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Phylogenetic Analysis of Cercospora and Mycosphaerella Based on the Internal Transcribed Spacer Region of Ribosomal DNA

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Phylogenetic Analysis of Cercospora and Mycosphaerella Based on the Internal Transcribed Spacer Region of Ribosomal DNA Ecology and Population Biology Phylogenetic Analysis of Cercospora and Mycosphaerella Based on the Internal Transcribed Spacer Region of Ribosomal DNA Stephen B. Goodwin, Larry D. Dunkle, and Victoria L. Zismann Crop Production and Pest Control Research, U.S. Department of Agriculture-Agricultural Research Service, Department of Botany and Plant Pathology, 1155 Lilly Hall, Purdue University, West Lafayette, IN 47907. Current address of V. L. Zismann: The Institute for Genomic Research, 9712 Medical Center Drive, Rockville, MD 20850. Accepted for publication 26 March 2001. ABSTRACT Goodwin, S. B., Dunkle, L. D., and Zismann, V. L. 2001. Phylogenetic main Cercospora cluster. Only species within the Cercospora cluster analysis of Cercospora and Mycosphaerella based on the internal produced the toxin cercosporin, suggesting that the ability to produce this transcribed spacer region of ribosomal DNA. Phytopathology 91:648- compound had a single evolutionary origin. Intraspecific variation for 658. 25 taxa in the Mycosphaerella clade averaged 1.7 nucleotides (nts) in the ITS region. Thus, isolates with ITS sequences that differ by two or more Most of the 3,000 named species in the genus Cercospora have no nucleotides may be distinct species. ITS sequences of groups I and II of known sexual stage, although a Mycosphaerella teleomorph has been the gray leaf spot pathogen Cercospora zeae-maydis differed by 7 nts and identified for a few. Mycosphaerella is an extremely large and important clearly represent different species. There were 6.5 nt differences on genus of plant pathogens, with more than 1,800 named species and at average between the ITS sequences of the sorghum pathogen Cercospora least 43 associated anamorph genera. The goal of this research was to sorghi and the maize pathogen Cercospora sorghi var. maydis, indicating perform a large-scale phylogenetic analysis to test hypotheses about the that the latter is a separate species and not simply a variety of Cerco- past evolutionary history of Cercospora and Mycosphaerella. Based on spora sorghi. The large monophyletic Mycosphaerella cluster contained a the phylogenetic analysis of internal transcribed spacer (ITS) sequence number of anamorph genera with no known teleomorph associations. data (ITS1, 5.8S rRNA gene, ITS2), the genus Mycosphaerella is mono- Therefore, the number of anamorph genera related to Mycosphaerella may phyletic. In contrast, many anamorph genera within Mycosphaerella were be much larger than suspected previously. polyphyletic and were not useful for grouping species. One exception was Cercospora, which formed a highly supported monophyletic group. Additional keywords: Dothistroma, Lecanosticta, mating type, Mycocen- Most Cercospora species from cereal crops formed a subgroup within the trospora. Fungi in the genus Cercospora are among the most prevalent it is not a universal pathogenicity factor because it is not produced and destructive plant pathogens. As a group, they are nearly uni- by all species (3,16,18,21). Fajola (18) concluded that cercosporin versally pathogenic, occurring on a wide range of hosts in almost production is associated with “true” Cercospora species and all major families of dicots, most monocot families, and even suggested that those species that do not produce cercosporin may some gymnosperms and ferns (26). Chupp (6) listed over 1,800 belong to other, related genera. However, the ability to produce species names in his monograph of the genus in 1954, and the list cercosporin is often specific to strains or isolates (16,21,35), and had grown to over 3,000 by 1987 (26). In a major effort to clarify is influenced by various environmental and nutritional conditions the taxonomy of the genus, Deighton (12–15) segregated and (21). These inconsistencies preclude definitive application of reclassified many Cercospora species into other genera, including cercosporin production to taxonomy. Cercosporella, Cercosporidium, Paracercospora, Pseudocerco- Due to the paucity of useful morphological and physiological spora, Pseudocercosporella, and Pseudocercosporidium, among characters, taxonomy of the Cercospora complex remains others. This broad assemblage is referred to as the Cercospora confusing and depends heavily on the host. This is further compli- complex, with members of Cercospora proper having conidia that cated because most species have no known sexual stage. For those are acicular, hyaline, and septate with a conspicuous hilum few species in which a sexual stage has been identified, the produced on pigmented, unbranched, septate, smooth conidio- teleomorph is in the genus Mycosphaerella (5–7,29,34). Examples phores (17,27). include the banana pathogens Mycosphaerella fijiensis (Cerco- Many species of Cercospora are characterized by the produc- spora fijiensis = Paracercospora fijiensis) and Mycosphaerella tion of a phytotoxic metabolite of polyketide origin called cerco- musicola (Cercospora musae = Pseudocercospora musae) and the sporin (3). Although this compound may enhance virulence (33), peanut pathogen Mycosphaerella arachidis (Cercospora arachi- dicola) (7). Many other associations between Cercospora species and Mycosphaerella teleomorphs have been reported but not Corresponding author: S. B. Goodwin; E-mail address: [email protected] confirmed. Names are necessary to report factually on available data. However, the USDA Mycosphaerella also is a very large genus, with over 1,800 neither guarantees nor warrants the standard of the product, and the use of the names and at least 500 species associated with more than 40 ana- name implies no approval of the product to the exclusion of others that also may morph genera (7). Similar to Cercospora, the taxonomy of Myco- be suitable. sphaerella is complicated, and several competing classification systems have been proposed (5,29,34). Due to the large number of Publication no. P-2001-0511-01R associated anamorphs, Crous and Wingfield (10) concluded that This article is in the public domain and not copyrightable. It may be freely re- printed with customary crediting of the source. The American Phytopathological Mycosphaerella was a polyphyletic assemblage of presumably Society, 2001. monophyletic anamorph genera. Barr (5) agreed, and separated 648 PHYTOPATHOLOGY species with Dothistroma and Lecanosticta anamorphs into a new cryptic species in addition to those within Cercospora zeae- genus, Eruptio. There clearly is a great need for increased maydis. For example, due to their different host specificities, understanding of the phylogenetic relationships within Myco- Chupp (6) suggested that the sorghum pathogen Cercospora sorghi sphaerella. and the corn pathogen Cercospora sorghi var. maydis might be Recent molecular analyses have begun to clarify the taxonomic different species, even though they are identical morphologically. confusion surrounding Mycosphaerella and a few of its associated However, the evolutionary relationships of these two taxa to each anamorph genera. Stewart et al. (30) used ribosomal DNA other, to the gray leaf spot pathogens, and to other species of sequence analyses to divide species with cercosporoid anamorphs Cercospora are not known. into three clusters. One group corresponded to the genus Cerco- The purpose of this research was to perform a large-scale spora sensu stricto, the second included Paracercospora and phylogenetic analysis of the genus Mycosphaerella and associated Pseudocercospora, and the third was composed of species of anamorphs to test hypotheses about the evolutionary history of the Passalora. Because no other species with Mycosphaerella teleo- genus Cercospora. The first goal was to test the hypothesis that morphs were included, it was not possible to determine the phylo- the Cercospora species from cereal crops form a monophyletic genetic relationships of the cercosporoid species to other anamorph group with the true Cercospora clade as defined by Stewart et al. genera. Goodwin and Zismann (20) identified a monophyletic (30). The second goal was to develop empirical data on the group that included six out of seven species of Mycosphaerella number of nucleotide differences within and between species to tested. The Mycosphaerella cluster included seven anamorph determine whether groups I and II of Cercospora zeae-maydis genera, two of which had no known teleomorph associations. The represent different species. The third goal was to test Chupp’s (6) only exception was Mycosphaerella pini (anamorph Dothistroma hypothesis that Cercospora sorghi and Cercospora sorghi var. septospora), which clustered outside the main Mycosphaerella maydis are different species. The fourth goal was to test the group. No species of Cercospora were included in that study. hypothesis that Cercospora species that produce cercosporin form Therefore, the relationships between Cercospora and the other a monophyletic group. Within Mycosphaerella, the primary goal anamorphs tested could not be determined. was to test the hypothesis of Crous and Wingfield (10) and Barr Neither of the previously described studies included species of (5) that the genus Mycosphaerella is polyphyletic. A secondary Cercospora infecting cereal crops. One Cercospora of recent goal within Mycosphaerella was to determine whether anamorph importance to grain production is the gray leaf spot pathogen of genera are monophyletic. maize, Cercospora zeae-maydis (23). Although epidemics of gray leaf spot have caused substantial economic losses in the mid- MATERIALS AND METHODS western and eastern
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