Mycologia
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DOI: 10.3852/mycologia.98.2.275
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Mycologia, 98(2), 2006, pp. 275-285.
© 2006 by The Mycological Society of America

Host range of Cercospora apii and C. beticola and description of C. apiicola, a novel species from celery


Marizeth Groenewald 1

     Centraalbureau voor Schimmelcultures, Fungal Biodiversity Centre, Uppsalalaan 8, 3584 CT Utrecht, and Laboratory of Phytopathology, Wageningen University, Binnenhaven 5, 6709 PD Wageningen, the Netherlands

Johannes Z. Groenewald

     Centraalbureau voor Schimmelcultures, Fungal Biodiversity Centre, Uppsalalaan 8, 3584 CT Utrecht, the Netherlands

Uwe Braun

     Martin-Luther-Universität, FB. Biologie, Institut für Geobotanik und Botanischer Garten, Neuwerk 21, D-06099 Halle (Saale), Germany

Pedro W. Crous

     Centraalbureau voor Schimmelcultures, Fungal Biodiversity Centre, Uppsalalaan 8, 3584 CT Utrecht, and Laboratory of Phytopathology, Wageningen University, Binnenhaven 5, 6709 PD Wageningen, the Netherlands

   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 

The genus Cercospora is one of the largest and most heterogeneous genera of hyphomycetes. Cercospora species are distributed worldwide and cause Cercospora leaf spot on most of the major plant families. Numerous species described from diverse hosts and locations are morphologically indistinguishable from C. apii and subsequently are referred to as C. apii sensu lato. The importance and ecological role that different hosts play in taxon delimitation and recognition within this complex remains unclear. It has been shown that Cercospora leaf spot on celery and sugar beet are caused respectively by C. apii and C. beticola, both of which are part of the C. apii complex. During this study we characterized a new Cercospora species, C. apiicola, which was isolated from celery in Venezuela, Korea and Greece. The phylogenetic relationship between C. apiicola and other closely related Cercospora species was studied with five different gene areas. These analyses revealed that the C. apiicola isolates cluster together in a well defined clade. Both C. apii and C. beticola sensu stricto form well defined clades and are shown to have wider host ranges and to represent distinct species.

Key words: Ascomycetes, Cercospora apii complex, Cercospora leaf spot, molecular phylogeny, species boundaries, taxonomy


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
The genus Cercospora Fresen. first was described in 1863 by Fresenius (Fuckel 1863Go) and currently is one of the largest and most heterogeneous genera of hyphomycetes (Crous and Braun 2003Go). Species belonging to this plant pathogenic genus are distributed worldwide and cause Cercospora leaf spot on most of the major plant families (Crous and Braun 2003Go). Since the description of the genus, the taxonomy of its species has become difficult because Cercospora for many years has been a dumping ground for all dematiaceous hyphomycetes with filiform conidia (Pons and Sutton 1988Go). Johnson and Valleau (1949)Go stated that most of the morphologically uniform Cercospora isolates belong to a single Cercospora species that occurs on a wide host range and morphologically is indistinguishable from C. apii Fresen. Cercospora apii is the oldest available name for this large complex of morphologically indistinguishable Cercospora taxa. This approach was questioned by Chupp (1954)Go, who stated in his monograph that species of Cercospora are generally host specific. Chupp subsequently formulated the concept of "one host species, genus or family equals one Cercospora species". Chupp’s concept led to the description of a large number of species based on host substrate, with more than 3000 names being listed by Pollack (1987)Go. Crous and Braun (2003)Go revised these species and redisposed many of them. A total of 659 Cercospora species were recognized, with a further 281 being referred to synonymy under C. apii s.l. This decision was substantiated by the various inoculation experiments that have been conducted on the C. apii complex (Vestal 1933Go, Johnston and Valleau 1949, Fajola 1978Go) and that raised doubts whether host specificity existed within this complex.

To date only a few species belonging to C. apii s.l. have been cultured, and molecular data addressing host specificity within this complex is still lacking (Crous et al 2004Go). Three scenarios are possible when examining the host-species association of taxa belonging to the C. apii complex. The first scenario is that a single species of Cercospora occurs on a wide host range; the second is that several species exist with overlapping host ranges; the third is that some Cercospora species are host specific whereas others are not.

The first evidence that distinct species exist within the C. apii morphotype recently was published by Groenewald et al (2005)Go. The latter study focused on Cercospora species isolated from sugar beet (Beta vulgaris) and celery (Apium graveolens). Characteristics examined for these isolates included morphology, cultural characteristics and cardinal temperature requirements for growth. These data were supplemented with amplified fragment length polymorphism analyses and phylogenetic analyses with five different genes. Groenewald et al (2005)Go showed that three distinct Cercospora species exist on sugar beet and/or celery, namely C. beticola on sugar beet, C. apii on both celery and sugar beet and a third that was isolated from celery in Venezuela and Korea.

The ability to infect different hosts during artificial inoculation is of questionable value as a character in species delimitation. For instance, a recent study revealed that C. beticola could infect safflower during artificial inoculation experiments (Lartey et al 2005Go). However C. beticola has yet to be isolated from this host in the field. Only a few taxa that belong to the C. apii complex have been studied in the past in an attempt to elucidate the relationship between fungal species and host. The first objective of this study, therefore, was to name the new Cercospora species from celery. The second objective was to use DNA sequence data to examine the host range of this species, including C. apii s.s. and C. beticola s.s. as defined by Groenewald et al (2005)Go.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 LITERATURE CITED
 
Isolates.— – Those used in this study were obtained from the Centraalbureau voor Schimmelcultures (CBS) in Utrecht, the Netherlands, as well as the working collection of Pedro Crous (CPC) that is housed at CBS (TABLE IGo). Single conidial isolates also were obtained from symptomatic material as explained in Crous (1998). Isolates were plated onto 2% malt-extract agar (MEA) and oatmeal agar (OA) (Gams et al 1998Go) and incubated at 24 C for 8 d.


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  		TABLE I. Cercospora isolates included in the study

 
DNA isolation, amplification and sequencing.— – The Fast-DNA kit (BIO 101, Carlsbad, California) was used according to the manufacturer’s instructions to isolate genomic DNA of 200–400 mg fungal mycelia grown on MEA plates. A sterile blade was used to scrape the mycelia from the surface of the plate. For the phylogenetic analyses, parts of these gene areas were used: the internal transcribed spacers and 5.8S rRNA gene (ITS), the actin gene (ACT), the translation elongation factor 1-{alpha} gene (EF), the calmodulin gene (CAL) and the histone H3 gene (HIS). PCR primers and amplification conditions followed the protocols outlined by Groenewald et al (2005)Go. PCR products were separated by electrophoresis at 80 V for 40 min on a 0.8% (w/v) agarose gel containing 0.1 µg/mL ethidium bromide in 1x TAE buffer (0.4 M Tris, 0.05 M NaAc, and 0.01 M EDTA, pH 7.85) and viewed under UV-light.

Amplicons were sequenced in both directions with the PCR primers and a DYEnamic ET Terminator Cycle Sequencing Kit (Amersham Biosciences, Roosendal, the Netherlands) according to the manufacturer’s recommendations. The products were analyzed on an ABI Prism 3700 DNA Sequencer (Perkin-Elmer, Foster City, California). A consensus sequence was computed from the forward and reverse sequences with SeqMan from the Lasergene package (DNAstar, Madison, Wisconsin).

Data analysis.— – The consensus sequences were assembled and added to alignment (TreeBASE matrix number M2242) of Groenewald et al (2005)Go with Sequence Alignment Editor 2.0a11 (Rambaut 2002Go), and manual adjustments for improvement were made by eye where necessary. The phylogenetic analyses of sequence data were done in PAUP (phylogenetic analysis using parsimony) 4.0b10 (Swofford 2003Go) and consisted of neighbor joining analysis with the uncorrected "p", the Jukes-Cantor and the HKY85 substitution models. Alignment gaps were treated as missing data and all characters were unordered and of equal weight. Any ties were broken randomly when encountered. For parsimony analysis, alignment gaps were treated as a fifth character state and all characters were unordered and of equal weight. Maximum parsimony analysis was performed for all datasets with the heuristic search option with 100 random taxa additions and tree bisection and reconstruction (TBR) as the branch-swapping algorithm. Branches of zero length were collapsed and all multiple, equally parsimonious trees were saved. The robustness of the trees was evaluated by 1000 bootstrap replications (Hillis and Bull 1993Go). Other measures calculated included tree length, consistency index, retention index and rescaled consistency index (TL, CI, RI and RC). The resulting trees were printed with TreeView 1.6.6 (p 1996). A partition homogeneity test was done in PAUP to test whether the different loci can be used in a combined analysis (Farris et al 1994Go). Sequences were deposited in GenBank (accession numbers listed in TABLE IGo) and the alignment and trees in TreeBASE (accession number SN2512).

Morphology.— – Fungal structures were mounted in lactic acid and examined under a light microscope (1000x). The extremes of spore measurements (30 observations) are given in parentheses. Colony colors were rated after 8 d on MEA and OA at 24 C in the dark with the color charts of Rayner (1970)Go.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 LITERATURE CITED
 
Sequence data analyses.— – A partition homogeneity test showed that all five datasets were not combinable (P = 0.001) but that four of the data sets (ITS, EF, ACT and CAL) could be combined (P = 1.000) and these therefore were analyzed as one combined set. The combined alignment contained 67 strains, including the three outgroups, and had a total length of 1262 characters, of which 935 were constant, six were parsimony uninformative and 321 were parsimony informative. The topology of the neighbor joining trees obtained with the different substitution models was the same. A similar topology was found for the most parsimonious trees. Parsimony analysis of the combined data resulted in a single parsimonious trees (FIG. 1Go) (TL = 350 steps; CI = 0.997; RI = 0.999; RC = 0.996). From the phylogenetic analysis (FIG. 1Go), three distinct and well supported clades were obtained. The first clade (99% bootstrap support) contains Cercospora isolates belonging to the C. beticola s.s. clade. Twenty-nine of these isolates were obtained from Beta species, but several isolates in this group also were obtained from five additional hosts (two from Chrysanthemum, one from Apium, one from Limonium, one from Malva and two from Spinacia). The isolates were obtained from Europe, Africa, Asia and New Zealand). The second clade (100% bootstrap support) contains C. apii s.s. isolates. These isolates also were obtained from a diverse range of hosts (three from Beta, three from Moluccella, one from Plantago, one from Plumbago and one from Helianthemum), but the primary host infected by isolates in this group appears to be Apium (eight isolates). Isolates from the second clade were from Europe, America and New Zealand. The third clade (100% bootstrap support) contains isolates of C. apiicola that thus far have been isolated only from Apium species in Venezuela, Korea and Greece.


Figure 1
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  		FIG. 1. Single most parsimonious tree obtained from a heuristic search with 100 random taxon additions of the combined ITS, EF, ACT and CAL sequence alignment. The scale bar shows ten changes and bootstrap support values from 1000 replicates are shown at the nodes. Type strains are shown in bold print. The tree was rooted to three Mycosphaerella thailandica strains.

 
Because the HIS dataset was not combinable with other sequence data, it was analyzed separately. The HIS alignment contained 67 strains including the three outgroups, and had a total length of 380 characters, of which 319 were constant, one was parsimony uninformative and 60 were parsimony informative. The topology of the neighbor joining trees obtained with the different substitution models was the same and was identical to the topology of the most parsimonious tree. Parsimony analysis of the HIS data resulted in the single most parsimonious tree (FIG. 2Go) (TL = 73 steps; CI = 0.986; RI = 0.998; RC = 0.984). From the phylogenetic analysis (FIG. 2Go), three well supported clades with 100% bootstrap values were obtained. The first clade contained eight isolates (seven from Beta species from different countries and one from Helianthemum in Rumania) that were present in the C. beticola s.s. clade obtained from the first analysis, except for the Helianthemum isolate which grouped in the C. apii s.s. clade (FIG. 1Go). The second clade contained the remaining C. beticola s.s. and C. apii s.s. isolates. The third clade consisted only of the C. apiicola isolates, which is consistent with the first analysis using the other four loci.


Figure 2
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  		FIG. 2. The single most parsimonious tree obtained from a heuristic search with 100 random taxon additions of the histone H3 sequence alignment. The scale bar shows a single change and bootstrap support values from 1000 replicates are shown at the nodes. Type strains are shown in boldface. The tree was rooted to three Mycosphaerella thailandica strains.

 
Taxonomy.— – Cercospora apii and C. beticola s.s. were circumscribed by Groenewald et al (2005)Go. During the present study several Cercospora isolates were obtained from celery exhibiting Cercospora leaf spot. A population of 47 plants collected in Venezuela by N. Pons, as well as individual diseased plants collected in Greece and Korea, were found to be associated with a novel species of Cercospora. The latter species is morphologically distinct from the C. apii s.l. complex. Its conidiophores are relatively short, 25–70 x 4–6 µm, and the conidia are obclavate-cylindrical, not acicular, measuring (50–)80–120(–150) x (3–)4–5 µm and being 1–6-septate (FIGS. 3Go, 4Go). This species therefore is described as new:


Figure 3
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  		FIG. 3. Cercospora apiicola (holotype). A. Conidiophore. B–F. Conidia. Bar = 5 µm.

 

Figure 4
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  		FIG. 4. Line drawing of conidiophores and conidia of the C. apiicola holotype (CBS 116457). Bar = 10 µm.

 
Cercospora apiicola M. Groenewald, Crous & U. Braun, sp. nov.

Differt a C. apii (s.s. et s.l.) conidiophoris relative brevibus, 25–70 x 4–6 µm, conidiis obclavatis-cylindraceis, nonacicularibus, tantum 1–6-septatis.

Specimen examined.. VENEZUELA. La Guanota, Caripe, Edo. Monagas, 1050 m.s.n.m., Apium sp., 23 Jul 2002, N. Pons, HOLOTYPE herb. CBS 18473, culture ex-type CBS 116457 MycoBank MB500768.

Leaf spots amphigenous, subcircular to irregular, 3–10 mm diam, medium brown, with a raised or inconspicuous, indefinite margin, not surrounded by a border of different color. Caespituli amphigenous, but primarily hypophyllous. Stromata lacking to well developed, 30–60 µm diam, medium brown. Conidiophores arising in fascicles of 4–10, moderately dense, arising from stromata, emerging through stomata or erumpent through the cuticle, subcylindrical, upper part geniculate-sinuous, unbranched, 1–3-septate, 25–70 x 4–6 µm, medium brown, becoming pale brown toward the apex, smooth, wall somewhat thickened. Conidiogenous cells integrated, terminal, 15–30 x 4–5 µm, occasionally unilocal, usually multilocal, sympodial; loci subcircular, planate, thickened, darkened, refractive, 2.5–3 µm wide. Conidia solitary, cylindrical when small, obclavate-cylindrical when mature, not acicular, (50–)80–120 (–150) x (3–)4–5 µm, 1–6-septate; apex subobtuse, base obconically subtruncate; hila 2–2.5 µm wide, thickened, darkened, refractive.

Cultural characteristics.. Colonies are smooth to folded, erumpent with smooth, even to uneven margins and sparse to moderate aerial mycelium; white to smoke-gray on MEA (surface), and olivaceous-gray to iron-gray beneath; on OA colonies are white to olivaceous-gray on the surface. Cardinal temperature requirements for growth, min 6 C, opt 24 C, max 30 C.

Host range and distribution.. Apium graveolens, Apium sp., Greece, Korea, Venezuela.


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
LITERATURE CITED
 
During a recent study in which we circumscribed C. apii and C. beticola s.s., we collected isolates of several Cercospora spp. that are part of the C. apii s.l. species complex. A whole population of "C. apii " collected on celery from Venezuela was revealed to be a distinct species. Several months later we isolated the same species on celery collected from Korea. At that time it was thought that this species had not yet invaded European celery fields because it was absent from European Cercospora isolates from this crop (Groenewald et al 2005Go). However in the present study we report the presence of this species on celery from Greece and describe it as C. apiicola sp. nov. Cultural and morphological examination of the C. apiicola strains support the observation made by Groenewald et al (2005)Go that this new Cercospora species is distinct from the two closely related species, C. beticola and C. apii, that previously have been isolated from celery. The isolation of this new Cercospora species on a well known crop such as celery is an indication that there may still be many other undescribed cercosporoid species on well known crops and ornamental plants awaiting description.

Chupp (1954)Go associated Cercospora leaf spot on sugar beet with infections of C. beticola, and that of celery with C. apii. Ellis (1971)Go discussed the C. apii s.l. isolates in detail and described a wide host range for this species, but five years later he changed his opinion and narrowed the host range of C. apii to celery and C. beticola to sugar beet (Ellis 1976Go). Crous and Braun (2003)Go linked 83 host genera to C. apii and nine host genera to C. beticola infections. Groenewald et al (2005)Go again cast doubt on the purported wide host ranges of these species. In the present study a survey of Cercospora isolates from 10 host genera identified several additional hosts for both C. apii s.s. and C. beticola s.s. From these data we can confirm four additional host genera for C. apii (Helianthemum, Moluccella, Plantago, Plumbago) and five additional host genera for C. beticola (Apium, Chrysanthemum, Limonium, Malva, Spinacia). According to Crous and Braun (2003)Go several Cercospora species (listed in parentheses) are associated with these hosts: Apium (C. apii), Beta (C. beticola), Helianthemum (C. cistinearum, C. helianthemi), Moluccella (C. molucellae), Plantago (C. pantoleuca, C. plantaginis), Plumbago (C. apii, C. plumbaginea), Limonium (C. apii, C. insulana, C. statices), Malva (C. althaeina, C. beticola, C. hyalospora, C. malvae, C. malvarum) and Spinacia (C. bertrandii, C. beticola, C. spinaciicola). In the treatment of Crous and Braun (2003)Go neither Apium, Chrysanthemum or Limonium are listed as hosts of C. beticola nor Beta, Helianthemum, Moluccella and Plantago as hosts of C. apii. This study provides the first molecular evidence that these two species have wider host ranges than had been accepted by Chupp (1954)Go and Ellis (1976)Go. However from the present study it appears that both species have narrower host ranges than that proposed by Crous and Braun (2003)Go, but this has to be investigated further by conducting pathogenicity studies on all the hosts previously listed for these species.

The host range data obtained in the present study illustrate that C. beticola s.s. and C. apii s.s. are not entirely host specific and that it is not possible to identify these two species solely based on host. Despite of the additional host genera that were found for C. apii and C. beticola, it is clear that C. apii s.s. is mainly isolated from celery, whereas C. beticola is mainly isolated from sugar beet, even though both of these species have been isolated from the other’s primary host in the past.

Crous and Groenewald (2005)Go introduced the pogo stick hypothesis to explain the colonization of necrotic Mycosphaerella lesions by other species of Mycosphaerella that jump hosts in the process of reaching their real hosts. The possibility that this process of substrate colonization and host jumps also occurs in asexual Mycosphaerella species could explain the isolation of specific Cercospora species from "atypical" hosts and needs to be investigated further. It would be especially interesting to determine whether Cercospora species occurring on "atypical" hosts are able to cause disease on these hosts or not.

As illustrated in this study, morphology, host specificity and geographic location are not suitable characters for the identification of species of the Cercospora apii complex. Groenewald et al (2005)Go used sequence data in combination with other features such as growth rate to establish species boundaries for C. apii, C. apiicola (as Cercospora sp.) and C. beticola. From these established species boundaries, species-specific primers were designed in polymorphic areas of the calmodulin gene for the three species. This combined approach probably represents the most reliable way to characterize and identify species within this complex.

Five loci were used in this study for phylogenetic analyses, although all five loci sequenced were not congruent and therefore could not be used in a combined phylogenetic analysis. Two separate analyses thus were performed, the first combining ITS, EF, ACT and CAL sequences and the second using only HIS sequences. The first analysis separated the C. apii s.s., C. beticola s.s. and C. apiicola isolates. Although the second analysis also was able to separate the C. apiicola isolates from the C. apii s.s./C. beticola s.s. isolates, it was unable to distinguish between C. apii s.s. and C. beticola s.s. isolates. Using HIS data a small cluster representing seven C. beticola s.s. and one C. apii s.s. isolate grouped separately from other C. apii s.s./C. beticola s.s. isolates. The unique polymorphisms (10 in total) observed in the histone H3 sequences of these isolates were identical and were not present in the other isolates or in our Cercospora sequence database. A possible explanation might be host jumping by the Helianthemum isolate, followed by recombination with the Beta isolates. However more Helianthemum isolates need to be studied to confirm whether this allele is unique to Helianthemum before one can address this issue. Caution therefore should be taken when using histone H3 sequence data for Cercospora phylogeny because variation in the histone H3 sequence may not indicate species differences.

It can be concluded from this study that strains belonging to the C. apii s.s. and C. beticola s.s. clades can be isolated from other hosts and, although these species are mainly isolated from celery and sugar beet, they are not host specific. It seems that the new species from celery described in this paper (viz. C. apiicola) is host specific because no other Cercospora strain isolated from other hosts and available in our sequence database has similar sequences. The reasons why host jumping by C. apii and C. beticola is so common remains unknown. However it is not unlikely that under stress—a shortage of host tissue or unsuitable weather—the new species might be able to jump from celery onto other hosts.


   ACKNOWLEDGMENTS
 
The authors thank H.D. Shin, N. Pons and A.N. Jama for respectively supplying the infected Apium leaf materials from Korea, Venezuela and Greece. This research was financially supported by the CBS-Odo van Vloten Stichting, and the Royal Netherlands Academy of Arts and Sciences.


   FOOTNOTES
 
Accepted for publication January 21, 2005.

1 Corresponding author. E-mail: m.groenewald{at}cbs.knaw.nl


   LITERATURE CITED
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
Chupp C. 1954. A monograph of the fungus genus Cercospora. Ithaca, New York: Published by the author.

Crous PW, Braun U. 2003. Mycosphaerella and its anamorphs 1. Names published in Cercospora and Passalora. CBS Biodivers Series 1:1–571.

———, Groenewald JZ. 2005. Hosts, species and genotypes: opinions versus data. Australas Pl Pathol (In press).

———, ———, Pongpanich K, Himaman W, Arzanlou M, Wingfield MJ. 2004. Cryptic speciation and host specificity among Mycosphaerella spp. occurring on Australian Acacia species grown as exotics in the tropics. Stud Mycol 50:457–469.

Ellis MB. 1971. Dematiaceous hyphomycetes. Kew, Surrey, UK: CMI.

———. 1976. More dematiaceous hyphomycetes. Kew, Surrey, UK: CMI.

Fajola AO. 1978. The effect of some environmental factors on the reproductive structures of some species of Cercospora. Nov Hedwig 29:922–934.

Farris JS, Källersjö M, Kluge AG, Bult C. 1994. Testing significance of incongruence. Cladistics 10:315–320.[CrossRef]

Fuckel KWGL. 1863. Fungi Rhenani exsiccati, Fasc. I–IV. Hedwigia 2:132–136.

Gams W, Hoekstra ES, Aptroot A. 1998. CBS Course of Mycology. 4th ed. Baarn, the Netherlands: Centraalbureau voor Schimmelcultures.

Groenewald M, Groenewald JZ, Crous PW. 2005. Distinct species exist within the Cercospora apii morphotype. Phytopathology 95:951–959.[CrossRef]

Hillis DM, Bull JJ. 1993. An empirical test of bootstrapping as a method for assessing confidence in phylogenetic analysis. Syst Biol 42:182–192.[CrossRef]

Johnson EM, Valleau WD. 1949. Synonomy in some common species of Cercospora. Phytopathology 39: 763–770.

Lartey RT, Caesar-Ton That TC, Caesar AJ, Shelver WL, Sol NI, Bergman JW. 2005. Safflower: a new host of Cercospora beticola. Plant Dis 89:797–801.[CrossRef]

Page RDM. 1996. TREEVIEW: an application to display phylogenetic trees on personal computers. Comput Appl Biosci 12:357–358.[Free Full Text]

Pollack FG. 1987. An annotated compilation of Cercospora names. Mycol Mem 12:1–212.

Pons N, Sutton BC. 1988. Cercospora and similar fungi on yams (Dioscorea spp.). Mycol Pap 160:1–78.

Rambaut A. 2002. Sequence Alignment Editor. Version 2.0. Oxford, UK: Department of Zoology, University of Oxford.

Rayner RW. 1970. A mycological colour chart. Kew, Surrey, UK: CMI and British Mycological Society.

Swofford DL. 2003. PAUP*: phylogenetic analysis using parsimony (*and other methods). Version 4. Sunderland, Massachusetts: Sinauer Associates.

Vestal EF. 1933. Pathogenicity, host response and control of Cercospora leaf spot of sugar beet. Iowa Agric Exp Sta Res Bull 168:43–72.





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