Soilborne Diseases in Cucurbitaceae: Pathogen Virulence and Host Resistance

B.D. Bruton1

United States Department of Agriculture, Agricultural Research Service,
South Central Agricultural Research Laboratory, Lane, OK 74555

Additional index words. vascular wilt, crown rot, root rot, genes, cucurbits, plant breeding

Abstract. Resistance to soilborne diseases in the cucurbits has played a major role in continued profitable production of cucurbits worldwide. Disease management strategies must be developed to maximize existing resistance. The future direction and success of plant breeding for disease resistance is dependent upon a thorough knowledge of the genetic structure of the plant pathogen population as well as knowledge of resistance genes. Linkages between disease resistance and molecular markers are being explored, which should facilitate the selection of soilborne disease resistance in cucurbits. Selected soilborne diseases, including vascular wilts, crown rots, and root rots have been addressed with emphasis on pathogen virulence and host resistance. A universal testing system should be developed for each soilborne cucurbit pathogen in evaluating pathogenicity and relative virulence of the pathogen as well as germplasm evaluations.

Mention of a trademark, propriety product, or vendor does not constitute a guarantee or warranty of the product by the USDA and does not imply its approval to the exclusion of other products of vendors that may also be suitable. I am grateful to the many people who provided unpublished data, helpful suggestions, and critical review: J. Armengol, A.A. Bell, R. Cohen, F. Dane, J. Garcia-Jimenez, W.D. Gubler, D.L. Hopkins, A.P. Keinath, M.E. Stanghellini, C.E. Thomas, F. Namiki, D.J. Vakalounakis, T.C. Wehner, and T.A. Zitter.

1Research plant pathologist.


The captains gave the Indians some tobacco, pork, flour, and meal. In return, "they sent us water millions (watermelons)."

Captain Meriwether Lewis

Lower Missouri River, 1804

The cucurbits are a diverse group of plants that provide food, oils, protein, medicinal purposes, fiber, utensils, ceremonial articles, and decorative ornamentals for mankind. Archaeological evidence suggests that several cucurbits have been cultivated by man in both the new and old world for thousands of years (Whitaker and Davis, 1962). During the 1804 expedition of the Northwest Territory, Lewis and Clark exchanged gifts with Native Americans and received watermelons from them in the area of the lower Missouri River, an area largely unexplored. Crookneck squash first appeared in a North American seed catalog in 1828 (Paris, 1989). Starnes (1897) published the

first comprehensive treatise of watermelon culture in United States at the turn of the twentieth century. Numerous cultivars had already been developed by the late 1800s as he evaluated 30 cultivars in field trials. One of the primary concerns at that time was the location of fields near the railroad so as to have a short horse-drawn wagon haul to the shipping point (Starnes, 1897). Up until 20 years ago, cucurbit production was composed primarily of open-pollinated cultivars. Open-pollinated cultivars have, for the most part, been replaced by an array of improved hybrids. Coinciding with this has been the adoption of many new cultural practices. These include transplanting, plastic mulch with trickle irrigation, and increased plant density. Many of these cultural practices have contributed significantly to increased yields and fruit quality but some have undoubtedly contributed to the increased incidence and severity of soilborne diseases (Bruton et al., 1998).

Soilborne diseases have become more widespread and are yield limiting in many cucurbit production areas of the world, particularly the vine declines. Most of the soilborne diseases are probably monocyclic and frequently managed by reducing initial inoculum, seed treatments, cultural practices, soil fumigation, and crop rotation.


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Inadequate crop rotation has likely contributed more than any other factor to the severity of these diseases. Many soilborne pathogens of varying economic importance have been reported to attack cucurbits (Zitter et al., 1996). Some are of minor importance or are restricted in geographical distribution and have received little study. Fungi known as root pruners often play a significant role in the disease syndrome. Most of the soilborne diseases consist of a complex of several pathogens interacting with the predominant pathogen and contributing to the disease syndrome. Root infection and root colonization are two distinct processes that should be distinguished in regard to disease development. Susceptibility to root infections can change dramatically with regard to environmental conditions as well as age and physiological condition of the plant. Susceptibility to colonization is equally important in the disease process and can be influenced by the same factors. This has been addressed in another chapter of this volume (Bruton et al., 1998). In many cases, it can be extremely difficult to prove Koch's Postulates by reproducing the symptoms under controlled conditions since the environmental interactions along with normal fruit set cannot be duplicated. Symptoms caused by soilborne pathogens may be strikingly similar and difficult to diagnose (Miller et al., 1995). One good example is sudden wilt in New York in which five dissertations have been written on the disease and still there is no consensus as to causal agent (Zitter, 1995). fusarium wilt in cucurbits has probably been the most misdiagnosed disease by farmers, field scouts, and plant pathologists. Gummy stem blight of cantaloupe has often been confused with charcoal rot and lasiodiplodia vine decline due to almost identical symptoms under certain environmental conditions. Accurate diagnosis of soilborne diseases in the cucurbits is often difficult but critical to disease management.

Disease resistance has played a major role in profitable cucurbit production around the world. Resistance alone is not sufficient for adequate control of soilborne diseases. Disease management strategies must be developed to maximize existing resistance through crop rotation, selection of cultivars with resistance to the pathogen or

race present, fertilization, and various other cultural practices. With the projected loss of methyl bromide and several reports of fungicide resistance (Kato et al., 1984; Keinath and Zitter, 1998; Malathrakis and Vakalounakis, 1983; Miller et al., 1997; Van Steekelenburg, 1987), it becomes clear that management strategies to maximize existing resistance to soilborne diseases are essential. Consequently, knowledge of disease potential in specific fields along with inoculum density are crucial to the selection of the most suitable cucurbit crop and cultivar. Excessively high inoculum density of the pathogen can overcome genetic resistance in many cases. Critical analysis of cropping history, disease history, inoculum density, and level of host resistance should be an integral part of the disease management strategy.

Early work (Stakman and Piemeisel, 1917) demonstrated that disease resistance was frequently conferred by a single gene. Consequently, breeders of many crops initiated programs with the expectation that the resulting resistance would be permanent. The rapid evolution of matching pathotypes virulent to previously resistant cultivars has forced plant breeders into a repetitive cycle of cultivar replacement demanding the continual introduction of new resistance genes. Historically, resistance has been studied extensively at the cellular, whole plant, and population levels in terms of genetics, histology, and associated biochemistry. Thus, for many diseases that attack cucurbits, sources of resistance have been identified, and resistant cultivars have been developed or are in the process of development. There is little information available on genetics of resistance for many important soilborne pathogens of cucurbits while much work has been achieved on some. Recently developed molecular technology allows for a more detailed analysis of resistance mechanisms. Sitterly (1972) compiled one of the first comprehensive reviews on breeding for disease resistance in cucurbits. Andrus, as cited by Sitterly (1972), noted that 1) susceptibility tends to be dominant in the F1 hybrid in respect to most of the common diseases; 2) disease resistance is rarely dominant in that heterozygotes tend to be intermediate in resistance; 3) the increased fruit load presumably resulting from heterosis in some F1

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hybrids tends to amplify the damage caused by disease; 4) hybrids often appear to be more susceptible than their genetic composition would lead one to expect; 5) productive, fast-growing, and extra early varieties and hybrids tend to develop more severe symptoms of foliage diseases, whereas late-maturing unproductive varieties develop less severe symptoms than their genetic composition would lead one to expect. This information is still applicable 26 years later with respect to the soilborne diseases, many of which, were unknown in 1972. Robinson et al. (1976) compiled a comprehensive list of the genes of the Cucurbitaceae including genes for disease resistance. More recently, McCreight et al. (1993) published a review on genetic improvement in Cucumis melo L. addressing some of the soilborne diseases. This is the first review article that has been totally dedicated to resistance to soilborne diseases in the Cucurbitaceae. Only a select few diseases that are presently causing or have the potential to cause severe losses in cucurbit production areas will be discussed. Due to the broad scope of this review, only the most pertinent literature is cited with the knowledge that some important papers may have been inadvertently omitted.

The intent of this review is to provide an overview of some of the more important soilborne diseases (vascular wilts, crown rots, and root rots) affecting cucurbits with an emphasis on the pathogens involved and genetic resistance in the host. Although melon is the preferred term, cantaloupe and honey dew are used because they often exhibit differential reaction to some of the soilborne diseases. Muskmelon is used where there appears to be no differences.

Vascular wilt

Fusarium wilt: watermelon. At one time, fusarium wilt was the greatest yield-limiting disease of watermelon worldwide. It has been one of the real success stories for the control of a devastating disease. Although fusarium wilt remains an important disease, it is no longer the number one constraint to watermelon production in most areas due to a high level of resistance. Strains of F. oxysporum are separated into forma specialis and race strictly based on their ability to cause disease

on certain hosts (Snyder and Hansen, 1940). Fusarium wilt of watermelon [Citrullus lanatus (Thunb.) Matsum. & Nakai], caused by Fusarium oxysporum f. sp. niveum (E.F. Sm.) Snyd. & Hans., was first reported in 1894 (Smith, 1894). Fusarium wilt symptoms include damping-off, seedling disease, or wilt during any stage of plant development. Propagules of the fungus may be spread by soil, plant debris, and farm implements. Taubenhaus (1935) noted that seed may be carriers of the fusarium wilt pathogen. Raising the soil pH to 6.5 with lime has been reported to decrease the severity of fusarium wilt (Everett and Blazquez, 1967). However, Hopkins and Elmstrom (1976) concluded that increasing soil pH and the use of nitrate nitrogen had no effect on the disease. Walker (1941) noted that temperatures around 27 oC are most favorable for fusarium wilt development in watermelon and that little infection occurs above 33 oC. Control of fusarium wilt is dependent upon the use of resistant cultivars and rotation of 6 years (Elmstrom and Hopkins, 1981; Hopkins and Elmstrom, 1984). Crop rotation is essential even when using cultivars classified as highly resistant because of high inoculum levels in infested fields (Elmstrom and Hopkins, 1981; Hopkins and Elmstrom, 1984; Hopkins et al., 1989). Continuous planting of susceptible cultivars can increase the inoculum substantially, which can exceed 2,000 CFU/g of soil (Larkin et al., 1993). Fusarium wilt suppressive soil has been induced through a 6 year monoculture to 'Crimson Sweet' watermelon (Larkin et al., 1993). Transplants tend to have less wilt than do direct seeded melons, presumably due to stage of development at which infection occurs (D.L. Hopkins, personal communication).

Differences in isolate virulence has been recognized for many years (McKeen, 1951). Crall (1963) reported the existence of two physiologic races in Florida. Cirulli (1972) also found two races in Italy and designated them as race 0 and race 1. Race 2 is a highly aggressive pathogen (Netzer and Dishon, 1973) and appears to be fairly widespread in the eastern Mediterranean region including Greece and Turkey (Netzer, 1976) and Cyprus (Ioannou and Poullis, 1991). Thus, three races have been described and designated as race 0, 1, and 2. F. oxysporum f. sp. niveum race 2 has been

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Table 1. Disease reactions of watermelon cultigens used to differentiate races of Fusarium oxysporum f. sp. niveum.z


Cultigen Race 0 Race 1 Race 2

Sugar Baby S S S

Charleston Gray R S S

Calhoun Gray R R S

PI 296341-FR R R R

zDeveloped from Cirulli (1972), Netzer (1976), and Martyn and Netzer (1991).

yR = resistant, S = susceptible.

Vegetative compatibility grouping (VCG) has been useful in evaluating genetic diversity present in a fungal population. Members of one VCG are considered to be genetically interactive and genetically isolated from strains in other VCGs. Kistler et al. (1998) recently provided guidelines for systematic numbering of VCGs within F. oxysporum. Larkin et al. (1990) demonstrated a clear relationship between aggressiveness and VCG. Although race 1 was placed in VCG 0080 and VCG 0081, VCG 0082 were comprised solely of race 2. Kim et al. (1992) reported six RFLP groups based on mitochondrial DNA (mtDNA) RFLP analysis, although, there was no relationship to VCG or race. Both cluster and parsimony analyses of mtDNA RFLPs indicated that all five F. oxysporum formae speciales in cucurbits are closely related (Kim et al., 1993). In some cases, isolates of different formae speciales were genetically more similar than isolates of the same forma specialis (Kim et al., 1993). They hypothesized that the genetic differences between the formae speciales were relatively small and that determinants for host specificity could be combined or lost in individual strains. In contrast, DNA fingerprinting of nuclear DNA clearly distinguished differences among Japanese formae speciales (Namiki et al., 1994). They suggested that the cucurbit-infecting formae speciales of F. oxysporum are intraspecies variants differing in nuclear DNA content and organization. Gordon and Martyn (1997) have recently reviewed the evolutionary biology of F. oxysporum. Concepts of isolate classification into formae specialis, VCGs, and race designations of F. oxysporum have also been addressed (Correll, 1991; Correll et al., 1987; Kistler, 1997; Kistler et al., 1991).

Orton (1913) developed the first wilt-resistant watermelon cultivar by crossing Eden with an African stock citron. Mohammed et al. (1981) suggested that wilt resistance in citron was due to a high level of preformed phenols and phytoalexins following infection. Cultivars are typically described as resistant or susceptible although there is actually a continuum from resistant to susceptible (Elmstrom and Hopkins, 1981; Schenck, 1961). This was further illustrated by using different inoculum concentrations (Martyn and McLaughlin, 1983). Resistance to race 1 of Fusarium

found in several watermelon production areas in the United States (Martyn and Bruton, 1989). Although all commercial cultivars are susceptible to race 2, spread of this race throughout the watermelon growing areas of Texas and Oklahoma has been inconsequential, which is in contrast to the report in the eastern Mediterranean region. Hopkins et al. (1989) reported that growing race 2-resistant cultivars in Florida appeared to increase the field frequency of race 2 over race 1. Race 0 causes wilt only in watermelon cultivars with no resistance genes. Races of F. oxysporum f.sp. niveum are presently identified using a set of differentials (Table 1). Race 1 can induce slight to moderate wilt on most cultivars that are classified as resistant to fusarium wilt, although, Armstrong and Armstrong (1978) concluded that differences between the strains were not sufficient to constitute distinct races. The study by Larkin et al. (1990) illustrate a continuum between races 1 and 2. Furthermore, the distinction between race 0 and race 1 has been questioned (Armstrong and Armstrong, 1978; Larkin et al., 1990; Martyn, 1987; McKeen, 1951; Reid, 1958; Sleeth, 1934). The tests for race differentiation are laborious and often inconclusive. Results may be influenced by age of test plants, environmental factors, inoculum level, and inoculation method (Martyn and McLaughlin, 1983; Shimotsuma et al., 1972). Race identification using host differentials is probably necessary but with severe limitations due to the virulence continuum exhibited in different strains. If researchers would concede that there exists a continuum of virulence within the forma specialis of F. oxysporum rather than try to force isolates to be a plus or minus as to a specific race, there would be less confusion with resulting data being more meaningful.

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oxysporum f. sp. niveum has been attributed to a single dominant gene (Henderson et al., 1970; Netzer and Weintall, 1980). Netzer and Martyn (1989) reported resistance to race 2 of F. oxysporum f. sp. niveum in the PI 296341. Martyn and Netzer (1991) suggested that genes for resistance in PI 296341 are not fixed. Zhang and Rhodes (1993) noted that resistance genes to race 2 in PI 296341 are epistatic with one or more recessive genes interacting with a dominant gene. Larkin et al. (1993) noted no clear pattern of surface colonization of watermelon roots by F. oxysporum f. sp. niveum. with respect to resistant or susceptible cultivars. Resistance appears to be related to rate and/or extent of colonization in the xylem. Elmstrom and Hopkins (1981) evaluated a number of cultivars and noted moderate to high resistance in several cultivars. Paulus et al. (1976) reported that seedless watermelon cultivars tested under field conditions in California were very susceptible. Currently, most of the seedless cultivars are susceptible to fusarium wilt. It would appear that many of the present-day triploids have a similar genetic background. With triploids commanding almost 30% of the watermelon market in 1998, fusarium wilt resistance has again become a major emphasis for seed companies.

Fusarium wilt: muskmelon. Symptoms suggestive of fusarium wilt of muskmelon were first noted in 1898 as stated by Leach and Currence (1938). Symptoms may consist of a hypocotyl rot and damping-off of seedlings to a general yellowing and/or wilt at any stage of development. Lesions on one side of the stem often extend along the vine causing a wilt and death of side branches fed by affected vascular bundles. Death of the plant soon follows. The disease has been reported from all major production areas of the world

causing severe losses in some. The disease can be seed transmitted (Sherf and MacNab, 1986). Leach and Currence (1938) demonstrated no cross-reaction in tests using the watermelon and muskmelon isolates and designated the muskmelon wilt pathogen as a new variety now referred to as Fusarium oxysporum Schlechtend.:Fr. f. sp. melonis (Leach & Currence) W.C. Snyder & H.N. Hansen. Stoddard (1948) found that liming the soil to pH 6.0 significantly reduced the incidence of fusarium wilt of muskmelon as compared to soils with a pH 4.8 or 4.1. Addition of calcium to the soil has been shown to reduce the severity of fusarium wilt (Spiegel et al., 1987). In muskmelon, wilt is most severe at temperatures of 18 to 20 oC (Mas et al., 1981). A high incidence of wilt is possible in susceptible cultivars with as few as 350 to 500 CFU/g of soil (Gordon et al., 1990). Wilt severity of muskmelon increases with an increase in inoculum density (Douglas, 1970). Control through rotation may not be adequate for the control of fusarium wilt on muskmelon since the fungus is capable of colonizing roots of several nonhost plants (Banihashemi and deZeeuw, 1975; Gordon et al., 1989). Alabouvette et al. (1979) present a thorough discussion of wilt-suppressive soils for effective control of multiple races of the fusarium wilt pathogen of muskmelon, regardless of inoculum density.

Although Reid (1958) identified ten races and Armstrong and Armstrong (1978) identified seven races of the muskmelon wilt fungus, four races (0, 1, 2, and 1,2) are presently recognized using the designation of Risser et al. (1976). Race 1,2 (previously referred to as race 3) was further divided into 1,2Y and 1,2W corresponding to a yellowing and a wilting strain, respectively (Bouhot, 1981). Races are designated based on strains of the patho

Table 2. Disease reactions of muskmelon genotypes used to differentiate races of Fusarium oxysporum f. sp. melonis.z


Genotype Race 0 Race 1 Race 2 Race 1,2 Resistance genes

Charentais T S S S S None

Doublon R S R S Fom-1

CM 17-187 R R S S Fom-2

MR-1 R R R S Fom-1/Fom-2

zDeveloped from Risser et al. (1976) and Zink and Thomas (1990).

yR = resistant, S = susceptible.

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gen with the ability to infect muskmelon cultivars containing resistance genes (Table 2). It is generally thought that growing resistant cultivars places a selection pressure for the development of new races capable of defeating the resistance genes. However, Bouhot (1981) noted that race 1,2 existed in France for at least 12 years prior to resistant cultivars being introduced. Inoculation method, inoculum concentration, and age of plant when inoculated can influence the ultimate disease reaction expressed in melon plants (Latin and Snell, 1986).

Jacobson and Gordon (1988) determined that multiple races could exist within one VCG and one race could exist in multiple VCGs. They further suggested that the pathogenic races within a VCG may differ at a relatively small number of loci. VCGs in F. oxysporum f. sp. melonis have been studied extensively with a total of eight VCGs being identified to date and with similar results (Appel and Gordon, 1994; Gordon and Okamoto, 1992; Jacobson and Gordon, 1988; Jacobson and Gordon, 1990a, 1990b; Katan et al., 1994; Zuniga et al., 1997). Consequently, VCG can be useful in evaluating genetic diversity within a population, but is not adequate for race differentiation. Based on restriction enzyme analysis of mtDNA, pathogens representing two different VCG were more closely related to nonpathogens of another VCG than to each other (Appel and Gordon, 1994). In an analysis of many isolates, Jacobson and Gordon (1990b) demonstrated that RFLP patterns of mtDNA were related to VCGs but not races. Kim et al. (1993) suggested a close evolutionary relationship among the different formae speciales and a monophyletic origin of isolates from cucurbits based on RFLP patterns of mtDNA. Namiki et al. (1994) found a high degree of variation among Japanese muskmelon strains using nuclear DNA fingerprinting. The muskmelon strains were clearly separated from other formae speciales of F. oxysporum causing wilt of cucurbits. Namiki et al. (1998) further demonstrated that Japanese strains of F. oxysporum f. sp. melonis could be distinguished at the race level by nuclear DNA fingerprinting. Strains of race 2 clustered in one group as did race 1,2y. In contrast, strains of race 0 were divided into two genetic groups. They suggested

that the cucurbit-infecting formae speciales of F. oxysporum are intraspecies variants differing in nuclear DNA content and organization.

Fom-1 and Fom-2 are two independently inherited, dominant genes that confer resistance to races 0 and 2 and races 0 and 1, respectively (Pitrat, 1991; Risser, 1973; Risser et al., 1976; Robinson et al., 1976; Zink and Thomas, 1990). The single dominant gene Fom-1 in Doublon confers resistance to races 0 and 2 (Risser, 1973), whereas, the single dominant gene Fom-2 in CM 17-187 confers resistance to races 0 and 1 (Risser et al., 1976). A single dominated gene Fom-3 in Perlita-FR was reported to confer resistance to races 0 and 2 (Zink and Gubler, 1985). However, Risser (1987) noted that resistance in Perlita-FR is controlled by Fom-1. A high level of resistance is conferred to races 0, 1, and 2 when both genes are present (Risser et al., 1976). Allelism tests showed that the single dominant genes in MR-1 that confer resistance to races 0 and 2 and races 0 and 1 are the same genes or alleles of Fom-1 in differential cultivar Doublon and Fom-2 in differential line CM 17-187, respectively (Zink and Thomas, 1990). However, the two genes are not linked. MR-1 is an inbred breeding line derived from PI 124111 (Thomas, 1986). Cohen et al. (1995) reported that melofon breeding lines were resistant to races 0 and 1 but susceptible to races 2 and 1,2. Melofon melons are recombinants derived from crossing cultivars of oriental pickling melons (C. melo L. ssp. melo Conomon Group) and snake melons (C. melo L. ssp. melo Flexuosus Group) with birdsnest muskmelons (C. melo L. . ssp. melo Cantalupensis Group) (Nerson et al., 1988). Paris et al. (1993) demonstrated that the wilt-resistant gene Fom-2 conferring resistance to races 0 and 1 exists in Freeman's cucumber, an oriental pickling melon, whichis genetically related to some of the melofon germplasm. Muskmelon cultivars possessing resistance genes Fom-1 and Fom-2 are susceptible to race 1,2. Gordon et al. (1990) reported that resistance to race 2, conferred by Fom-1 and Fom-3, was correlated with lack of vascular colonization above the cotyledons and not due to infection frequency. Evidence indicates that b-(1-3)-glucanase activity may play a role in the observed differential colonization of race 0 resistant and susceptible near-isogenic lines

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of muskmelon (Netzer et al., 1979). Wechter et al. (1995) reported a random amplified polymorphic DNA (RAPD) marker in the multidisease-resistant breeding line MR-1 that is tightly linked to the Fom-2 gene. Subsequently, sequence specific primers were developed capable of differentiating between race 1 resistant and susceptible germplasm (Wechter et al., 1998). With such molecular tools available, accurate and rapid screening is possible, whichsaves germplasm and speeds the development of new releases. Ng and Kantzes (1995) screened many cultivars over multiple years and found several commercial cultivars with a high level of resistance to race 1 and race 2.

Fusarium wilt: cucumber. Fusarium wilt is widespread in cucumber (Cucumis sativus L.) production areas causing economic losses in the industry. Selby (1899) may have been the first to report what is now recognized as fusarium wilt of cucumber. Owen (1956) demonstrated that the Fusarium oxysporum from cucumber was a new specialized form designated as F. oxysporum Schlechtend.:Fr. f. sp. cucumerinum J.H. Owen. Symptoms of the disease may be a pre- or postemergence damping-off and wilt of vines. Wilt symptoms are often exhibited on one or more of the runners followed by total wilt and death of the plant. The disease is favored at high soil temperatures of 29 oC (Vakalounakis, 1996). Seed transmission has been demonstrated, although at a low rate (Jenkins and Wehner, 1983).

Armstrong et al. (1978) proposed 3 races (1, 2, and 3) of F. oxysporum f. sp. cucumerinum based on a set of three host differentials (Table 3). There are several reports of the cucumber strain of F. oxysporum causing wilt in cucumber and musk

melon (Costache and Tomescu, 1990; Owen, 1956; Van Koot, 1943). McMillan (1986) reported that a cucumber strain from the Bahamas caused wilt in cucumber, muskmelon, and watermelon. Gerlagh and Blok (1988) demonstrated that a cucumber isolate from the Netherlands was also capable of inducing wilt in cucumber, muskmelon, and watermelon. The ability of one forma specialis to infect multiple cucurbit species has generally, but not always, been under artificial conditions in the greenhouse. This does not invalidate the importance of such cross reactions and is consistent with several reports that formae speciales of F. oxysporum within the Cucurbitaceae are genetically related. Some of the isolates studied by Gerlagh and Blok (1988) are actually a new forma specialis (D.J. Vakalounakis and G.A. Fragkiadakis, personal communication). This disease is discussed in the crown rot section. As noted earlier, Kim et al. (1993) hypothesized that the genetic differences between the formae speciales were relatively small. Namiki et al., (1994) were able to differentiate between the cucurbit formae speciales using nuclear DNA fingerprinting.

Sixteen disease resistance loci and more than 100 morphological marker genes have been identified in cucumber (Pierce and Wehner, 1989, 1990; Robinson et al., 1976; Vakalounakis, 1993). Vakalounakis and Klironomou (1994) noted that knowledge of the linkage relationships among these simply inherited traits could possibly accelerate the identification of resistant genotypes. Inheritance of resistance to fusarium wilt in cucumber is controlled by a single dominant gene (Netzer et al., 1977) or by one or more recessive genes (Toshimitsu and Noguchi, 1975; Kanno et al.,

Table 3. Disease reactions of cucumber cultigens used to differentiate races of Fusarium oxysporum f. sp. cucumerinum and forma specialis of cucumber Fusarium oxysporum.z


F. oxysporum f. sp. cucumerinum F. oxysporum f. sp.

Cultigen Race 1 Race 2 Race 3 radicis-cucumerinum

Ashley S S S S

Chipper (MSU 441034) S S R S

MSU 8519 S R R S

PI 390265 R S R R

Santo F1 R R R S

zDeveloped from Armstrong et al. (1978) and Vakalounakis (1996).

yR = resistant, S = susceptible.

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1991). Resistance in WIS-248 is controlled by a single dominant gene, whichwas designated as Foc (Netzer et al., 1977). Vakalounakis (1993, 1995) determined that resistance to race 1 and race 2 in SMR-18 was controlled by a single dominant gene designated Fcu-1. In addition, he noted that resistance to race 1 of F. oxysporum f. sp. cucumerinum was completely linked to scab resistance caused by Cladosporium cucumerinum. Resistance to races 1 and 2 in WI-2757 is also controlled by the Fcu-1 gene (Vakalounakis and Smardas, 1995). Vakalounakis (1995) noted that the isolate of F. oxysporum f. sp. cucumerinum used by Netzer et al. (1977) is race 2 according to Armstrong et al. (1978). In an allelism test, it was proven that the Fcu-1 gene and the Foc genes are indistinguishable (Vakalounakis, 1996). According to the rules of gene nomenclature for the Cucurbitaceae (Robinson et al., 1976), Vakalounakis (1996) recommended that the symbol Foc be adopted for the resistance gene in cucumber to F. oxysporum f. sp. cucumerinum races 1 and 2.

Verticillium wilt. Verticillium dahliae Kleb. can cause heavy yield losses in some cucurbit production areas. V. dahliae produces hyaline mycelium, whichlater turns black due to microselerotial development. The fungus infects cucurbit roots early in plant development, but symptoms may not be expressed until sometime after fruit set (Gubler, 1996). Under adverse environmental conditions, 3 to 4 microsclerotia/g of soil can cause losses in the more susceptible cucurbit cultivars (W.D. Gubler, personal communication). Fitzell et al. (1980) noted that microsclerotia germinate in the rhizosphere of immune and susceptible roots. They also suggested that some root infections may remain superficial. Crop rotation has only limited value because of the wide host range of the fungus. Krikun and Bernier (1987) noted that plants within Gramineae can maintain populations of V. dahliae. Wilhelm (1955) determined that V. dahliae was present in soil after eight years of cropping with grain and pasture. Soil temperatures in the range of 18 to 24 oC are conducive to disease development (W.D. Gubler, personal communication). Plants infected in the seedling stage often collapse once temperatures increase or the vines are drought stressed. V. albo-

atrum Reinke & Berthier. has also been reported to cause vascular wilts in cucurbits (Gubler, 1996). V. dahliae has been isolated from muskmelon, squash, and watermelon exhibiting symptoms of sudden wilt in New York (Zitter and Bruton, personal observation). However, the association of verticillium wilt with sudden wilt is unknown.

Puhalla and Hummel (1983) designated 16 VCGs within V. dahliae. Based on the revised system of Strausbaugh et al. (1992), there may be only four VCGs in V. dahliae. Although limited information is available, it would appear that cucurbit isolates fall within VCG 2 and VCG 4. V. dahliae often exhibits a degree of specificity in that isolates from one host species may not cause wilt on other plant species. However, V. dahliae isolated from other hosts tends to be pathogenic to the cucurbits (Ben-Yephet, 1979; Skotland, 1971). In greenhouse evaluations, watermelon exhibited wilt symptoms more readily at low light intensity than at high light intensity (Ben-Yephet, 1979). Low temperature appears to be an important factor in the intensity of disease development in cucurbits. Costache and Tomescu (1990) reported a highly virulent isolate from' cucumber in Romania, whichthey designated as race 2. However, VCG may be more appropriate for strain designation than race designation in V. dahliae (A.A. Bell, personal communication).

Verticillium wilt can occur in all cucurbits, although some species appear to have a high degree of resistance and produce a marketable crop even though infected. Cantaloupe are more resistant than honey dew and casaba to verticillium wilt. Zink and Gubler (1987) noted that 'Top Mark' carries resistance to V. dahliae. The Persian melon is highly susceptible to verticillium wilt (Gubler, 1996). Cucurbits appear to possess a moderate to high level of resistance to Verticillium sp.

Crown rot

Charcoal rot. Macrophomina phaseolina (Tassi) Goidanich causes a severe vine decline of cantaloupe in many production areas. Because there is no known teleomorph, the fungus exists as vegetative mycelium and microsclerotia [Rhizoctonia bataticola (Taubenhaus) Briton-Jones] and the py

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cnidial stage M. phaseolina. Microsclerotia produced by the fungus can remain viable for several years and are generally considered to be the primary inoculum. Microsclerotial populations can range from 10 to 60/g of soil (Bruton and Reuveni, 1985) with as few as 10 microsclerotia/g of soil capable of causing severe vine decline under favorable conditions (Bruton et al., 1985). The disease can be seed transmitted (Reuveni et al., 1983; Sultana et al., 1994). Bruton et al. (1987) demonstrated that cantaloupe root infection by M. phaseolina, expressed as percentage of plants with infected roots, was sigmoidal. Infection occurs on the secondary and tertiary roots and moves into the primary root and crown of cantaloupe. More than 80% of root systems can be infected with M. phaseolina 49 days after planting, but lesions in the crown do not develop until shortly before harvest. Microsclerotia are produced in roots and crown of infected plants, although, microsclerotia/g of roots may be greatly reduced in roots that are mycorrhizal (B.D. Bruton and C.M. Heald, unpublished data). Root rot can occur, but is not the primary disease symptom of M. phaseolina in cucurbits. The primary expression of the disease is as a crown rot of cantaloupe, although, crown lesions are occasionally observed in other cucurbits (Apablaza, 1993). In the initial stage of crown lesion development, only the outer tissue is affected. The fungus gradually moves through the cortex and into the vascular bundles causing plant death. Nutrient composition and availability following infection has been suggested to play a major role in the development of vine decline of cantaloupe caused by M. phaseolina (Bruton et al., 1996a). The role of fertility has not been determined in cucurbits, however, vigorous plants appear to be more prone to vine decline than plants receiving low levels of fertility.

Variability of isolates has been observed ranging from weakly virulent to highly virulent. Since the fungus causes a fruit rot, comparison of isolates can be achieved using fruit inoculations. Most cucurbit isolates are chromogenic producing a red pigment in muskmelon fruit or in liquid culture using glycine as the nitrogen source (Dunlap and Bruton, 1986). Chromogenic isolates tend to be more virulent than the nonchromoge

nic isolates. Both chromogenic isolates and nonchromogenic isolates are capable of producing pycnidia. Only 70% to 80% of the isolates produce pycnidia. Oleic acid can induce pycnidial formation (Oosthuizen and Potgieter, 1974). During extended wet periods, pycnidia are occasionally produced in the crown of affected plants, although, the pycnidial stage is rarely observed and not considered important in the disease epidemiology. There is no evidence for support of race designation in M. phaseolina.

Crown lesions are rarely observed on honey dew type melons in the Lower Rio Grande Valley of Texas. There is much variation among cantaloupe cultivars as to resistance to charcoal rot. Evaluation of several hybrid cultivars (Petoseed Company) demonstrated 100% disease incidence in the most susceptible cultivars with no crown lesions in the most resistant (Bruton, personal observations). All cucurbits appear to be susceptible to root infection. However, tolerance may be exhibited in colonization rate of the crown tissue. Preliminary evidence suggests that resistance in cantaloupe to M. phaseolina is not simply inherited (Bruton and Wann, 1996). Honey dew, watermelon, cucumber, and squash appear to have a high level of resistance to the crown rot phase of charcoal rot.

Gummy stem blight. Gummy stem blight, caused by Didymella bryoniae (Auersw.) Rehm, inflicts great economic losses since most cucurbits are susceptible to the leaf spot, fruit rot, and crown rot phase of the disease. The anamorph, Phoma cucurbitacearum (Fr.:Fr.) Sacc., and teleomorph, D. bryoniae, can occur in the lesion at the same time. The fungus can be seed transmitted (Lee et al., 1984), although, natural inoculum is more than adequate for severe disease outbreaks during optimum environmental conditions (Schenck, 1968). Primary inoculum can consist of dormant mycelium, conidia, and/or ascospores depending on climatic conditions (Sherf and MacNab, 1986). Much of the epidemiological data is from glasshouse cucumber culture. Crown and stem lesions may develop from infections at the cotyledons, leaf axials, and tendrils. In addition, crown lesions often develop at or near the soil line and move up into the crown. Whether these lesions

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arise from soil infections at or below the soil line or from seed infection has not been determined. Crown lesions in cantaloupe and watermelon generally occur as the fruit are approaching maturity suggesting a differential response to infection or colonization with respect to age of plants. If environmental conditions remain conducive, the lesions enlarge and coalesce and can eventually kill watermelon, muskmelon, and cucumber. Gummy stem blight severity increases under high nitrogen fertilization (Van Steekelenburg, 1982), although, Neergaard et al. (1993) note that nutrition had no effect on disease development in the stems. Root infection of glasshouse cucumbers by D. bryoniae has been reported (Thinggaard, 1987). However, root rot is not normally associated with gummy stem blight. Once infection occurs, the optimum temperature for disease development in watermelon and cantaloupe is 24 and 18 oC, respectively (Sherf and MacNab, 1986). Muskmelon resistance to gummy stem blight increases at temperatures above 18 oC. Both temperature and moisture are important elements of gummy stem blight incidence and severity. However, moisture appears to be the more important for the infection process (Arny and Rowe, 1991). Sitterly (1969) noted that rotation of 18 months was necessary for economic control of gummy stem blight of cucumber. Powdery mildew and cucumber beetle feeding damage appears to predispose cucurbits to gummy stem blight development (Burgstrom et al., 1982; Zitter and Kyle, 1992).

Gummy stem blight has caused losses in cucurbits for more than 100 years with few studies made on the physiological aspects of the fungus. Variability in virulence among isolates has been reported (St. Amand and Wehner, 1995a; Chiu and Walker, 1949; Keinath et al., 1995; Van Steekelenburg, 1982). Van Steekelenburg (1982) demonstrated that fungal growth rate on PDA is correlated with virulence. Although D. bryoniae/P. cucurbitacearum causes gummy stem blight of cucurbits, other Phoma sp. have occasionally been suspected of causing similar symptoms. Keinath et al. (1995) clearly differentiated between D. bryoniae/P. cucurbitacearum and Phoma sp. isolated from cucurbits using RFLP analysis of genomic DNA and fungal morphology. In addition, they

demonstrated that the Phoma sp. were nonpathogenic or weakly virulent. Age and size of seedlings and inoculum concentration can have a significant impact on the observed disease resistance evaluations (McGrath et al., 1993; Zhang et al., 1997). Increased light intensity can increase resistance to D. bryoniae in cucumber leaves (Svedelius and Unestam, 1978). Reliable seedling screening tests that clearly differentiate levels of resistance that correlate with heavy disease pressure in the field is a continuing challenge. However, seedling screening techniques have been developed in muskmelon (Zhang et al., 1997) and cucumber (St. Amand and Wehner, 1995b) that are highly correlated with observed field resistance. Data do not support the existence of races in D. bryoniae (St. Amand and Wehner, 1995a).

Resistance to benzimidazole fungicide has been reported in D. bryoniae from several cucurbit production areas (Keinath and Zitter, 1998; Kato et al., 1984; Malathrakis and Vakalounakis, 1983; Miller et al., 1997; Van Steekelenburg, 1987), which illustrates the necessity to utilize host resistance in conjunction with good cultural practices and judicial use of fungicide.

Sowell et al. (1966) screened 1161 PIs and identified a high level of resistance in C. melo ssp. melo Dudaim Group (PI 140471). Resistance in PI 140471 is conferred by a single dominant gene (Mc), whereas, moderate resistance in breeding lines C-1 and C-8 is conferred by a single gene (Mci) (Prasad and Norton, 1967). From PI 140471, four gummy stem blight resistant cultivars were developed (Norton, 1971; 1972; Norton et al., 1985; Norton and Cosper, 1989). However, Sowell (1981) noted that PI 140471 did not have a sufficient level of resistance under severe disease pressure in South Carolina. Additional germplasm was screened for resistance, in which, PI 296345, PI 266935, and PI 436533 were identified as having a high level of resistance (Sowell, 1981). McGrath et al. (1993) noted that no melon cultivar available had a sufficient level of resistance to gummy stem blight. They noted that PI 266934 possessed a much higher level of resistance than PI 266935. Zhang et al. (1997) identified 13 PIs with resistance equal to or greater than PI 140471. In general, there is a high correlation between disease incidence on

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leaves and stems (Zhang et al., 1997).

In watermelons, moderate resistance was identified in PI 1781392, PI 189225, and PI 186875 (Sowell and Pointer, 1962). Another line, PI 271778, has an intermediate level of resistance that is considered adequate (Sowell, 1975). Norton (1979) reported that resistance in PI 189225 is controlled by a single recessive gene. However, Kwon et al. (1998) noted that resistance in PI 189225 appears to be quantitative with additive dominant features. Commercial varieties of watermelons vary in their reaction to this disease. Of three varieties, Congo is least susceptible, Fairfax is intermediate, and Charleston Gray is most susceptible (Sherf and MacNab, 1986). Linkages between gummy stem blight resistance and amplified fragment length polymorphism (AFLP) markers are being explored, whichcould facilitate the selection of gummy stem blight resistance in watermelon (Kwon et al., 1998).

Wehner and St. Amand (1993) found that cucumber cultivars and breeding lines reported to be resistant elsewhere were susceptible in field evaluations in North Carolina. Results of greenhouse screening trials have not always correlated with disease reaction in the field (St. Amand and Wehner, 1993, 1995b). Wehner and St. Amand (1993) evaluated 83 cucumber PIs, cultivars, and breeding lines noting that PI 164433, 'Slice', PI 390264, M-17, and M-12 have a moderately high level of resistance. St. Amand and Wehner (1995b) suggest that gummy stem blight resistance in cucumber may be additive and not specific. Resistance to stem and foliar infection is not correlated with increased fruit rot resistance in cucumber (Van Steekelenburg, 1983; Van Steekelenburg and Vooren, 1980).

Zhang et al. (1995) screened 308 PI accessions of Cucurbita sp. and seven C. martinezii for resistance to gummy stem blight. They identified two C. moschata (PI 201474 and PI 4385790), three C. pepo (PI 10107, PI 358969, PI 442312), and all seven C. martinezii (PI 406683, PI 438968, PI 5120999, PI 512103, PI 512106, PI 540899, PI 540900) as having a high level of resistance.

Fusarium crown rot. Fusarium crown rot of squash was first reported in South Africa (Doidge and Kresfelder, 1932). Subsequently, the trino

mial Fusarium solani App. and Wr. f. cucurbitae Snyd. & Hans. was established indicating specificity to cucurbits (Snyder and Hansen, 1941). The teleomorph is Nectria haematococca Berk. & Broome. Infection occurs at or below the soil line by direct penetration into the epidermal tissue (Samac and Leong, 1989). Symptoms include elongated water-soaked lesions soon after infection. Hyphae colonize the tissue intracellular and intercellular and gradually move into the cortex. The lesion is initially light tan to brown and water-soaked but darkens with age. Removal of soil from the crown exposes the often large lesion characterized by cortical sloughing with only vascular strands remaining. The first symptom observed in the field is wilting of affected plants and death within a few days. The root below the lesion may appear reasonably healthy and unaffected. Germination and seedling emergence can be significantly reduced (Sumner, 1976). The incidence of fusarium crown rot appears to be increasing in recent years. Vannacci and Gambogi (1980) determined that a high percentage of seeds can be infected (external and internal) by the fungus. A two year rotation has been effective in controlling fusarium crown rot (Conroy, 1953; Nash and Alexander, 1965; Toussoun and Snyder, 1961). Since the initial report and description, the disease has become worldwide in distribution, although not necessarily widespread within specific regions. Fusarium crown rot has the potential to become a major soilborne disease of cucurbits.

Two races (race 1 and 2) are recognized based on tissue specificity (Toussoun and Snyder, 1961). Race 1 corresponds to mating population 1 (MP1) and race 2 corresponds to mating population V (MPV) (Matuo and Snyder, 1973). Although both fungal strains have the same teleomorph (Nectria haematococca), they are different species based on rDNA sequence analysis (O'Donnell and Gray, 1995) and RAPD patterns (Crowhurst et al., 1991). O'Donnell and Gray (1995) note that Nectria is an artificial genus and may result in a nomenclatural change with Nectria being eliminated and replaced with Neocosmospora as the teleomorph of the F. solani clade. The old system will be maintained for the purpose of this review. Race 1 attacks the root, stem, and fruit while race 2 attacks only the fruit

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(Toussoun and Snyder, 1961). It is interesting to note that race 1 macroconidia possess an adhesion factor (Jones and Epstein, 1989), which may account for the ability for direct penetration of the epidermis (Samac and Leong, 1989). Epstein et al. (1994) noted that only the macroconidia produce the adherence factor. Race 2 can germinate and grow on the cucurbit stem surface but does not penetrate. Recognition events on the host surface may determine the outcome of the infection process. Further discussion will be limited to race 1. Variability in virulence between isolates has been noted (Nagao et al., 1994; Bruton, unpublished data; Prasad, 1949). Paternotte (1987) noted a direct relationship between inoculum density and dead plants and that resistance within C. pepo could be ascertained using inoculum levels of 102 to 103. Since race 1 can also cause fruit rot, Georgopoulos (1963) used the large fruits of banana squash to test numerous isolates for evaluation of relative virulence. Inheritance of pathogenicity in race 1 appears to be controlled by multiple genes (Prasad, 1949; Georgopoulos, 1963; Hawthorne et al., 1994). Heterothallism in MPI requires opposite alleles at the mating type locus (MAT 1) for a fertile cross. Consequently, the minimal requirements for a fertile cross is isolates with opposite alleles at MAT 1 and the genetic potential of one isolate to function as a male and the other as a female (Van Etten and Kistler, 1988). Chromosome number for race 1 (MPI) has been reported as four (El-Ani, 1956). Van Etten and Kistler (1988) has compiled a list of all loci described for race 1.

Although fusarium crown rot is generally associated with squash (Cucurbita pepo L.) and pumpkin, the disease has been observed causing moderate damage to field-grown cantaloupe and honey dew (Bruton, personal observation; Toussoun and Snyder, 1961). Based on descriptions of the disease and identification only as F. solani, Fusarium crown rot has been reported causing a major problem in muskmelon production in India (Radhakrishnan and Sen, 1986). Severe crown rot has occasionally been observed in field and greenhouse cucumbers (Conroy, 1961; Toussoun and Snyder, 1961). Host range studies have shown species of Benincasa, Cucurbita, Cucu

mis, Citrullus, Lagenaria, and Luffa to be susceptible to F. solani f. sp. cucurbitae race 1 (Kinjo and Tokashiki, 1989; Paternotte, 1987; Toussoun and Snyder, 1961; Vannacci and Gambogi, 1980). In contrast, Boyette et al. (1984) reported that watermelon (Citrullus) was resistant. Nagao et al. (1994) reported differential susceptibility among the cucurbits with C. maxima cultivars being most susceptible followed by C. pepo, C. moschata, and C. sativus in decreasing order of susceptibility. Drennan and Zitter (1997) reported that C. melo and C. pepo seedlings were most susceptible, followed by C. sativus. In contrast, very few C. moschata (cvs. 'Butternut' and 'Buttercup') plants wilted, although stem damage often occurred at the soil line. Sumner (1976) concluded that C. pepo was more susceptible than C. moschata. A major concern with this disease is that root stock used for the control of Fusarium wilt is susceptible (Kerling and Bravenboer, 1967; Kinjo and Tokashiki, 1989). Paternotte (1987) demonstrated that rootstock R.S. 841 and Benincasa hispida (cerifera) were moderately resistant. Van Etten and Kistler (1988) noted that single-gene resistance has not been described. However, there appears to be some degree of quantitative resistance (Nagao et al., 1994). It is clear that genetic differences exists within the cucurbits to Fusarium crown rot and that future efforts need to be directed toward possible improvement of the inoculation procedure of Nagao et al. (1994) that allows identification of resistance or tolerance. Uniform greenhouse screening along with field testing is desperately needed for this disease.

Fusarium root and stem rot of cucumber. A new root and stem rot disease of cucumber caused by a new Fusarium oxysporum forma specialis has been reported occurring in plastic houses from Greece (Vakalounakis, 1996). The proposed name for the fungus is F. oxysporum f. sp. radicis-cucumerinum D.J. Vakalounakis. Symptoms exhibited are a root and collar rot that develops into a stem rot on plants coinciding with set fruit. The lesion on the stem is characterized by a unilateral cortical rot that may extend basipetally for 20 to 40 cm. In mature plants, a slow wilting with progressive leaf yellowing may be observed. Infected plants having a heavy fruit load wilt on sunny

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days, may recover at night, but eventually die. Vascular discoloration does extend into the stem. Presently, the fungus is the most destructive pathogen of greenhouse cucumbers in Crete (D.J. Vakalounakis, personal communication). The disease is most severe at low soil temperatures around 17 oC. Of 18 cultivated plant species that were artificially inoculated, only C. sativus, C. melo, and L. aegyptiaca exhibited symptoms similar to those observed on cucumber (Vakalounakis, 1996). The validity of the this new forma specialis has been confirmed by VCG and RAPD fingerprinting (D.J. Vakalounakis and G.A. Fragkiadakis, personal communication). The fungus causes cortical rot in the basal stem tissue and roots of cvs. Ashley, Straight-8, Chipper, MSU-8519, SMR-18, and Santo F1, but not in PI 390265. PI 390265 exhibited only a light vascular discoloration extending up to two nodes above the hypocotyl. Some of the F. oxysporum isolates used in the study by Gerlagh and Blok (1988) have been determined to be F. oxysporum f. sp. radicis-cucumerinum (D.J. Vakalounakis, personal communication. It would appear that the disease may have been confused with Fusarium wilt of cucumber in the past (Costache and Tomescu, 1990; Owen, 1956; Van Koot, 1943; McMillan, 1986). In order to differentiate formae speciales of F. oxysporum, Santo F1 should be included as one of the cucumber differential hosts used to identify races of F. oxysporum f. sp. cucumerinum (Table 3).

Purple stem. Phomopsis cucurbitae McKeen is the causal agent of purple stem of glasshouse cucumbers and field grown cantaloupe in Canada, Lower Rio Grande Valley of Texas, and Central America (Bruton, 1996; McKeen, 1957). The teleomorph, Diaporthe melonis Beraha & O'Brien, is rarely observed and difficult to induce. Little information is available on purple stem epidemiology of muskmelon. Dixon (1981) noted that the disease may be seed-transmitted. Infections can occur at petiole and tendril junctions and move into the crown (McKeen, 1957). Stem lesions above the crown may girdle the stem and kill the runner beyond. Infections also occur at or below the soil line and move up the crown producing a purple pigmentation in the early stages of disease development (Bruton, unpublished data). Pycnidia are

produced in the latter stages of disease development in the crown although the initial inoculum source is unknown. Although, P. cucurbitae is occasionally isolated from the lower portion of the primary or secondary roots, root rot is not observed. Crown lesions typically develop just prior to harvest. The lesions initially are shallow, colonizing crown tissue only a few cells deep and subsequently colonize the cortex. Once the fungus penetrates the vascular bundles, the vine is rapidly killed. To date, the disease has been restricted in distribution and severity. However, heavy losses have been observed in cantaloupe in Costa Rica (Bruton, personal observation).

Cucumbers appear to be very susceptible under greenhouse conditions (McKeen, 1957). In artificial inoculation studies, cantaloupe, cucumber, and watermelon developed crown lesions 21 to 28 days following inoculation at soil line (Bruton, unpublished data). The fungus caused vine decline symptoms similar to those observed in cantaloupe in the field. Vine decline of watermelon has not been observed in the field nor did buttercup squash develop crown lesions under greenhouse conditions.

Root rot

Monosporascus root rot­vine decline. Vine decline, caused by Monosporascus cannonballus Pollack & Uecker, is a yield limiting disease in many hot and arid to semiarid muskmelon and watermelon production areas (Martyn and Miller, 1996). Root infection occurs soon after planting. Twenty days after planting, >70% of muskmelon plants can have infected roots (Reuveni et al., 1983). Vine decline symptoms are not exhibited until late in the growing season, normally within two weeks of harvest. Stanghellini et al. (1996) reported ascospore numbers in the range of 1 to 4.3/g of soil in commercial cantaloupe fields in Arizona. Mertely et al. (1993b) noted 3 to 15 ascospores/g of soil, although ascospore number could not be correlated with root disease severity. Previous attempts to induce ascospore germination have generally failed (Martyn et al., 1992), although, Stanghellini et al. (1996) clearly demonstrated ascospore germination and infection of cantaloupe roots. The fungus attacks primary and

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secondary roots, especially at the juncture of the roots. The root system often appears relatively white until late in the season, although close examination revels reduced secondary and tertiary roots (Miller and Bruton, unpublished data). Discrete cortical lesions often develop as the fruit begin to enlarge with vine collapse occurring 1 to 2 weeks prior to harvest (Reuveni et al., 1983; Mertely et al., 1991). Tylose formation in the xylem vessels has also been proposed as one of the mechanisms involved in the vine collapse of plants (M.E. Stanghellini, personal communication). Crown rot is not observed in affected plants. Excess water (rain or irrigation) near the end of the season can greatly intensify vine collapse. High temperature in the later part of the growing season has been associated with increased vine decline (Krikun, 1985; Pivonia et al., 1997; Wolff, 1996). Night temperatures above 25 oC may be as important as high day temperatures in the development of vine decline incited by M. cannonballus (M.E. Stanghellini, personal communication).

Two species of Monosporascus have been associated with vine decline of cucurbits (Reuveni et al., 1983; Mertely et al., 1991). Sivanesan (1991a, 1991b) noted that M. cannonballus and M. eutypoides are similar, if not identical, in all morphological characters except in the number of ascospores/ascus and ability to germinate. He concluded that they should be considered conspecific. M. eutypoides was originally identified as the causal agent involved in some of the vine declines in Israel (Reuveni et al., 1983) and Spain (J. Garcia-Jimenez, personal communication). However, more recent examination of many isolates from Israel (M.E. Stanghellini and R. Cohen, personal communication) and Spain (B.D. Bruton, J. Garcia-Jimenez, and J. Armengol, unpublished data) clearly shows that M. cannonballus is the dominant species present in those countries since M. eutypoides was never found. Lovic et al. (1995) reported that the internal transcribed spacer regions of the ribosomal DNA repeat unit were identical in DNA sequence from isolates representing both "species." Based on the existing information, M. cannonballus and M. eutypoides will be considered synonymous in this review with M. cannonballus taking precedence. This issue may

not yet be settled, however, until isolates truly representing both species can be studied, they should be considered conspecific.

Considerable variation in virulence exists in M. cannonballus isolates ranging from weakly virulent to highly virulent (Bruton et al., unpublished data; Martyn and Miller, 1996). Although the presence of dsRNA is involved to some degree with hypovirulence (Martyn and Miller, 1996), our data supports additional mechanisms in that there is considerable variation in virulence, regardless of the presence or absence of dsRNA. To adequately detect biologically significant differences in virulence between isolates, at least three inoculum concentrations (10, 20, and 40 colony forming units (CFU)/g of soil) are required. Races of M. cannonballus have not been demonstrated.

Mertely et al. (1993a) reported differences in susceptibility to M. cannonballus in muskmelon cultivars under greenhouse conditions noting tolerance in two breeding lines and several cultivars. Watermelon cultivars consistently had higher root disease ratings (more disease) than other cucurbit species tested. However, early-planted watermelon in the Lower Rio Grande Valley of Texas normally have a low incidence of monosporascus vine decline, whereas, crops planted later in the spring can exhibit severe vine decline (Miller and Bruton, personal observations). Honeydew melons tend to exhibit a much higher level of field tolerance to monosporascus vine decline than do cantaloupes. It would appear that greenhouse screening of different genotypes may be useful in identifying tolerance to M. cannonballus (Mertely et al., 1993a; Bruton, unpublished data). However, there are insufficient studies to determine the value of greenhouse evaluations for assessment of field tolerance. Inoculation with 20 CFU/g of soil may be adequate for evaluation of cucurbit germplasm (Bruton et al., 1995b, 1996b). Inoculation with a known inoculum concentration is critical for consistent and useful results. Temperature range of 25 to 35 oC appears to be adequate for evaluation but this needs to be verified using controlled temperatures. 'Ananas', 'Persian', and 'XPH 6244' melon cultivars exhibited a high level of tolerance to M. cannonballus in field studies in Arizona (Alcantara et al., 1995; Stanghellini et al.,

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1995). Cohen et al. (1995) initially reported tolerance to sudden wilt in some melofon breeding lines may have a dominant nature. They further noted that the breeding line P6a is highly tolerant to sudden wilt that may offer germplasm for breeding of commercial melon cultivars tolerant to the disease. However, in later evaluations, Cohen et al. (1996) suggested that tolerance to sudden wilt in Israel was likely from additive gene action. Wolff and Miller (1998) evaluated 125 muskmelon cultivars and breeding lines and determined that the Charentais, Ananas, and Galia types exhibited a moderate to high level of tolerance. A major obstacle to evaluating muskmelon cultivars has been variability between cultivars with respect to fruit maturity. For example, early maturing cultivars exhibit a high incidence of vine decline compared to later maturing cultivars. However, the later maturing cultivars often exhibit similar levels at maturity. Vine decline severity has been associated with fruit load (Pivonia et al., 1997; Wolff, 1996; Wolff et al., 1997). Consequently, field evaluations must be made in relation to plant development and fruit load. Wolff (1995) stated that genotypes are being evaluated with reference to fruit load and root vigor or size.

Acremonium collapse. Acremonium collapse is a newly described disease on muskmelon in Spain (Garcia-Jimenez et al., 1994b), and is suspected of causing a similar disease in the upper San Joaquin and Sacramento Valleys of California (Bruton et al., 1995a; Gwynne et al. 1997). Acremonium cucurbitacearum A. Alfaro-Garcia, W. Gams, et J. Garcia-Jimenez (Alfaro-Garcia et al., 1996) was only recently identified as the causal agent of acremonium collapse. Although A. cucurbitacearum is isolated from muskmelon and watermelon in the Rio Grande Valley of Texas, the fungus occurs at a low frequency and is not considered to be important at this time (Miller and Bruton, unpublished data). Infection by A. cucurbitacearum occurs early in the season, causing a lesion at the stem­root junction, discoloration of roots, death of secondary and tertiary roots, and root corking later in the season (Garcia-Jimenez et al., 1994b, 1989). The fungus can be isolated from the root­stem junction four days after planting in naturally infested soil (Armengol et al., 1996b;

Armengol, 1997). A somewhat unique symptom often produced by A. cucurbitacearum in the seedling stage is a brown lesion at the peg or stem­root junction, and subsequent hypocotyl rot (Garcia-Jimenez et al., 1994b; Gubler, 1982). In addition, The fungus attacks the cortical area causing a suberization of the cell walls giving the roots a roughened appearance (Armengol et al., 1996b; Armengol, 1997). In transplants, root hairs deteriorate shortly after the roots exit the artificial soil mix. Tan to brown lesions develop at the juncture between secondary and primary roots. Vine collapse normally occurs within 1 to 2 weeks of harvest. There are no crown lesions associated with acremonium collapse. Crop rotation for 8 years in a field with a history of acremonium collapse was found to be inadequate for disease control (J. Garcia-Jimenez, personal communication). Chlamydospores appear to be the survival structures of the fungus (Armengol, 1997). Although germination of chlamydospores has been demonstrated, their ability to infect muskmelon roots is unknown. Other crop plants and weeds do not appear to be hosts of A. cucurbitacearum, although some root colonization can occur (Armengol et al., 1998).

Acremonium cucurbitacearum isolates from the Lower Rio Grande Valley of Texas (Bruton et al., 1996c), upper San Joaquin and Sacramento Valleys of California have been demonstrated to be pathogenic to muskmelon (Bruton et al., 1995b). Additional studies have shown that isolates from Texas and California are as virulent as the Spanish isolates (Bruton et al., unpublished data). Temperature plays an important role in the incidence and severity of vine declines. Acremonium collapse appears to be associated with cooler Mediterranean type climates, whichmay help explain why the fungus is a minor problem in the hotter climate of the LRGV of Texas. Variation in isolate virulence has been observed in both Spanish isolates and Texas isolates (Armengol et al., 1996a; Bruton et al., 1996b) ranging from moderately virulent to highly virulent. Evaluation of pathogenicity and relative virulence can be influenced by inoculum concentration. Consequently, at least three inoculum concentrations (5 ¥ 103, 1 ¥ 104, and 2 ¥ 104 CFU/g of soil) should be used in evaluating

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relative virulence of A. cucurbitacearum isolates. Ten distinct VCGs have been designated within the population from California, Spain, and Texas (Abad et al., 1997; Vicente et al., 1994). Almost 75% of the 47 strains tested belonged to 2 VCGs indicating little genetic diversity between isolates from the United States and Spain. There have been no indication that races of the this fungus exist.

Acremonium cucurbitacearum can cause disease of many species within the Cucurbitaceae family with muskmelon and watermelon being the most susceptible (Armengol et al., 1998). Cucurbita maxima, Luffa acutangula, L. aegyptiaca, Benincasa hispida, Cyclanthera pedata, and Cucumis miriocarpus are considered highly resistant. C. maxima is highly resistant to the fungus and is being evaluated as rootstock for muskmelon to control the disease in Spain (Garcia-Jimenez et al., 1990). Similar results were obtained with Texas isolates in which muskmelon and watermelon were the most susceptible of 39 cucurbits tested (Bruton et al., unpublished data). Even though watermelon cultivars are highly susceptible in greenhouse studies, watermelon is planted in Spanish fields that are no longer planted to muskmelon because of the disease. Therefore, watermelon cultivars appear to have a high degree of field resistance to A. cucurbitacearum. Eighty-seven commercial muskmelon cultivars were evaluated in fields with a history of acremonium collapse with no cultivar exhibiting sufficient tolerance to recommend for highly infested fields (Garcia-Jimenez et al., 1994a).


Kistler and Miao (1992) in a recent review of genetic change in filamentous fungi noted that the true extent of chromosomal changes in fungi is probably underestimated. Mutations interject new variants into a population that may be absent in other populations. McDermott and McDonald (1993) discuss gene flow concerned with the fate of pathogen individuals as they move in their environment and how that movement affects population dynamics and distribution of genetic variation. Gene flow, in conjunction with other evolutionary influences, can result in the spread of single genes (or DNA sequences), genotypes, and

even the establishment of whole populations in different regions. Mutation, sexual recombination, and/or somatic hybridization are the traditionally recognized methods of genetic variation within a pathogen population. Virulence alleles with a favorable selective trait will likely be maintained at a high frequency within the pathogen population. Although there is no consensus of agreement, there has been much written on the dynamics and equilibrium of the genotypic frequencies of host resistance genes and pathogen virulence genes (Kirby and Burdon, 1997; Leonard, 1994; Leonard and Czochor, 1980; Sedcole, 1978; Sun and Yang, 1998).

To be most effective, breeding programs must be based on knowledge of the genes and inheritance of resistance. However, it is equally crucial to know the genetic traits of the soilborne pathogen. Although race designation is arbitrary, it serves a useful purpose to identify new variant strains of the fungus. This review illustrates a serious gap in definitive information on soilborne pathogens. Perhaps the most compelling objective is in the development of a "Universal Testing System" for comprehensive evaluation of resistance of germplasm as well as establishing pathogenicity and virulence of the pathogen. The literature is full of different methods for testing cucurbit fungal isolates for pathogenicity, virulence, and germplasm evaluation. Inoculum concentration has been shown over and over to have an effect on disease reaction of the host plant. Yet, different inoculum concentrations continue to be used by researchers. Temperature and light intensity often play an important role in disease reaction. These variables cannot always be controlled, but, they can be monitored. The tests should be further evaluated under field conditions to determine correlation of greenhouse screening with field resistance. We have all been a party to this and we can all be part of the solution. In addition, seeds of the host genotype for differentiating races can be difficult to obtain without making additional increases. Armstrong et al. (1978) obtained the same cucumber genotype from different sources and found that those from one source were resistant while those from another source were susceptible. Perhaps a seed reserve should be established for

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dispersal of genetically pure host differential genotypes.

Breeding for resistance represents the most satisfactory form of disease control. Although specific resistance may be competent and even advantageous in certain situations, general resistance should be identified genetically whenever possible and used in breeding programs. The literature reveals relatively few clearly defined instances of general resistance to soilborne pathogens in cucurbits. However, general resistance is probably widespread. It has not been reported frequently in the literature possibly because it is more difficult to identify genetically. As research on the molecular genetics of disease resistance in cucurbits becomes more available, we may expect general resistance to be identified for many diseases and to be used more extensively in breeding programs. We are living in an age of technological revolution. Recent advances in molecular biology has opened many new opportunities to study the host and pathogen. Prior to molecular markers, linkage of useful traits was associated with certain morphological markers. Staub (1995) has discussed the application of molecular markers and genetic map construction in cucurbits. Mapping genes that control disease resistance traits will have tremendous impact for plant breeders and plant pathologists alike. Several labs are either in the process or have developed genetic maps for some of the cucurbits. Recently, AFLP was developed as a new DNA marker system combining the features of RFLP and PCR, whichmay be more efficient for mapping the genome than RAPD markers (Wang et al., 1997). The outlook is exciting with new technology being integrated into research programs that will surely contribute to a strong cucurbit industry in the future.

Literature cited

Abad, P., T. Hack, M.J. Vicente, B.D. Bruton, and J. Garcia-Jimenez. 1997. Vegetative compatibility groups in Acremonium cucurbitacearum, p. 287­289. In: H.-W. Dehne, G. Adam, M. Diekmann, J. Frahm, A. Mauler-Machnik, and P. van Halteren (eds.). Diagnosis and identification of plant pathogens: Proc. 4th Intl. Symp. European Foundation for Plant Pathology, 9­12 Sept. 1996, Bonn, Germany. Developments in plant pathology. Kluwer Academic Publishers, The Netherlands.

Alabouvette, C., F. Rouxel, and J. Louvet. 1979. Characteristics of Fusarium wilt-suppressive soils and prospects for their utilization in biological control, p. 165­182. In: B. Schippers and W. Gams (eds.). Soil-borne plant pathogens. Academic Press, New York.

Alcantara, T.P., S.L. Rasmussen, D.H. Kim, N. Oebker, and M.E. Stanghellini. 1995. Field tolerance of melons to Monosporascus cannonballus. Phytopathology 85:1192 (abstr.).

Alfaro-Garcia, A., J. Armengol, B.D. Bruton, W. Gams, J. Garcia-Jimenez, and G. Martinez-Ferrer. 1996. The taxonomic position of the causal agent of acremonium collapse of muskmelon. Mycologia 88:804­808.

Apablaza, H.G.E. 1993. Determinacion de la pudricion basal de la sandia y del melon (Macrophomina phaseolina (Tassi), Goidanich) en la region metropolitana de Chile. Ciencia e Investigacion Agraria 20:101­105.

Appel, D.J. and T.R. Gordon. 1994. Local and regional variation in population of Fusarium oxysporum from agricultural field soils. Phytopathology 84:786­791.

Armengol, J. 1997. Aspectos patológicos, epidemiológicos y culturales de Acremonium cucurbitacearum Alfaro-Garcia, W. Gams et J. Garcia-Jiménez. PhD diss. Universidad Politecnica de Valencia, Valencia, Spain.

Armengol, J., E. Sanz, G. Martinez-Ferrer, R. Sales, B.D. Bruton, and J. Garcia-Jimenez. 1998. Host range of Acremonium cucurbitacearum, cause of acremonium collapse of muskmelon. Plant Pathol. 47:29­35.

Armengol, J., G. Martínez-Ferrer, E. Sanz, B.D. Bruton, and J. García-Jiménez. 1996a. Influencia de la fecha de observación y la densidad de inóculo en la patogenicidad de Acremonium cucurbitacearum a melón. VIII Cong. Nac. de la Soc. Española de Fitopatol. p. 181 (abstr.).

Armengol, J., G. Martínez-Ferrer, R. Sales, Junior, and J. García-Jiménez. 1996b. Estudios preliminares sobre la histopatología del ataque de Acremonium cucurbitacearum a melón. VIII Cong. Nac. de la Soc. Española de Fitopatol. p. 156 (abstr.).

Armstrong, G.M. and J.K. Armstrong. 1978. Formae speciales and races of Fusarium oxysporum causing wilts of the Cucurbitaceae. Phytopathology 68:19­28.

Armstrong, G.M., J.K. Armstrong, and D. Netzer. 1978. Pathogenic races of the cucumber­wilt Fusarium. Plant Dis. Rptr. 62:824­828.

Arny, C.J. and R.C. Rowe. 1991. Effects of temperature and duration of surface wetness on spore production and infection of cucumbers by Didymella bryoniae. Phytopathology 81:206­209.

Banihashemi, Z. and D.J. deZeeuw. 1975. The behavior of Fusarium oxysporum f. sp. melonis in the presence and absence of host plants. Phytopathology 65:1212­1217.

Ben-Yeohet, Y. 1979. Isolate source and daylight intensity effects on the pathogenicity of Verticillium dahliae in watermelon seedlings. Phytopathology 69:1069­1072.

Bouhot, D. 1981. Some aspects of the pathogenic potential in formae speciales and races of Fusarium oxysporum on Cucurbitaceae, p. 318­326. In: P.E. Nelson, T.A.

Cucurbitaceae '98

Toussan, and R.J. Cook (eds.). Fusarium: Diseases, biology and taxonomy. Pa. State Univ. Press, University Park.

Boyette, C.D., G.E. Templeton, and L.R. Oliver. 1984. Texas gourd (Cucurbita texana) control with Fusarium solani f. sp. cucurbitae. Weed Sci. 32:649­655.

Bruton, B.D., C.L. Biles, and J.R. Dunlap. 1996a. Nutrient utilization of Macrophomina phaseolina: A chromogenic isolate from cantaloupe fruit. Subtrop. Plant Sci. 47:46­52.

Bruton, B.D. 1996. Phomopsis black rot and purple stem, p. 52­53. In: T.A. Zitter, D.L. Hopkins, and C.E. Thomas (eds.). Compendium of cucurbit diseases. Amer. Phytopathol. Soc., St. Paul, Minn.

Bruton, B.D. and E.V. Wann. 1996. Charcoal rot, p. 9­11. In: T.A. Zitter, D.L. Hopkins, and C.E. Thomas (eds.). Compendium of cucurbit diseases. Amer. Phytopathol. Soc., St. Paul, Minn.

Bruton, B.D. and R. Reuveni. 1985. Vertical distribution of microsclerotia of Macrophomina phaseolina under various soil types and host crops. Agr. Ecosyst. Environ. 12:165­169.

Bruton, B.D., J. Garcia-Jimenez, J. Armengol, and G. Martinez-Ferrer. 1996b. Colapso del melon en las provincias del este y del sur de Espana. VIII Cong. Nac. de la Soc. Espanola de Fitopatol. p. 124 (abstr.).

Bruton, B.D., M.E. Miller, and J. Garcia-Jimenez. 1996c. Comparison of Acremonium sp. from the Lower Rio Grande Valley of Texas with Acremonium sp. from Spain. Phytopathology 86:S3 (abstr.).

Bruton, B.D., M.J. Jeger, and R. Reuveni. 1987. Macrophomina phaseolina infection and vine decline in cantaloupe in relation to planting date, soil environment, and plant maturation. Plant Dis. 71:259­263.

Bruton, B.D., R.M. Davis, and T.R. Gordon. 1995a. Occurrence of Acremonium sp. and Monosporascus cannonballus in the major cantaloupe and watermelon growing areas of California. Plant Dis. 79:754.

Bruton, B.D., T.K. Hartz, and E.L. Cox. 1985. Vine decline in muskmelon as influenced by cultivar and planting date. HortScience 20:899­901.

Bruton, B.D., T.R. Gordon, and R.M. Davis. 1995b. Optimum CFU concentrations for testing pathogenicity of California cucurbit isolates of Monosporascus cannonballus and an Acremonium sp. Phytopathology 85:1119. (Abstr.)

Bruton, B.D., V.M. Russo, J. Garcia-Jimenez, and M.E. Miller. 1998. Carbohydrate partitioning, cultural practices, and vine decline diseases of cucurbits, p. 189­200. In: J. McCreight (ed.). Cucurbitaceae '98. ASHS Press, Alex., Va.

Burgstrom, G.C., D.E. Knavel, and J. Kuc. 1982. Role of insect injury and powdery mildew in the epidemiology of the gummy stem blight disease of cucurbits. Plant Dis. 66:683­686.

Chiu, W.F. and J.C. Walker. 1949. Physiology and pathogenicity of the cucurbit black-rot fungus. J. Agr. Res. 78:589­615.

Cirulli, M. 1972. Variation of pathogenicity in Fusarium oxysporum f. sp. niveum and resistance in watermelon cultivars, p. 491­500. In: Actas Congr. Un. Fitopathol. Mediter. Oeiras, 3rd.

Cohen, R., S. Schreiber, and H. Nerson. 1995. Response of melofon breeding lines to powdery mildew, downy mildew, fusarium wilt, and sudden wilt. Plant Dis. 79:616­619.

Cohen, R., Y. Elkind, Y. Burger, R. Offenbach, and H. Nerson. 1996. Variation in the response of melon genotypes to sudden wilt. Euphytica 87:91­95.

Conroy, R.J. 1953. Fusarium root rot of cucurbits in New South Wales. J. Austral. Inst. Agr. Sci. 19:106­108.

Conroy, R.J. 1961. A field occurrence of Fusarium solani (Mart.) App. and Wr. forma cucurbitae Snyd. and Hans. on Cucumis sativus L. Austral. J. Sci. 23:412.

Correll, J.C. 1991. The relationship between formae speciales, races, and vegetative compatibility groups in Fusarium oxysporum. Phytopathology 81:1061­1064.

Correll, J.C., C.J.R. Klittich, and J.F. Leslie. 1987. Nitrate nonutilizing mutants of Fusarium oxysporum and their use in vegetative compatibility tests. Phytopathology 77:1640­1646.

Costache, M. and A. Tomescu. 1990. Research on the cucumber wilt produced by Fusarium oxysporum (Schlecht) Snyder et Hansen and Verticillium dahliae Kleb. II. Specialization of the pathogens, p. 199­204. In: Bul. no. 15. de L'Academie des Sciences Agrioles et Forestieres, Romania.

Crall, J.M. 1963. Physiologic specialization in Fusarium oxysporum f. niveum. Phytopathology 53:873 (abstr.).

Crowhurst, R.N., Hawthorne, B.T., Rikkerink, E.H.A., and Templeton, MD. 1991. Differentiation of Fusarium solani f. sp. solani races 1 and 2 by random amplification of polymorphic DNA. Current Genet. 20:391­396.

Dixon, G.R. 1981. Vegetable crop diseases. AVI Publ. Co., Westport, Conn.

Doidge, E.M. and L.J. Kresfilder. 1932. A wilt disease of cucurbits. Farming S. Afr. 7:299­300.

Douglas, D.R. 1970. The effect of inoculum concentration on the apparent resistance of muskmelons to Fusarium oxysporum f. sp. melonis. Can. J. Bot. 48:687­693.

Drennan, J.L. and T.A. Zitter. 1997. Fusarium crown and foot rot on cucurbit seedlings and pumpkin fruit. Phytopathology 87:S25­26 (abstr.).

Dunlap, J.R. and B.D. Bruton. 1986. Pigment biosynthesis by Macrophomina phaseolina: the glycine-specific requirement. Trans. Brit. Mycol. Soc. 86:111­115.

El-Ani, A.S. 1956. Ascus development and nuclear behavior in Hypomyces solani f. cucurbitae. Amer. J. Bot. 43:769­778.

Elmstrom, G.W. and D.L. Hopkins. 1981. Resistance of watermelon cultivars to fusarium wilt. Plant Dis. 65:825­827.

Epstein, L., Y.H. Kwon, D.E. Almond, L.M. Schached, and M.J. Jones. 1994. Genetic and biochemical characterization of Nectria haematococca strains with adhesive and adhesive-reduced macroconidia. Appl. Environ.

Cucurbitaceae '98

Microbiol. 60:524­430.

Everett, P.H. and Blazquez. 1967. Influence of lime on the development of fusarium wilt of watermelon. Proc. Fla. St. Hort. Soc. 80:143­148.

Fitzell, R., G. Evans, and P.C. Fahy. 1980. Studies on the colonization of plant roots by Verticillium dahliae Klebahn with use of immunofluorescent staining. Austral. J. Bot. 28:357­368.

Garcia-Jimenez, J., J. Armengol, G. Martinez-Ferrer. 1994a. Resistencia y comportamento en campo de diversos cultivares de melon crecidos en suelo infestado naturalmente con Acremonium sp. Investigacion Agraria, Produccion y Proteccion Vegetales Fuera Serie 2:263­274.

Garcia-Jimenez, J., M. Garcia-Morato, M.T. Velazquez, and A. Alfaro. 1990. Ensayos preliminares de control de la muerte súbita del melón mediante la utilizatión de portainjertos resistentes. Bol. San. Veg. Plagas 16:709­715.

Garcia-Jimenez, J., M.T. Velazquez, and A. Alfaro. 1989. Secuencia de sintomas en el colapso del melon. Bol. San. Veg. Plagas 4:333­342.

García-Jiménez, J., T. Velázquez, C. Jorda, and A. Alfaro-García. 1994b. Acremonium sp., causal agent of muskmelon collapse in Spain. Plant Dis. 78:416­419.

Georgopoulos, S.G. 1963. Pathogenicity of chlorinated-nitrobenzine-tolerant strains of Hypomyces solani f. cucurbitae race 1. Phytopathology 53:1081­1085.

Gerlagh, M. and W.J. Blok. 1988. Fusarium oxysporum f. sp. cucurbitacearum n. f. embracing all formae speciales of F. oxysporum attacking cucurbitaceous crops. Neth. J. Plant Pathol. 94:17­31.

Gordon, T.R. and D. Okamoto. 1992. Population structure and the relationship between pathogenic and nonpathogenic strains of Fusarium oxysporum. Phytopathology 82:73­77.

Gordon, T.R. and R.D. Martyn. 1997. The evolutionary biology of Fusarium oxysporum. Annu. Rev. Phytopathol. 35:111­128.

Gordon, T.R., D. Okamoto, and D.J. Jacobson. 1989. Colonization of muskmelon and nonsusceptible crops by Fusarium oxysporum f. sp. melonis and other species of Fusarium. Phytopathology 79:1095­1100.

Gordon, T.R., D.J. Jacobson, D.M. May, K.B. Tyler, and F.W. Zink. 1990. Fruit yield, disease incidence, and root colonization of hybrid muskmelons resistant to fusarium wilt. Plant Dis. 74:778­781.

Gubler, W.D. 1982. Epidemiology and control of cephalosporium root and hypocotyl rot of melon in California. PhD diss., Univ. California, Davis.

Gubler, W.D. 1996. Verticillium wilt, p. 22­23. In: T.A. Zitter, D.L. Hopkins, and C.E. Thomas (eds.). Compendium of cucurbit diseases. Amer. Phytopathol. Soc., St. Paul, Minn.

Gwynne, B.J., R.M. Davis, and T.R. Gordon. 1997. Occurrence and pathogenicity of fungi associated with melon vine decline in California. Phytopathology 87:S37 (abstr.).

Hawthorne B.T, Ball R.D., and Rees-George J. 1994. Genetic analysis of variation of pathogenicity in Nectria haematococca (Fusarium solani) on Cucurbita sp. Mycol. Res. 98:1183­1191.

Henderson. W.R., S.F. Jenkins, and J.O. Railings. 1970. The inheritance of fusarium wilt resistance in watermelon, Citrullus lanatus (Thumb.) Mans. J. Amer. Soc. Hort. Sci. 95:276­282.

Hopkins, D.L and G.W. Elmstrom. 1984. Fusarium wilt in watermelon cultivars grown in a 4-year monoculture. Plant Dis. 68:129­131.

Hopkins, D.L. and G.W. Elmstrom. 1976. Effect of soil pH and nitrogen source on fusarium wilt of watermelon on land previously cropped in watermelons. Proc. Fla. St. Hort. Soc. 89:141­143.

Hopkins, D.L., R.P. Larkin, and R.J. Lobinske. 1989. Effect of watermelon cultivar monoculture on aggressiveness of Fusarium oxysporum f. sp. niveum. Phytopathology 78:1542 (abstr.).

Ioannou, N. and C.A. Poullis. 1991. Fusarium wilt of resistant watermelon cultivars associated with a highly virulent local strain of Fusarium oxysporum f. sp. niveum. Ministry Agr. Nat. Resources, Agr. Res. Inst. Tech. Bul. 129.

Jacobson, D.J. and T.R. Gordon. 1988. Vegetative compatibility and self-incompatibility within Fusarium oxysporum f. sp. melonis. Phytopathology 78:668­672.

Jacobson, D.J. and T.R. Gordon. 1990a. Further investigations of vegetative compatibility within Fusarium oxysporum f. sp. melonis. Can. J. Bot. 68:1245­1248.

Jacobson, D.J. and T.R. Gordon. 1990b. Variability of mitochondrial DNA as an indicator of relationships between populations of Fusarium oxysporum f. sp. melonis. Mycol. Res. 94:734­744.

Jenkins, S.F., Jr. and T.C. Wehner. 1983. Occurrence of Fusarium oxysporum f. sp. cucumerinum on greenhouse-grown Cucumis sativus seed stocks in North Carolina. Plant Dis. 67:1024­1025.

Jones, M.J. and L. Epstein. 1989. Adhesion of Nectria haematococca macroconidia. Physiol. Mol. Plant Pathol. 35:453­461.

Kanno, T. X. Han, and Y. Tabei. 1991. Genetic analysis of resistance in cucumber to Fusarium oxysporum f. sp. cucumerinum. Bul. Veg. Breeding Dept., Nat. Res. Inst. Veg., Ornamental Plants and Tea 4:27­30.

Katan, T., J. Katan, T.R. Gordon, and D. Pozniak. 1994. Physiological races and vegetative compatibility within Fusarium oxysporum f. sp. melonis. Phytopathology 78:668­672.

Kato, T., K. Suzuki, J. Takahashi, and K. Kamoshita. 1984. Negatively correlated cross-resistance between benzimidazole fungicides and methyl N-(3,5-dichlorophenyl) carbamate. J. Pesticide Sci. 9:489­495.

Keinath, A.P. and T.A. Zitter. 1998. Resistance to benomyl and thiophanate-methyl in Didymella bryoniae from South Carolina and New York. Plant Dis. 82:479­484.

Keinath, A.P., F.W. Farnham, and T.A. Zitter. 1995. Morphological, pathological, and genetic differentiation of

Cucurbitaceae '98

Didymella bryoniae and Phoma spp. isolated from cucurbits. Phytopathology 85:364­369.

Kerling, L.C.P. and L. Bravenboer. 1967. Foot rot of Cucurbita ficifolia, the rootstock of cucumber, caused by Nectria haematococca var. cucurbitae. Neth. J. Plant Pathol. 73:15­24.

Kim, D.H., R.D. Martyn, and C.W. Magill. 1992. Restriction fragment length polymorphism groups and physical map of mitochondrial DNA from Fusarium oxysporum f. sp. niveum. Phytopathology 82:346­353.

Kim, D.H., R.D. Martyn, and C.W. Magill. 1993. Mitochondrial DNA (mtDNA)-relatedness among formae speciales of Fusarium oxysporum in the Cucurbitae. Phytopathology 83:91­97.

Kinjo, K. and T. Tokashiki. 1989. Fusarium solani f. sp. cucurbitae race 1 isolated from root stocks of withered balsam pear grafted on squash. Bul. Okinawa Agr. Expt. Sta. 13:95­98.

Kirby, G.C. and J.J. Burdon. 1997. Effects of mutation and random drift on Leonard's gene-for-gene coevolution model. Phytopathology 87:488­493.

Kistler, H.C. 1997. Genetic diversity in the plant-pathogenic fungus Fusarium oxysporum. Phytopathology 87:474­479.

Kistler, H.C. and V.P.W. Miao. 1992. New modes of genetic change in filamentous fungi. Annu. Rev. Phytopathol. 30:131­152.

Kistler, H.C., C. Alabouvette, R.P. Baayen, S. Bentley, D. Brayford, A. Coddington, J. Correll, M.-J. Daboussi, D. Elias, D. Fernandez, T.R. Gordon, T. Katan, H.G. Kim, J.F. Leslie, R.D. Martyn, Q. Migheli, N.Y. Moore, K. O'Donnell, R.C. Ploetz, M.A. Rutherford, B. Summerell, C. Waalwijk, and S. Woo. 1998. Systematic numbering of vegetative compatibility groups in the plant pathogenic fungus Fusarium oxysporum. Phytopathology 88:30­32.

Kistler, H.C., E.A. Momol, and U. Benny. 1991. Repetitive genomic sequences for determining relatedness among strains of Fusarium oxysporum. Phytopathology 81:331­336.

Krikun, J. 1985. Observations on the distribution of the pathogen Monosporascus eutypoides as related to soil temperature and fertigation. Phytoparasitica 13:225­228.

Krikun, J. and C.C. Bernier. 1987. Infection of several crop species by two isolates of Verticillium dahliae. Can. J. Plant Pathol. 9:241­245.

Kwon, Y.-S., Y.H. Om, L. Hawkins, and F. Dane. 1998. Molecular tagging of gummy stem blight resistance in watermelon. HortScience 33:472 (abstr.).

Larkin, R.P., D.L. Hopkins, and F.N. Martin. 1990. Vegetative compatibility within Fusarium oxysporum f. sp. niveum and its relationship to virulence, aggressiveness, and race. Can. J. Microbiol. 36:352­358.

Larkin, R.P., D.L. Hopkins, and F.N. Martin. 1993. Ecology of Fusarium oxysporum f. sp. niveum in soils suppressive and conducive to fusarium wilt of watermelon. Phytopathology 83:1105­1116.

Latin, R.X., and S.J. Snell. 1986. Comparison of methods for inoculation of muskmelon with Fusarium oxysporum f. sp. melonis. Plant Dis. 70:287­300.

Leach, J.G. and T.M. Currence. 1938. Fusarium wilt of muskmelon in Minnesota. Minnesota Agr. Expt. Sta. Tech. Bul. 129.

Lee, D.-H., S.B. Mathur, and P. Neergaard. 1984. Detection and location of seed-borne inoculum of Didymella bryoniae and its transmission in seedlings of cucumber and pumpkin. Phytopath. Z. 109:301­308.

Leonard, K.J. 1994. Stability of equilibria in a gene-for-gene coevolution model of host­parasite interactions. Phytopathology 84:70­77.

Leonard, K.J. and R.J. Czochor. 1980. Theory of genetic interactions among populations among populations of plants and their pathogens. Annu. Rev. Phytpathol. 18:237­258.

Lovic, B.R., R.D. Martyn, and M.E. Miller. 1995. Sequence analysis of the ITS regions of rDNA in Monosporascus spp. reveals its potential for PCR-mediated detection. Phytpathology 85:655­661.

Malathrakis, N.E. and K.J. Vakalounakis. 1983. Resistance to benzimidazole fungicides in the gummy stem blight pathogen Didymella bryoniae on cucurbits. Plant Pathol. 32:395­399.

Martyn, R., J. Mertely, M. Miller, C. Katsar, and R. Baasiri. 1992. Morphology and germination of Monosporascus cannonballus ascospores. Phytopathology 82:1115 (abstr.).

Martyn, R.D. 1987. Fusarium oxysporum f. sp. niveum race 2: A highly aggressive race new to the United States. Plant Dis. 71:233­236.

Martyn, R.D. and B.D. Bruton. 1989. An initial survey of the United States for races of Fusarium oxysporum f. sp. niveum. HortScience 24:696­698.

Martyn, R.D. and D. Netzer. 1991. Resistance to races 0, 1, and 2 of fusarium wilt of watermelon in Citrullis sp. PI 296341-FR. HortScience 26:429­432.

Martyn, R.D. and M.E. Miller. 1996. Monosporascus root rot and vine decline: An emerging disease of melons worldwide. Plant Dis. 80:716­725.

Martyn, R.D. and R.J. McLaughlin. 1983. Effects of inoculum concentration on the apparent resistance of watermelons to Fusarium oxysporum f. sp. niveum. Plant Dis. 67:493­495.

Mas, P., P.M. Molot, and G. Risser. 1981. Fusarium wilt of muskmelon, p. 169­177. In: P.E. Nelson, T.A. Toussoun, and R.J. Cook (eds.). Fusarium: Diseases, biology, and taxonomy. Pa. State Univ. Press, University Park.

Matuo, T. and W.C. Snyder. 1973. Use of morphology and mating populations in the identification of formae specialis in Fusarium solani. Phytopathology 63:562­565.

McCreight, J.D., H. Nerson, and R. Grumet. 1993. Melon Cucumis melo L., p. 267­294. In: G. Kalloo and B.O. Bergh (eds.). Genetic improvement of vegetable crops. Pergamon Press, New York.

McDermott, J.M. and B.A. McDonald. 1993. Gene flow in

Cucurbitaceae '98

plant pathosystems. Annu. Rev. Phytopathol. 31: 353­373.

McGrath, D.J., L. Vawdrey, and I.O. Walker. 1993. Resistance to gummy stem blight in muskmelon. HortScience 28:930­931.

McKeen, C.D. 1951. Investigations of fusarium wilt of muskmelons and watermelons in southwestern Ontario. Sci. Agr. 31:413­423.

McKeen, C.D. 1957. Phomopsis black rot of cucurbits. Can. J. Bot. 35:43­50.

McMillan, R.T. 1986. Cross pathogenicity studies with isolates of Fusarium oxysporum from either cucumber or watermelon pathogenic to both crop species. Ann. Appl. Biol. 109:101­105.

Mertely, J.C., R. D. Martyn, M.E. Miller, and B.D. Bruton. 1991. Role of Monosporascus cannonballus and other fungi in a root rot/vine decline disease of muskmelon. Plant Dis. 75:1133­1137.

Mertely, J.C., R.D. Martyn, M.E. Miller, and B.D. Bruton. 1993a. An expanded host range for the muskmelon pathogen Monosporascus cannonballus. Plant Dis. 77:667­673.

Mertely, J.C., R.D. Martyn, M.E. Miller, and B.D. Bruton. 1993b. Quantification of Monosporascus cannonballus ascospores in three commercial muskmelon fields in south Texas. Plant Dis. 77:766­771.

Miller, M.E., T. Isakeit, J.X. Zhang, and B.D. Bruton. 1997. Gummy stem blight and black rot of melons, p. 1­19. In: M.E. Miller (ed.). Melon production system in southern Texas. Annu. Res. Rpt., Texas A&M Univ., Weslaco.

Miller, M.E., R.D. Martyn, B. R. Lovic, and B.D. Bruton. 1995. An overview of vine decline diseases of melons, p. 31­35. In: G. Lester and J. Dunlap (eds.). Cucurbitaceae'94: Evaluation and enhancement of cucurbit germplasm. Gateway Printing, Edinburg, Texas.

Mohammed, M.A., A.A. Hassan, I.I. Oksh, and R. Hilal. 1981. Nature of resistance to fusarium wilt in watermelon. Egypt. J. Hort. 8:1­12.

Nagao, H., Sato K., and Ogiwara S. 1994. Susceptibility of Cucurbita spp. to the cucurbit root-rot fungus, Fusarium solani f sp cucurbitae race 1. Agronomie 2: 95­102.

Namiki, F., S. Izumi, T. Kayamura, and T. Shiomi. 1992. Specialization of pathogenic strains of Fusarium oxysporum in the Cucurbitaceae. Ann. Phytopathol. Soc. Jpn. 58:540­541.

Namiki, F., T. Shiomi, K. Nishi, T. Kayamura, and T. Tsuge. 1998. Pathogenic and genetic variation in the Japanese strains of Fusarium oxysporum f. sp. melonis. Phytopathology 88:804­810.

Namiki, F., T. Shiomi, T. Kayamura, and T. Tsuge. 1994. Characterization of the formae speciales of Fusarium oxysporum causing wilts of cucurbits by DNA fingerprinting with nuclear repetitive DNA sequences. Appl. Environ. Microbiol. 60:2684­2691.

Nash, S.M. and J.V. Alexander. 1965. Comparative survival of Fusarium solani f. cucurbitae and F. solani f. phaseoli in soil. Phytopathology 55:963­966.

Neergaard, E. de, G. Haupt, and K. Rasmussen. 1993. Studies of Didymella bryoniae: The influence of nutrition and cultural practices on the occurrence of stem lesions and internal and external fruit rot on different cultivars of cucumber. Neth. J. Plant Pathol. 99:335­343.

Nerson, H. H.S. Paris, M. Edelstein, Y. Burger, and Z. Karchi. 1988. Breeding pickling melons for a concentrated yield. HortScience 23:136­138.

Netzer, D. 1976. Physiological races and soil population levels of fusarium wilt of watermelon. Phytoparasitica 4:131­136.

Netzer, D. and C. Weintall. 1980. Inheritance of resistance in watermelon to race 1 of Fusarium oxysporum f. sp. niveum. Plant Dis. 64:853­854.

Netzer, D. and I. Dishon. 1973. Screening for resistance and physiological specialization of Fusarium oxysporum in watermelon and muskmelon. 2nd Intl. Congr. Plant Pathol. Minneapolis, Minn. (abstr. 941).

Netzer, D. and R.D. Martyn. 1989. PI 296341, a source of resistance in watermelon to race 2 of Fusarium oxysporum f. sp. niveum. Plant Dis. 73:518.

Netzer, D., G. Kritzman, and I. Chet. 1979. b-(1,3) Glucanase activity and quantity of fungus in relation to fusarium wilt in resistant and susceptible near-isogenic lines of muskmelon. Physiol. Plant Pathol. 14:47­55.

Netzer, D., S. Niego, and E. Galun. 1977. A dominant gene conferring resistance to fusarium wilt in cucumber. Phytopathology 67:525­527.

Ng, T.J. and J.G. Kantzes. 1995. Field screening for resistance to races 1 and 2 of Fusarium oxysporum f. sp. melonis in melon (Cucumis melo L.), p. 110­116. In: G. Lester and J. Dunlap (eds.). Proc.Cucurbitaceae'94: Evaluation and enhancement of cucurbit germplasm. Gateway Printing, Edinburg, Texas.

Norton, J.D. 1971. Gulfcoast­A sweet cantaloupe for the produce chain store market. Ala. Agr. Expt. Sta. Lflt. 82.

Norton, J.D. 1972. Chilton­A high quality fruit for the commercial market. Ala. Agr. Expt. Sta. Lflt. 84.

Norton, J.D. 1979. Inheritance of resistance to gummy stem blight in watermelon. HortScience 14:630­632.

Norton, J.D., and R.D. Cosper. 1989. AC-70-154, a gummy stem blight resistant muskmelon breeding line. HortScience 24:709­711.

Norton, J.D., R.D. Cosper, D.A. Smith, and K.S. Rymal. 1985. AUrora­A high quality disease resistant cantaloupe. Ala. Agr. Expt. Sta. Circ. 278.

O'Donnell K, and L.E. Gray . 1995. Phylogenetic relationships of the soybean sudden death syndrome pathogen Fusarium solani f. sp. phaseoli inferred from rDNA sequence data and PCR primers for its identification. Mol. Plant­Microbe Interact. 8:709­716.

Oosthuizen, M.M.J. and D.J.J. Potgieter. 1974. Induction of photosporogenis in Macrophomina phaseoli by an octadecenoic acid from peanuts. Phytochemistry 13:1027­1029.

Cucurbitaceae '98

Orton, W.A. 1913. The development of disease-resistant varieties of plants. 4th Conf. Intl. Genetique, Paris 4:247­267.

Owen, J.H. 1956. Cucumber wilt, caused by Fusarium oxysporum f. cucumerinum n. f. Phytopathology 46:153­157.

Paris, H.S. 1989. Historical records, origins, and development of the edible cultivar groups of Cucurbita pepo (Cucurbitaceae). Economic Bot. 43:423­443.

Paris, H.S., R. Cohen, Y. Danin-Poleg, and S. Schreiber. 1993. Gene for resistance to fusarium wilt race 1 in oriental pickling melon. Cucurbit Genet. Coop. Rpt. 16:42­43.

Paternotte, S.J. 1987. Pathogenicity of Fusarium solani f. sp. cucurbitae race 1 to courgette. Neth. J. Plant Pathol. 93:245­252.

Paulus, A.O., O.A. Harvey, J. Nelson, and F. Shibuya. 1976. Fusarium-resistant watermelon cultivars. Calif. Agr. 30:5­6.

Pierce, L.K. and T.C. Wehner. 1989. Gene list for cucumber. Cucurbit Genet. Coop. Rpt. 12:91­103.

Pierce, L.K. and T.C. Wehner. 1990. Review of genes and linkage groups in cucumber. HortScience 25:605­615.

Pitrat, M. 1991. Linkage groups in Cucumis melo L. J. Hered. 82:406­411.

Pivonia, S., R. Cohen, U. Kafkafi, I.S. Ben Ze'ev, and J. Katan. 1997. Sudden wilt of melons in southern Israel: Fungal agents and relationship with plant development. Plant Dis. 81:1264­1268.

Prasad, K. and J.D. Norton. 1967. Inheritance of resistance to Mycosphaerella citrullina in muskmelon. Proc. Amer. Soc. Hort. Sci. 91:396­400.

Prasad, N. 1949. Variability of the cucurbit root-rot fungus, Fusarium (Hypomyces) solani f. cucurbitae. Phytopathology 39:133­141.

Puhalla, J.E. and M. Hummel. 1983. Vegetative compatibility groups within Verticillium dahliae. Phytopathology 73:1305­1308.

Radhakrishnan, P. and B. Sen. 1986. Comparative studies on muskmelon wilt induced by Fusarium oxysporum f. sp. melonis and F. solani. Indian Phytopath. 39:376­379.

Reid, J. 1958. Studies on the fusaria which cause wilt in melons I. The occurrence and distribution of races of the muskmelon and watermelon fusaria and a histological study of the colonization of muskmelon plants susceptible or resistant to fusarium wilt. Can. J. Bot. 36:393­410.

Reuveni, R., J. Krikun, and U. Shani. 1983. The role of Monosporascus eutypoides in a collapse of melon plants in an arid area of Israel. Phytopathology 73:1223­1226.

Risser, G. 1973. Etude de l'heredite de la resistance du melon (Cucumis melo) aux races 1 et 2 de Fusarium oxysporum f. melonis. Ann. Amelior. Plant. 23:259­263.

Risser, G. 1987. Controversy on resistance to fusarium wilt in 'Perlita' (Cucumis melo L.). Cucurbit Genet. Coop. Rpt. 10:60­61.

Risser, G., Z. Banihashemi, and D.W. Davis. 1976. A proposed nomenclature of Fusarium oxysporum f. sp.

melonis races and resistance genes in Cucumis melo. Phytopathology 66:1105­1106.

Robinson, R.W., H.M. Munger, T.W. Whitaker, and G.W. Bohn. 1976. Genes of the Cucurbitaceae. HortScience 11:554­568.

Samac, D.A. and S.A. Leong. 1989. Disease development in Cucurbita maxima (squash) infected with Fusarium solani f. sp. cucurbitae. Can. J. Bot. 67:3486­3489.

Schenck, N.C. 1961. Resistance of commercial watermelon varieties to fusarium wilt. Proc. Fla. State Hort. Soc. 74:183­186.

Schenck, N.C. 1968. Epidemiology of gummy stem blight (Mycosphaerella citrullina) on watermelon: Ascospore incidence and disease development. Phytopathology 58:1420­1422.

Sedcole, J.R. 1978. Selection pressures and plant pathogens: Stability and equilibria. Phytopathology 68:967­970.

Selby, A.D. 1899. Further studies of cucumber, melon, and tomato diseases, with experiments. Ohio Agr. Expt. Sta. Bul. 105:217­236.

Sherf, A.F., and A.A. MacNab. 1986. Cucurbits, p. 307­380. In: Vegetable diseases and their control. 2nd ed. Wiley, New York.

Shimotsuma, M., J. Kuc, and C.M. Jones. 1972. The effects of prior inoculations with non-pathogenic fungi on fusarium wilt of watermelon. HortScience 7:72­73.

Sitterly, W.R. 1969. Effect of crop rotation on gummy stem blight. Plant Dis. Rptr. 53:417­419.

Sitterly, W.R. 1972. Breeding for disease resistance in cucurbits. Annu. Rev. Phytopathol. 10:471­490.

Sivanesan, A. 1991a. Monosporascus cannonballus. Mycopathologia 114:53­54.

Sivanesan, A. 1991b. Monosporascus eutypoides. Mycopathologia 114:55­56.

Skotland, C.B. 1971. Pathogenic and nonpathogenic Verticillium species from south central Washington. Phytopathology 61:435­436.

Sleeth, B. 1934. Fusarium niveum, the cause of watermelon wilt. W.Va. Agr. Expt. Sta. Bul. 257:1­23.

Smith, E.F. 1894. The watermelon disease of the south. Proc. Amer. Assn. Adv. Sci. 43:289­290.

Snyder, W.C. and H.N. Hansen. 1940. The species concept in Fusarium. Amer. J. Bot. 27:64­67.

Snyder, W.C. and H.N. Hansen. 1941. The species concept in Fusarium with reference to section Martiella. Amer. J. Bot. 28:738­742.

Sowell, G., Jr. 1975. An additional source of resistance to gummy stem blight in watermelon. Plant Dis. Rptr. 59:413­415.

Sowell, G., Jr. 1981. Additional sources of resistance to gummy stem blight of muskmelon. Plant Dis. 65:253­254.

Sowell, G., Jr., and G.R. Pointer. 1962. Gummy stem blight resistance of introduced watermelons. Plant Dis. Rptr. 46:883­885.

Sowell, G., Jr., K. Prasad, and J.D. Norton. 1966. Resistance of Cucumis melo introductions to Mycosphaerella

Cucurbitaceae '98

citrullina. Plant Dis. Rptr. 50:661­663.

Spiegel, Y., D. Netzer, and U. Kafkafi. 1987. The role of calcium nutrition on fusarium-wilt syndrome in muskmelon. J. Phytopathol. 118:220­226.

St. Amand, P.C. and T.C. Wehner. 1993. Correlations between years for foliar gummy stem blight disease ratings on field grown cucumbers. Cucurbit Genet. Coop. Rpt. 16:1­2.

St. Amand, P.C. and T.C. Wehner. 1995a. Eight isolates of Didymella bryoniae from geographically diverse areas exhibit variation in virulence but no isolate by cultivar interaction on Cucumis sativus. Plant Dis. 79:1136­1139.

St. Amand, P.C. and T.C. Wehner. 1995b. Greenhouse, detached-leaf, and field testing methods to determine cucumber resistance to gummy stem blight. J. Amer. Soc. Hort. Sci. 120:673­680.

Stakman, E.C. and F.J. Piemeisel. 1917. Biologic forms of Puccinia gramminis on cereals and grasses. J. Agr. Res. 10:429­495.

Stanghellini, M.E., D.H. Kim, and S.L. Rasmussen,. 1996. Ascospores of Monosporascus cannonballus: Germination and distribution in cultivated and desert soils in Arizona. Phytopathology 86:509­514.

Stanghellini, M.E., S.L. Rasmussen, D.H. Kim, and N. Oebker. 1995. Vine-decline of melons caused by Monosporascus cannonballus in Arizona: Epidemiology and cultivar susceptibility, p. 71­80. In: 1994­1995 Vegetable report. Univ. Ariz., Tucson, Coop. Ext. Rpt. Ser. P-100.

Starnes, H.N. 1897. Watermelons. Univ. Ga. Expt. Sta. Bul. 38.

Staub, J.E. 1995. Molecular markers: Genetic map construction and its application, p. 86­91. In: G. Lester and J. Dunlap (eds.). Cucurbitaceae'94: Evaluation and enhancement of cucurbit germplasm. Gateway Printing, Edinburg, Texas.

Stoddard, D.L. 1948. Nitrogen, potassium, and calcium in relation to fusarium wilt of muskmelon. Phytopathology 37:875­884.

Strausbaugh, C.A., M.N. Schroth, A.R. Weinhold, and J.G. Hancock. 1992. Assessment of vegetative compatibility of Verticillium dahliae tester strains and isolates from California potatoes. Phytopathology 82:61­68.

Sultana, N., A.K. Khanzada, and A. Ghaffar. 1994. Location of Macrophomina phaseolina in seeds of pumpkin and development of charcoal rot disease. Pakistan J. Bot. 26:177­180.

Sumner, D.R. 1976. Etiology and control of root rot of summer squash in Georgia. Plant Dis. Rptr. 60:923­927.

Sun, P. and X.B. Yang. 1998. Stability of a gene-for-gene coevolution system under constant perturbations. Phytopathology 88:592­597.

Svedelius, G. and T. Unestam. 1978. Experimental factors favouring infection of attached cucumber leaves by Didymella bryoniae. Trans. Brit. Mycol. Soc. 71:89­97.

Taubenhaus, J.J. 1935. Seeds of watermelons and okra as

possible carriers of fusarium wilt. Phytopathology 25:969 (abstr.).

Thinggaard, K. 1987. Attack of Didymella bryoniae on roots of cucumber. J. Phyotopathol. 120:372­375.

Thomas, C.E. 1986. Downy and powdery mildew resistant muskmelon breeding line MR-1. HortScience 21:329.

Toshimitsu, Y. and T. Noguchi. 1975. Inheritance of resistance to fusarium wilt in cucumber. Proc. Jpn. Hort. Soc. p. 150­151.

Toussoun T.A. and W.C. Snyder. 1961. The pathogenicity, distribution, and control of two races of Fusarium (Hypomyces) solani f. cucurbitae. Phytopathology 51:17­22.

Vakalounakis, D.J. 1993. Inheritance and genetic linkage of fusarium wilt (Fusarium oxysporum f. sp. cucumerinum race 1) and scab (Cladosporium cucumerinum) resistance genes in cucumber (Cucumis sativus). Ann. Appl. Biol. 123:359­365.

Vakalounakis, D.J. 1995. Inheritance and linkage or resistance in cucumber line SMR-18 to races 1 and 2 of Fusarium oxysporum f. sp. cucumerinum. Plant Pathol. 44:169­172.

Vakalounakis, D.J. 1996. Allelism of the Fcu-1 and Foc genes conferring resistance to fusarium wilt in cucumber. Eur. J. Plant Pathol. 102:855­858.

Vakalounakis, D.J. and E. Klironomou. 1994. Independence between scab resistance and morphological traits in cucumber. HortScience 29:1180­1181.

Vakalounakis, D.J. and K. Smardas. 1995. Genetics of resistance to Fusarium oxysporum f. sp. cucumerinum races 1 and 2 in cucumber line Wisconsin-2757. Ann. Appl. Biol. 127:457­461.

Van Etten, H.D. and H.C. Kistler. 1988. Nectria haematococca mating populations I and VI, p. 180­206. In: D.S. Ingram and P.H. Williams (eds.). Advances in plant pathology. vol. 6. Academic Press, New York.

Van Koot, J. 1943. Enkele onderzoegingen betreffende de fusarium ziekte bif de komkomer. Tijdshr. over Plantenziekten 49:52­72.

Van Steekelenburg, N.A.M. 1982. Factors influencing external fruit rot of cucumber caused by Didymella bryoniae. Neth. J. Plant Pathol. 88:47­56.

Van Steekelenburg, N.A.M. 1983. Epidemiological aspects of Didymella bryoniae, the cause of stem and fruit rot of cucumber. Neth. J. Plant Pathol. 89:75­86.

Van Steekelenburg, N.A.M. 1987. Resistance to benzimidazole and dicarboximide fungicides in Botrytis cinerea and Didymella bryoniae in cucumbers in the Netherlands. Med. Fac. Landbouww. Rijksuniv. Gent. 52:875­880.

Van Steekelenburg, N.A.M. and J. van de Vooren. 1980. Influence of the glasshouse climate on development of diseases in a cucumber crop with special reference to stem and fruit rot caused by Didymella bryoniae. Acta Hort. 118:45­56.

Vannacci, G. and P. Gambogi. 1980. Fusarium solani f. sp. cucurbitae razza 1 su semi di Cucurbita pepo L.:

Cucurbitaceae '98

Reperimento del pahtogeno e influenza di condizioni colturali sull'andamento della malattia. Phytopathol. Mediterr. 19:103­114.

Vicente, M.J., P. Abad, and J.L. Cenis. 1994. RFLPs del ADN mitochondrial, RAPDs y VCGs de Acremonium sp.: Marcadores geneticos para su identificacion taxonomica, p. 401­415. In: J.M. Garcia Baudin, A. Garrido Vivas, and R. Jimenez Diaz (eds.). La Proteccion Vegetal en Espana. Instituto Nacional de Investigacion y Tecnologia Agraria y Alimentaria, Madrid.

Walker, M.N. 1941. Fusarium wilt of watermelons. I. Effect of soil temperature on the wilt disease and the growth of watermelon seedlings. Fla. Agr. Expt. Sta. Bul. 33:3­29.

Wang, Y.-H., C.E. Thomas, and R.A. Dean. 1997. A genetic map of melon (Cucumis melo L.) based on amplified fragment length polymorphism (AFLP) markers. Theor. Appl. Genet. 95:791­798.

Wechter, W.P., M.P. Whitehead, C.E. Thomas, and R.A. Dean. 1995. Identification of a randomly amplified polymorphic DNA marker linked to the Fom 2 fusarium wilt resistance gene in muskmelon MR-1. Phytopathology 85:1245­1249.

Wechter, W.P., R.A. Dean, and C.E. Thomas. 1998. Development of sequence specific primers that amplify a 1.5-kb DNA marker for race 1 fusarium wilt resistance in Cucumis melo L. HortScience 33:291­292.

Wehner, T.C. and P.C. St. Amand. 1993. Field tests for cucumber resistance to gummy stem blight in North Carolina. HortScience 28:327­329.

Whitaker, T.W. and D.W. Davis. 1962. Cucurbits: Botany, cultivation and utilization. Intersience, New York.

Wilhelm, S. 1955. Longivity of the verticillium wilt fungus in the laboratory and field. Phytopathology 45:180­181.

Wolff, D.W. 1995. Evaluation of melon germplasm for resistance to monosporascus root rot/vine decline, p. 224­228. In: G. Lester and J. Dunlap (eds.). Cucurbitaceae'94: Evaluation and enhancement of cucurbit germplasm. Gateway Printing, Edinburg, Texas.

Wolff, D.W. 1996. Genotype, fruit load, and temperature affect monosporascus root rot/vine decline symptom expression in melon (Cucumis melo L.), p. 280­284. In: M.L. Gomez-Guillamon, C. Soria, J. Cuartero, J.A. Tores, and R. Fernandez-Munoz (eds.). Cucurbits to

wards 2000: Proc. 7th Eucarpia Meeting on Cucurbit Genetics and Breeding. C.S.I.C., Malaga, Spain.

Wolff, D.W. and M.E. Miller. 1998. Tolerance to monosporascus root rot and vine decline in melon (Cucumis melo L.) germplasm. HortScience 33:287­290.

Wolff, D.W., D.I. Leskovar, M.C. Black, and M.E. Miller. 1997. Differential fruit load in melon (Cucumis melo L.) affects shoot and root growth, and vine decline symptoms. HortScience 32:526 (abstr.).

Zhang, X. and B. Rhodes. 1993. Inheritance of resistance to races 0, 1, and 2 of Fusarium oxysporum f. sp. niveum in watermelon (Citrullus sp. PI 296341). Cucurbit Genet. Coop. Rpt. 16:77­78.

Zhang, Y., K. Anagnostou, M.M. Kyle, and T.A. Zitter. 1995. Seedling screens for resistance to gummy stem blight in squash. Cucurbit Genet. Coop. Rpt. 18:59­61.

Zhang, Y., M. Kyle, K. Anagnostou, and T.A. Zitter. 1997. Screening melon (Cucumis melo) for resistance to gummy stem blight in the greenhouse and field. HortScience 32:117­121.

Zink, F.W. and C.E. Thomas. 1990. Genetics of resistance to Fusarium oxysporum f. sp. melonis race 0, 1, and 2 in muskmelon line MR-1. Phytopathology 80:1230­1232.

Zink, F.W. and W.D. Gubler. 1985. Inheritance of resistance in muskmelon to fusarium wilt. J. Amer. Soc. Hort. Sci. 110:600­604.

Zink, F.W. and W.D. Gubler. 1987. U.C. PMR 45 and U.C. Top Mark fusarium wilt-resistant (Fom-3) muskmelon breeding lines. HortScience 22:172.

Zitter, T.A. 1995. Sudden wilt of melons from a northeastern U.S. perspective, p. 44­47. In: G. Lester and J. Dunlap (eds.). Cucurbitaceae'94: Evaluation and enhancement of cucurbit germplasm. Gateway Printing, Edinburg, Texas.

Zitter, T.A. and M.M. Kyle. 1992. Impact of powdery mildew and gummy stem blight on collapse of pumpkins (Cucurbita pepo L.). Cucurbit Genet. Coop. Rpt. 15:93096.

Zitter, T.A., D.L. Hopkins, and C.E. Thomas (eds.). 1996. Compendium of cucurbit diseases. Amer. Phytopathol. Soc., St. Paul, Minn.

Zuniga, T.L., T.A. Zitter, T.R. Gordon, D.T. Schroeder, and D. Okamoto. 1997. Characterization of pathogenic races of Fusarium oxysporum f. sp. melonis causing fusarium wilt of melon in New York. Plant Dis. 81:592­596.

Cucurbitaceae '98