Current Status of Fusarium oxysporum Formae Speciales and Races

charline lecomte

The Fusarium oxysporum species complex includes both plant pathogenic and nonpathogenic strains, which are commonly found in soils. F. oxysporum has received considerable attention from plant pathologists for more than a century owing to its broad host range and the economic losses it causes. The narrow host specificity of pathogenic strains has led to the concept of formae speciales, each forma specialis grouping strains with the same host range. Initially restricted to one plant species, this host range was later found to be broader for many formae speciales. In addition, races were identified in some formae speciales, generally with cultivar-level specialization. In 1981, Armstrong and Armstrong listed 79 F. oxysporum formae speciales and mentioned races in 16 of them. Since then, the known host range of F. oxysporum has considerably increased, and many new formae speciales and races have been identified. We carried out a comprehensive search of the literature to propose this rev...

Phytopathology • 2019 • 109:512-530 • https://doi.org/10.1094/PHYTO-08-18-0320-RVW Current Status of Fusarium oxysporum Formae Speciales and Races V. Edel-Hermann† and C. Lecomte Agroécologie, AgroSup Dijon, INRA, University of Bourgogne Franche-Comté, F-21000 Dijon, France. Accepted for publication 19 November 2018. ABSTRACT The Fusarium oxysporum species complex includes both plant pathogenic and nonpathogenic strains, which are commonly found in soils. F. oxysporum has received considerable attention from plant pathologists for more than a century owing to its broad host range and the economic losses it causes. The narrow host specificity of pathogenic strains has led to the concept of formae speciales, each forma specialis grouping strains with the same host range. Initially restricted to one plant species, this host range was later found to be broader for many formae speciales. In addition, races were identified in some formae speciales, generally with cultivar-level specialization. In 1981, Armstrong and Armstrong listed 79 F. oxysporum formae speciales and mentioned races in 16 of them. Since then, the known host range of F. oxysporum has considerably increased, and many new formae speciales and races have been identified. We carried out a comprehensive search of the literature to propose this review of F. oxysporum formae speciales and races. We recorded 106 well-characterized formae speciales, together with 37 insufficiently documented ones, and updated knowledge on races and host ranges. We also recorded 58 plant species/genera susceptible to F. oxysporum but for which a forma specialis has not been characterized yet. This review raises issues regarding the nomenclature and the description of F. oxysporum formae speciales and races. Keywords: diversity, forma specialis, host specificity, host range, pathogenicity, race, root rot, vascular wilt. The Fusarium oxysporum Schlechtend. species complex is comprised of soilborne fungi found in cultivated and uncultivated soils worldwide under various climates (Burgess 1981; Joffe and Palti 1977; Kommedahl et al. 1988; Mandeel et al. 1995). This species complex includes plant pathogens, human pathogens, and many nonpathogens. Pathogenic strains are morphologically indistinguishable from nonpathogenic strains. F. oxysporum displays high functional and genetic diversity (Kistler 1997; Nelson et al. 1981; O’Donnell et al. 2009; Steinberg et al. 2016). Evidence of its diversity lies in its impressive plant host range, which includes both dicots (e.g., bean, carnation, and tomato) and monocots (e.g., banana, orchids, and palms). Pathogenic F. oxysporum can affect perennial and annual plants, including mostly land-based, but also aquatic plants (e.g., lotus). From a practical point of view, pathogenic F. oxysporum strains cause wilts or root and crown rots on economically important field crops (banana, cotton, soybean), † Corresponding author: V. Edel-Hermann; E-mail: veronique.edel-hermann@inra.fr Authors contributed equally to the writing of this review. *The e-Xtra logo stands for “electronic extra” and indicates that three supplementary files are published online. This article is in the public domain and not copyrightable. It may be freely reprinted with customary crediting of the source. The American Phytopathological Society, 2019. 512 PHYTOPATHOLOGY many market garden crops (melon, onion, and tomato), as well as ornamental crops (cyclamen, gerbera, and orchids), and even on weeds or parasitic plants (broomrape and witchweed). However, individual strains display selective pathogenicity to a more or less narrow range of host plants. Strains with the same host range, generally one plant species, are grouped into a forma specialis. For example, strains responsible for Fusarium wilt of tomato belong to the forma specialis lycopersici, while those causing wilting on banana belong to the forma specialis cubense. The forma specialis concept was first created to distinguish strains of Puccinia graminis Pers. displaying similar morphological features but different host ranges. This new rank was designated as “spezialisierten formen” (Eriksson 1894). A definition was given in 1910 during the International Botanical Congress of Brussels: “In the case of parasites, especially parasitic fungi, authors who do not give specific value to forms characterized from a biological standpoint but scarcely or not at all from a morphological standpoint, should distinguish within the species special forms (forma specialis, f. sp.) characterized by their adaptation to different hosts” (Proceedings of the 3rd International Botanical Congress, 1910, Brussels Chapter II, Recommendation I bis). Since 1930, the existence of this intraspecific rank has been admitted by the International Code of Botanical Nomenclature (commonly named International Code of Nomenclature for algae, fungi and plants), but it is not codified by this international authority because accepting physiological traits represents a hurdle (Gordon 1965). Snyder and Hansen (1940) reported 25 “biologic forms” within F. oxysporum based on their host ranges. In 1965, F. oxysporum pathogenic strains were no longer designated as forms but as formae speciales (f. sp.) (Gordon 1965). In addition, some formae speciales are subdivided into races, defined by cultivar-level specialization and, in some cases, by known resistance genes in these cultivars (Gordon and Martyn 1997). Much attention has been devoted to F. oxysporum over the last hundred years; it is still among the most important fungal plant pathogens based on its scientific and economic importance (Dean et al. 2012). New formae speciales and races are regularly described, but their list has not been updated for more than 35 years (Armstrong and Armstrong 1981). We searched the scientific literature and extension journals to propose this review of currently described F. oxysporum formae speciales and races, and of the plant species susceptible to F. oxysporum diseases. This review also raises issues regarding the nomenclature and the description of F. oxysporum formae speciales and races. DISEASES CAUSED BY F. OXYSPORUM Knowledge on root infection by F. oxysporum was recently reviewed (Gordon 2017). Pathogenic F. oxysporum strains are responsible for two types of symptoms, i.e., most often vascular wilting and in some cases rotting. F. oxysporum causing vascular wilting penetrates the host roots to reach the xylem vessels, which it colonizes upwards, resulting in progressive yellowing and wilting of the plant (Olivain and Alabouvette 1999). This type of symptom is the most commonly encountered one. According to the Committee on standardization of common names for plant diseases, it is associated with several disease names that are Fusarium yellows, Fusarium blight, and Fusarium wilt (The American Phytopathological Society on the standardization of common names for plant diseases, 2017; http://www.apsnet.org/publications/commonnames/Pages/default. aspx). F. oxysporum that causes rotting progresses in the roots and hypocotyl cortical tissues without reaching the vascular system (Jarvis and Shoemaker 1978). Its growth causes the formation of discolored tissues evolving into brown to black necrotic spots that end up in the rotting of the plant. Diseases with rotting symptoms are called basal rot, Fusarium stem rot, or crown and root rot. Rot diseases predominantly affect plants with storage organs such as bulbs (e.g., lily), corms (e.g., crocus), tubers (e.g., potato), and rhizomes (e.g., ginger) (Boerema and Hamers 1988, 1989; Manici and Cerato 1994; Trujillo 1963). As such organs are characterized by a shortened stem, we may hypothesize that the fungus adjusts its progression strategy in the plant tissues according to the anatomical peculiarity of the plant. The first case of rot disease caused by F. oxysporum was reported on lupine (Weimer 1944). To distinguish root-rot-producing strains from those producing typical vascular wilt, Weimer (1944) proposed the name F. oxysporum f. sp. radicis-lupini. Since then, the term “radicis” has differentiated rot-producing strains from wilt-producing strains. The formae speciales causing rot were taken into account in Gordon’s review (Gordon 1965) but were removed from subsequent reviews (Armstrong and Armstrong 1968, 1981). However, the scientific community accepted the concept of “radicis”-type forma specialis. For example, formae speciales radicis-lycopersici and radiciscucumerinum are recognized as such for the root rot they cause on tomato and cucumber, respectively (Jarvis and Shoemaker 1978; Vakalounakis 1996). Including the term “radicis” in the name of the forma specialis allows for an immediate identification of the type of symptoms. However, some formae speciales, for example cepae, lilii, and opuntarium, cause rotting but are not referred to as formae speciales “radicis-host plant name” (Baayen et al. 1998; Brayford 1996; Polizzi and Vitale 2004). On the other hand, F. oxysporum that causes disease on vanilla was initially described as forma specialis vanillae, but it was recently renamed forma specialis radicis-vanillae regarding the disease symptoms it causes (Koyyappurath et al. 2015). Nevertheless, some plants can be attacked by two different formae speciales causing the two types of symptoms. For example, tomato is susceptible to the formae speciales lycopersici causing wilt and radicis-lycopersici causing rot. In rare cases, damping off caused by F. oxysporum has also been reported, on Pinaceae and on Allium cepa for instance (Abawi and Lorbeer 1972; Bloomberg 1971; Stewart et al. 2012). Pathogenic F. oxysporum strains are occasionally reported as part of a consortium of pathogens (Beccari et al. 2010). HOW MANY F. OXYSPORUM FORMAE SPECIALES AND RACES? The latest review that many scientists still refer to dates back to more than 35 years (Armstrong and Armstrong 1981). The authors reported 79 formae speciales and mentioned races in 16 formae speciales. Since then, the known host range of F. oxysporum has considerably increased, and many new formae speciales and races have been described. Through a comprehensive review of the literature (up to August 2018), we counted 106 formae speciales that we considered to be well documented (Table 1), 37 formae speciales that we considered as insufficiently documented (Table 2), and 58 additional host plants for which no forma specialis has been characterized so far (Table 3). The host range of the formae speciales listed in Table 1 consists of plants belonging to 45 families, among which Asteraceae, Cucurbitaceae, Fabaceae, and Solanaceae are the most represented. Symptoms caused by these formae speciales correspond mainly to wilt, and for some of them to rot. Some formae speciales were described very recently, such as the formae speciales lavandulae, cichorii, crassulae, and mori (Ortu et al. 2013, 2018; Pastrana et al. 2017; Poli et al. 2012). The initially restricted host range was expanded from one to several plant species for many formae speciales (see next section). Races mostly based on cultivar-level specialization were identified in 25 of the 106 formae speciales listed in Table 1. However, the notion of race is not always used in the same way by authors, and this makes it difficult to characterize pathogenic variants within F. oxysporum. For example, pathogens of different Brassicaceae species have been described as different formae speciales (conglutinans, matthioli, and raphani), or as races of the forma specialis conglutinans (Table 1). Therefore, special focus is brought to the concept of race in a following section. Table 2 groups 37 formae speciales that we consider as insufficiently documented. These formae speciales mainly correspond to (i) pathogens isolated from diseased plants and assigned to a forma specialis without having been inoculated on the plant species of origin to confirm their pathogenicity, (ii) pathogens whose host specificity was not analyzed, and (iii) pathogens reported in Gordon’s (1965) or Armstrong and Armstrong’s (1968, 1981) reviews for which we did not have access to a publication describing the forma specialis. Moreover, some pathogens initially identified as F. oxysporum may belong to other closely related species such as some strains causing disease on pine and which actually belong to the recently described species F. commune (Gordon et al. 2015). We also included in Table 2 the formae speciales cucurbitacearum and iridacearum that have been proposed to group all formae speciales pathogenic on plants from the families Cucurbitaceae and Iridaceae, respectively (Gerlagh and Blok 1988; Palmero et al. 2014; Roebroeck 2000). Furthermore, the host range of F. oxysporum is regularly extended with the emergence of new diseases. We recorded 58 plant species or genera in the literature described as susceptible to F. oxysporum but whose forma specialis has not been characterized yet (Table 3). These 58 host plants belong to 38 different families, among which 17 are not identified in Tables 1 and 2. A total of 45 of these 58 new host plants were reported very recently, i.e., in the 2000s. The diseases caused by these “new” pathogens are mostly wilt, rot to a lesser extent, and more rarely a few other symptoms (Table 3). It is likely that the number of F. oxysporum formae Vol. 109, No. 4, 2019 513 speciales and races will keep increasing in the future. F. oxysporum host plants have been identified on all continents except the Antarctic, and its overall host range listed in the three tables presented in this review includes 73 different plant families that already represent a large host spectrum. In addition, most of these known hosts are plants of agronomic and ornamental interest, which for practical and economic reasons have so far attracted more attention than wild plants. The currrent need to control weeds by alternatives to chemical methods reveals that these plants are also infested by pathogens, including F. oxysporum strains that are potential candidates for weed biological control (Boari and Vurro 2004; Elzein et al. 2008). Moreover, the distribution of F. oxysporum is ubiquitous, so that there is a good chance that new F. oxysporum_host plant interactions, and thus new formae speciales will soon be revealed in addition to those already proposed (Table 3). Such a wide geographical distribution and wide host spectrum confirms the adaptability of F. oxysporum to the diverse biotic and abiotic environmental conditions encountered worldwide (Steinberg et al. 2016). AN EVOLVING FORMA SPECIALIS CONCEPT? F. oxysporum formae speciales are mainly described as highly specific. Their host range was initially supposed to be restricted to one plant species, but it was found to be broader for many formae speciales over time. Only 53 of the 106 formae speciales listed in Table 1 remain associated with a unique plant species to date. This number can even be less, based as few potential hosts have been tested even for well-studied formae speciales. Thus, the actual host range for any given forma specialis could well be much wider than currently recognized. Several of them were found to be pathogenic to (i) several species within a genus, e.g., forma specialis narcissi, or (ii) several genera within a plant family, e.g., forma specialis gladioli that is pathogenic to different Iridaceae plants, or finally (iii) plants belonging to different families, e.g., forma specialis vasinfectum (Table 1). Some plant species may be more permissive than others to various fungal attacks. Thus, Maltese cross appears to be a secondary host for three different formae speciales (conglutinans, dianthi, and spinaciae) (Table 1). The difficulty in defining the host specificity of F. oxysporum pathogenic strains is confounding for several formae speciales. That is why cross-pathogenicity of formae speciales cucumerinum, niveum, lagenariae, and luffae on their respective host plants led Gerlagh and Blok (1988) to propose to group all formae speciales pathogenic on cucurbitaceous crops into the new forma specialis cucurbitacearum. The situation is also confused for F. oxysporum that attacks iridaceous crops. Formae speciales gladioli, croci, and saffrani have all been described as pathogenic on Crocus spp., and the host range of the forma specialis gladioli includes several Iridaceae genera. Roebroeck (2000) proposed to assign all the strains pathogenic to iridaceous crops to a new forma specialis called iridacearum. Half of the formae speciales described so far (Table 1) are, to our current knowledge, each pathogenic to one host plant only, while the other half includes strains whose interaction specificity is much wider and sometimes leads to cross-pathogenicity. It is always possible to think that the conditions under which pathogenicity tests are carried out favor the infection of plants by strains that may not necessarily be pathogenic in natural situations. However, it is difficult to imagine that half of the tests performed so far were “false positives” caused by too high inoculum doses. Nevertheless, most of the extended host ranges reported in Table 1 were obtained under artificial inoculation conditions. This was not the case for the forma specialis radiciscucumerinum that attacked cucumber but also melon under natural conditions (Vakalounakis et al. 2005). It is now well documented that a strain of F. oxysporum pathogenic to a given host plant can be genetically closer to a strain 514 PHYTOPATHOLOGY pathogenic to another plant species, or even closer to a nonpathogenic strain than to a strain pathogenic to the same host plant (Baayen et al. 2000; Fourie et al. 2009; Inami et al. 2014; O’Donnell et al. 2009). The existence of many transposons is likely to generate mutations leading to the expression of different effectors (Chalvet et al. 2003; Daboussi and Capy 2003). Horizontal gene transfer is another mechanism that can explain genetic diversity among strains that are pathogenic to a given plant species (Ma 2014). Horizontal gene transfer may also explain cross-pathogenicity phenomena. Horizontal gene transfer between pathogenic and nonpathogenic F. oxysporum strains has indeed been demonstrated under controlled conditions, but competition among F. oxysporum populations at the plant root surface in the host plant rhizosphere provides favorable conditions for such horizontal gene transfers. SPECIAL FOCUS ON THE CONCEPT OF RACE The concept of physiological race was mentioned for Puccinia graminis in 1913 (Stakman 1913). It was defined as “a biotype or group of biotypes, within a species or lower taxon, which can be distinguished with reasonable facility and certainty from other biotypes or groups of biotypes by physiologic characters, including pathogenicity” (Stakman et al. 1962). Like the forma specialis, the race is not a formal taxonomic rank and is not codified by the International Code of Nomenclature for algae, fungi and plants. Therefore, there is no standardized procedure for naming races. They are generally numbered in chronological order of discovery. In some cases, they are defined according to the avirulence genes born by the strains included in the races, or according to the host plant resistance genes they overcome, as in the case of F. oxysporum f. sp. lycopersici (Alexander and Tucker 1945; Bohn and Tucker 1939). In the absence of a known genefor-gene relationship, races are often defined according to differential pathogenicity on different cultivars (Habgood 1970). The use of variable criteria to describe new races has led to confusion in several formae speciales. For example, up to 11 races were initially described in the forma specialis pisi before a revision cut that number down to four (Table 1). In some formae speciales, races are described according to climatic predisposition (e.g., forma specialis cubense races subtropical and tropical 4), or according to differences in plant symptoms (e.g., forma specialis melonis races 1-2 W and 1-2 Y causing wilting and yellowing symptoms, respectively) (Ploetz 2006; Risser et al. 1976). Such subgroupings are convenient as, in some cases, different patterns of symptom development are indicative of genetically distinct strains. F. oxysporum races reflect variations in virulence within the forma specialis, revealed by differential interactions with different host genotypes sometimes linked to known resistance genes. Thus, the definition of a new race intrinsically requires evaluating the pathogenicity of the strains on several host plant genotypes. The distinction between a forma specialis and a race may be narrow in some cases. For example, forma specialis conglutinans was initially described as responsible for wilting on Brassicaceae (Kendrick 1930; Pound and Fowler 1951). Later, forma specialis conglutinans strains responsible for wilting on stock and radish were reclassified as forma specialis matthioli and forma specialis raphani, respectively (Baker 1948; Kendrick and Snyder 1942), and later again as races 2 and 3 of forma specialis conglutinans (Armstrong and Armstrong 1952, 1981). Later on, Bosland and Williams (1987) restored the formae speciales conglutinans, matthioli, and raphani on the basis of pathogenic and genetic diversity. To avoid such classification issues, races should be ideally based on a gene-for-gene relationship between a pathogenic strain and its host plant; if not applicable, they should be at least defined by a clear-cut cultivar-level specialization. TABLE 1 Fusarium oxysporum formae speciales and races and their corresponding host plants Forma specialis Races Host plants (common name)a Host plant family Original references for the description of diseases, formae speciales, races, and host plantsb adzukicola 1 to 3 Vigna angularis (adzuki bean) Fabaceae Hanzawa 1906; Kitazawa and Yanagita 1984; Kondo and Kodama 1989 aechmeae (syn. aechmea) None Aechmea spp. Bromeliaceae Gordon 1965; Sauthoff and Gerlach 1957 albedinis None Phoenix dactylifera (date palm) Arecaceae Killian and Maire 1930; Gordon 1965 allii None Allium chinense syn. A. bakeri (rakkyo, Baker’s garlic) Amaryllidaceae Watanabe and Wakaida 1955; Matuo et al. 1979, 1986 anethi None Anethum graveolens (dill) Apiaceae Janson 1951; Gordon 1965 angsanae None Pterocarpus indicus (angsana) Fabaceae Crowhurst et al. 1995; Ploetz 2006b anoectochili None Anoectochilus sp. (jeweled orchid) Orchidaceae Huang et al. 2014 apii 1 to 4 Apium graveolens (celery) Apiaceae Pisum sativum (pea) Fabaceae Tithonia rotundifolia (Mexican sunflower) Asparagus officinalis (asparagus), Gossypium spp. (cotton), Solanum melongena (eggplant) Asteraceae Nelson et al. 1937; Snyder and Hansen 1940; Schneider and Norelli 1981; Puhalla 1984; Epstein et al. 2017 Armstrong and Armstrong 1957 Armstrong and Armstrong 1966a Armstrong and Armstrong 1969 Asparagaceae, Malvaceae, Solanaceae arctii None Arctium lappa (greater burdock) Asteraceae Matsuda and Ozaki 1971; Matuo et al. 1975 asparagi None Asparagus officinalis (asparagus) Asparagaceae Cohen and Heald 1941; Cohen 1946 basilici (syn. basilicum) None Ocimum basilicum (sweet basil) Lamiaceae Vergovskii 1956; Dzidzariya 1968 batatas Between 2 and 4 races Ipomoea batatas (sweet potato) Nicotiana tabacum (tobacco) Gossypium sp. (cotton) Convolvulaceae Wollenweber 1914; Snyder and Hansen 1940; Smith and Shaw 1943; Armstrong and Armstrong 1958a, 1968; Clark et al. 1998; Rodriguez-Molina et al. 2013 Solanaceae Malvaceae benincasae None Benincasa hispida (wax gourd) Cucurbitaceae Gerlagh and Ester 1985; Gerlagh and Blok 1988 betae None Beta vulgaris (sugar beet), Amaranthus retroflexus (redroot pigweed) Amaranthaceae Allium cepa (onion), Phaseolus vulgaris (common bean) Spinacia oleraceae (spinach) Amaryllidaceae, Fabaceae Stewart 1931; Snyder and Hansen 1940; MacDonald and Leach 1976; Hanson et al. 2018 Webb et al. 2013 Syn. spinaciae race 2 Amaranthaceae Armstrong and Armstrong 1976 (Continued on next page) a b According to the Integrated Taxonomic Information System (ITIS). Supplementary File S1 provides a complete list of the references listed in this table. Vol. 109, No. 4, 2019 515 TABLE 1 (Continued from previous page) Forma specialis Races Host plants (common name)a Host plant family Original references for the description of diseases, formae speciales, races, and host plantsb bouvardiae None Bouvardia sp. Rubiaceae Marziano et al. 1987 callistephi 1, 2, 3 (syn f. sp. rhois), 4 Callistephus chinensis (China aster), Tagetes erecta (African marigold), Rhus typhina (staghorn sumac) Asteraceae, Anacardiaceae Beach 1918; Snyder and Hansen 1940; Armstrong and Armstrong 1955b, 1971; Olsen 1965 canariensis None Phoenix canariensis (Canary Island date palm) Arecaceae Mercier and Louvet 1973; Summerell et al. 2001 cannabis None Cannabis sativa (hemp) Cannabaceae Noviello and Snyder 1962 capsici None Capsicum spp. (pepper) Solanaceae Leonian 1919; Rivelli 1989; Black 2003 carthami 1 to 4 Carthamus tinctorius (safflower) Asteraceae Klisiewicz and Houston 1962; Gordon 1965; Klisiewicz and Thomas 1970a, b; Klisiewicz 1975 cassiae None Senna tora syn. Cassia tora Fabaceae Several other plant hosts Several families Armstrong and Armstrong 1954b, 1966c; Gordon 1965 Armstrong and Armstrong 1966c cattleyae None Cattleya sp. Orchidaceae Foster 1955 cepae None Allium cepae (onion) Amaryllidaceae Other Allium spp. Amaryllidaceae Hanzawa 1914; Snyder and Hansen 1940; Brayford 1996a Entwistle 1990; Brayford 1996a Chrysanthemum × morifolium (chrysanthemum) Argyranthemum frutescens (Paris daisy), Gerbera jamesonii (gerbera), Osteospermum sp. (African daisy), Rudbeckia fulgida (orange coneflower) Asteraceae chrysanthemi 3 races Asteraceae Armstrong et al. 1970; Huang et al. 1992; Troisi et al. 2013 Minuto et al. 2007; Garibaldi et al. 2017; Matić et al. 2018 ciceris (syn. ciceri) 0, 1A, 1B/C, 2 to 6 Cicer arietinum (chickpea), Cicer spp. Fabaceae Prasad and Padwick 1939; Armstrong and Armstrong 1968; Haware and Nene 1982; Trapero-Casas and Jiménez-Diaz 1985; Jiménez-Diaz et al. 1989; Kaiser et al. 1994 cichorii None Cichorium intybus (chicory) Asteraceae Garibaldi et al. 2011a; Poli et al. 2012 citri None Citrus spp. Rutaceae Timmer et al. 1979; Timmer 1982; Hannachi et al. 2014 colocasiae None Colocasia esculenta (taro) Araceae Nishimura and Kudo 1994 (Continued on next page) 516 PHYTOPATHOLOGY TABLE 1 (Continued from previous page) Forma specialis conglutinans Races 1, 2 (syn. f. sp. raphani), 3 (syn. f. sp. matthioli race 1), 4 (syn. f. sp. matthioli race 2), 5 Host plants (common name)a Host plant family Brassica oleracea (cabbage), Raphanus sativus (radish), Matthiola incana (stock) Brassicaceae Silene chalcedonica syn. Lychnis chalcedonica (Maltese cross), Valerianella locusta syn. V. olitoria (lamb’s lettuce) Caryophyllaceae, Valerianaceae Original references for the description of diseases, formae speciales, races, and host plantsb Kendrick 1930; Wollenweber 1913; Snyder and Hansen 1940; Armstrong and Armstrong 1952, 1966b; Ramirez-Villupadua et al. 1985; Bosland and Williams 1987 Armstrong and Armstrong 1966b; Gilardi et al. 2008 crassulae None Crassula ovata (jade plant) Crassulaceae Garibaldi et al. 2011b; Ortu et al. 2013 croci None Crocus sp. (crocus) Iridaceae Boerema and Hamers 1989; Palmero et al. 2014 cubense 1, 2, subtropical race 4, tropical race 4 Musa spp. (banana) Musaceae 1 Asparagus officinalis (asparagus) Heliconia spp. (heliconia) Asparagaceae Smith 1910; Snyder and Hansen 1940; Stover and Waite 1960; Ploetz 2006a Armstrong and Armstrong 1969 Waite 1963; Ploetz and Bentley 2001 3 (syn. f. sp. heliconiae) Heliconiaceae cucumerinum 1 to 3 Cucumis sativus (cucumber), C. melo (melon syn. muskmelon), Citrullus lanatus syn. C. vulgaris (watermelon) Cucurbitaceae van Koot 1943; Owen 1956; Armstrong et al. 1978; Kim et al. 1993 cumini None Cuminum cyminum (cumin) Apiaceae Patel et al. 1957 cyclaminis None Cyclamen persicum (cyclamen) Primulaceae Other Cyclamen spp. (cyclamen) Primulaceae Wollenweber and Reinking 1935; Gerlach 1954 Orlicz-Luthardt 1998 delphinii None Delphinium spp. (delphinium) Ranunculaceae Martin 1922; Laskaris 1949; Kondo et al. 2013 dianthi 1, 2, 4 to 11 (race 3 was reclassified as F. redolens f. sp. dianthi) Dianthus caryophyllus (carnation) Caryophyllaceae None Other Dianthus spp., Silene chalcedonica syn. Lychnis chalcedonica (Maltese cross) Caryophyllaceae Prillieux and Delacroix 1899; Snyder and Hansen 1940; Garibaldi 1975; Baayen et al. 1997 Armstrong and Armstrong 1954a echeveriae None Echeveria spp. Crassulaceae Farr et al. 1989; Ortu et al. 2015a; Garibaldi et al. 2015a elaeidis None Elaeis guineensis (oil palm) Arecaceae Wardlaw 1946; Toovey 1949; Gordon 1965 erythroxyli None Erythroxylum coca, E. novogranatense (coca) Erythroxylaceae Sands et al. 1997 (Continued on next page) Vol. 109, No. 4, 2019 517 TABLE 1 (Continued from previous page) Forma specialis Races Host plants (common name)a Host plant family Original references for the description of diseases, formae speciales, races, and host plantsb eucalypti None Eucalyptus gonphocephala, E. rudis (eucalyptus) Myrtaceae Arya and Jain 1962 eustomae None Eustoma grandiflorum (lisianthus) Gentianaceae Raabe 1981; Bertoldo et al. 2015 exaci None Exacum affine (Persian violet) Gentianaceae Elmer and O’Dowd 2001 fabae None Vicia faba (broad bean) Fabaceae Yu and Fang 1948 fatshederae None ×Fatshedera lizei Araliaceae Triolo and Lorenzini 1983 fragariae None Fragaria sp. (strawberry) Rosaceae Winks and Williams 1965; Brayford 1996b garlic None Allium sativum (garlic) Amaryllidaceae Matuo et al. 1986; Brayford 1996a gladioli 1 and 2 Gladiolus sp. (gladiolus) Iridaceae Babiana sp., Crocus sativus (saffron), Crocus sp. (crocus), Freesia sp. (freesia), Iris sp. (iris), Ixia sp. (corn lily), Sparaxis sp. (wandflower), Streptanthera cuprea, Tritonia spp., Watsonia sp. (bugle lily) Iridaceae Massey 1926; Snyder and Hansen 1940; Roebroeck and Mes 1992 McClellan 1945; Di Primo et al. 2002 glycines None Glycine max (soybean) Fabaceae Armstrong and Armstrong 1965a hebae (syn. habae, hebe) None Hebe spp. Plantaginaceae Raabe 1957, 1985 heliconiae (syn. cubense race 3) None Heliconia spp. (heliconia) Heliconiaceae Waite 1963; Ploetz and Bentley 2001; Ploetz 2006a heliotropae None Heliotropium europaeum (heliotrope) Heliotropiaceae Netzer and Weintal 1987 koae None Acacia spp. (koa) Fabaceae Gardner 1978; Gardner 1980 laciniati None Solanum laciniatum Solanaceae Pandotra et al. 1971 lactucae (syn. lactucum) 1 to 4 Lactuca sativa (lettuce) Asteraceae Motohashi et al. 1960; Matuo and Motohashi 1967; Hubbard and Gerik 1993; Fujinaga et al. 2001, 2003; Gilardi et al. 2017 lagenariae (syn. lagenaria) None Lagenaria siceraria syn. L. vulgaris (bottle gourd), Cucurbita ficifolia (figleaf gourd syn. malabar gourd), C. maxima (winter squash) Cucurbitaceae Matuo and Yamamoto 1965; Armstrong and Armstrong 1978a; Nomura 1992; Namiki et al. 1994 lathyri None Lathyrus sativus Fabaceae Bhide and Uppal 1948; Gordon 1965 lavandulae None Lavandula × allardii (lavander) Lamiaceae Garibaldi et al. 2015b; Ortu et al. 2018 (Continued on next page) 518 PHYTOPATHOLOGY TABLE 1 (Continued from previous page) Forma specialis Races Host plants (common name)a Host plant family Original references for the description of diseases, formae speciales, races, and host plantsb lentis 1 to 8 Lens culinaris syn. L. esculenta (lentil) Fabaceae Vasudeva and Srinivasan 1952; Gordon 1965; Pouralibaba et al. 2016; Hiremani and Dubey 2018 lilii None Lilium spp. (lily) Liliaceae Imle 1940, 1942; Baayen et al. 1998 lini Unclear Linum usitatissimum (flax) Linaceae Bolley 1901; Snyder and Hansen 1940; Brayford 1996c; Kroes et al. 1999 loti None Lotus corniculatus (birdsfoot trefoil) Fabaceae Gotlieb and Doriski 1983; Wunsch et al. 2009 luffae None Luffa aegyptiaca (sponge gourd), Cucumis melo (melon syn. muskmelon) Cucurbitaceae Kawai et al. 1958; Armstrong and Armstrong 1978a lupini 1 to 3 Lupinus spp. (lupine) Fabaceae Wollenweber and Reinking 1935; Snyder and Hansen 1940; Armstrong and Armstrong 1964 lycopersici 1 to 3 Solanum lycopersicum (tomato) Solanaceae Saccardo 1886; Bohn and Tucker 1939; Snyder and Hansen 1940; Alexander and Tucker 1945; Grattidge and O’Brien 1982 matthioli (syn. mathioli, matthiolae) 1 (syn. f. sp. conglutinans race 3) and 2 (syn. f. sp. conglutinans race 4) Matthiola incana (stock) Brassicaceae Baker 1948; Armstrong and Armstrong 1952; Bosland and Williams 1987 medicaginis None Medicago sativa (alfalfa) Fabaceae Asparagus officinalis (asparagus) Asparagaceae Weimer 1927, 1928; Snyder and Hansen 1940 Armstrong and Armstrong 1969 melongenae None Solanum melongena (eggplant) Solanaceae Matuo and Ishigami 1958; Armstrong and Armstrong 1969 melonis 0, 1, 2, 1.2Y, 1.2W (previously 1 to 4) Cucumis melo (melon syn. muskmelon) Cucurbitaceae 1 to 7 Cucumis melo (melon syn. muskmelon) Cucurbitaceae Leach and Currence 1938; Snyder and Hansen 1940; Risser and Mas 1965; Risser et al. 1969, 1976 Armstrong and Armstrong 1978a momordicae None Momordica charantia (bitter gourd) Cucurbitaceae Sun and Huang 1983 mori None Rubus subgenus Rubus (blackberry) Rosaceae Gordon et al. 2016; Pastrana et al. 2017 narcissi None Narcissus spp. (narcissus) Amaryllidaceae Cooke 1887; Snyder and Hansen 1940; Linfield 1992 nelumbicolum (syn. nelumbicola) None Nelumbo sp. (lotus) Nelumbonaceae Nisikado and Watanabe 1953; Gordon 1965; Armstrong and Armstrong 1981 (Continued on next page) Vol. 109, No. 4, 2019 519 TABLE 1 (Continued from previous page) Forma specialis niveum Races 0 to 3 Host plants (common name)a Host plant family Citrullus lanatus (watermelon) Cucurbitaceae Cucurbita pepo (squash) Cucurbitaceae Original references for the description of diseases, formae speciales, races, and host plantsb Smith 1894; Snyder and Hansen 1940; Cirulli 1972; Netzer and Dishon 1973; Netzer 1976; Zhou et al. 2010 Martyn and McLaughlin 1983 opuntiarum None Opuntia ficus-indica (tuna cactus syn. spineless cactus), Echinocactus grusonii (golden barrel cactus), Espostoa lanata (peruvian old man cactus), Schlumbergera truncata (Thanksgiving cactus), Ferocactus latispinus (devil’s tongue barrel cactus), Mammillaria zeilmanniana, Astrophytum myriostigma, Cereus spp. Euphorbia mammillaris Cactaceae Pettinari 1951; Gordon 1965; Polizzi and Vitale 2004; Lops et al. 2013; Garibaldi et al. 2014, 2016; Bertetti et al. 2017 Euphorbiaceae Bertetti et al. 2017 palmarum None Syagrus romanzoffiana (queen palm), Washingtonia robusta (Mexican fan palm), Phoenix canariensis (Canary Island date palm), × Butyagrus nabonnandii (mule palm) Arecaceae Elliott et al. 2010, 2017; Elliott 2011 papaveris None Papaver nudicaule (iceland poppy) Papaveraceae Papaver spp., Chelinodium majus Papaveraceae Katan 1999; Garibaldi et al. 2012; Ortu et al. 2015b Bertetti et al. 2018 passiflorae None Passiflora edulis (passionflower), other Passiflora spp. Passifloraceae McKnight 1951; Gordon 1965; Gardner 1989 perillae None Perilla frutescens (perilla) Lamiaceae Kim et al. 2002 perniciosum None Albizia julibrissin (mimosa tree) Albizia julibrissin (race 1), A. procera (race 2) Fabaceae Hepting 1939; Snyder et al. 1949 Toole 1952 1.2 Phaseolus vulgaris (common bean), P. coccineus Fabaceae phaseoli 1 to 7 27 races Phaseolus vulgaris Fabaceae pisi 1, 2, 5, 6 (up to 11 races before a revision of the race classification) Pisum sativum (garden pea) Fabaceae Cicer arietinum (chickpea) Fabaceae Fabaceae Harter 1929; Kendrick and Snyder 1942a; Ribeiro and Hagedorn 1979; Woo et al. 1996; AlvesSantos et al. 2002 Henrique et al. 2015 Lindford 1928; Snyder 1933; Snyder and Hansen 1940; Schreuder 1951; Bolton et al. 1966; Haglund and Kraft 1970, 1979; Kraft and Haglund 1978 De Curtis et al. 2014 (Continued on next page) 520 PHYTOPATHOLOGY TABLE 1 (Continued from previous page) Forma specialis Races Host plants (common name)a Host plant family Original references for the description of diseases, formae speciales, races, and host plantsb psidii None Psidium guajava (guava) Myrtaceae Hayes 1945; Prasad et al. 1952; Pandey and Dwivedi 1985 pyracanthae None Pyracantha spp. (firethorn) Rosaceae McRitchie 1973; Armstrong and Armstrong 1981 radicis-betae None Beta vulgaris (sugar beet) Amaranthaceae Martyn et al. 1989; Harveson and Rush 1998; Hanson et al. 2018 radicis-capsici None Capsicum annuum, C. chinense (pepper) Solanaceae Lomas-Cano et al. 2014, 2016; Pérez-Hernández et al. 2014 radicis-cucumerinum None Cucumis sativus (cucumber), C. melo (melon syn. muskmelon), Luffa aegyptiaca (sponge gourd), Citrullus lanatus syn. C. vulgaris (watermelon), Cucurbita pepo (squash) Cucurbitaceae Vakalounakis 1996; Punja and Parker 2000; Vakalounakis et al. 2005; Cohen et al. 2015 radicis-lupini None Lupinus spp. (lupine) Fabaceae Weimer 1941, 1944 radicis-lycopersici None Solanum lycopersicum (tomato) Solanaceae Solanum melongena (eggplant) Fabaceae spp. Solanaceae Leary and Endo 1971; Jarvis and Shoemaker 1978 Rowe 1980 Fabaceae Rowe 1980; Menzies et al. 1990 Pirayesh et al. 2018 Cucurbitaceae spp. Cucurbitaceae radicis-vanillae (syn. vanillae) None Vanilla spp. (vanilla) Orchidaceae Thomas 1918; Tucker 1927; Koyyappurath et al. 2015 ranunculi None Ranunculus sp. (buttercup) Ranunculaceae Garibaldi 1980; Garibaldi and Gullino 1985 rapae None Brassica rapa Brassicaceae Takeuchi and Kagawa 1996; Enya et al. 2008 raphani (syn. conglutinans race 2) None Raphanus sativus (radish), Diplotaxis tenuifolia (wild rocket), Eruca vesicaria syn. sativa (rocket salad) Brassicaceae Kendrick and Snyder 1942b; Bosland and Williams 1987; Garibaldi et al. 2006 rauvolfii None Rauvolfia serpentina Apocynaceae Janardhanan et al. 1964 rhois (syn. callistephi race 3) None Rhus typhina (staghorn sumac) Anacardiaceae Toole et al. 1948; Toole 1949; Snyder et al. 1949; Armstrong and Armstrong 1981 saffrani None Crocus sativus (saffron) Iridaceae Palmero et al. 2014 simmondsia None Simmondsia chinensis (jojoba) Simmondsiaceae Tsror (Lahkim) and Erlich 1996; Tsror (Lahkim) et al. 2007 spinaciae 1, 2 Spinacia oleracea (spinach), Beta vulgaris (beet) Amaranthaceae Hungerford 1923; Armstrong and Armstrong 1955a, 1976 (Continued on next page) Vol. 109, No. 4, 2019 521 Races have been described in 25 of the 106 formae speciales described to date. These are formae speciales corresponding to plants of agronomic or ornamental interest. Although causality has not been demonstrated, it is difficult not to incriminate the role of humans in the current distribution and the emergence of new races within formae speciales. When interaction frequency between the host plant and the pathogenic F. oxysporum is low, as is the case with a few cultivated plants or plants not submitted to intensive cultivation, we may reasonably think that the first races that are described result from coevolution between pathogenic F. oxysporum strains within a forma specialis and the host plant, therefore gene-for-gene relationships are expected. In view of the genetic selection done by breeders, it is more difficult to know if the newly cultivated genotypes act as accelerators of the evolution of phytopathogenic fungi or only reveal preexisting bypass genes that nothing could highlight otherwise. It is therefore clear that molecular markers are needed to unambiguously identify the races within formae speciales but also to understand the mechanisms of their emergence, even if this results in revising the initially defined genefor-gene contours of the race concept. TABLE 1 (Continued from previous page) Forma specialis Races Host plants (common name)a Host plant family Original references for the description of diseases, formae speciales, races, and host plantsb Silene chalcedonica syn. Lychnis chalcedonica (Maltese cross) Caryophyllaceae Armstrong and Armstrong 1966b, 1976 strigae None Striga hermonthica, S. asiatica, S. gesnerioides (witchweed) Orobanchaceae Ciotola et al. 1995; Marley et al. 2005; Elzein et al. 2008 tracheiphilum 1 to 4 Vigna unguiculata (cowpea), Glycine max (soybean) Fabaceae Chrysanthemum × morifolium (chrysanthemum), Gerbera jamesonii (gerbera) Asteraceae Smith 1895; Snyder and Hansen 1940; Armstrong and Armstrong 1950; Hare 1953; Armstrong and Armstrong 1965a, 1968; Smith et al. 1999 Armstrong and Armstrong 1965b; Troisi et al. 2010 trifolii None Trifolium spp. (clover) Fabaceae Jaczewski 1917; Bilai 1955; Gordon 1965; Pratt 1982 tuberosi None Solanum tuberosum (potato) Solanaceae Wollenweber 1916; Smith and Swingle 1904; Snyder and Hansen 1940; Manici and Cerato 1994 tulipae None Tulipa spp. (tulip) Liliaceae Apt 1958a, b; Baayen et al. 1998 vasinfectum 1, 2, 3, 4, 6, 8 Gossypium spp. (cotton), Abelmoschus esculentus syn. Hibiscus esculentus (okra) Malvaceae Senna sp. syn. Cassia tora, Medicago sp. (alfalfa), Glycine sp. (soybean), Nicotiana sp. (tobacco), Physalis alkekengi, Tithonia rotundifolia (Mexican sunflower) Fabaceae, Solanaceae, Asteraceae Atkinson 1892; Fahmy 1927; Armstrong et al. 1942; Armstrong and Armstrong 1958b, 1960, 1978b; Ibrahim 1966; Chen et al. 1985; Nirenberg et al. 1994; Cianchetta and Davis 2015 Armstrong et al. 1942; Armstrong and Armstrong 1954b, 1958b, 1959, 1960, 1969 voandzeiae None Vigna subterranea syn. Voandzeia subterranea (bambarra groundnut) Fabaceae Ebbels and Billington 1972; Armstrong et al. 1975 zingiberi None Zingiber officinale (ginger) Zingiberaceae Trujillo 1963; Armstrong and Armstrong 1968; Stirling 2004 522 PHYTOPATHOLOGY HOW TO DESCRIBE A NEW FORMA SPECIALIS OR RACE? The forma specialis is not a taxonomic rank, therefore the nomenclature of formae speciales is not codified by the International Code of Nomenclature for algae, fungi and plants (Art. 4 Note 4). In other words, the definition of a new forma specialis does not follow the rules of nomenclature established by the International Code of Nomenclature for algae, fungi and plants. Any author describing a new forma specialis is free to choose its name. As a result, many formae speciales were named according to the host plant Latin name, either the genus name or the species name, or according to the host plant common name (Table 1). The lack of any standardized nomenclature causes confusion in the definition of TABLE 2 Insufficiently documented Fusarium oxysporum formae speciales Forma specialis Host plants (common name)a Referencesb Host plant family Comments adzuki Glycine max Fabaceae John et al. 2010 Insufficiently documented forma specialis aleuritidis Vernicia fordii (tungoil tree) Euphorbiaceae Suelong 1981 Insufficiently documented forma specialis amaranthi Amaranthus hybridus (amaranth) Amaranthaceae Chen and Swart 2001; Leslie and Summerell 2006 Insufficiently documented forma specialis barbati Dianthus barbatus (sweet William) Caryophyllaceae Snyder 1941; Armstrong and Armstrong 1954; Gordon 1965; Baayen et al. 1997 Possible confusion with F. redolens f. sp. barbati blasticola Conifers Several families Bilai 1955; Gordon 1965 Synonym of forma specialis pini according to Gordon 1965 coffeae Coffea arabica (coffee) Rubiaceae Garcia 1945 Insufficiently documented forma specialis coriandrii Coriandrum sativum (coriander) Apiaceae Narula and Joshi 1963; Koike and Gordon 2005 Insufficiently documented forma specialis cucurbitacearum Cucurbitaceae spp. Cucurbitaceae Gerlagh and Blok 1988 Gerlagh and Blok (1988) proposed to group together all the formae speciales pathogenic to plants from the family Cucurbitaceae dahliae Dahlia sp. (dahlia) Asteraceae Solovjova and Madumarov 1969; Armstrong and Armstrong 1981 Insufficiently documented forma specialis dioscoreae Dioscorea rotundata (yam) Dioscoreaceae Wellman 1972 Insufficiently documented forma specialis elaeagni Elaeagnus sp. Elaeagnaceae Armstrong and Armstrong 1968 Insufficiently documented forma specialis eleocharidis Eleocharis dulcis syn. tuberosa (Chinese water chestnut) Cyperaceae Donghua et al. 1988 Insufficiently documented forma specialis erucae Eruca vesicaria syn. sativa (rocket salad) Brassicaceae Chatterjee and Rai 1974; Garibaldi et al. 2003, 2006 The wilt of Eruca versicaria could be caused by F. oxysporum f. sp. raphani freesia Freesia sp. Iridaceae Baayen et al. 2000; Taylor et al. 2016 Misidentification of two strains of f. sp. gladioli isolated from Freesia gerberae Gerbera jamasonii, hybrids (gerbera) Asteraceae von Arx 1952; Gordon 1965 Insufficiently documented forma specialis herbemontis Vitis spp. (grape) Vitaceae Tochetto 1954; Gordon 1965 Insufficiently documented forma specialis hyacinthi Hyacinthus sp. (hyacinth) Asparagaceae Muller 1978; Baayen et al. 2001 Possible confusion with F. hostae iridacearum Iridaceae spp. Iridaceae Roebroeck 2000; Palmero et al. 2014 Roebroeck (2000) proposed to group together all the formae speciales pathogenic to plants from the family Iridaceae (Continued on next page) a b According to the Integrated Taxonomic Information System (ITIS). Supplementary File S2 provides a complete list of the references listed in this table. Vol. 109, No. 4, 2019 523 formae speciales. Thus, some formae speciales have multiple names, e.g., the forma specialis matthioli also named mathioli or matthiolae. Any description of a new forma specialis or race should only be published after a meticulous search in the literature to avoid any duplicate entry. Moreover, pathogenicity should be evaluated in such conditions that the full pathogenic potentiality of the fungal isolate is expressed, i.e., controlled conditions, nonexcessive inoculum dose and clearly identified susceptible cultivar. We suggest that proposing a new forma specialis or race should require the following at a minimum: - Morphological and molecular identifications of the new isolate at the species level. TABLE 2 (Continued from previous page) Host plants (common name)a Forma specialis Host plant family Referencesb Comments magnoliae Magnolia sp. Magnoliaceae Lin and Chen 1994 Insufficiently documented forma specialis nicotianae Nicotiana tabacum (tobacco), Ipomoea batatas (sweet potato) Solanaceae, Convolvulaceae Johnson 1921; Snyder and Hansen 1940; Clark et al. 1998; Rodriguez-Molina et al. 2013 F. oxysporum causes wilt of tobacco but the existence of the forma specialis nicotianae is debated among scientists orthoceras Orobanche sp. (broomrape) Orobanchaceae Wollenweber 1917; Snyder and Hansen 1940; Bilai 1955; Gordon 1965; Bedi 1994; Thomas et al. 1998 F. orthoceras was a synonym of F. oxysporum in early classifications of Fusarium. Some F. oxysporum strains are pathogenic to Orobanche spp. but the corresponding forma specialis is insufficiently described phormii Phormium tenax (New Zealand flax) Xanthorrhoeaceae Wager 1947 Insufficiently documented forma specialis physali Physalis peruviana (cape gooseberry) Solanaceae Simbaqueba 2017 Insufficiently documented forma specialis pini Pinus spp. (pine) Pinaceae Hartig 1892; Ten Houten 1939; Snyder and Hansen 1940; Matuo and Chiba 1966; Gordon et al. 2015 Insufficiently documented forma specialis. Possible confusion with F. subglutinans f. sp. pini, or F. commune querci Quercus sp. (oak) Fagaceae Georgescu and Mocanu 1956; Gordon 1965 Insufficiently documented forma specialis quitoense Solanum quitoense (naranjilla) Solanaceae Ochoa et al. 2001; Ochoa et al. 2004 Insufficiently documented forma specialis ricini Ricinus communis (castor bean) Euphorbiaceae Gordon 1965 Insufficiently documented forma specialis rosellae Hibiscus sabdariffa (roselle) Malvaceae Ooi and Salleh 1999; Ploetz et al. 2007 Insufficiently documented forma specialis sansevieriae Sansevieria cylindrica Asparagaceae Gupta et al. 1982 Insufficiently documented forma specialis sedi Sedum sp. Crassulaceae Raabe 1960 Insufficiently documented forma specialis sesami Sesamum indicum (sesame) Pedaliaceae Castellani 1950 Insufficiently documented forma specialis sesbaniae Sesbania sesban syn. S. aegyptiaca Fabaceae Singh 1956 Insufficiently documented forma specialis stachydis Stachys sieboldii Lamiaceae Jotani 1953; Gordon 1965 Insufficiently documented forma specialis tabernaemontanae Tabernaemontana divaricata syn. T. coronaria Apocynaceae Pande and Rao 1990 Insufficiently documented forma specialis tanaceti Tanacetum parthenium (feverfew) Asteraceae Hirooka et al. 2008 Insufficiently documented forma specialis vanillae Vanilla spp. (vanilla) Orchidaceae Thomas 1918; Tucker 1927; Gordon 1965; Koyyappurath et al. 2015 Renamed as f. sp. radicisvanillae vasconcella Carica × heilbornii (babaco) Caricaceae Ochoa et al. 2000, 2004 Insufficiently documented forma specialis 524 PHYTOPATHOLOGY - A full description of the protocol used for validating Koch’s postulates, including the protocol and results of the pathogenicity test(s) together with the observed symptoms. - Evaluation of the specificity of the interaction between the new pathogenic strain and the host plant, and characterization of the host spectrum of the strain; appropriate crops to include would be those in the same plant family and/or grown in rotation with the known susceptible host. - The name of the new forma specialis according to the host plant Latin name when possible. - The race number according to the chronological order of discovery, and the identified virulence gene, if any. - The accepted Latin binomial name of the host plant and the identified resistance gene, if any. - The names of one or more cultivars that have been demonstrated to be susceptible, along with differential cultivars where races have been described. Ideally, these are publicly available cultivars. - The deposition of representative isolates in an international collection of microorganisms. - The preservation of the host plant germplasms in an international collection, especially when a new race is described. - Publication in a peer-reviewed journal including all the biological details and providing the accession numbers in the text. TABLE 3 Fusarium oxysporum host plants for which no forma specialis has been described Host plants (common name)a Host plant family Actinotus helianthi (flannel flower) Apiaceae Symptoms Referencesb Wilt Bullock et al. 1998 Aloe vera syn. A. barbadensis (Barbados aloe) Xanthorrhoeaceae Root and crown rot Vakalounakis et al. 2015 Alstroemeria spp. (lily of the Incas) Alstroemeriaceae Wilt Shanmugam et al. 2007 Anemone sp. syn Pulsatilla koreana (pasqueflower) Ranunculaceae Root rot Su and Fu 2013 Astrophytum ornatum Cactaceae Wilt Quezada-Salinas et al. 2017 Bougainvillea glabra (paper flower) Nyctaginaceae Wilt Polizzi et al. 2010a Carya cathayensis (Chinese hickory) Juglandaceae Rot Zhang et al. 2015 Chrozophora tinctorial (turnsole) Euphorbiaceae Wilt Trapero-Casas and Kaiser 1998 Cichorium endivia (endive) Asteraceae Wilt Garibaldi et al. 2009 Cladrastis kentukea (yellowwood) Fabaceae Wilt Graney et al. 2017 Coleus forskohlii Lamiaceae Wilt Zheng et al. 2012 Coreopsis verticillata Asteraceae Wilt Elmer et al. 2007 Cucurbita pepo (zucchini) Cucurbitaceae Wilt Park et al. 2015 Cymbidium spp. Orchidaceae Root and stem rot Benyon et al. 1996; Yao et al. 2018 Daphne sp. Thymelaeaceae Wilt Kim et al. 2005 Daucus carota (carrot) Apiaceae Wilt Han et al. 2012 Dendrobium spp. Orchidaceae Wilt Xiao et al. 2012; Zhang et al. 2017 Eremophila spp. Scrophulariaceae Wilt Polizzi et al. 2010b Fallopia multiflora (tuber fleeceflower, hasuo) Polygonaceae Wilt Park et al. 2015 Firmiana simplex (Phoenix tree, Chinese parasol tree) Malvaceae Stem canker Zhang et al. 2013 Helichrysum spp. Asteraceae Wilt Summerell and Rugg 1992 Hevea brasiliensis (rubber tree) Euphorbiaceae Stem rot Li et al. 2014 Hoodia gordonii Apocynaceae Wilt Philippou et al. 2013 Hosta sp. (plantain lily) Asparagaceae Root and crown rot Wang and Jeffers 2000 Gastrodia elata Orchidaceae Tuber rot Zhao et al. 2017 Glycyrrhiza spp. (licorice) Fabaceae Rot, wilt Cao et al. 2013; Abedi-Tizaki and Zafari 2014 Gypsophila spp. Caryophyllaceae Wilt Werner and Irzykowska 2007 Lavandula pubescens Lamiaceae Wilt Perveen and Bokhari 2010 Lewisia spp. (bitterroot) Montiaceae Wilt Garibaldi et al. 2005; Gullino et al. 2015 (Continued on next page) a b According to the Integrated Taxonomic Information System (ITIS). Supplementary File S3 provides a complete list of the references listed in this table. Vol. 109, No. 4, 2019 525 TOWARD MOLECULAR TOOLS TO IDENTIFY F. OXYSPORUM FORMAE SPECIALES AND RACES The internal transcribed spacer (ITS) has been proposed as the barcode for fungal species identification (Seifert 2009). However, this DNA marker cannot identify all Fusarium species unequivocally (O’Donnell and Cigelnik 1997). The translation elongation factor 1-a (TEF1) and the DNA-directed RNA polymerase II largest subunit (RPB1) and second largest subunit (RPB2) are Fusarium phylogenetically informative loci and allow for species identification (O’Donnell et al. 2013, 2015). The TEF1 locus is also informative at the intraspecific level and can be combined with others such as the ribosomal intergenic spacer to reveal the complex genetic diversity within F. oxysporum (Canizares et al. 2015; EdelHermann et al. 2012, 2015; Lecomte et al. 2016; O’Donnell et al. 2009; Ortu et al. 2018). Sequence resources are available in the FUSARIUM-ID database (http://isolate.fusariumdb.org/guide.php; Geiser et al. 2004; Park et al. 2011) and the Fusarium MLST database (http://www.westerdijkinstitute.nl/fusarium/; O’Donnell et al. 2010). The literature about F. oxysporum genetic diversity is very abundant. Studies are based on the use of various molecular tools that have evolved over time, as well as on the use of vegetative compatibility groups (VCGs) that group together genetically similar strains (Puhalla 1985). The number of VCGs in a given forma specialis is generally between 1 and 10, but can be up to 24 as in forma specialis cubense (Aguayo et al. 2017; Katan 1999; Kistler et al. 1998). F. oxysporum diversity studies aim at identifying specific forma specialis markers to design diagnostic tools (Lievens et al. 2008). Many formae speciales are known to be polyphyletic, making it difficult to identify specific molecular markers (Baayen et al. 2000; Epstein et al. 2017; Fourie et al. 2009; Hill et al. 2011; Koyyappurath et al. 2015; O’Donnell et al. 1998, 2009). Additionally, soilborne and endophytic nonpathogenic F. oxysporum isolates can be highly variable genetically and closely related to pathogenic ones (Baayen et al. 2000; Edel et al. 2001; Fourie et al. 2009; Imazaki and Kadota 2015; Inami et al. 2014). One approach used to identify molecular markers of F. oxysporum formae speciales or races relies on insertion TABLE 3 (Continued from previous page) Host plants (common name)a Host plant family Referencesb Symptoms Limonium sinuatum (statice) Plumbaginaceae Wilt Taylor et al. 2017 Mandevilla (syn. Dipladenia) sp. Apocynaceae Wilt Sella et al. 2010 Medinilla myriantha Melastomataceae Stem rot Hernández-Lauzardo et al. 2018 Miscanthus × giganteus Poaceae Rhizome rot Beccari et al. 2010 Pandanus utiliz (screwpine) Pandanaceae Leaf spot Guo et al. 2016 Paris polyphylla (Rhizoma Paridis) Melanthiaceae Stem rot Zhou et al. 2018 Phalaenopsis spp. Orchidaceae Wilt Kim et al. 2006 Philodendron hederaceum var. oxycardium (syn. P. oxycardium) Araceae Stem rot Wang et al. 2016 Plantago ovata (desert Indianwheat) Plantaginaceae Wilt Russell 1975 Plukenetia volubilis (Sacha Inchi) Euphorbiaceae Root and stem rot Chai et al. 2018 Portulaca molokiniensis (ihi) Portulacaceae Stalk and root rot Ma et al. 2018 Protea spp. Proteaceae Wilt Swart et al. 1999 Prunus avium (sweet cherry) Rosaceae Root and crown rot Úrbez-Torres et al. 2016 Pseudotsuga menziesii (Doublas-fir) Pinaceae Damping off Bloomberg 1971; Stewart et al. 2012 Pterocarpus angolensis Fabaceae Wilt Piearce 1979 Rheum sp. (rhubarb) Polygonaceae Leaf blight Thakur et al. 2015 Rhus aromatica (fragrant sumac), R. trilobata (skunkbush sumac) Anacardiaceae Wilt O’Mara and Tisserat 1997 Rosmarinus officinalis (rosemary) Lamiaceae Wilt Ashrafi et al. 2010 Saccharum sp. (sugarcane) Poaceae Foliar disease Bao et al. 2016 Salvia sclarea (clary sage) Lamiaceae Seedling disease Subbiah et al. 1996 Sanguinaria canadensis (bloodroot) Papaveraceae Crown rot Elmer and Marra 2012 Smallanthus sonchifolius (yacon potato) Asteraceae Root rot Moraes et al. 2017 Solanum aculeatissimum syn. S. khasianum (nightshade) Solanaceae Wilt Bordoloi et al. 1972 Tectona grandis (teak) Lamiaceae Wilt Borges et al. 2018 Torreya grandis Taxaceae Crown and root rot Zhang et al. 2016 Trigonella foenum-graecum (fenugreek) Fabaceae Wilt Shivpuri and Bansal 1987 Vaccinium corymbosum (blueberry) Ericaceae Wilt Liu et al. 2014 Ziziphus jujuba Rhamnaceae Rot Rao 1964 526 PHYTOPATHOLOGY sites of transposable elements; it provided specific detection tools for formae speciales albedinis and lactucae, among others (Fernandez et al. 1998; Pasquali et al. 2007). In other cases, random amplified polymorphic DNA allowed researchers to identify sequencecharacterized amplified region (SCAR) markers. Following this strategy, detection tools were developed for formae speciales basilici, cyclaminis, phaseoli, eustomae, cucumerinum, and radicis-cucumerinum (Alves-Santos et al. 2002; Chiocchetti et al. 2001; Lecomte 2016; Li et al. 2010; Lievens et al. 2007). A few SCAR primers specifically detected races, e.g., in formae speciales ciceri and melonis (Jiménez-Gasco and Jiménez-Dı́az 2003; Luongo et al. 2012). Molecular identification of F. oxysporum formae speciales would ideally target pathogenicity-related genes. Although knowledge on these genetic determinants was scarce until recently, it has considerably improved in the last decade. One of the first such tools was developed for the forma specialis lycopersici, based on a host-specific virulence gene (Rep et al. 2004; Lievens et al. 2009). The gene encodes a small protein secreted in the xylem (SIX) which confers virulence to the fungus. Fourteen SIX genes are currently known, and a few homologs were found in other formae speciales such as cepae, cubense, and conglutinans (Fraser-Smith et al. 2014; Li et al. 2016; Taylor et al. 2016; van Dam et al. 2016). PCR primers were designed from SIX sequences to discriminate the formae speciales cubense and lycopersici from other formae speciales (Fraser-Smith et al. 2014; Lievens et al. 2009). Molecular markers based on other virulence factors were also designed for forma specialis phaseoli and for race 4 of forma specialis cubense (Aguayo et al. 2017; Sousa et al. 2015). Apart from effector genes, other genes involved in F. oxysporum pathogenicity have been described as genes encoding cell wall-degrading enzymes or transcriptional regulators (Jonkers et al. 2009; Michielse et al. 2009a, 2009b). However, comparative genomics is the next step to identify host specificity in F. oxysporum. van Dam et al. (2016) performed whole genome sequencing of 45 F. oxysporum strains and managed to differentiate formae speciales cucumerinum, niveum, melonis, radicis-cucumerinum, and lycopersici on the basis of their effector pattern. Two years later, van Dam et al. (2018) designed PCR primers to discriminate the seven formae speciales that affect Cucurbitaceae based on candidate effectors extracted from 82 genome assemblies. There is no doubt that the expanding access to whole-genome sequences will continuously improve F. oxysporum host range identification. SUMMARY AND FUTURE PROSPECTS Many authors admit that the number of F. oxysporum formae speciales and races described in the review of Armstrong and Armstrong (1981) is out of date and suggest various and unfounded estimates of this number in the introduction of many papers dealing with F. oxysporum. More than the need to correct these estimates, the concomitant evolution of knowledge about the ecology of this complex species, the economic importance of its pathogenic/ nonpathogenic activity, the development of tools—especially molecular-based genomic tools—to study it, and the redefinition of the concepts related to its characterization motivated our study and led us to revisit the literature on F. oxysporum in depth. Our analysis reveals that to date, 106 formae speciales have indeed been clearly described within F. oxysporum, and among these, 25 harbor from 2 to 24 races. However, these numbers are not definitive and are likely to change very soon for several reasons. The first reason is that 37 putative formae speciales have been described, but their characterization is insufficient to assert that they are indeed formae speciales, and 58 additional host plants have been reported. The second reason is related to the fact that studies have mainly focused on the pathogenic activity of F. oxysporum on plants of economic interest, but many uncultivated (wild) plants can also be infected by new formae speciales that remain to be described. Considering the proven numbers of formae speciales and formae speciales hosting races provided by Armstrong and Armstrong (1981) (79 and 16, respectively) and those given by our study (106 and 25, respectively), the relative proportion of formae speciales hosting races has increased slightly. This increase might reflect a somewhat worrisome trend, as more and more new races are described within formae speciales in connection with the re-emergence of diseases on market gardening and ornamental crops but also on large scale crops, such as banana Fusarium wilt caused by race TR4 of F. oxysporum f. sp. cubense (Gilardi et al. 2017; Ploetz 2015; Zhou et al. 2010). Greater diversity in F. oxysporum and within formae speciales may be revealed over time by using new plant genotypes derived from breeding. However, it is difficult to rule out, although not yet demonstrated, the role of mutagenic factors related to intensive culture conditions in the emergence of new diseases caused by F. oxysporum. Local appearance of race 3 from race 2 population within F. oxysporum f. sp. lycopersici in California underlines such possibility (Cai et al. 2003). The frequency of the occurrence of horizontal gene transfer as a factor of the evolution of F. oxysporum pathogenicity is not known but is probably low. However, given the natural inoculum density of this fungus in the soil and rhizosphere of many plants around the world, the process may not be anecdotal and may thus contribute to the emergence of new diseases caused by F. oxysporum, whether new formae speciales or new races within these formae speciales. What farmers need most is early diagnostic tools. For some soilborne diseases, quantifying the infectious potential of soils helps to decide whether or not growing the host plant is possible. These measures are not applicable in the case of diseases caused by F. oxysporum (Alabouvette et al. 2006). This is why molecular tools to detect the presence and activity of pathogenic F. oxysporum isolates are needed. These tools must be able to discriminate between races and formae speciales, but also to distinguish them from nonpathogenic forms that are putative biocontrol agents. Recent comparative analysis of F. oxysporum genomes provided information on the genome organization and on the genomic region that governs pathogenicity (Ma et al. 2010, 2013). Genomic comparison of whole formae speciales genomes revealed that the effector repertoire of each forma specialis likely determines host specificity (van Dam et al. 2016, 2018). Such studies provide promising insights into the diversity and evolution of F. oxysporum pathogenicity. Future large-scale projects aimed at sequencing whole F. oxysporum genomes will assuredly improve host range identification and disease management. By combining the promising progress of genomics in characterizing the pathogenic effectors of each F. oxysporum forma specialis and race, and the potential of molecular techniques that are constantly evolving, a concrete and feasible challenge will be to develop diagnostic tools to preventively detect the risk of infection by F. oxysporum for a given crop and then to take the appropriate measures. ACKNOWLEDGMENTS We thank C. Steinberg who supervised the writing of this review and D. Millot for her effective assistance in searching documents including original scientific articles. LITERATURE CITED Abawi, G. S., and Lorbeer, J. W. 1972. Several aspects of the ecology and pathology of Fusarium oxysporum f. sp. cepae. Phytopathology 62: 870-876. 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