Systematics of Plant Pathogenic Fungi – Why It Matters

Amy Y. Rossman Systematic Mycology & Microbiology Laboratory, USDA-Agricultural Research Service, Beltsville, MD

Mary E. Palm-Hernández Molecular Diagnostics Laboratory, USDA-Animal and Plant Health Inspection Service, Beltsville, MD

Systematics of Plant Pathogenic Fungi: Why It Matters

Systematics is the study of biological di- comparison of portions of the genome are with that name suggests that this organism versity; more specifically, it is the science also used to characterize fungi, especially is more likely to decay dead cellulosic that discovers, describes, and classifies all in determining species concepts and rela- material. organisms. Taxonomy, nomenclature, and tionships among fungi at all levels ranging As an example of scientific names phylogeny are all part of systematics. Fun- from population genetics to the phylogeny changing to reflect increased knowledge, gal systematic studies result in the discov- of major groups of fungi as well as fungal- one can examine a fungal pathogen caus- ery and description of fungi, the principles like organisms. ing root rot of woody plants known for of nomenclature guide the naming of or- many years as Armillaria mellea (Vahl:Fr.) ganisms, and phylogenetic studies contrib- What’s in a name? Karst., which has the common names in ute to the classification of taxa into geneti- Names are the means by which informa- English of honey mushroom, shoestring, or cally related groups. A taxon (pl. taxa) is a tion is communicated about an object, in bootlace fungus (Fig. 1). Decades ago, A. taxonomic group at any rank, e.g., order, this case an organism. The name of an mellea was considered to be just one ubiq- family, genus, species, and subspecies organism may be a common name or sci- uitous species infecting many different among others. entific name. Common names of organ- hosts (60). Hints of the fact that A. mellea Systematics is a dynamic science. As isms can vary considerably from place to was a species complex came from mating systematists obtain new data about fungi, place and among different languages and experiments in which several groups were they use that to more accurately determine are therefore much less precise than scien- shown to be genetically isolated by a com- the concept of a taxon and relationships tific names. Scientific names are used to plex mating system (3,67,68). More re- among taxa. When new relationships are accurately define an organism or set of cently, molecular sequence data have con- discovered or old relationships are found organisms and to communicate about firmed the existence of the groups defined to be incorrect, systematists must account them. As systematic scientists learn more by mating studies (17,18). Upon careful for those discoveries. Necessarily, this new about each species or other taxon and the examination of specimens representing the knowledge may result in changes of scien- relationships among them, scientific names different groups, morphological characters tific names. Centuries ago, fungal speci- change to reflect this increased knowledge. were discovered that reflected the distinc- mens were described simply by looking at Based on the knowledge associated with tiveness of the groups. them with the unaided eye, and then mac- the name, it is possible to predict the be- As a result of scientific advances in sys- roscopically using a ×20 hand lens. This havior or biology of that organism. For tematics, at least eight species in North approach was followed by the use of the example, if one isolates and identifies a America and five species in Europe are compound light microscope that could Phytophthora from woody plant material, recognized that would previously have magnify the image of structures up to the name Phytophthora suggests a poten- been called by one name, Armillaria ×1,000. In the late twentieth century, the tially destructive plant pathogen. On the mellea (2). Combining morphological, scanning electron microscope allowed the other hand, if a Chaetomium is found, one biological, and genetic data, narrow spe- close observation of external features of can predict that this fungus is unlikely to cies have been defined that reflect knowl- morphological structures such as ascospore cause a disease, and knowledge associated edge including the biology of each species ornamentation, while the transmission electron microscope led to the discovery of internal organelles and structures of cells. All of these tools for observing specimens are still useful. Today, sequencing and

As allCorresponding author: Amy Y. Rossman, Systematic Mycology & Microbiology Laboratory, USDA-Agricultural Research Service, Rm. 304, B011A, 10300 Baltimore Ave., Beltsville, MD 20705 USA; E-mail: [email protected] doi:10.1094/ PDIS-92-10-1376 This article is in the public domain and not copy- Fig. 1. Species of Armillaria. A, Armillaria mellea sensu stricto, associated with Fagus rightable. It may be freely reprinted with custom- grandifolia (beech), North Carolina, Schenck Forest, October 1998. B, Armillaria ary crediting of the source. The American Phyto- ostoyae on Quercus coccinea (scarlet oak), North Carolina, Bent Creek, October 1998. pathological Society, 2008. Photos by Larry F. Grand, North Carolina State University.

1376 Plant Disease / Vol. 92 No. 10 (9,14,33). For example, Armillaria tional Code of Zoological Nomenclature on adaptation to a different host. Although luteobubalina Watling & Kile occurs only governs the naming of animals, while bac- this designation is recognized by the in Australia, where this fungus is a primary teria and other prokaryotic organisms are ICBN, its use is not governed by those pathogen of Eucalyptus causing decline named according to the International Code rules. and death especially in plantations (36). of Nomenclature of Bacteria. The first time a scientific name is men- Now recognized as distinct, this species The International Code of Botanical No- tioned in a research article, the author(s) was recently reported from Chile (17). menclature has been developed over many who initially described a taxon, often a Another segregate species, Armillaria decades based on principles that have re- species, is associated with that name, as is ostoyae (Romagn.) Herink, occurs in the mained relatively stable since about the the author(s) who may later transfer that Northern Hemisphere (Fig. 1B). Making 1950s. These basic principles are: (i) the name to another genus. As an example, we the distinction between these species using first scientific name applied to a species or will use Neonectria coccinea (Pers.:Fr.) their scientific names is essential for pre- other taxon has priority; (ii) each name Rossman & Samuels, cause of beech bark venting the movement of A. luteobubalina must be based on a type that represents canker in Europe. This name was origi- to South Africa or spreading A. ostoyae to that entity. In the case of a species, the nally described as Sphaeria coccinea New Zealand. If a pest risk assessment type is a specimen; for a genus, the type is Pers.:Fr. by Persoon in 1800 (49) and then were based on A. mellea as it was defined a species; for a family, the type is a genus, listed in Fries’s 1823 Systema Myco- 50 years ago as one cosmopolitan species, etc.; (iii) a name must be published in a logicum (27). Because this name is men- it is possible that conifers would be moved specific manner, i.e., with a Latin descrip- tioned by Fries (27), it is sanctioned ac- from the Northern Hemisphere to New tion, a type designated, the publication cording to the ICBN. This sanctioned Zealand, not knowing that this posed the widely distributed, among other require- status is denoted by the “:Fr.” and, because risk of introducing a pathogenic species ments; and (iv) a species can have only one it is sanctioned, this name has priority over not known to be present in that country. correct scientific name except in the case other names for this species published Species previously recognized as Armil- of fungi that have alternate states (Article prior to Fries (27). According to the ICBN, laria mellea sensu lato (in the broad sense) 59, ICBN). The ICBN also governs how to Fries’s major publications are considered are now known as precisely defined spe- transfer a species name from one genus to the starting point for the nomenclature of cies with names that communicate their another as the concept of the genus or ascomycetes and certain other groups of biological differences, including host species changes, as well as many more fungi. Later, Fries (28) revised his concept range, pathogenicity, and geographic dis- details about the naming of plants and of Sphaeria, a genus that initially included tribution. fungi. Changes are made to the ICBN all perithecial ascomycetes, and placed this following much discussion, debate, and a species in Nectria, a genus that included What rules govern the scientific vote at the Nomenclature Session during fleshy, colored, uniloculate, perithecial names of fungi? the International Botanical Congresses ascomycetes. With that taxonomic deci- Nomenclature is the branch of systemat- held every six years. Although the details sion, the scientific name of this species ics that determines the correct scientific and complexity of the ICBN have changed became Nectria coccinea (Pers.:Fr.) Fr. name for a taxon. The naming of fungi is over time, the basic principles have re- The abbreviation Fr. outside the parenthe- governed by the International Code of mained the same. The stability of scientific ses refers to the author who placed the Botanical Nomenclature (ICBN) (42) be- names of plants and fungi is facilitated species name in that genus. Later, when cause of the historical assumption that through application of the ICBN to issues Rossman et al. (54) placed this species in fungi and plants were closely related. We of nomenclature. the genus Neonectria as N. coccinea now know fungi in the traditional sense Each scientific name for a species con- (Pers.:Fr.) Rossman & Samuels, their comprise a diverse range of organisms sists of two or more portions, minimally, a names were placed outside the parenthe- including true Fungi (Kingdom Fungi), genus and a species epithet. A specific ses. Notice that the generic name may be stramenopiles (Kingdom Chromista), and name is placed in a defined hierarchy that abbreviated with the first letter, occasion- various kinds of slime molds (Kingdom usually includes the family, order, class, ally two or three letters, always referring to Protozoa). True Fungi represent a distinct phylum, and kingdom. Species may also the previously listed generic name. Thus, kingdom that is more closely related to be given a subspecific designation such as the N. listed above refers to Neonectria, animals than to plants (see below). Never- variety or subspecies. Of interest to plant not Nectria. The author name(s) is often theless, the naming of fungi in the tradi- pathologists, the subspecific taxon forma included when a species name is first men- tional sense is still governed by the ICBN. specialis, or form species, is often used to tioned in a publication, especially in taxo- A different set of rules called the Interna- indicate a physiological difference based nomic papers, in order to define precisely

Fig. 2. Beech bark canker in North America caused by Neonectria faginata; type of genus Nectria, N. cinnabarina. A, Beech bark canker disease in North America caused by Neonectria faginata. Photo by Martin MacKenzie, USDA-Forest Service, Salinas, CA. B, As- comata of Neonectria faginata BPI 864079. Photo by Gary J. Samuels, USDA-ARS. C, Nectria cinnabarina, cause of coral canker disease of hardwood trees, showing ascomata and Tubercularia asexual state. Photo copyrighted by Jeff Keller, Switzerland.

Plant Disease / October 2008 1377 the concept of that name. For all scientific cies of Neonectria, N. ramulariae Wol- canker and other hardwoods in North names governed by the ICBN, the authors lenw., that also has a Cylindrocarpon America (Fig. 2A and B). The analyses of associated with scientific names are abbre- asexual state and similar ascomatal wall multiple genes from these isolates demon- viated according to agreed-upon standards structure. Therefore, Nectria coccinea is strated that a different species is associated published in Brummitt and Powell (12), a now placed in the genus Neonectria as with beech bark canker on Fagus in North list that is updated and available online at Neonectria coccinea (54). America. One of the pathogens causing http://www.ipni.org/. Most recently with the use of molecular beech bark canker in North America had sequence data, the concept of Neonectria been recognized as Neonectria coccinea Why do scientific names change? coccinea has been even more narrowly var. faginata Lohman et al. Castlebury et Scientific names change as systematists defined. Using a multigene phylogeny, al. (13) suggest that N. coccinea is distinct learn more about a species, including its Castlebury et al. (13) demonstrated that the from Neonectria coccinea var. faginata, morphology, biology, and evolutionary species name N. coccinea should be re- and that this variety should be recognized relationships. stricted to a group of fungi that occur only at the species level as Neonectria faginata Changes in scientific names can be an- on Fagus (beech) in Europe. In this re- (Lohman et al.) Castl. & Rossman (Fig. noying to users of those names. However, search, several genes were sequenced and 2B). Based on the more precise definition if one knows the reasons behind name analyzed from isolates of fungi appearing of this species, it is found to occur only on changes and understands that a new name similar to N. coccinea on various plant Fagus in North America. Although many provides more information about that hosts throughout the world. These data isolates from Fagus in Europe were in- taxon than the old name, these changes are revealed the existence of several lineages cluded in this study, none of them proved easier to accept. Continuing the example of related but distinct species, only one of to be the same as N. faginata that occurs in from above, we discuss the fungi that which could be N. coccinea. All were de- North America. cause beech bark canker in North America termined to belong in the genus Neonectria. A second species, Nectria galligena (Neonectria faginata, Fig. 2A and B) and How can the “real” Neonectria coccinea Bres., also referred to as Neonectria galli- Europe (Neonectria coccinea). be determined? When Sphaeria coccinea gena (Bres.) Rossman & Samuels, has Early in mycological history, fungal spe- was described in 1800 by Persoon, he been associated with beech bark canker in cies were very broadly defined such that designated a particular specimen as the North America. Many isolates of N. galli- all pyrenomycetes (ascomycetes with tiny type specimen that serves as the standard gena from Fagus and many other hard- fruiting bodies often seen as bumps pro- or definition of that species. This type wood hosts and the closely related N. ditis- truding on the plant surface) were placed specimen occurs on Fagus sylvatica in sima (Tul. & C. Tul.) Samuels & Rossman in the genus Sphaeria and all little red Germany, and a portion of the type speci- were included in the study. Analyzing the perithecial fungi were called Sphaeria men is housed at the U.S. National Fungus sequences of multiple genes, Castlebury et coccinea. With the use of microscopes and Collections in Beltsville, MD. This portion al. (13) determined that the isolates of N. the study of fungi in culture, mycologists of the type specimen was examined to ditissima including one representing the observed that some little red perithecial determine the precise morphological type specimen and those of N. galligena fungi were different from others based on characteristics of Neonectria coccinea. were genetically closely related. They are characteristics of the ascomata, asci, and The type specimen of N. coccinea was so closely related that Castlebury et al. ascospores. Thus, Sphaeria coccinea was determined to agree morphologically with (13) made the taxonomic decision that placed in the genus Nectria as Nectria a living culture from a similar looking, Neonectria galligena and N. ditissima are coccinea, with other bright-colored, fleshy, recently collected specimen on F. sylvatica synonyms, i.e., they are the same species. uniloculate perithecial species with uni- in Germany. A single ascospore isolate was Because the name Nectria ditissima Tul. & tunicate asci. Further comparison of micro- made from this specimen that produced a C. Tul. 1865, the basionym of Neonectria scopic characteristics of species of Nectria living culture. This specimen and derived ditissima (Tul. & C. Tul.) Samuels & revealed that N. coccinea was distinct from culture were used to interpret and charac- Rossman, was described prior to N. galli- other red perithecial species such as Nec- terize the dead type specimen. In the publi- gena Bres. 1901, the principle of priority tria cinnabarina, N. episphaeria, and cation by Castlebury et al. (13), this speci- from the ICBN dictates that the earliest many other species. Most recently, differ- men was designated the epitype specimen name should be used. Thus, the correct ences in ascomatal wall structure, asexual with the living culture considered the ex- name for this species known for many states, and biology have been noted among epitype culture. An epitype specimen is years as Nectria galligena is now Neo- species of red Nectria-like fungi such that one that is used to interpret a type speci- nectria ditissima. these species are placed in several newly men that may not have all the characteris- What does this research with the resul- defined or described genera (54). tics needed to define a species such as tant name changes mean for plant patholo- The genus Nectria is based on the type DNA that can be sequenced. Using the gists and plant quarantine officials? Actu- or defining species Nectria cinnabarina epitype specimen and the ex-epitype cul- ally, quite a bit! First, Neonectria faginata (Tode:Fr.) Fr. (Fig. 2C). Species in the ture that agree with the original type speci- associated with beech bark canker only genus Nectria sensu stricto (in the narrow men on Fagus in Germany, the species occurs on Fagus in North America. Appar- sense) are those most closely related to N. Neonectria coccinea is now well-charac- ently, this species was not introduced into cinnabarina. Species in the genus Nectria terized based on morphology and molecu- North America as had been previously sensu stricto have certain morphological lar sequence data. In the molecular se- thought. Second, N. ditissima, another characteristics in common such as a Tuber- quence study, isolates of Neonectria that species associated with beech bark canker, cularia asexual state, a specific ascomatal group with the ex-epitype isolate of N. occurs on a wide range of hardwood trees wall structure, and similar biology as well coccinea are considered to be the same in North America and Europe. Neonectria as grouping with N. cinnabarina when species, while isolates distinct from those ditissima causes diseases of various hard- molecular sequences are analyzed. On the grouping with N. coccinea are considered woods, such as birch canker and apple other hand, Nectria coccinea, now known different species. Thus, it was determined canker disease, suggesting that breeding as Neonectria coccinea, has a Cylindrocar- that N. coccinea occurs only on Fagus in these host trees for resistance to diseases pon asexual state, an ascomatal wall struc- Europe and does not occur on any other caused by N. ditissima may be difficult ture that is different from N. cinnabarina, host plants, nor does it occur in North because of the broad host range of the and does not group with N. cinnabarina America. pathogen. Finally, Neonectria coccinea using molecular sequence data. Rather, it This research included many isolates of sensu stricto occurs only on Fagus in is morphologically similar to the type spe- related fungi associated with beech bark Europe. This is important information for

1378 Plant Disease / Vol. 92 No. 10 plant regulatory officials when considering and, for example, frosty pod disease proba- pathogenic fungi. As a result of this knowl- the movement of beech germplasm be- bly could not be controlled by benomyl. edge, a plant pathologist should suspect tween North America and Europe. Knowing that the cause of frosty pod is that strategies for controlling frosty pod Accurate scientific names based on nar- a basidiomycete suggests that perhaps it is caused by M. roreri may also be effective rowly defined species reflect what is related to the other basidiomycete cacao against witches’-broom caused by the known about the biology, host range, and pathogen in spite of the fact that Crinipel- closely related, but macromorphologically geographic distribution of the species. The lis perniciosa produces conspicuous mush- different, M. perniciosa. knowledge associated with accurate scien- rooms on decaying cacao pods (Fig. 3) tific names is important for plant patholo- while M. roreri produces only a single How can I find the most accurate, gists, for example, in developing strategies layer of spores on the cacao pods. Aime up-to-date name for my fungal to control fungal diseases or determining and Phillips-Mora (1) analyzed molecular pathogen? actions to prevent the introduction of new sequence data from isolates of species in Keeping up-to-date on the most accurate pathogens. the genus Crinipellis including the type scientific names of fungi can be difficult species as well as isolates of C. perniciosa and time-consuming. In order to make this Why does it matter whether and M. roreri. They used this approach to as easy as possible, resources have been scientific names reflect the determine the relatedness of the two established for this purpose. Increasingly, phylogeny of fungal pathogens? basidiomycete pathogens and if Crinipellis this information is available on the Internet Accurate scientific names should convey perniciosa was placed in the correct genus. and can be rapidly accessed, but at present as much information as is known about an This research showed that the two spe- none of these sources are complete with entity, including its classification and phy- cies causing diseases of cacao were closely the up-to-date scientific names for all logeny, also referred to as evolutionary related to each other; that is, the fungus fungi. history. An accurate name that reflects known as Crinipellis perniciosa causing Several resources exist to help a user de- phylogeny will allow a prediction about a witches’-broom was closely related to the termine the accurate scientific name of a plant-associated fungus, including its po- fungus causing frosty pod, Moniliophthora fungus. One is the Index Fungorum http:// tential pathogenicity and appropriate con- roreri, even though the latter species does www.indexfungorum.org/Names/Names.as trol measures. For example, species in the not produce a mushroom-like structure. p developed by CAB International. This is genus Erysiphe are obligate parasites that This was a surprise! However, close obser- a list of all described fungal names, over cause powdery mildew diseases on living vation of microscopic characteristics of 400,000 of them, with a family placement plants. On the other hand, an isolate deter- these two species revealed less conspicu- for each name. An attempt is made to mined to be a species of Phomopsis may ous similar structures that confirmed this provide the currently accepted scientific be pathogenic or harmlessly endophytic relationship. In addition, Crinipellis perni- name, although for many names an update depending on the health of the host. An ciosa was determined to be only distantly is unavailable or inaccurate and the date or accurate generic classification implies related to the type and other species of the rationale for the updated name is not information about the biological character- genus Crinipellis, a genus that includes given. Complementary to Index Fungorum istics of the species included in that genus. primarily saprobic tropical fungi. To re- is the Catalog of Life http://www.catalogue An accurate identification of the causal flect this evolutionary relationship, Aime oflife.org/search.php, which includes a agent of a plant disease is essential for and Phillips-Mora (1) transferred C. perni- phylogeny for most groups of true Fungi determining the appropriate choice of con- ciosa to Moniliophthora so that the two and Oomycota. This site is useful for trol measures. As an example, consider the closely related species are in the same determining the higher level relationships fungi that cause two serious diseases of genus. The etiological agent of witches’- of all organisms and it is updated annually. cacao or the chocolate plant (Theobroma broom is now known as Moniliophthora However, the Catalog of Life includes only cacao, Malvaceae) in the Western Hemi- perniciosa (Stahel) Aime & Phillips-Mora, the most common species of fungi with sphere. reflecting the close relationship to M. even fewer synonyms. The Centraalbureau Witches’-broom of cacao is caused by a roreri and the similar biology of these two voor Schimmelcultures (CBS) Fungal fungus that until recently was known as Crinipellis perniciosa (Stahel) Singer. This pathogen causes an abnormal growth on the host; thus, the name witches’-broom has been given to the disease. This fungus produces a mushroom-type reproductive structure. Another serious cacao disease known as frosty pod appears as a whitish bloom on cacao pods with the associated fungus reproducing as a single layer of spore-bearing structures giving the pods a “frosty” appearance. The fungus causing frosty pod was originally identified as Monilia roreri Cif. (35). The generic name Monilia suggests that this is the asexual state of the ascomycete Neurospora. Upon close microscopic examination, Evans (23) and Evans et al. (24) determined that the spores produced by M. roreri were actually basidiospores; thus, to reflect this observation, they established the genus Monilioph- thora with the type species, Monilioph- thora rorei (Cif.) H.C. Evans et al. (24). The generic name Moniliophthora carries Fig. 3. Moniliophthora perniciosa, the fungus that causes witches’-broom disease of the knowledge that this pathogen is not an cacao. A, Mushroom-type fruiting body of M. perniciosa. Photo by USDA-ARS. B, Ca- ascomycete related to Neurospora crassa cao pods with beans destroyed by M. perniciosa. Photo by USDA-ARS.

Plant Disease / October 2008 1379 Biodiversity Centre has initiated a database disease-causing fungi associated with nyms and alternative state name, the re- of accurate scientific names of fungi along plants worldwide. All of the 13,000 ac- ports of that species on plant hosts any- with descriptions and literature. In ad- cepted species of fungi that were included where in the world under all synonyms, dition, this database provides access to the in Fungi on Plants and Plant Products in literature about that species, and data on most recently described fungal species the United States (25) are treated. Scien- specimens in three different herbaria. This through an initiative known as MycoBank tific names for important groups of plant resource relies on accurate nomenclature (http://www.mycobank.org/). New names pathogens such as Phytophthora and those because the ability to gather information for fungi are entered into the MycoBank on the APHIS Regulated Plant Pest List about any particular fungus depends on the database, and the name is given a number have been evaluated and published (15,16). ability to search for information using all that is used in the publication. In that way, The scientific names of plant pathogenic synonyms. all new scientific names for fungi will be fungi will continue to be evaluated and In addition to the accurate names of and known without the need to access all the updated as additional changes occur and information about plant associated fungi, literature in which fungal names might new species are described. the SMML website provides several re- have been published. Plans have been At the SMML website, information in sources for the identification of plant path- made to combine these databases of fungal addition to nomenclature can be retrieved ogenic fungi. These include interactive names along with the one mentioned be- such as host range, worldwide distribution, keys with descriptions and illustration to low. This would greatly help to meet the disease and plant part affected as well as species of bunt-fungi (Tilletia) in North needs of plant pathologists who want to recent literature about the species and America (26), rust fungi on legumes po- know the correct scientific names for fun- specimens in the U.S. National Fungus tentially confused with soybean rust (47), gal pathogens. Collections, Arthur Herbarium of Purdue species of the rust genus Ravenelia (34), A resource for determining the accurate University, and Plant Pathology Herbarium and species of Trichoderma used in the scientific name of fungal plant pathogens of Washington State University. Although biological control of plant pathogenic as well as the host range, geographic distri- determining the accurate scientific name fungi. In addition, descriptions and illus- bution, literature, and, for some species, for a fungus can be a time-consuming trations are available for invasive plant descriptions and illustrations, is the fungal process, once the nomenclature of a spe- pathogens, http://nt.ars-grin.gov/sbmlweb/ database at the USDA ARS Systematic cies has been evaluated and updated, data fungi/diagnosticfactsheets.cfm, such as Mycology & Microbiology Laboratory from each of the databases for that species Puccinia horiana Henn., cause of chry- (SMML) (http://ars.usda.gov/ba/psi/smml). under all of its scientific names can be santhemum white rust; P. hemerocallis The nomenclatural part of this database retrieved at once. Information about the Thüm., cause of daylily rust; and Perono- has the advantage of documenting taxo- host range and geographic distribution can spora radii de Bary, cause of downy mil- nomic information and decisions so that be determined using any of the various dew of marguerite daisy, among others (50). one can consult the literature upon which synonyms of both the sexual and asexual the taxonomic decision was based. The states of a species. By selecting the Quick Recent Advances in Systematics number of species names that have been Search option http://nt.ars-grin.gov/fungal The revolution resulting from the ability reviewed is limited, about 40,000 species databases/index.cfm, one can search for to obtain molecular data has greatly influ- at present; however, the emphasis is on the accurate scientific name with syno- enced the field of systematics such that an increasing body of genetic information about organisms exists. Following are some advances in knowledge that have been made as the result of applying molecular sequencing data to the understand- ing of relationships among fungi and other organisms. Fungi are more closely related to animals than to plants. Although some evidence existed several decades ago to suggest that fungi were quite unlike plants in many ways, molecular sequence data have now been used to prove that the true Fungi are more closely related to animals than to plants (8,69; Fig. 4). This discovery ex- plains why it has been so difficult to develop antimycotic pharmaceuticals that are effective against human fungal pathogens without negatively affecting the human host. Oomycetes are related to the yellow- brown algae. The Oomycota or Perono- sporomycetes consist of more than 800 species that may be saprobic or parasitic on terrestrial or aquatic plants and animals. The oomycetes, including Phytophthora, Pythium, and downy mildews, have long been considered to be fungi because they obtain their nutrients via absorption and many of them produce the filamentous Fig. 4. A kingdom-level phylogeny of Eukaryotes based on combined protein data threads characteristic of most fungi. As showing that fungi are most closely related to animals (Metazoa) and the Oomycota new tools for determining phylogenetic belong in the Heterokonta. Figure taken from Baldauf et al., Science 290:972-977 (3 relationships were developed, they have November 2000). Reprinted with permission from AAAS. been applied to questions such as whether

1380 Plant Disease / Vol. 92 No. 10 the Oomycota are more closely related to structures were also produced, mostly Schweinitz (1780–1830). The example of the heterokont algae or the true Fungi placed in the anamorphic genus Oidium, Neonectria coccinea presented above dem- (Chytridiomycota, Glomeromycota, Zygo- but relatively little attention had been paid onstrates a change in species concept over mycota, Ascomycota, Basidiomycota). Re- to them as taxonomic characters. With the time based on available tools. Below we sults from a number of studies using application of molecular sequence data will use the genus Fusarium to further molecular sequence data combined with (57,64–66), this classification system has illustrate changing species concepts and ultrastructural observations confirm un- been considerably revised. Molecular data why it is important to apply accurate scien- equivocally that the Oomycota share a demonstrated that the morphological sig- tific names to meaningfully defined species. common ancestor with the other members nal, i.e., the morphological characteristics The genus Fusarium was first described of the heterokont algae. The heterokont that correlate with the phylogeny, is exhib- in 1809 and was sanctioned by Fries in algae include the Phaeophyta or brown ited by the asexual state. Today, the ge- 1821 based on Fusarium roseum Link for algae, Xanthophyta or yellow-green algae, neric concepts in the Erysiphales are based “species with fusiform, non-septate spores Chrysophyta or golden algae, and Bacil- primarily on characteristics of the conidio- borne on a stroma” (11). Species were lariophyta or diatoms as well as several phores and conidia rather than on the ap- added to Fusarium, but no monographic smaller groups. Some controversy still pendages of the chasmothecia. treatments, i.e., comprehensive accounts remains about exactly what to call this Fusarium: Molecular systematics re- based on systematics, were published for group of organisms. Most authors refer sults in more precisely defined species. this genus until a German plant pathologist them to the Kingdom Chromista, Phylum The concept of a species has changed con- Wollenweber (70) and later Wollenweber Heterokonta (37), while others place them siderably since the time of the father of and Reinking (71) published landmark in the Kingdom Stramenopila (also spelled mycology Elias Fries (1794–1878) and the papers about Fusarium that laid the Straminipila) (48). father of American mycology David groundwork for future, premolecular stud- A number of characteristics distinguish the Oomycota from the true Fungi. These include differences in sexual reproduction, the nuclear state of the vegetative myce- Table 1. Major distinctions between the Oomycota (Kingdom Chromista) and the true Fungi lium, cell wall composition, type of flagel- Character Oomycota True Fungi lae, and mitochondria (Table 1 from 52). Five major classes of true Fungi are Product of sexual Produces oospores Oospores not produced; sexual recognized, including arbuscular my- reproduction reproduction results in corrhizae in a class of their own. Two zygospores, ascospores, or basidiospores NSF-funded initiatives called Deep Hypha and Assembling the Fungal Tree of Life Nuclear state of Diploid Mostly haploid or dikaryotic (AFTOL) produced a comprehensive re- vegetative mycelium view of the classification of true Fungi Cell wall composition Beta glucans-cellulose Chitin, cellulose rarely present with the results published in Mycologia Type of flagellae on Heterokont, of two types, one If flagellae produced, usually of 98(6), 2006. In this issue, the latest phy- zoospores, if whiplash directed posteriorly, only one posterior whiplash logeny of all major groups of true Fungi is produced the other fibrous, ciliated, type presented with an overview article by directed anteriorly Blackwell et al. (10). The Ascomycota and Mitochondria With tubular cristae With flattened cristae Basidiomycota are two of the major classes of fungi along with the Chytridio- mycota and Zygomycota. The arbuscular mycorrhizal fungi were determined to be distinct from these major classes and are now recognized as the class Glomeromy- cota along with a number of smaller groups of unusual fungi. Some evidence suggests that the Microsporidia are true Fungi as well, but these results are still equivocal. Powdery mildews are defined by co- nidial state characters. As each group of Fungi is scrutinized using molecular tools, concepts of taxa at every level from class and order down to family, genus, and species are more precisely and sometimes differently defined. One example that was a surprise to many concerns a major group of plant pathogens, the Erysiphales or powdery mildews, in which new concepts of genera have been recognized based on the analyses of molecular sequence data. Many species of Erysiphales produce a sexual fruiting structure known as a chas- mothecium (a closed fruiting body), often with appendages that are curved, hooked, branched, or straight (Fig. 5). In the past, genera were defined based on these ap- Fig. 5. Ascomata of powdery mildew, Erysiphe magnifica, showing branched append- pendages thought to influence the mode of ages and asci emerging from ruptured ascomata. Photo by Larry F. Grand, North distribution. Fairly nondescript asexual Carolina State University.

Plant Disease / October 2008 1381 ies recognizing 142 species in 16 groups Fusarium. These groups correlated with With the advent of non-morphological and six subgroups. A few years later, two the biology of species as well as their approaches to systematics including mat- Americans, Snyder and Hansen (61–63), known sexual states, although for some ing type studies and molecular sequence reduced all Fusarium taxa to nine species groups no sexual states are known. The analyses, the genus Fusarium was tackled more or less roughly equivalent to Wollen- cereal pathogens of Fusarium in Sections by several mycologists with a resulting weber and Reinking’s groups (11). While Discolor, Elegans, and Liseola have Gib- proliferation of more narrowly defined the identification of species was relatively berella sexual states, while the root rot species (5,38,46), often reflecting biologi- easy using the Snyder and Hansen system, pathogens including F. solani were placed cal differences. As an example, one can little distinction was made between species in Section Martiella having Haematonec- examine Fusarium solani (Mart.) Appel & that, for example, were plant pathogens tria sexual states (54). The unusual species Wollenw. sensu lato, the only species in causing cereal diseases or root rots and F. decemcellulare Brick and related species the section Martiella based on the nine- those useful in biological control of scale in Section Spicarioides have sexual states species system proposed by Snyder and insects and other fungi. placed in Albonectria (54). Species in Hansen (62). Mating type studies were In the 1970s and 1980s, Booth (11), Section Epispheria including slow-grow- undertaken in which at least seven repro- Gerlach and Nirenberg (31), Marasas et al. ing species that occur on other fungi and ductively isolated biological species of (40), and Nelson et al. (43) were in relative section Coccophilum on scale insects have Fusarium solani were characterized, often agreement about the major groups within sexual states placed in Cosmospora (54). referred to as its sexual state Nectria haematococca Berk. & Broome (41). Ana- lyzing molecular sequences of mating type loci suggested that each of these represented a different species but that many more species existed. Eventually, O’Donnell (45) recognized 26 phylogenetically distinct species within Fusarium solani, many of which have a distinct biology. The causal agent of soybean sudden death syndrome (56) was referred to as Fusarium solani sensu lato or F. solani f. sp. glycines (39,55). This is a disease (Fig. 6) that occurs throughout the world and now is known to be caused by four different species of Fusarium. To more accurately determine the causal agents of this disease, multiple genes were sequenced and analyzed from a diversity of isolates representing Fusarium solani sensu lato. Those isolates known to cause soybean sudden death syndrome in North America have been segregated as a distinct species named F. virguliforme O’Donnell & T. Aoki (6) (Fig. 7). Three related but different species of Fusarium, including F. t u - Fig. 6. Symptoms of soybean sudden death syndrome in South America caused by cumaniae T. Aoki et al. and F. virguli- Fusarium tucumaniae. A, Leaf symptoms. B, Root symptoms. Photos by Takayuki Aoki, forme, are associated with this disease in Tsukuba, Japan. South America (7). Pairings of these

Fig. 7. Conidiophores and two kinds of conidia of Fusarium virguliforme, cause of soybean death syndrome in North America. A, Macroconidia on solitary conidiophore of F. virguliforme. B, Macroconidia of F. virguliforme. C, Aggregated conidiophores of F. virguliforme. D, Comma-shaped conidia of F. virguliforme. Photos by Takayuki Aoki, Tsukuba, Japan.

1382 Plant Disease / Vol. 92 No. 10 closely related species resulted in sexual molecular sequence data is the inclusion of community, but making the switch to one reproduction among isolates of F. t u c u m a - Macrophomina phaseolina (Tassi) Goid., name will not be easy (29,53). niae but not between F. tucumaniae and F. cause of charcoal rot and ashy stem blight, Initiatives will provide tools for the virguliforme. These mating studies are in the ascomycete family Botryosphaeri- accurate identification of fungi. The another confirmation of the validity of aceae (21). Macrophomina phaseolina DNA Barcode of Life Initiative seeks to these species distinctions (19). Based on produces large numbers of sclerotia, but no provide a unique DNA sequence for the the putative existence of only one mating spores. For this reason, the fungus was identification of all biological species type, this research also suggests that F. considered to be related to other common (http://barcoding.si.edu/). The unique DNA virguliforme might have been introduced sclerotial-forming fungi such as Rhizocto- sequence would be from a standardized into North America and is still the only nia solani J.G. Kühn, a basidiomycete. position in the genome and would serve as species known to cause soybean sudden Knowing that Macrophomina phaseolina a molecular diagnostic tool for species- death syndrome in North America. The is an ascomycete rather than a basidiomy- level identification. Progress has been hypothesis that the fungus causing sudden cete means that different strategies should made toward developing DNA barcodes death syndrome in North America was be used to control the diseases caused by for specific groups of fungi. Among most introduced could not have been proposed this fungus. groups of animals, the mitochondrial without these accurately defined species Another surprising example of integrat- cytochrome oxidase I (COI) gene can be distinctions. ing asexual plant pathogenic fungi into the used to distinguish and rapidly identify Why break up large, well-known species ascomycetes concerns the cause of barley species. Although the COI gene works for into narrowly defined taxa with new and rye leaf spot and leaf scald, Rhyn- the nonfungal Oomycota and a few groups names? The benefit is in the precise infor- chosporium secalis (Oudem.) Davis. This of true Fungi (59), the existence of introns mation conveyed by the scientific name. In fungus is asexually reproducing, with only of variable lengths and other problems the case of Fusarium solani sensu lato simple unbranched conidiogenous struc- eliminate it as the best gene for a universal associated with soybean sudden death tures that produce hyaline, 1-septate co- DNA barcode for true Fungi. An interna- syndrome, no distinction was made among nidia. No sexual state has ever been en- tional workshop was held in May 2007 to the biologically distinct and geographically countered for this fungus. Molecular se- coordinate these efforts and decide on the separated entities. Once F. virguliforme quence studies of R. secalis revealed that best gene to use for DNA barcodes for was defined and named, the scientific this asexual fungus belongs in the Helotia- fungi. A consensus was reached that the name conveys the knowledge that this les or inoperculate discomycetes related to most appropriate gene known at present species alone causes sudden death syn- the genus Pyrenopeziza and Tapesia (32). for DNA barcoding of true Fungi is the drome of soybean in North America but At about the same time, another group of ITS region of the nuclear rDNA (51). that other species of Fusarium could also scientists demonstrated that this asexual Some DNA barcoding resources exist for be accidentally introduced. Without this pathogen is related to the serious grass the rapid identification of Fungi including knowledge, the epidemiology, control pathogen, Tapesia yallundae Wallwork & one for Fusarium using the ITS region strategies, timing, and breeding programs Spooner, cause of eyespot of cereals and (30) and another for the biocontrol fungus would be targeted at a species complex grasses, subsequently placed in its own Trichoderma using both ITS and EF1alpha representing broad fungal genetic diversity. genus as Oculimacula yalludae (Allwork for accurate species identification (22; Once narrowly defined, control strategies & Spooner) Crous & W. Gams in the Hel- http://www.isth.info/). can be designed based on the narrow ge- otiales (20). Identification using standardized known netic diversity of the causal agent. In addi- Theoretically, asexual fungi can be inte- DNA barcodes requires accurate system- tion, this information can be used by plant grated both taxonomically and nomencla- atic knowledge of the group of organisms quarantine officials to develop appropriate turally into a known phylogeny. In reality, involved. At the same time, developing and regulatory policies. the nomenclatural integration of asexual applying DNA barcodes unveils cryptic Most asexually reproducing fungi are fungi into an ascomycete phylogeny is species, i.e., species that are difficult to ascomycetes. Most species of plant-asso- proving difficult. The acceptance of two distinguish based on morphology, and thus ciated fungi are predominantly asexual or names for one species of fungus is allowed contributes to an even more accurate un- have no sexual state. Traditionally, they by Article 59 of the ICBN. The name for derstanding of a group of organisms. More have been placed in artificial groups such the asexual state is considered a form- sites for rapid identification of plant patho- as the hyphomycetes and coelomycetes taxon, and the correct name for the fungus genic fungi using DNA barcodes are an- based on the manner in which the conidia as a whole must be based on a teleomorph. ticipated. are produced and the presence or absence Many genera of sexual fungi correlate one- At present, plant pathologists have used and kind of fruiting body. The molecular for-one with genera of asexual fungi. The DNA sequences blasted to sequences in revolution has been extremely useful in ICBN indicates that teleomorph names GenBank for the identification of some determining relationships of asexually must be used in most cases. Are plant fungi. This method has serious limitations reproducing fungi to sexually defined pathologists willing to give up some of the that merit caution. Many sequences depos- groups. Most anamorphs have been deter- commonly used names such as Botrytis ited in GenBank, possibly as many as 27% mined to be ascomycetes, although some cinerea Pers.:Fr. in favor of Botryotinia of the ITS sequences, have been found to are basidiomycetes. Knowledge of the fuckeliana (De Bary) Whetzel in order to be from erroneously identified specimens relationship of the asexual species to sex- use just one name for this species? Or or cultures (44) and will result in a wrong ual fungi may assist in discovering the should the rules of the ICBN be changed to identification. GenBank is working to note sexual state, thereby completing knowl- allow the name Botrytis to have priority which sequences represent reliable refer- edge of the life history of a plant patho- over Botryotinia? Most scientists would ence sequences for species as has been genic fungus. For many asexual fungi, a agree that closely related species should be done for species in Trichoderma (58). To sexual state may not exist, but knowledge placed in the same genus, but which ge- confirm an identification using a DNA of the phylogeny allows scientists to make neric name should be used if one species sequence, one should always investigate predictions about the biology especially has a sexual state while the other species is the data associated with a GenBank se- pathogenicity of these species. known only as an asexual species? These quence even examining a voucher speci- In integrating the asexual species into an are questions that mycologists have been men if one has been deposited and com- ascomycete phylogeny, some surprising and still are pondering and discussing. In paring the unknown with descriptions and relationships have become evident. One the long run, use of one name for each illustrations of the sequenced known fun- example of a relationship revealed using species may best serve the plant pathology gus. After all, most described species of

Plant Disease / October 2008 1383 fungi have not yet been sequenced. Be- Carolina, and South Carolina (4). Unfortu- dried, then sent with detailed collection cause a sequence does not match some- nately, the basis for these reports is not data to an herbarium. Dried cultures for thing in GenBank does not mean that one known, nor are there specimens to docu- deposit are made by removing strips of is working with an undescribed species. In ment them. Because of these reports, Japan fungus on agar in petri plates, then gluing fact, it is likely that the unknown is just has been hesitant to accept tomatoes from them in cardboard slide mailers placed in one of the many described fungal species the United States for fear of their infection silica gel to dry (Fig. 8B). Instructions for without a sequence deposited in GenBank. with Peronospora hyoscyami. In order to making specimens of diseased plant mate- Another initiative potentially useful to prove the non-susceptibility of tomatoes, rial and dried cultures are available at: plant pathologists is the Encyclopedia of extensive pathogenicity tests have been http://www.ars.usda.gov/Services/docs.htm Life (http://www.eol.org/) in which a web made with negative results (http://www. ?docid=9403. Research in plant pathology page will be created for every biological uky.edu/Ag/kpn/kpn_97/pn971201.htm). should be documented so that future scien- species. Each species page will have basic Whether the initial reports of P. hyoscyami tists can verify and build upon today’s information for either a layperson or a on tomatoes were accurate will never be research results using these cultures and professional including general and techni- known because they were not documented specimens. cal data with links to sources of additional with voucher specimens. The expense and information. The first meeting to discuss extensive testing could have been avoided Conclusion how to develop such web pages for the if those reports had been documented, and The science of systematics that discov- fungi will take place in August 2008. thus could have been proven erroneous. ers, describes, and classifies organisms is In plant pathology research, after Koch’s essential for plant pathology. Systematic Document, Document, Document postulates have been fulfilled, a representa- study of plant pathogenic fungi results in Research involving fungal pathogens tive of the causal organism should be de- accurate scientific names that reflect know- should be documented with voucher speci- posited in a publicly accessible culture ledge and communicate information about mens and living cultures. One reason to do collection. Additionally, a dried specimen these organisms including their evolution- this is the possibility that the causal fungus of the diseased tissue with diagnostic fea- ary history. Accurate names of plant patho- is inaccurately identified or should be re- tures should be placed in a publicly acces- gens provide information essential for studied as species concepts change. Given sible collection. And, depositing cultures determining appropriate disease control that species concepts are dynamic and will and specimens is free! Many institutions measures and serve as the basis for making change as knowledge increases, the need to exist for documenting our science. For decisions that protect agricultural and document research plant pathogenic fungi cultures, the American Type Culture Col- natural resources from invasive fungal is critical. Such a requirement is more than lection (ATCC) in Manassas, VA, and the pathogens. of purely academic interest. When the Centraalbureau voor Schimmelcultures United States is requesting permission to (CBS), Utrecht, The Netherlands, among Acknowledgments export a commodity to a foreign country, others, accept living cultures without any We thank those who contributed illustrations for reports of pathogens and their distribution charge to the depositor. Voucher specimens this paper, specifically, Takayuki Aoki, Tsukuba, in the United States are scrutinized by the either as a fungal pathogen on the host Japan; Larry Grand, North Carolina State Univer- other country to determine if any patho- plant or as a dried culture specimen should sity, Raleigh; Jeff Keller, Switzerland; Martin gens in the United States are a threat to the be deposited at the U.S. National Fungus MacKenzie, USDA-Forest, Salinas, CA; and Gary country of import. For example, Perono- Collections (BPI) in Beltsville, MD (Fig. Samuels, Systematic Mycology & Microbiology Laboratory, USDA-ARS, Beltsville, MD. David spora hyoscyami (Rabenh.) deBary (=P. 8A), New York Botanical Garden (NY), Farr, Systematic Mycology & Microbiology Labo- tabacina D.B. Adam), which causes to- Bronx, NY, Oregon State University Her- ratory, USDA-ARS, was invaluable in assembling bacco blue mold, primarily infects to- barium (OSC), Corvallis, OR, or any num- the plates. In addition, we appreciate the comments bacco, Nicotiana tabacum (Solanaceae). ber of fungal herbaria. Official abbrevia- provided by presubmission reviewers: Margery However, a few reports exist from the tions for herbaria are listed in Index Her- Daughtrey, Cornell University, Long Island Horti- cultural Research Station, Riverhead, NY; Drew 1930s that this fungus occurs on Solanum bariorum (http://sciweb.nybg.org/science2/ Minnis, Systematic Mycology & Microbiology lycopersicum (=Lycopersicon esculentum, IndexHerbariorum.asp). Plant material Laboratory, USDA-ARS, Beltsville, MD; and tomato, Solanaceae) in Georgia, North with the pathogen can be pressed and Melodie Putnam, Oregon State University, Corvallis.

Fig. 8. A, David Farr and Erin McCray looking at rust specimens among open herbarium cabinets in the U.S. National Fungus Collec- tions (BPI). B, Making a dried culture specimen from a living culture for deposit in a permanent repository such as the U.S. National Fungus Collections (BPI). Photos by USDA-ARS.

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Plant Disease / October 2008 1385 ogy 96:195-206. 59. Seifert, K. A., Samson, R. A., deWaard, J. R., Houbraken, J., Levesque, C. A., Moncalvo, J.- M., Louis-Seize, G., and Hebert, P. D. N. 2007. Prospects for fungus identification using CO1 DNA barcodes, with Penicillium as a test case. Proc. Natl. Acad. Sci. U.S.A. 104:3901- 3906. 60. Singer, R. 1956. The Armillariella mellea group. Lloydia 19:176-178. 61. Snyder, W. C., and Hansen, H. N. 1940. The species concept in Fusarium. Am. J. Bot. 27:64-67. 62. Snyder, W. C., and Hansen, H. N. 1941. The species concept in Fusarium with reference to section Martiella. Am. J. Bot. 28:738-742. 63. Snyder, W. C., and Hansen, H. N. 1945. The species concept in Fusarium with reference to Discolor and other sections. Am. J. Bot. 32:657-666. 64. Takamatsu, S., Hirata, T., Sato, Y., and No- mura, Y. 1999. Phylogenetic relationships of Amy Y. Rossman Mary E. Palm-Hernández Microsphaera and Erysiphe section Erysiphe Dr. Rossman is research leader of the Dr. Palm-Hernández is the director of (powdery mildews) inferred from the rDNA Systematic Mycology & Microbiology the USDA Animal and Plant Health ITS sequences. Mycoscience 40:259-268. Laboratory, USDA Agricultural Re- Inspection Service, Plant Protection 65. Takamatsu, S., Inagaki, M., Niinomi, S., Kho- daparast, S. A., Shin, H. D., Grigaliunaite, B., search Service, and Director of the and Quarantine (APHIS, PPQ), Mo- and Havrylenko, M. 2008. Comprehensive mo- U.S. National Fungus Collections in lecular Diagnostic Laboratory in Belts- lecular phylogenetic analysis and evolution of Beltsville, MD. After receiving her ville, MD. She also is an adjunct asso- the genus Phyllactinia (Ascomycota: Erysi- Ph.D. from Oregon State University in ciate professor in the Department of phales) and its allied genera. Mycol. Res. 1975 specializing in systematic mycol- Plant Pathology at Penn State Univer- 112:299-315. ogy, she was awarded the Anna Jen- sity. She received a B.A. from St. Olaf 66. Takamatsu, S., Matsuda, S., Niinomi, S., and kins Postdoctoral Fellowship at Cor- College in 1976 and a M.Sc. and Havrylenko, M. 2006. Molecular phylogeny nell University. She served as the Ph.D. in plant pathology with an em- supports a Northern Hemisphere origin of plant quarantine mycologist for the phasis in mycology from the University Golovinomyces (Ascomycota: Erysiphales). USDA and thus has an appreciation of Minnesota in 1979 and 1983, re- Mycol. Res. 110:1093-1101. for the complexity of plant-associated spectively. From 1984 to 2006, she 67. Ullrich, R. C., and Anderson, J. B. 1978. Sex fungi. Her research addresses the was the PPQ National Mycologist in Armillaria mellea and diploidy in . Exp. Mycol. systematics of plant pathogenic fungi, Beltsville, where she identified exotic 2:119-129. 68. Ullrich, R. C., and Anderson, J. B. 1988. Ar- with emphasis on ascomycetes in the fungi on plants and products entering millaria mellea, cause of rots in woody spe- Diaporthales and Hypocreales and the United States through ports of cies. Adv. Plant Pathol. 6:491-499. their asexual states. In addition to entry. Her interests include biosyste- 69. Wainright, P. O., Hinkle, G., Sogin, M. L., and publishing over 120 scientific papers, matics of plant pathogenic fungi, fungi Stickel, S. K. 1993. Monophyletic origins of she has co-authored four books in- on Proteaceae, and diagnostics of the Metazoa: An evolutionary link with fungi. cluding Fungi on Plants and Plant plant pathogens. Science 260:340-341. Products in the United States and 70. Wollenweber, H. W. 1913. Studies on the Protocols for an All Taxa Biodiversity Fusarium problem. Phytopathology 3:24-50. Inventory of Fungi. 71. Wollenweber, H. W., and Reinking, O. A. 1935. Die Fusarien. Berlin, Paul Parey.

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