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Epitypification and phylogeny of Colletotrichum acutatum J.H. Simmonds

January 2008
Fungal Diversity 28

January 2008
28

Authors:

Roger Shivas

University of Southern Queensland

Rajesh Jeewon

University of Mauritius

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Simmonds introduced Colletotrichum acutatum in 1965, validated in 1968, with a broad concept, as demonstrated by the selection of several type specimens from a range of hosts. This has created some confusion in the species concept and identification of C. acutatum. There are no viable ex-type cultures of C. acutatum and furthermore there are no existing cultures of C. acutatum on Carica papaya from the type locality in south-east Queensland. The application of molecular phylogenetic studies to isolates of C. acutatum is only meaningful if the taxonomy is stable and species are properly named. In order to clarify the species concept of C. acutatum, an isolate of Colletotrichum acutatum from Carica papaya from Yandina in Southeast Queensland (Australia) is designated as an epitype. A detailed morphological description is provided. Phylogenies based on a combined ITS and beta-tubulin gene analysis indicate that C. acutatum bears close phylogenetic affinities to C. gloeosporioides and C. capsici. Results also indicate that C. acutatum is monophyletic and there is a close relationship between the epitype and other Australian C. acutatum isolates from Carica papaya. Molecular data, however did not provide further evidence to properly elucidate the taxonomie affinities of C. acutatum especially the holotype and epitype. Our studies indicate that given the complexity of the genus Colletotrichum, there is a need to check previously described type specimens and redesign neotypes where necessary in order to clarify taxonomie uncertainties.

Colletotrichum acutatum . A. Conidiogenous cell. B. Appressoria. C. Conidia. D & E. upward and reverse sides of culture on PDA 7-days after inoculation of epitype (BRIP 28519) (Bar = 15 μm).

…

. The type specimens of Colletotrichum acutatum (Simmonds 1968)

…

Phylogram of one of twelve trees generated from parsimony analysis based on rDNA-ITS sequences of Colletotrichum acutatum isolates (TL = 104.00, CI = 0.885, RI = 0.987, RC = 0.873, HI = 0.115). Data were analysed with random addition sequence, weighed parsimony and treating gap as missing data. Values above branching node indicate bootstrap supports obtained from bootstrap analysis with 1000replicates. (Bar = 1 % sequence divergence).

…

continued). Sources of isolates used in this study and reference sequences from Gen Bank used in analysis

…

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Fungal Diversity

Epitypification and phylogeny of Colletotrichum acutatum J.H. Simmonds

Than, P.P.1,2, Shivas, R.G.4, Jeewon, R.3, Pongsupasamit, S.2, Marney, T.S.4, Taylor, P.W.J.5

and Hyde, K.D.6,7*

1Mushroom Research Centre, 128 Moo3 T. Pa Pae, A. Mae Taeng, Chiang Mai 50150, Thailand

2Department of Agronomy, Maejo University, Sansai, Chiang Mai 50290, Thailand

3Centre for Research in Fungal Diversity, School of Biological Sciences, The University of Hong Kong, Pokfulam

Road, Hong Kong SAR, PR China

4Plant Pathology Herbarium, Department of Primary Industries & Fisheries, Indooroopilly, Queensland 4068, Australia

5BioMarka, School of Agriculture and Food Systems, The University of Melbourne, Victoria 3010, Australia

6International Fungal Research & Development Centre, The Research Institute of Resource Insects, Chinese Academy

of Forestry, Balonssi, Kunming 650224, PR China

7School of Science, Mae Fah Luang University, Tasud, Chiang Rai 57100, Thailand

Than, P.P., Shivas, R.G., Jeewon, R., Pongsupasamit, S., Marney, T.S., Taylor, P.W.J. and Hyde, K.D. (2008).

Epitypification and phylogeny of Colletotrichum acutatum J.H. Simmonds. Fungal Diversity 28: 97-108.

Simmonds introduced Colletotrichum acutatum in 1965, validated in 1968, with a broad concept, as demonstrated by

the selection of several type specimens from a range of hosts. This has created some confusion in the species concept

and identification of C. acutatum. There are no viable ex-type cultures of C. acutatum and furthermore there are no

existing cultures of C. acutatum on Carica papaya from the type locality in south-east Queensland. The application of

molecular phylogenetic studies to isolates of C. acutatum is only meaningful if the taxonomy is stable and species are

properly named. In order to clarify the species concept of C. acutatum, an isolate of Colletotrichum acutatum from

Carica papaya from Yandina in Southeast Queensland (Australia) is designated as an epitype. A detailed morphological

description is provided. Phylogenies based on a combined ITS and beta-tubulin gene analysis indicate that C. acutatum

bears close phylogenetic affinities to C. gloeosporioides and C. capsici. Results also indicate that C. acutatum is

monophyletic and there is a close relationship between the epitype and other Australian C. acutatum isolates from

Carica papaya. Molecular data, however did not provide further evidence to properly elucidate the taxonomic affinities

of C. acutatum especially the holotype and epitype. Our studies indicate that given the complexity of the genus

Colletotrichum, there is a need to check previously described type specimens and redesign neotypes where necessary in

order to clarify taxonomic uncertainties.

Key words: Carica papaya, Colletotrichum acutatum, epitype, plant pathogen, taxonomy

Article Information

Received 13 November 2007

Accepted 20 December 2007

Published online 31 January 2008

*Corresponding author: Kevin D Hyde: e-mail: kdhyde1@gmail.com

Introduction

The taxonomy of Colletotrichum

acutatum is ambiguous (Sreenivasaprasad and

Talhinhas, 2005). The broad putative host

range has created problems for plant

pathologists who need to identify specific plant

pathogens for disease management. Molecular

techniques have provided additional data for

solving problems in fungal identification, and

have been applied to taxonomically difficult

genera including Fusarium (O’Donnell et al.,

1998, Maxwell et al., 2006), Pestalotiopsis

(Jeewon et al., 2002, 2003a,b, 2004, Lui et al.,

2007), Mycosphaerella and its anamorphs

(Crous et al., 2000; Mancini et al., 2005), and

to a lesser extent to Colletotrichum (Sreeni-

vasaprasad et al., 1996; Moriwaki et al., 2002;

Du et al., 2005; Photita et al., 2005; Than et

al., 2007). Gene sequence data is increasingly

used to solve taxonomic problems from species

level through to higher taxonomic levels.

However these studies are generally flawed by

the fact the type species have not been studied.

Table 1. The type specimens of Colletotrichum acutatum (Simmonds 1968)

QDPI&F

Plant

Disease

Log Book

No.

BRIP (ex BRIU)

Specimen type

IMI

accession no

Geographic location/ date of

collection/

collector

Host plant

16741B1 BRIP 4693

(ex BRIU 2437)

Microscope slide

Isotype

IMI 117617

Holotype

Ormiston*, Brisbane, Queensland,

Australia/ J.H.Simmonds / 1 Oct. 1965

Carica papaya

16741B Not held in BRIP

(ex BRIU 2431)

Isoparatype

IMI 117618

Paratype

Ormiston*, Brisbane, Queensland,

Australia/ J.H.Simmonds / 1 Oct. 1965

Carica papaya

16741A -

pink type

Not held in BRIP

(ex BRIU 2432)

Isoparatype

IMI 117619

Paratype

Ormiston*, Brisbane, Queensland,

Australia/ J.H.Simmonds / 1 Oct. 1965

Carica papaya

16633D –

pink type

BRIP 49837

(ex BRIU 2435)

Dried culture plates

Isoparatype

IMI 117620

Paratype

Ormiston*, Brisbane, Queensland,

Australia/ J.H.Simmonds / 5 Jul. 1965

Carica papaya

16633A BRIP 49838

(ex BRIU 2434)

Dried culture plates

Isoparatype

IMI 117621

Paratype

Ormiston*, Brisbane, Queensland,

Australia/ J.H.Simmonds / 5 Jul. 1965

Carica papaya

11711A BRIP 4684, BRIP 11083

(ex BRIU 2433)

Dried culture plates and

living culture

Isoparatype

IMI 117622

Paratype

Eight Mile Plains, Brisbane,

Queensland, Australia/

J.H.Simmonds / 14 Jul. 1955

Capsicum

frutescens

16738C –

pink type

BRIP 4697

(ex BRIU 2436)

Dried culture plates

Isoparatype

IMI 117623

Paratype

Nambour, Queensland, Australia/

K.G.Pegg / 1 Oct. 1965

Delphinium sp.

13483-0 BRIP 11084

Non-viable lyophilized

culture

Topotype

- Ormiston*, Brisbane, Queensland,

Australia/ J.H.Simmonds / 29 Jan.

1959

Carica papaya

Further more, species in the taxonomically

different genera are often identified without

reference to the type specimens (e.g.

characterization of causal agents from chilli

anthracnose in Thailand by Than et al., 2007)

and one must question whether the taxon was

correctly identified. No matter how many

strains of fungi are sequenced, unless the type

material is examined, taxonomic implications

are speculative and conclusions are weak

because there is no certainty that the strains

used represent the type of the species or genus.

In order to stabilize the application of the

species names, it is necessary to examine and

sequence types (preferably the holotype or

isotypes) if they exist. If this is not possible

then it may be necessary to examine paratypes

or even to designate an epitype that clearly

represents the type species.

When Simmonds (1965) initially

published the name Colletotrichum acutatum

he omitted to designate a type specimen. In

order to rectify this Simmonds (1968) listed a

holotype (IMI 117617) and six paratypes (IMI

117618-117623) with the corresponding iso-

type and six isoparatypes grouped together

(BRIU 2431-2437). Importantly, Simmonds’

type specimens were selected from three hosts:

the holotype and four paratypes from Carica

papaya, and a paratype from each of Capsicum

frutescens and Delphinium ajacis. Unfortu-

nately this was not made clear when he listed

Fungal Diversity

the type specimens (Simmonds, 1968). All of

the specimens were dried agar cultures. The

BRIU specimens were subsequently incorpo-

rated into herbarium BRIP. All of these type

specimens have been examined during this

study and corresponding IMI and BRIP

accession numbers were tabulated (Table 1).

Two of the type specimens (dried cultures) viz.

the holo-type (IMI 117617) and the paratype

(IMI 117619), both from Carica papaya, have

been subjected to phylogenetic analysis

specifically of the rDNA ITS region (Vinnere

et al., 2001).

Simmonds (unpublished correspondence

with IMI) chose type specimens that showed

the range of characters he considered

represented the inherent variability of this

taxon. Simmonds’ (1965) concept of

Colletotrichum acutatum was that it had

conidia that were variable in length and

infected a range of hosts, causing particularly

serious diseases on papaya and strawberry. The

distinguishing morphological character was

that the conidia had pointed ends.

In our view, Simmonds’ (1965, 1968)

broad concept of Colletotrichum acutatum, as

demonstrated by the selection of several type

specimens from a range of hosts, has created

uncertainties in the species concept of C.

acutatum. There are no viable ex-type cultures

of Colletotrichum acutatum and further there

are no viable cultures of Colletotrichum

acutatum on papaya from the type locality

(Queensland Department of Primary Industries

& Fisheries, Redlands Research Station,

Ormiston, Brisbane, Queensland, Australia).

Article 9.7 of the International Code of

Botanical Nomenclature (Vienna Code, 2006)

states that “An epitype is a specimen or

illustration selected to serve as an interpretative

type when the holotype, lectotype, or

previously designated neotype, or all original

material associated with a validly published

name, is demonstrably ambiguous and cannot

be critically identified for purposes of the

precise application of the name of a taxon.

When an epitype is designated, the holotype,

lectotype, or neotype that the epitype supports

must be explicitly cited.” We have conse-

quently chosen an isolate of C. acutatum (BRIP

28519) from Carica papaya from Yandina in

South-east Queensland (Australia) to represent

the epitype of C. acutatum. In addition,

phylogenetic analyses from DNA sequences

generated from the rDNA-ITS regions and β-

tubulin gene were performed to investigate the

relationships with other closely related species.

Description

Colletotrichum acutatum J.H. Simmonds,

Queensland J. Agric. Anim. Sci. 25: 178A

(1968).

= Colletotrichum acutatum J.H. Simmonds,

Queensland J. Agric. Anim. Sci. 22: 458 (1965), nom.

inval.

Holotype: AUSTRALIA, Queensland, Brisbane,

Ormiston, Redlands Research Station, on Carica

papaya, 1 Oct. 1965, J.H. Simmonds. (IMI 117617;

isotype BRIP 4693 ex BRIU 2437).

Epitype: MycoBank: 511272. AUSTRALIA,

Queensland, Yandina, on fruit of Carica papaya, May

1987, L.M. Coates, specimen of living culture stored at

QDPI&F Plant Pathology Herbarium, Indooroopilly,

Australia (BRIP 28519); ex-epitype living culture in

Biotech Culture Collection, Thailand (BCC 28680),

Centraalbureau voor Schimmelcultures, Netherlands

(CBS122122), The University of Hong Kong Culture

Collection, the University of Hong Kong, Hong Kong

(HKUCC 10928), Korean Agricultural Culture

Collection (KACC 43258) and International Collection

of Microorganisms from Plants (ICMP 17298).

Colonies on PDA circular, raised, at first

orange-white, sometimes grey and becoming

pale orange with age, aerial mycelia white,

dense, cottony without visible conidial masses,

reverse bright orange but sometimes yellowish-

brown to olive-brown, very slow-growing with

growth rate of 2.3-2.6 mm (

= 2.5 ± 0.14, n =

5) (Fig. 1). Sclerotia absent. Acervuli absent in

culture. Setae absent. Conidiophores 3-45 µm

long (

= 20 ± 13.44, n = 10) × 2-6 µm wide

(

= 4 ± 1.58, n = 10) hyaline, cylindrical,

unicellular common, but sometimes septate,

single common, but sometimes aggregated and

branched, tapering towards the end, acute at the

apex. Conidiogenous cells 6-10 µm long (

8 ± 1.13, n = 10) × 2.5-4 µm wide (

= 3 ±

0.42, n = 10) hyaline, ellipsoidal to subglobose,

smooth, tapering towards a truncate apex.

Conidia common in mycelium 7-14 µm long

(

= 10 ± 1.67, n = 20) × 2.5-3.5 µm wide (

= 3 ± 0.18, n = 20), one-celled, gluttulate,

hyaline, fusiform with both ends pointed.

Appressoria in slide cultures 7-15 µm long

100

Table 2. Sources of isolates used in this study and reference sequences from Gen Bank used in analysis

Culture collection

accession number

Gene bank

Acc# ITS β- tubulin Isolates / source Colletotrichum

species Location Host

BCC 28680 EF143974 EF143970 BRIP28519/ Than et al., 2007 C. acutatum Yandina, QLD, Australia Carica papaya

CBS 122122

ICMP 17298

HKUCC 10928

KACC 43258

- EF143975 - BRIP28517/ Than et al., 2007 C. acutatum Yandina, QLD, Australia Carica papaya

- EF143971 EF143967 BRIP4703/ Than et al., 2007 C. acutatum Townsville, QLD, Australia Fragaria ananassa

- EF143972 EF143968 BRIP4704/ Than et al., 2007 C. acutatum Forest Glen, QLD, Australia Fragaria ananassa

- EF143973 EF143969 BRIP11086/ Than et al., 2007 C. acutatum Nambour, QLD, Australia Fragaria ananassa

HKUCC 10891 DQ453418 DQ454066 S2/ Than et al., 2007 C. acutatum Chiangmai, Thailand Fragaria sp.

HKUCC 10872 DQ453419 DQ454063 S3/ Than et al., 2007 C. acutatum Chiangmai, Thailand Fragaria sp.

HKUCC 10873 DQ453420 DQ454062 S4/ Than et al., 2007 C. acutatum Chiangmai, Thailand Fragaria sp.

HKUCC 10890 DQ453421 DQ454065 S5/ Than et al., 2007 C. acutatum Chiangmai, Thailand Fragaria sp.

HKUCC 10814 DQ453422 DQ454064 S6/ Than et al., 2007 C. acutatum Chiangmai, Thailand Fragaria sp.

HKUCC 10871 DQ453423 DQ454067 S7/ Than et al., 2007 C. acutatum Chiangmai, Thailand Fragaria sp.

HKUCC 10848 DQ453406 DQ454058 Mj2/ Than et al., 2007 C. acutatum Chiangmai, Thailand Capsicum annuum

HKUCC 10865 DQ453407 - Mj3/ Than et al., 2007 C. acutatum Chiangmai, Thailand Capsicum annuum

HKUCC 10879 DQ453408 DQ454059 Mj4/ Than et al., 2007 C. acutatum Chiangmai, Thailand Capsicum annuum

HKUCC 10851 DQ453409 DQ454060 Mj5/ Than et al., 2007 C. acutatum Chiangmai, Thailand Capsicum annuum

HKUCC 10893 DQ453410 DQ454061 Mj6/ Than et al., 2007 C. acutatum Chiangmai, Thailand Capsicum annuum

HKUCC 10850 DQ453411 DQ454068 Mj9/ Than et al., 2007 C. acutatum Chiangmai, Thailand Capsicum annuum

HKUCC 10894 DQ453412 DQ454069 Mj10/ Than et al., 2007 C. acutatum Chiangmai, Thailand Capsicum annuum

- AY266405 - G2/Photita et al 2004 C. acutatum Thailand Fragaria sp.

- AB042301 - MAFF 306406/ Moriwaki et al, 2002 C. acutatum Japan Eriobotrya japonica

- AF411701 -

IMI 117619(holotype)/Vinnere et al, 2001 C. acutatum Australia Carica papaya

- AJ301921 -

BBA 70349/ Nirenberg et al., 2002 C. acutatum Indonesia Capsicum sp.

- AJ301920 -

BBA 70348/ Nirenberg et al., 2002 C. acutatum Indonesia Capsicum sp.

- AJ748617 - PR220/ Talhinhas et al., 2005 C. gloeosporioides Portugal Olea europaea

- AJ748616 - VM206/ Talhinhas et al., 2005 C. gloeosporioides Portugal Olea europaea

- AJ314718 - 8/ Talhinhas et al., 2002 Colletotrichum sp Australia Fragaria sp.

Fungal Diversity

101

Table 2 (continued). Sources of isolates used in this study and reference sequences from Gen Bank used in analysis

Culture collection

accession number

Gene bank

Acc# ITS β- tubulin Isolates / source Colletotrichum species Location Host

- AB255249 - JP18/Morakotkarn et al (unpublished) Colletotrichum sp. Japan Bambusa sp.

- AY266381 - ZE0040/Photita et al., 2004 C. gloeosporioides Thailand Fragaria sp.

- - AJ748633 CA455/ Talhinhas et al., 2002 C. acutatum United Kingdom Photinia sp.

- - AJ748611 PT186/ Talhinhas et al., 2005 C. acutatum Portugal Olea europaea

- - AJ748608 PT166/ Talhinhas et al., 2005 C. acutatum Portugal Olea europaea

- - AJ748607 PT135/ Talhinhas et al., 2005 C. acutatum Portugal Olea europaea

- - AJ748615 PT 201/ Talhinhas et al., 2005 C. acutatum Portugal Olea europaea

- - AJ748605 PT108/ Talhinhas et al., 2005 C. acutatum Portugal Olea europaea

- - AJ314722 1/ Talhinhas et al., 2005 Colletotrichum sp Portugal Lupinus albus

- - AJ409300 3/ Talhinhas et al., 2005 C. acutatum Portugal Lupinius albus

- - AJ409296

99/ Talhinhas et al., 2005 C. acutatum USA Fragaria sp.

- - AJ748636 PD88-673 / Talhinhas et al., 2002 C. acutatum Netherlands Anemone sp.

- - AJ314716 20/ Talhinhas et al., 2002 Colletotrichum sp. Portugal Fragaria sp

- - AJ409298 2/ Talhinhas et al., 2002 Colletotrichum sp. Portugal Lupinus albus

- - AJ300709 15/ Talhinhas et al., 2002 Colletotrichum sp. Portugal Lupinus albus

- - AJ314712 29 /Talhinhas et al., 2002 Colletotrichum sp Portugal Lupinus sp.

- - AJ314720 PT232/Talhinhas et al., 2002 C. acutatum Portugal Olea europaea

- - AJ748632 PD85-694/ Talhinhas et al., 2005 C. acutatum Netherlands Chrysanthemum sp.

- - AJ748635 PD89-582/Talhinhas et al., 2005 C. acutatum Netherlands Cyclamen sp.

HKUCC 10883 DQ453992 DQ454036 Ku2/ Than et al., 2007 C. gloeosporioides Ratchaburi, Thailand Capsicum annuum

HKUCC 10864 DQ453995 DQ454030 Ku5/ Than et al., 2007 C. gloeosporioides Kanchanaburi, Thailand Capsicum annuum

HKUCC 10889 DQ453996 DQ454034 Ku6/ Than et al., 2007 C. gloeosporioides Kanchanaburi, Thailand Capsicum annuum

HKUCC 10860 DQ453401 DQ454043 M1/ Than et al., 2007 C. gloeosporioides Chiangmai, Thailand Mangifera indica

HKUCC 10861 DQ453402 - M2/ Than et al., 2007 C. gloeosporioides Chiangmai, Thailand Mangifera indica

HKUCC 10862 DQ453403 - M3/ Than et al., 2007 C. gloeosporioides Chiangmai, Thailand Mangifera indica

HKUCC 10863 DQ453404 DQ454046 M4/ Than et al., 2007 C. gloeosporioides Chiangmai, Thailand Mangifera indica

HKUCC 10849 DQ453405 DQ454047 M5/ Than et al., 2007 C. gloeosporioides Chiangmai, Thailand Mangifera indica

HKUCC 10876 DQ453427 DQ454050 U10/ Than et al., 2007 C. capsici Ubonrachathani, Thailand Capsicum annuum

HKUCC 10867 DQ453428 DQ454051 U12/ Than et al., 2007 C. capsici Ubonrachathani, Thailand Capsicum annuum

HKUCC 10852 DQ453414 DQ454056 R5/ Than et al., 2007 C. capsici Chiangmai, Thailand Capsicum annuum

102

Table 2 (continued). Sources of isolates used in this study and reference sequences from Gen Bank used in analysis

Culture collection

accession number

Gene bank

Acc# ITS β- tubulin Isolates / source Colletotrichum species Location Host

HKUCC 10869 DQ453415 DQ454053 R7/ Than et al., 2007 C. capsici Chiangmai, Thailand Capsicum annuum

HKUCC 10870 DQ453416 DQ454049 R11/ Than et al., 2007 C. capsici Chiangmai, Thailand Capsicum annuum

HKUCC 10880 DQ453417 - R12/ Than et al., 2007 C. capsici Chiangmai, Thailand Capsicum annuum

HKUCC 10857 DQ453988 DQ454047 Ccmj3/ Than et al., 2007 C. capsici Chiangmai, Thailand Capsicum annuum

HKUCC 10859 DQ453990 DQ454054 Ccmj10/ Than et al., 2007 C. capsici Chiangmai, Thailand Capsicum annuum

HKUCC 10855 DQ453424 DQ454052 Skp4 / Than et al., 2007 C. capsici Chiangmai, Thailand Capsicum annuum

- AY376544 AY376591 STE-U5291/ Lubbe et al., 2004 C. gloeosporioides USA Fragaria sp.

- AY376508 AY376556 STE-U5303/ Lubbe et al., 2004 C. acutatum India Hevea brasiliensis

- AY376526 AY376574 STE-U5304/ Lubbe et al., 2004 C. capsici Tanzania Arachis hypogaea

- AY376510 AY376558 STE-U5292/ Lubbe et al., 2004 Glomerella acutata South Africa Olea europaea

- AY376525 AY376573 STE-U2289/ Lubbe et al., 2004 C. boninense - -

AJ749679 AJ748636 PD-88-673/ Talhinhas et al., 2005 C. acutatum Netherlands Anemone sp.

BRIP: Queensland Department of Primary Industries Plant Pathology Herbarium; CAB: Centraalbureau voor Schimmelcultures, Netherlands; HKUCC: The University of Hong

Kong Culture Collection, The University of Hong Kong, Hong Kong; KACC: Korean Agricultural Culture Collection; ICMP: International Collection of Microorganisms from

Plants; STE-U: University of Stellenbosch Culture Collection.

Fungal Diversity

103

Fig. 1. Colletotrichum acutatum. A. Conidiogenous cell. B. Appressoria. C. Conidia. D & E. upward and reverse sides

of culture on PDA 7-days after inoculation of epitype (BRIP 28519) (Bar = 15 µm).

(

= 10.5 ± 2.46, n = 20) × 5-8 µm long (

= 6

± 0.84, n = 20), dark brown, ovate, clavate and

sometimes irregularly lobed. Supporting

hyphae hyaline, branched and septate.

Additional specimens examined: AUSTRALIA,

Queensland, Brisbane, Ormiston, Redlands Research

Station, on Carica papaya, 1 Oct. 1965, J.H. Simmonds

(paratype in IMI 117618, ex BRIU 2431, not held in

BRIP); Queensland, Brisbane, Ormiston, Redlands

Research Station, on Carica papaya, 1 Oct. 1965, J.H.

Simmonds (paratype IMI 117619, ex BRIU 2432, not

held in BRIP); Queensland, Brisbane, Ormiston,

Redlands Research Station, on Carica papaya, 5 Oct.

1965, J.H. Simmonds (paratype BRIP 49837 ex BRIU

2435, IMI 117620); Queensland, Brisbane, Ormiston,

Redlands Research Station, on Carica papaya, 5 Oct.

1965, J.H. Simmonds (paratype in BRIP 49838 ex

BRIU 2434, IMI 117621); Queensland, Brisbane, Eight

Mile Plains, on Capsicum frutescens, 14 Jul. 1955, J.H.

Simmonds (paratype BRIP 4684 = BRIP 11083 ex

BRIU 2433, IMI 117622); Queensland, Nambour, on

Delphinium ajacis, 1 Oct. 1965, K.G. Pegg (paratype

BRIP 4697 ex BRIU 2436, IMI 117623); Queensland,

Upper Ross River, Townsville, on Fragaria ananassa,

May 1971, W. Pont (BRIP 4703); Queensland, Forest

Glen, Sep. 1972, R.A. Peterson, (BRIP 4704);

Queensland, Nambour, Mar. 1965, K.G. Pegg (BRIP

11086); THAILAND, Chiangmai, Mae Jo-Sansai Street,

Mae Doo, on Capsicum annuum, 24 Sep. 2005, P.P.

Than (HKUCC 10848, HKUCC 10865, HKUCC 10879,

HKUCC 10851, HKUCC 10893, HKUCC 10850).

Phylogenetic assessment of Colletotrichum

acutatum epitype

The phylogeny of the epitype and closely

related species were investigated using

individual and combined sequence analyses of

nuclear ribosomal DNA (ITS rDNA) and beta

tubulin gene fragments. ITS ribosomal DNA

based phylogenies indicate that all C. acutatum

104

Fig. 2. Phylogram of one of twelve trees generated from parsimony analysis based on rDNA-ITS sequences of Colletotrichum acutatum isolates (TL =

104.00, CI = 0.885, RI = 0.987, RC = 0.873, HI = 0.115). Data were analysed with random addition sequence, weighed parsimony and treating gap as

missing data. Values above branching node indicate bootstrap supports obtained from bootstrap analysis with 1000replicates. (Bar = 1 % sequence

divergence).

BRIP 28519 EPITYPE Carica

a Australia

AY266405 Fra

aria s

. Thailand

AB042301 Fragaria sp. Japan

S5 BRIP 28517 Carica papaya Australia

5 Ca

sicum annuum Thailand

AF411701 HOLOTYPE Carica papaya Australia

AJ301921

AJ301920

2 Ca

sicum annuum Thailand

BRIP 11086

BRIP 4703

BRIP 4704

AY177317

AY177316

AY177318

AB255249

Ku6

Ku2

AY266381

U10

U12

Ccm

R12

AY376526

AY376525

. boninense

100

Fragaria sp. Thailand

Capsicum annuum Thailand

Capsicum annuum Indonesia

C. acutatum

C. capsici

Fragaria sp. Australia

Fungal Diversity

105

Fig. 3. Phylogram of one of four trees generated from parsimony analysis based on β-tubulin (tub2) sequences of

Colletotrichum acutatum isolates (TL=104.00, CI=0.885, RI=0.987, RC=0.873, HI=0.115). Data were analysed with

random addition sequence, weighed parsimony and treating gap as missing data. Values above branching node indicate

bootstrap support obtained from 1000replicates. Tree is rooted with Colletotrichum boninense. (Bar = 1 % sequence

divergence).

AJ748633 Photinia sp. UK

AJ748611 Olea europaea Portugal

AJ748608 Olea europaea Portugal

AJ748607 Olea europaea Portugal

AJ748615 Olea europaea Portugal

AJ748605 Olea europaea Portugal

AJ314722 Lupinus albus Portugal

AY376556 Hevea brasiliensis India

AJ409300 Lupinus albus Portugal

S5 F ragaria sp. Thailand

S7 Fragaria sp. Thailand

S3 Fragaria sp. Thailand

AJ409296 Fragaria sp. USA

AJ748636 Anemone sp. Netherlands

S6 Fragaria sp. Thailand

S2 Fragaria sp. Thailand

S4 Fragaria sp. Thailand

AJ314716 Fragaria sp. Portugal

Mj6 Capsicum annuum Thailand

Mj10 Capsicum annuum Thailand

Mj5 Capsicum annuum Thailand

Mj4 Capsicum annuum Thailand

Mj9 Capsicum annuum Thailand

Mj2 Capsicum annuum Thailand

AJ409298 Lpinus albus Portugal

AJ300709 Lupinus albus Portugal

AJ314712 Lupinus albus Portugal

AJ314720 Olea europaea Portugal

AJ748632 Chrysanthemum sp. Netherlands

BRIP 4703 Fragaria sp. Australia

BRIP 11086 Fragaria sp. Australia

BRIP 4704 Fragaria sp. Australia

BRIP 28519 Carica papaya Australia

AJ748635 Cyclamen sp. Netherlands

AY376570 Colletotrichum boninense

100

III

EPITYPE

106

Fig. 4. Phylogram of single tree generated from parsimony analysis based on rDNA ITS and b-tubulin (tub2) sequences

of Colletotrichum acutatum isolates (TL = 540, CI = 0.830, RI = 0.958, RC = 0.843, HI = 0.120). Data were analysed

with random addition sequence, weighed parsimony and treating gap as missing data. Values above branching node

indicate bootstrap supports obtained from 1000replicates. (Bar = 10 % sequence divergence).

strains, including the holotype sequence (AF

411701) from Capsicum, Carica papaya and

Fragaria hosts constitute a strongly supported

monophyletic clade (100% BS, Fig 2). Within

this monophyletic clade, there are 3 subclades,

albeit poorly supported. In particular it is noted

that BRIP 28517 and the holotype are in

different subclades although they have been

isolated from the same host and region. The

basal subclade consists of BRIP 11086, BRIP

4703 and BRIP 4704, which were all isolated

from Fragaria. Conclusive relationships based

on host associations of C. acutatum is unwise

as there are a number of isolates that have been

isolated from Fragaria, but they cluster with

the epitype which has been isolated from

Carica papaya. Host fungal relationships based

on phylogeny have been discussed in detail in

Jeewon et al. (2004) and any association

between hosts and species within

Colletotrichum does not seem to be justified at

present.

In contrast, phylogeny from partial

sequences of beta-tubulin 2-gene analysis

depicts a slightly different result (Fig. 3). The

epitype clusters with other C. acutatum

S5 Fragaria sp. Thailand

STE-U 4459

Mj9

Mj6

Mj4

Mj5

BRIP 11086

BRIP 4703

BRIP 4704

BRIP 28519 EPITYPE

STE

U 5292

Ku6

Ku2

Ku5

STE-U 5291

U10

STE-U 5304

R11

Ccmj10

STE-U 2289 C. boninense

Fragaria sp. Thailand

Capsicum annuum Thailand

Fragaria sp. Australia

100

III

100

. acutatum

C. gloeosporioides

capsici

Carica papaya Australia

Carica

a Australia IV

Fungal Diversity

107

Australian isolates such as BRIP 11086, BRIP

4703 and BRIP 4704 with relatively high

support (87%). There is a similar phylogenetic

scenario from the combined dataset (Fig. 4). At

present, given the limited taxon sampling,

unknown or doubtful identify of other isolates,

any conclusive phylogenetic affinities of the

epitype could be misleading. Further studies,

are necessary to clarify intra-specific

phylogenetic relationships of Colletotrichum

acutatum. The designation of an epitype,

available as an ex-epitype culture at BRIP,

CBS, HKUCC, KACC and ICMP (Table 2)

will help remove ambiguity about the

application of the name C. acutatum.

The diversity of pathogenic species of

Colletotrichum in the South East Asian region

is largely underexplored (Photita et al., 2005).

In addition, species are morphologically

complex and inter (or infra) species classi-

fication has been hampered by either incom-

plete or inadequate characterization (Cannon et

al., 2000). A number of previously described

species are either in poor condition or cannot

provide essential data for molecular document-

tation. There is a need to review and redescribe

a number of previously described specimens

and in many cases, neotypes, lectotypes or

epitypes will have to be designated. This has

been established in Botryosphearia (Phillips et

al., 2007) and Diplodia (Alves et al., 2006).

This paper is a continuity of our previous effort

to revise economically important species of

Colletotrichum (Shenoy et al., 2007; Than et

al., 2007). In these studies we have identified

pitfalls with phylogenetic analyses and

previously described type specimens. With the

availability of epitypes from recent collections

and cultures derived from them, we believe that

this is an important direction in the systematics

of these fungi and hope that there will be a

steady progression in resolving their taxonomy.

Acknowledgements

We are grateful to Mushroom Research Founda-

tion, Chiangmai, Thailand and the ATSE Crawford

Fund, Australia for funding.

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May 1998

Phylogenetic relationships of the phytopathogenic Gibberella fujikuroi species complex were investigated by maximum parsimony analysis of DNA sequences from multiple loci. Gene trees inferred from the beta-tubulin gene exons and introns, mitochondrial small subunit (mtSSU) rDNA, and 5' portion of the nuclear 28S rDNA were largely concordant, and in a combined analysis, provide strong statistical support for a phylogeny consistent with species radiations in South America, Africa, and Asia. These analyses place the American clads as a monophyletic sister-group of an African-Asian clade. Africa is the most phylogenetically diverse area examined with 16 species, followed by America (12 species) and Asia (8 species). The biogeographic hypothesis proposed from the phylogenetic evidence is based primarily on the formation of natural barriers associated with the fragmentation of the ancient super-continent Gondwana. Discordance of the nuclear ribosomal internal transcribed spacer (ITS) based tree with gene trees from the other loci sequenced is due to nonorthologous ITS2 sequences. The molecular evidence suggests the divergent ITS2 types were combined by an ancient interspecific hybridization (xenologous origin) or gene duplication (paralogous origin) that predates the evolutionary radiation of the G. fujikuroi complex. Two highly divergent nonorthologous ITS2 types designated type I and type II were identified and characterized with conserved ITS and ITS2 type-specific polymerase chain reaction (PCR) primers and DNA sequence analysis. Only the major ITS2 type is discernible when conserved ITS primers are used; however, a minor ITS2 type was amplified from every strain tested with type-specific PCR primers. The evolutionary pattern exhibited by the major ITS2 type is homoplastic when mapped onto the species lineages inferred from the combined nuclear 28S rDNA, mtSSU rDNA, and beta-tubulin gene sequences. Remarkably, the data indicate the major ITS2 type has switched between a type I and type II sequence at least three times during the evolution of the G. fujikuroi complex, but neither type has been fixed in any of the 45 species examined. Twenty-six of the 45 species included in this study represent either new species (23 species), new combinations (F. bulbicola and F. phyllophilum), or a rediscovered species (F. lactis). The results further indicate that traditional sectional and species-level taxonomic schemes for this lineage are artificial and a more natural classification is proposed.

The genus Mycosphaerella and its anamorphs

Article

Full-text available

May 2000

More than 2000 names have been described in Mycosphaerella and Sphaerella (Dothideales). Based on various morphological features depicted by earlier workers, six sections are recognized in the genus. About 27 anamorph genera have been linked to Mycosphaerella, 23 of which are recognized here. Based on phylogenetic analyses of the ITS-1, 5.8S and ITS-2 DNA sequence data of 46 species of Mycosphaerella species (58 strains), one large cluster was distinguished containing primarily taxa with cercosporoid anamorphs, as well as another smaller cluster for species with Dissoconium anamorphs.

Multi-gene genealogies and morphological data support Diplodia cupressi sp. nov., previously recognized as D. pinea f. sp. cupressi, as a distinct species

Article

Full-text available

Oct 2006

The causal agent of Diplodia canker of cypress (Cupressus spp.) in the Mediterranean region was originally thought to represent a sub-population of the pine pathogen Diplodia pinea and was referred to as D. pinea f. sp. cupressi. In the USA a similar fungus causing canker and dieback of Juniperus spp. was referred to as Diplodia mutila (teleomorph: Botryosphaeria stevensii). The aim of this study was to characterise the cypress pathogen in terms of morphology and sequences of the ITS region, the beta-tubulin and translation elongation factor 1-alpha genes. Phylogenetic analyses showed that the cypress canker pathogen resides in a clade together with other Diplodia species. It is, however, distinct from both D. pinea and D. mutila and more closely related to Botryosphaeria tsugae. The distinct phylogenetic position is supported by differences in conidial morphology and it is, therefore, described as Diplodia cupressi sp. nov.

Characterization and pathogenicity of Colletotrichum species associated with anthracnose on chilli (Capsicum spp.) in Thailand

Article

Full-text available

Jan 2008
PLANT PATHOL

Fungal isolates from chilli (Capsicum spp.) fruits in Thailand that showed typical anthracnose symptoms were identified as Colletotrichum acutatum, C. capsici and C. gloeosporioides. Phylogenetic analyses from DNA sequence data of ITS rDNA and β-tubulin (tub2) gene regions revealed three major clusters representing these three species. Among the morphological characters examined, colony growth rate and conidium shape in culture were directly correlated with the phylogenetic groupings. Comparison with isolates of C. gloeosporioides from mango and C. acutatum from strawberry showed that host was not important for phylogenetic grouping. Pathogenicity tests validated that all three species isolated from chilli were causal agents for chilli anthracnose when inoculated onto fruits of the susceptible Thai elite cultivar Capsicum annuum cv. Bangchang. Cross-infection potential was shown by C. acutatum isolates originating from strawberry, which produced anthracnose on Bangchang. Interestingly, only C. acutatum isolates from chilli were able to infect and produce anthracnose on PBC 932, a resistant genotype of Capsicum chinense. This result has important implications for Thai chilli breeding programmes in which PBC 932 is being hybridized with Bangchang to incorporate anthracnose resistance into chilli cultivars.

Type specimens of Colletotrichum gloeosporioides var. minor and Colletotrichum acutatum

Article

Jan 1968

J.H. Simmonds

A study of the Colletotrichum causing ripe fruit rots in Queensland

Article

Jan 1965

J.H. Simmonds

The causal agent of anhracnose of Rhododendron in Sweden and Latvia

Article

Jan 2002
MYCOL RES

Anthracnose caused by Colletotrichum is a severe foliar disease in rhododendron plantations in Sweden and Latvia. Isolates of this pathogen were collected and characterised based on morphological and molecular criteria. Out of 37 isolates examined, two with falcate spores were identified as C. dematium. The remainder of the isolates had straight cylindrical conidia, which were too variable to be reliably assigned to C. gloeosporioides (syn. C. azaleae) the reported causal agent of anthracnose of Rhododendron spp. These isolates were compared with the reference strains of C. gloeosporioides, with holo- and paratypes and with reference isolates of C. acutatum. The light and scanning electron microscopy examinations revealed that conidial shape was not a reliable criterion for separation of these two taxa and for the identification of our isolates. The two internal transcribed spacers (ITS1 and ITS2) and the 5.8S rRNA gene were PCR amplified and sequenced from all the rhododendron isolates and the reference strains, including the holo-and paratype materials. In addition, a segment of mitochondrial small subunit ribosomal DNA (mtSSU rDNA) and a fragment of a β-tubulin gene from several representatives of isolates of rhododendron as well as the reference strains were amplified and sequenced. The sizes of the amplified fragments among the isolates studied were heterogeneous only for mtSSU rDNA, which allowed separation of C. acutatum from C. gloeosporioides. Parsimony analysis of the individual and combined nucleotide sequence data sets were concordant and indicated that all isolates originating from rhododendrons belonged to C. acutatum. The grouping of the isolates was further supported by bootstrap analysis. Thus, C. acutatum was identified as the causal agent of anthracnose of Rhododendron in Sweden and Latvia. To our knowledge, this is the first report of C. acutatum and C. dematium on Rhododendron. This study is also the first to determine the genetic status of the holotype of C. acutatum and also one of the paratypes on the basis of ITS sequences in comparison with world-wide living isolates of this taxon.

Grouping of Colletotrichum Species in Japan Based on rDNA Sequences

Article

Dec 2002

Internal transcribed spacers (ITS) of the ribosomal RNA gene (rDNA) were sequenced for 236 isolates covering 25 Colletotrichum species collected in Japan. The Japanese isolates could be grouped into 20 ribosomal groups (RGs) based on the sequences of ITS1, correlating the species identified by the morphology. Colletotrichum gloeosporioides sensu lato separated into three RGs that were morphologically different. Colletotrichum destructivum, C. linicola and C. higginsianum were possibly conspecific. Colletotrichum dematium sensu lato including C. capsici and other species that produce falcate conidia except for graminicolous ones were separated into three RGs that were difficult to distinguish morphologically. In the phylogenetic study using ITS2 and the 28S rDNA domain 2 region, topologies compiled by neighbor-joining and maximum-parsimony methods were almost the same, reflecting the conidial morphology. The phylogenetic group 1 (PG1) produced conidia with acute ends, e.g., C. acutatum, C. destructivum and C. graminicola; PG2 produced those with obtuse ends, e.g., C. gloeosporioides, and C. orbiculare. Colletotrichum theae-sinensis, which produced the smallest conidia, was grouped as PG3, far from other species, indicating it should not belong to Colletotrichum. Grouping and phylogenetic analysis using ribosomal DNA was an effective tool to classify and identify Colletotrichum species without using morphology.

Description of Colletotrichum lupini comb. nov. in Modern Terms

Article

Mar 2002

Gloeosporium lupini Bondar is transferred to Colletotrichum. The fungus is characterized morphologically and illustrated. The two varieties, Colletotrichum lupini (Bondar) Nirenberg, Feiler & Hagedorn, comb. nov. var. lupini and Colletotrichum lupini var. setosum Nirenberg, Feiler & Hagedorn var. nov. are described. They are compared with additional Colletotrichum species reported from lupins and other hosts by morphological and physiological methods as well as by RAPD-PCR and DNA-sequencing.

Epitypification and phylogeny of Colletotrichum acutatum J.H. Simmonds

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