, VJ (2012) Phytophthora obscura sp. nov., a new species of the novel Phytophthora subclade 8d. Plant Pathology 61: 610–622.Google Scholar
  50. Haas, BJ, Kamoun, S, Zody, MC, Jiang, RHY, Handsaker, RE, et al. (2009) Genome sequence and analysis of the Irish potato famine pathogen Phytophthora infestans. Nature 461: 393–398.PubMedPubMed CentralGoogle Scholar
  51. Hall, TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41: 95–98.Google Scholar
  52. Hamm, P, Hansen, EM (1983) Phytophthora pseudotsugae, a new species causing root rot of Douglas-fir. Canadian Journal of Botany 61: 2626–2631.Google Scholar
  53. Hansen, EM, Maxwell, DP (1991) Species of the Phytophthora megasperma complex. Mycologia 83: 376–381.Google Scholar
  54. Hansen, EM, Reeser, P, Sutton, W, Brasier, CM (2015) Redesignation of Phytophthora taxon Pgchlamydo as Phytophthora chlamydospora sp. nov. North American Fungi 10: 1–14.Google Scholar
  55. Hansen, EM, Reeser, PW, Davidson, JM, Garbelotto, M, Ivors, K, et al. (2003) Phytophthora nemorosa, a new species causing cankers and leaf blight of forest trees in California and Oregon, U.S.A. Mycotaxon 88: 129–138.Google Scholar
  56. Hansen, EM, Reeser, PW, Sutton, W (2012) Phytophthora borealis and Phytophthora riparia, new species in Phytophthora ITS Clade 6. Mycologia 104: 1133–1142.PubMedGoogle Scholar
  57. Hansen, EM, Wilcox, WF, Reeser, PW, Sutton, W (2009) Phytophthora rosacearum and P. sansomeana, new species segregated from the Phytophthora megasperma “complex”. Mycologia 101: 129135.Google Scholar
  58. Henricot, B, Perez Sierra, A, Jung, T (2014) Phytophthora pachypleura sp. nov., a new species causing root rot of Aucuba japonica and other ornamentals in the United Kingdom. Plant Pathology 63: 1095–1109.Google Scholar
  59. Heyman, F, Blair, JE, Persson, L, Wikstrom, M (2013) Root rot of pea and faba bean in southern Sweden caused by Phytophthora pisi sp. nov. Plant Disease 97: 461–471.PubMedGoogle Scholar
  60. Hickman, CJ (1940) The red core root disease of the strawberry caused by Phytophthora fragariae n. sp. Journal of Pomology and Horticultural Society 18: 89–118.Google Scholar
  61. Hong, C, Gallegly, ME, Richardson, PA, Kong, P (2011) Phytophthora pini Leonian resurrected to distinct species status. Mycologia 103: 351–360.PubMedGoogle Scholar
  62. Hong, CX, Gallegly, ME, Browne, GT, Bhat, RG, Richardson, PA, et al. (2009) The avocado subgroup of Phytophthora citricola constitutes a distinct species, Phytophthora mengei sp. nov. Mycologia 101: 833–840.PubMedGoogle Scholar
  63. Hong, CX, Gallegly, ME, Richardson, PA, Kong, P, Moorman, GW (2008) Phytophthora irrigata, a new species isolated from irrigation reservoirs and rivers in Eastern United States of America. FEMS Microbiology Letters 285: 203–211.PubMedGoogle Scholar
  64. Hong, CX, Gallegly, ME, Richardson, PA, Kong, P, Moorman, GW, et al. (2010) Phytophthora hydropathica, a new pathogen identifed from irrigation water, Rhododendron catawbiense and Kalmia latifolia. Plant Pathology 59: 913–921.Google Scholar
  65. Hong, CX, Richardson, PA, Hao, W, Ghimire, SR, Kong, P, et al. (2012) Phytophthora aquimorbida sp. nov. and Phytophthora taxon ‘aquatilis’ recovered from irrigation reservoirs and a stream in Virginia, USA. Mycologia 104: 1097–1108.PubMedGoogle Scholar
  66. Hotson, JW, Hartge, L (1923) A disease of tomato caused by Phytophthora mexicana sp. nov. Phytopathology 13: 520–531.Google Scholar
  67. Husson, C, Aguayo, J, Revellin, C, Frey, P, loos, R, et al. (2015) Evidence for homoploid speciation in Phytophthora alni supports taxonomic reclassifcation in this species complex. Fungal Genetics and Biology 77: 12–21.PubMedGoogle Scholar
  68. Ilieva, E, Veld Wa M, Veenbaas-Rijks, W, Pieters, R (1998) Phytophthora multivesiculata, a new species causing rot in Cymbidium. European Journal of Plant Pathology 104: 677–684.Google Scholar
  69. Irwin Ja G (1991) Phytophthora macrochlamydospora, a new species from Australia. Mycologia 83: 517–519.Google Scholar
  70. Jung, T, Burgess, TI (2009) Re-evaluation of Phytophthora citricola isolates from multiple woody hosts in Europe and North America reveals a new species, Phytophthora plurivora sp. nov. Persoonia 22: 95–110.PubMedPubMed CentralGoogle Scholar
  71. Jung, T, Cooke, DEL, Blaschke, H, Duncan, JM, Oßwald, W (1999) Phytophthora quercina sp. nov., causing root rot of European oaks. Mycological Research 103: 785–798.Google Scholar
  72. Jung, T, Hansen, EM, Winton, L, Oßwald, W, Delatour, C (2002) Three new species of Phytophthora from European oak forests. Mycological Research 106: 397–411.Google Scholar
  73. Jung, T, Jung, MH, Scanu, B, Seress, D, Kovâcs, GM, et al. (2017) Six new Phytophthora species from ITS Clade 7a including two sexually functional heterothallic hybrid species detected in natural ecosystems in Taiwan. Persoonia 38: 100–135.PubMedGoogle Scholar
  74. Jung, T, Nechwatal, J (2008) Phytophthora gallica sp. nov., a new species from rhizosphere soil of declining oak and reed stands in France and Germany. Mycological Research 112: 1195–1205.PubMedGoogle Scholar
  75. Jung, T, Nechwatal, J, Cooke, DEL, Hartmann, G, Blaschke, M, et al. (2003) Phytophthora pseudosyringae sp. nov., a new species causing root and collar rot of deciduous tree species in Europe. Mycological Research 107: 772–789.PubMedGoogle Scholar
  76. Jung, T, Stukely, MJC, Hardy GESJ, White, D, Paap, T, et al. (2011) Multiple new Phytophthora species from ITS Clade 6 associated with natural ecosystems in Australia: evolutionary and ecological implications. Persoonia 26: 13–39.PubMedPubMed CentralGoogle Scholar
  77. Kang, S, Mansfeld, MA, Park, B, Geiser, DM, Ivors, KL, et al. (2010) The promise and pitfalls of sequence-based identifcation of plant-pathogenic fungi and oomycetes. Phytopathology 100: 732–737.PubMedGoogle Scholar
  78. Katsura, K (1976) Two new species of Phytophthora causing damping-off of cucumber and trunk rot of chestnut. Transactions of the Mycological Society of Japan 17: 238–242.Google Scholar
  79. Kaufmann, MJ, Gerdemann, JW (1958) Root and stem rot of soybean caused by Phytophthora sojae n. sp. Phytopathology 48: 201208.Google Scholar
  80. Kennedy, DM, Duncan, JM (1995) A papillate Phytophthora species with specifcity to Rubus. Mycological Research 99: 57–68.Google Scholar
  81. Klebahn, H (1905) Eine neue Pilzkrankheit der Syringen (A new fungal disease of Syringae). Zentralblatt für Bakteriologie, Parasitenkunde und Infektionskrankheiten 15: 335–336.Google Scholar
  82. Ko, WH, Ann, PJ (1985) Phytophthora humicola, a new species from soil of a citrus orchard in Taiwan. Mycologia 77: 631–636.Google Scholar
  83. Kröber, H, Marwitz, R (1993) Phytophthora tentaculata sp. nov. und Phytophthora cinnamomi var. parvispora var. nov., zwei neue Pilze von Zierpflanzen in Deutschland. Zeitschrift Fur Pflanzenkrankheiten Und Pflanzenschutz 100: 250–258.Google Scholar
  84. Kroon LPNM, Bakker, FT, Van Den Bosch, GBM, Bonants, PJM, Flier, WG (2004) Phylogenetic analysis of Phytophthora species based on mitochondrial and nuclear DNA sequences. Fungal Genetics and Biology 41: 766–782.PubMedGoogle Scholar
  85. Kroon LPNM, Brouwer, H, De Cock AWAM, Govers, F (2012) The genus Phytophthora anno 2012. Phytopathology 102: 348–364.PubMedGoogle Scholar
  86. Lara, E, Belbahri, L (2011) SSU rRNA reveals major trends in oomycete evolution. Fungal Diversity 49: 93–100.Google Scholar
  87. Larkin, MA, Blackshields, G, Brown, NP, Chenna, R, Mcgettigan, PA, et al. (2007) Clustal, W and Clustal, X version 2.0. Bioinformatics 23: 2947–2948.Google Scholar
  88. Leonian, LH (1922) Stem and fruit blight of pepper caused by Phytophthora capsici sp. nov. Phytopathology 12: 401–408.Google Scholar
  89. Li, WW, Zhao, WX, Huai, WX (2017) Phytophthora pseudopolonica sp. nov., a new species recovered from stream water in subtropical forests of China. International Journal of Systematic and Evolutionary Microbiology 67: 3666–3675.PubMedGoogle Scholar
  90. Maddison, WP, Maddison, DR (2017) Mesquite: a modular system for evolutionary analysis. http://mesquiteproject.org.Google Scholar
  91. Man In’t Veld, WA, De Cock, A, Ilieva, E, Lévesque, CA (2002) Gene flow analysis of Phytophthora porri reveals a new species: Phytophthora brassicae sp. nov. European Journal of Plant Pathology 108: 51–62.Google Scholar
  92. Man In’t Veld, WA, Rosendahl KCHM, Brouwer, H, De Cock AWAM (2011) Phytophthora gemini sp. nov., a new species isolated from the halophilic plant Zostera marina in the Netherlands. Fungal Biology 115: 724–732.Google Scholar
  93. Man In’t Veld, WA, Rosendahl KCHM, Hong, C (2012) Phytophthora xserendipita sp. nov. and P. xpelgrandis, two destructive pathogens generated by natural hybridization. Mycologia 104: 1390–1396.Google Scholar
  94. Man In’t Veld, WA, Rosendahl KCHM, Van Rijswick, PCJ, Meffert, JP, Westenberg, M, et al. (2015) Phytophthora terminalis sp. nov. and Phytophthora occultans sp. nov., two invasive pathogens of ornamental plants in Europe. Mycologia 107: 54–65.Google Scholar
  95. Man In’t Veld, WA (2007) Gene flow analysis demonstrates that Phytophthora fragariae var. rubi constitutes a distinct species, Phytophthora rubi comb. nov. Mycologia 99: 222–226.Google Scholar
  96. Martin, FN, Abad, ZG, Balci, Y, Ivors, K (2012) Identification and detection of Phytophthora: reviewing our progress, identifying our needs. Plant Disease 96: 1080–1103.PubMedGoogle Scholar
  97. Martin, FN, Blair, JE, Coffey, MD (2014) A combined mitochondrial and nuclear multilocus phylogeny of the genus Phytophthora. Fungal Genetics and Biology 66: 19–32.PubMedGoogle Scholar
  98. Martin, FN, Tooley, PW (2003) Phylogenetic relationships among Phytophthora species inferred from sequence analysis of mitochondrially encoded cytochrome oxidase, I and, II genes. Mycologia 95: 269–284.PubMedGoogle Scholar
  99. Maseko, B, Burgess, TI, Coutinho, TA, Wingfield, MJ (2007) Two new Phytophthora species from South African Eucalyptus plantations. Mycological Research 111: 1321–1338.PubMedGoogle Scholar
  100. Mcrae, W (1918) Phytophthora meadii n. sp. on Hevea brasiliensis. Memoirs of the Department of Agriculture in India, Botanical Series 9: 219–273.Google Scholar
  101. Mirabolfathy, M, Cooke, DEL, Duncan, JM, Williams, NA, Ershad, D, et al. (2001) Phytophthora pistaciae sp. nov. and, P melonis: the principal causes of pistachio gummosis in Iran. Mycological Research 105: 1166–1175.Google Scholar
  102. Mostowfizadeh-Ghalamfarsa, R, Cooke, DEL, Banihashemi, Z (2008) Phytophthora parsiana sp. nov., a new high-temperature tolerant species. Mycological Research 112: 783–794.PubMedGoogle Scholar
  103. Naher, M, Motohash, K, Watanabe, H, Chikuo, Y, Senda, M, et al. (2011) Phytophthora chrysanthemi sp. nov., a new species causing root rot of chrysanthemum in Japan. Mycological Progress 10: 21–31.Google Scholar
  104. Nechwatal, J, Bakonyi, J, Cacciola, SO, Cooke, DEL, Jung, T, et al. (2013) The morphology, behaviour and molecular phylogeny of Phytophthora taxon Salixsoil and its redesignation as Phytophthora lacustris sp. nov. Plant Pathology 62: 355–369.Google Scholar
  105. Nelson, SC, Abad, ZG (2010) Phytophthora morindae, a new species causing black flag disease on noni Morinda citrifolia L.) in Hawaii. Mycologia 102: 122–134.PubMedGoogle Scholar
  106. Nirenberg, HI, Gerlach, WF, Graefenhan, T (2009) Phytophthora xpelgrandis, a new natural hybrid pathogenic to Pelargonium grandiflorum hort. Mycologia 101: 220–231.PubMedGoogle Scholar
  107. Oliva, RF, Kroon LPNM, Chacon, G, Flier, WG, Ristaino, JB, et al. (2010) Phytophthora andina sp. nov., a newly identified heterothallic pathogen of solanaceous hosts in the Andean highlands. Plant Pathology 59: 613–625.Google Scholar
  108. Oudemans, P, Coffey, MD (1991) A revised systematics of twelve papillate Phytophthora species based on isozyme analysis. Mycological Research 95: 1025–1046.Google Scholar
  109. Pânek, M, Fér, T, Mrâcek, J, Tomsovsky, M (2016) Evolutionary relationships within the Phytophthora cactorum species complex in Europe. Fungal Biology 120: 836–851.PubMedGoogle Scholar
  110. Park, B, Martin, F, Geiser, DM, Kim, HS, Mansfield, MA, et al. (2013) Phytophthora database 2.0: update and future direction. Phytopathology 103: 1204–1208.PubMedGoogle Scholar
  111. Petersen, HE (1910) An account of Danish freshwater-phycomycetes, with biological and systematical remarks. Annales Mycologici 8: 494–560.Google Scholar
  112. Pethybridge, GH (1913) On the rotting of potato tubers by a new species of Phytophthora having a method of sexual reproduction hitherto undescribed. Scientific Proceedings of the Royal Dublin Society 13: 529–565.Google Scholar
  113. Pethybridge, GH, Lafferty, AH (1919) A disease of tomato and other plants caused by a new species of Phytophthora. Scientific Proceedings of the Royal Dublin Society 15: 487–505.Google Scholar
  114. Posada, D (2008) jModelTest: phylogenetic model averaging. Molecular Biology and Evolution 25: 1253–1256.Google Scholar
  115. Puglisi, I, De Patrizio, A, Schena, L, Jung, T, Evoli, M, et al. (2017) Two previously unknown Phytophthora species associated with brown rot of Pomelo (Citrus grandis) fruits in Vietnam. PLoS ONE 12: e0172085.Google Scholar
  116. Purss, GS (1957) Stem rot: a disease of cowpeas caused by an undescribed species of Phytophthora. Queensland Journal of Agricultural Science 14: 125–154.Google Scholar
  117. Raciborski, M (1900) Parasitische Algen und Pilze Java’s. Buitenzorg: Botanisches Institut.Google Scholar
  118. Rahman, MZ, Mukobata, H, Suga, H, Kageyama, K (2014a) Phytophthora asiatica sp. nov., a new species causing leaf and stem blight of kudzu in Japan. Mycological Progress 13: 759769.Google Scholar
  119. Rahman, MZ, Uematsu, S, Kimishima, E, Kanto, T, Kusunoki, M, et al. (2015) Two plant pathogenic species of Phytophthora associated with stem blight of Easter lily and crown rot of lettuce in Japan. Mycoscience 56: 419–433.Google Scholar
  120. Rahman, MZ, Uematsu, S, Takeuchi, T, Shirai, K, Ishiguro, Y, et al. (2014b) Two new species, Phytophthora nagaii sp. nov. and P. fragariaefolia sp. nov., causing serious diseases on rose and strawberry plants, respectively, in Japan. Journal of General Plant Pathology 80: 348–365.Google Scholar
  121. Rands, RD (1922) Streepkanker van Kaneel, Veroorzaakt Door Phytophthora cinnamomi n. sp. Batavia: Drukkerij Ruygrok.Google Scholar
  122. Rea, AJ, Burgess, TI, Hardy GESJ, Stukely, MJC, Jung, T (2011) Two novel and potentially endemic species of Phytophthora associated with episodic dieback of Kwongan vegetation in the south-west of Western Australia. Plant Pathology 60: 1055–1068.Google Scholar
  123. Rea, AJ, Jung, T, Burgess, TI, Stukely, MJC, Hardy GESJ (2010) Phytophthora elongata sp. nov., a novel pathogen from the Eucalyptus marginata forest of Western Australia. Australasian Plant Pathology 39: 477–491.Google Scholar
  124. Reeser, P, Sutton, W, Hansen, E (2013) Phytophthora pluvialis, a new species from mixed tanoak-Douglas-fir forests of western Oregon, U.S.A. North American Fungi 8: 1–8.Google Scholar
  125. Reeser, PW, Hansen, EM, Sutton, W (2007) Phytophthora siskiyouensis, a new species from soil, water, myrtlewood (Umbellularia californica) and tanoak (Lithocarpus densiflorus) in southwestern Oregon. Mycologia 99: 639–643.PubMedGoogle Scholar
  126. Rizzo, DM, Garbelotto, M, Davidson, JM, Slaughter, GW, Koike, ST (2002) Phytophthora ramorum as the cause of extensive mortality of Quercus spp. and Lithocarpus densiflorus in California. Plant Disease 86: 205–214.PubMedGoogle Scholar
  127. Rizzo, DM, Garbelotto, M, Hansen, EA (2005) Phytophthora ramorum: integrative research and management of an emerging pathogen in California and Oregon forests. Annual Review of Phytopathology 43: 309–335.PubMedGoogle Scholar
  128. Robideau, GP, De Cock AWAM, Coffey, MD, Voglmayr, H, Brouwer, H, et al. (2011) DNA barcoding of oomycetes with cytochrome c oxidase subunit, I and internal transcribed spacer. Molecular Ecology Resources 11: 1002–1011.PubMedPubMed CentralGoogle Scholar
  129. Ronquist, F, Teslenko, M, Van Der Mark, P, Ayres, DL, Darling, A, et al. (2012) MrBayes 3.2: efficient bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61: 539–542.PubMedPubMed CentralGoogle Scholar
  130. Safaiefarahani, B, Mostowfizadeh-Ghalamfarsa, R, Hardy, G, Burgess, TI (2015) Re-evaluation of the Phytophthora cryptogea species complex and the description of a new species, Phytophthora pseudocryptogea sp. nov. Mycological Progress 14: 108.Google Scholar
  131. Safaiefarahani, B, Mostowfizadeh-Ghalamfarsa, R, Hardy, GES, Burgess, TI (2016) Species from within the Phytophthora cryptogea complex and related species, P erythroseptica and P sansomeana, readily hybridize. Fungal Biology 120: 975–987.PubMedGoogle Scholar
  132. Sawada, K (1927) Descriptive catalogue of the Formosan fungi III. Report of the Department of Agriculture Government Research Institute of Formosa 27: 1–62.Google Scholar
  133. Scanu, B, Hunter, GC, Linaldeddu, BT, Franceschini, A, Maddau, L, et al. (2014) A taxonomic re-evaluation reveals that Phytophthora cinnamomi and P cinnamomi var. parvispora are separate species. Forest Pathology 44: 1–20.Google Scholar
  134. Scanu, B, Linaldeddu, BT, Deidda, A, Jung, T (2015) Diversity of Phytophthora species from declining Mediterranean maquis vegetation, including two new species, Phytophthora crassamura and P ornamentata sp. nov. PLoS ONE 10: e0143234.Google Scholar
  135. Schröter, J (1886) Die Pilze Schlesiens In: Kryptogamen-Flora von Schlesien (Cohn, F, ed.): 3 (1): 1–814. Breslau: J, U Kern’s Verlag.Google Scholar
  136. Scott, PM, Burgess, TI, Barber, PA, Shearer, BL, Stukely, MJC, et al. (2009) Phytophthora multivora sp. nov., a new species recovered from declining Eucalyptus, Banksia, Agonis and other plant species in Western Australia. Persoonia 22: 1–13.PubMedPubMed CentralGoogle Scholar
  137. Simamora, AV, Stukely, MJC, Hardy, GES, Burgess, TI (2015) Phytophthora boodjera sp. nov., a damping-off pathogen in production nurseries and from urban and natural landscapes, with an update on the status of P. alticola. IMA Fungus 6: 319335.Google Scholar
  138. Smith, RE, Smith, EH (1906) A new fungus of economic importance. Botanical Gazette 42: 215–221.Google Scholar
  139. Stamatakis, A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30: 1312–1313.PubMedPubMed CentralGoogle Scholar
  140. Swofford, DL (2002) PAUP*: phylogenetic analysis using parsimony (*and other methods). Sunderland, MA: Sinauer Associates.Google Scholar
  141. Taylor, PA, Pascoe, IG, Greenhalgh, FC (1985) Phytophthora clandestina sp. nov. in roots of subterranean clover. Mycotaxon 22: 77–85.Google Scholar
  142. Thaxter, R (1889) A new American Phytophthora. Botanical Gazette 14: 273–274.Google Scholar
  143. Thompson, A (1929) Phytophthora species in Malaya. The Malayan Agricultural Journal 17: 53–100.Google Scholar
  144. Tomlinson, JA (1952) Brown core root rot of Primula caused by Phytophthora primulae n. sp. Transactions of the British Mycological Society 35: 221–235.Google Scholar
  145. Tucker, CM (1931) Taxonomy of the Genus Phytopthora de Bary. Research Bulletin of the Missouri Agricultural Experiment Station 153: 1–208.Google Scholar
  146. Tucker, CM, Milbrath, JA (1942) Root rot of Chamaecyparis caused by a species of Phytophthora. Mycologia 34: 94–103.Google Scholar
  147. Turner, RS (2005) After the famine: Plant pathology, Phytophthora infestans, and the late blight of potatoes, 1845–1960. Historical Studies in the Physical and Biological Sciences 35: 341–370.Google Scholar
  148. Tyler, BM, Tripathy, S, Zhang, XM, Dehal, P, Jiang, RHY, et al. (2006) Phytophthora genome sequences uncover evolutionary origins and mechanisms of pathogenesis. Science 313: 1261–1266.PubMedPubMed CentralGoogle Scholar
  149. Uzuhashi, S, Tojo, M, Kakishima, M (2010) Phylogeny of the genus Pythium and description of new genera. Mycoscience 51: 337365.Google Scholar
  150. Vettraino, AM, Brasier, CM, Brown, AV, Vannini, A (2011) Phytophthora himalsilva sp. nov. an unusually phenotypically variable species from a remote forest in Nepal. Fungal Biology 115: 275–287.PubMedGoogle Scholar
  151. Villa, NO, Kageyama, K, Asano, T, Suga, H (2006) Phylogenetic relationships of Pythium and Phytophthora species based on ITS rDNA, cytochrome oxidase, II and beta-tubulin gene sequences. Mycologia 98: 410–422.PubMedGoogle Scholar
  152. Waterhouse, GM (1963) Key to the species of Phytophthora de Bary. Mycological Papers 92: 1–22.Google Scholar
  153. Weir, BS, Paderes, EP, Anand, N, Uchida, JY, Pennycook, SR, et al. (2015) A taxonomic revision of Phytophthora Clade 5 including two new species, Phytophthora agathidicida and P. cocois. Phytotaxa 205: 21–38.Google Scholar
  154. Werres, S, Marwitz, R, Man in’t Veld, WA, De Cock, AW, Bonants, PJ, et al. (2001) Phytophthora ramorum sp. nov., a new pathogen on Rhododendron and Viburnum. Mycological Research 105: 1155–1165.Google Scholar
  155. Yang, X (2014) New Species and Phylogeny of the Genus Phytophthora. PhD thesis, Virginia Tech.Google Scholar
  156. Yang, X, Balci, Y, Brazee, NJ, Loyd, AL, Hong, C (2016) A unique species in Phytophthora clade 10, Phytophthora intercalaris sp. nov., recovered from stream and irrigation water in the eastern USA. International Journal of Systematic and Evolutionary Microbiology 66: 845–855.PubMedPubMed CentralGoogle Scholar
  157. Yang, X, Copes, WE, Hong, CX (2013) Phytophthora mississippiae sp. nov., a new species recovered from irrigation reservoirs at a plant nursery in Mississippi. Journal of Plant Pathology & Microbiology 4: 180.Google Scholar
  158. Yang, X, Copes, WE, Hong, CX (2014a) Two novel species representing a new clade and cluster of Phytophthora. Fungal Biology 118: 72–82.PubMedGoogle Scholar
  159. Yang, X, Gallegly, ME, Hong, CX (2014b) A high-temperature tolerant species in clade 9 of the genus Phytophthora: P. hydrogena sp. nov. Mycologia 106: 57–65.PubMedGoogle Scholar
  160. Yang, X, Hong, C (2014) Halophytophthora fluviatilis sp. nov. from freshwater in Virginia. FEMS Microbiology Letters 352: 230–237.PubMedGoogle Scholar
  161. Yang, X, Hong, CX (2013) Phytophthora virginiana sp. nov., a high- temperature tolerant species from irrigation water in Virginia. Mycotaxon 126: 167–176.Google Scholar
  162. Yang, X, Richardson, PA, Hong, C (2014c) Phytophthora xstagnum nothosp. nov., a new hybrid from irrigation reservoirs at ornamental plant nurseries in Virginia. PLoS ONE 9: e103450.Google Scholar
  163. Ye, W, Wang, Y, Shen, D, Li, D, Pu, T, et al. (2016) Sequencing of the litchi downy blight pathogen reveals it is a Phytophthora species with downy mildew-like characteristics. Molecular Plant-Microbe Interactions 29: 573–583.PubMedGoogle Scholar

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