From Native Plants in Central Europe to Cultivated Crops Worldwide: The Emergence of Didymella bryoniae as a Cucurbit Pathogen

in HortScience

Didymella bryoniae (Auersw.) Rehm [anamorph Phoma cucurbitacearum (Fr.) Sacc.], the plant pathogenic fungus that causes gummy stem blight and black rot on cucurbits, was first described in 1869 from Bryonia (bryony or wild hops) in central Europe. Today, this pathogen is found on six continents on at least 12 genera and 23 species of cucurbits. How did D. bryoniae progress from a pathogen of a native plant in central Europe to a worldwide threat to cucurbits cultivated in humid environments? Clues from the early discoveries of this fungus, its characteristics as a seedborne pathogen, and its broad adaptation to cucurbit hosts will provide some answers to this question.

Abstract

Didymella bryoniae (Auersw.) Rehm [anamorph Phoma cucurbitacearum (Fr.) Sacc.], the plant pathogenic fungus that causes gummy stem blight and black rot on cucurbits, was first described in 1869 from Bryonia (bryony or wild hops) in central Europe. Today, this pathogen is found on six continents on at least 12 genera and 23 species of cucurbits. How did D. bryoniae progress from a pathogen of a native plant in central Europe to a worldwide threat to cucurbits cultivated in humid environments? Clues from the early discoveries of this fungus, its characteristics as a seedborne pathogen, and its broad adaptation to cucurbit hosts will provide some answers to this question.

Early Reports of Didymella bryoniae and Gummy Stem Blight

Both Bernhard Auerswald and Karl Fuckel, working independently, described Didymella bryoniae in 1869 from specimens collected on the cucurbit Bryonia growing in Germany (Corlett, 1981; Robert et al., 2005). Although each mycologist assigned the fungus to a different genus, they coined the same species name “bryoniae” following the convention that the specific epithet of the fungus should be taken from the generic name of the plant host (Table 1). Because Auerswald's report was published first in 1869, he is credited with the discovery, and his name has priority according to most mycologists. Fuckel's report was not published until 1870, when volumes 23 (1869) and 24 (1870) of the journal were published together (Robert et al., 2005). Note that the genus Didymella was not created until 1880 by Pier Andrea Saccardo. In 1881, Heinrich Rehm transferred species bryoniae to Didymella. However, this did not prevent subsequent collectors from creating additional names for this fungus (Table 1).

Table 1.

Pre-1900 collections of Didymella bryoniae (Auersw.) Rehm.

Table 1.

The earliest collection and unambiguous report of D. bryoniae on a cultivated cucurbit is from Cucumis melo L. in Italy collected in an unknown year and described as Didymella melonis Pass. by Giovanni Passerini in 1885 (Corlett, 1981) (Table 1). In 1891, three collections from cultivated cucurbits were made: William Dudley found D. bryoniae on cucumber (Cucumis sativus L.) in a greenhouse on the Cornell University campus, New York (Farr and Rossman, 2010); Casimir Roumeguère found it on cucumber in France (Chiu and Walker, 1949); and Frederick Chester found it on watermelon [Citrullus lanatus (Thunb.) Matsum. & Nakai] in Delaware. Frederick Chester, a plant pathologist, noted that the disease had already occurred “for some years past” and resulted in “widespread financial disaster wherever it gains foothold” (Chester, 1891). All three collectors observed only pycnidia on their specimens, because they named their pathogens Phyllosticta cucurbitacearum Sacc., Ascochyta cucumis Fautr. & Roum. and Phyllosticta citrullina Chester with generic names of anamorphic fungi. Roumeguère and Chester created new species names that again were based on the particular host, because they apparently thought they had discovered a unique fungus. Several years later, D. bryoniae was found in the midwestern United States, again on cucumber, by the botanist and plant pathologist Augustine Selby (Table 1). In the first decade of the 20th century, additional collections and reports appeared from additional states in the United States and Puerto Rico (Farr and Rossman, 2010).

Note that what is assumed to be the first report of D. bryoniae was by Elias Fries (Table 1), one of the founders of mycology, who found a novel fungus growing on a cucurbit (genus unknown) and named it Sphaeria cucurbitacearum (Robert et al., 2005). The genus Sphaeria was used by early mycologists for fungi that produced pycnidia (asexual fruiting bodies) or perithecia (sexual fruiting bodies) (Kirk et al., 2008). Saccardo assumed that Fries found pycnidia, because he used this species epithet as the basis for his name Phoma cucurbitacearum (Fr.) Sacc., which is used by most scientists for the anamorph (asexual) stage of the fungus that produces pycnidia. Recently, the new name, Stagonosporopsis cucurbitacearum (Fr.) Aveskamp, Gruyter & Verkley, has been proposed for the anamorph based on molecular analysis and division of species of Phoma into numerous clades (Aveskamp et al., 2010). In reality, the distinction between asexual and sexual states of D. bryoniae is not terribly important biologically, because the fungus is homothallic and readily produces both fruiting bodies on a variety of hosts (Keinath, 2010).

It is interesting to note that 1) the earliest confirmed collections of D. bryoniae were on Bryonia; and 2) pseudothecia were present in each case. In contrast, the collections in the 1890s were all from cultivated cucurbits on which either only pycnidia had formed or the collectors overlooked pseudothecia. It took several more decades until the connection was made between D. bryoniae and its asexual state. Whether D. bryoniae spread from Bryonia to cultivated cucurbits cannot be determined, because there were no early collections of the fungus from both hosts in the same location. More likely, with the increased knowledge of basic plant pathology, gummy stem blight came to be recognized as a disease of cucurbits caused by a fungus. That this happened independently during this period can be seen from the variety of names assigned to the pathogen. Thus, most botanists, mycologists, and plant pathologists discovered D. bryoniae because it attracted their attention in their localities, not because they had read reports in the literature. However, Dudley and Selby, who worked at the land-grant universities Cornell and Ohio State, respectively, chose a name from the literature for their collections. Presumably, access to current literature at their places of employment influenced their identifications.

In the meantime, one of the early hosts, B. alba (white byrony), was introduced into the United States several times in the 19th century as an ornamental and medicinal plant. Subsequently, it escaped from cultivation and became established in the Pacific Northwest (Novak and Mack, 1995). Currently, B. alba is present in Washington, Idaho, Montana, and Utah; in Washington, it is considered a noxious weed. D. bryoniae has never been found on B. alba in the United States (S.J. Novak, personal communication, 19 June 1997). The most likely reason for this is that B. alba is found in arid environments such as southeastern Washington that are not conducive for D. bryoniae. In addition, the phenology of B. alba reduces the likelihood of contact between pathogen and host. B. alba is deciduous; “the stems emerge from the tuberous root in mid to late spring, and this is after the majority of the years' precipitation has fallen” (S.J. Novak, personal communication, 19 June 1997).

A Seedborne Cucurbit Pathogen

D. bryoniae may be present both on and in cucurbit seed. Although it is impossible to know with certainty, two of the early reports of gummy stem blight in 1891 may have involved seedborne inoculum. According to Chiu and Walker (1949), the cucumber grown in France on which Roumeguère observed gummy stem blight was a Chinese variety, which would have been imported through seed. Dudley's observation of gummy stem blight on greenhouse cucumber also indicates that external or environmental sources of inoculum were not involved in that outbreak. One of the first reports to confirm contaminated seed as the source of inoculum for an outbreak of gummy stem blight came from England. Infested seed used for commercial crops of greenhouse cucumbers that developed gummy stem blight produced 6% diseased seedlings in a blotter test (Brown et al., 1970).

Certainly, the transition from direct seeding to transplanting cucurbits in modern agricultural systems has heightened the importance of D. bryoniae as a cucurbit pathogen. It consistently, albeit infrequently, appears on cucurbit seedlings in greenhouses, generally when the first true leaf appears. For example, between 1993 and 2009, gummy stem blight was found in South Carolina on greenhouse-grown watermelon and melon transplants 16 times: 11 times on seedlings grown in South Carolina and five times on seedlings grown in other states that were purchased by South Carolina growers (Keinath, 2009; Keinath, unpublished data). The typical pattern in a greenhouse flat is a dead plant that grew from a contaminated seed (primary infection) surrounded by symptomatic plants (secondary infections). In greenhouse experiments, 11% to 15% of seedlings adjacent to infected source seedlings became infected (Keinath, 1996), although higher rates of infection have been observed in commercial transplant greenhouses (Keinath, unpublished data).

van Steekelenburg (1986) demonstrated that cucumber fruit became infected after blossoms were inoculated with D. bryoniae. de Neergaard (1989a) traced the path of infection from conidia applied to the stigma through the style and funiculus to the ovules, which provided evidence of how cucurbit seed becomes infected with D. bryoniae. In a study done at The Danish Seed Health Center for Developing Countries in Copenhagen, cucurbit seeds from several countries were dissected and cultured. D. bryoniae was present primarily on or in the seedcoat and perisperm and occurred less frequently on the cotyledons (Lee et al., 1984). In addition, an internal fruit rot of cucumber was reported first in Japan in 1960 and then in Central America, Europe, and other locations (de Neergaard, 1989a; Kagiwata, 1970; Sitterly, 1968; van Steekelenburg, 1986). In Europe, affected fruit lacked any external symptoms. Growth of D. bryoniae as black mycelium also has been observed inside melon and giant pumpkin (C. maxima) fruits (Keinath, unpublished data). It is possible that this type of internal fruit infection could lead to seeds becoming infested with D. bryoniae on the outside of the seedcoat. Because fruit are externally asymptomatic, they could easily be harvested and processed to extract seed.

The use of grafted cucurbits further increases the risk of gummy stem blight development from seedborne inoculum. After grafting, plants are held at high humidity or under frequent misting to promote healing of the graft union. These environmental conditions are very favorable for development of gummy stem blight (Arny and Rowe, 1991). Recently, gummy stem blight was observed on grafted watermelon in Tunisia as cankers at the graft union that killed affected plants (Boughalleb et al., 2007). Because gummy stem blight was not observed on non-grafted plants or on leaves, it is likely that the grafted plants became infected in the greenhouse, because it is unlikely that another source of D. bryoniae inoculum was present in the arid North African climate.

Interactions between D. bryoniae and Its Cucurbit Hosts

D. bryoniae is host-specific on cucurbits (Corlett, 1981). It, like many foliar fungal pathogens, is limited to members of one host plant family. The five reports on non-cucurbit hosts in Farr and Rossman (2010) probably are misidentifications of the pathogen. Given the natural variability in severity of symptoms on inoculated plants, the host from which isolates are recovered has no consistent effect on virulence of isolates on other cucurbit species (Lee et al., 1984; Zúniga, 1999). This implies that isolates of D. bryoniae from wild hosts, e.g., Bryonia or Sicyos angulatus, would readily infect cultivated species. On the other hand, D. bryoniae is very well-adapted to cucurbits. At least 12 cucurbit genera and 23 species are hosts, i.e., can be infected and become diseased (Table 2). Nevertheless, there are consistent differences among some cucurbits. For example, summer squashes (C. pepo) are resistant to—or less susceptible to—gummy stem blight relative to other commonly cultivated cucurbits (Keinath, 2010; Sitterly, 1969).

Table 2.

Cucurbit genera reported to be infected by Didymella bryoniae.

Table 2.

D. bryoniae grows rapidly in planta. Lesion expansion has been estimated to be 0.5 cm in 12 h (Keinath, unpublished data). Epidemic progress of 6% (0.06) increase in leaf area diseased per day has been recorded on fall watermelon growing in a conducive environment without fungicide applications (Keinath, 1995). The pathogen appears to be tolerant of desiccation after infection and likely survives in planta as dormant mycelium (Chiu and Walker, 1949). It survives in dead, infected host debris for up to 2 years in semitropical climates (Keinath, 2008), which is longer than it survived in northern climates (Chiu and Walker, 1949; van Steekelenburg, 1983). Clearly, the pathogen also survives in seed (Lee et al., 1984), which provides the pathogen a selective advantage in climates where the host goes dormant and helps maintain a close host–parasite relationship (Burdon and Thrall, 2009).

D. bryoniae reproduces readily on all parts of cucurbits, including leaves, petioles, vines, stems, tendrils, pedicels, flowers, peduncles, fruits, seeds, and roots (Chester, 1891; Chiu and Walker, 1949; de Neergaard, 1989a; Keinath, 2010; Lee et al., 1984; Thinggaard, 1987). Because D. bryoniae is a necrotrophic fungus, fruiting bodies are found in the center or the oldest part of lesions. In general, pycnidia are formed earlier than pseudothecia, although the opposite also has been reported on cucumber (de Neergaard, 1989b). Mean number of fruiting bodies per square centimeter of leaf lesions ranged from 222 ± 58 to 579 ± 58 (Keinath, 2010). There were no differences in number of fruiting bodies per unit area on different cucurbit species. Thus, all cucurbit hosts could provide a substrate for production of airborne ascospores capable of disseminating the pathogen (Schenck, 1968). However, how far viable ascospores are capable of traveling has not been determined.

Current theory on coevolution of pathogens and host plants holds that resistance to a pathogen is most likely to occur when the pathogen is present in the plant's center of origin and exerts selection pressure on the host (see for example Burdon and Thrall, 2009). Whether susceptibility to D. bryoniae in cucurbits—or lack thereof—can be explained by coevolution of host and pathogen is unclear. For example, three Cucurbita spp. (C. pepo, C. maxima, and C. moschata) generally were less susceptible to foliar gummy stem blight than Citrullus lanatus or Cucumis melo with mean severities of 12%, 95%, and 94% leaf area diseased, respectively (Keinath, 2010). The overlap between prehistoric host geographic range and modern pathogen distribution is a closer match for Cucurbita spp. than for Citrullus spp. or Cucumis melo (Table 3; Fig. 1). In particular, subspecies of C. pepo, which is the least susceptible Cucurbita species, originated in humid areas in North America, which would have been conducive to gummy stem blight (Pickersgill, 2007; Robinson and Decker-Walters, 1997). Plants of Cucurbita spp. affected with gummy stem blight generally still produce an abundance of fruits, an important adaptation to colonization by a pathogen for the plant—and the domesticator.

Fig. 1.
Fig. 1.

Current worldwide distribution of Didymella bryoniae and centers of origin of Cucurbita pepo, C. maxima, C. moschata, Citrullus lanatus, and Cucumis melo. Dark gray = countries from which D. bryoniae has been reported based on Farr and Rossman (2010); Kagiwata (1970); Lee et al. (1984); Nga et al. (2010); and Punithalingam and Holliday (1972). Gray = approximate centers of origin of cucurbit hosts according to Pickersgill (2007), and Robinson and Decker-Walters (1997). See Table 3 for details of host origins. Black = centers of host origin from which D. bryoniae also has been reported.

Citation: HortScience horts 46, 4; 10.21273/HORTSCI.46.4.532

Table 3.

Comparison of geographic centers of origin for cultivated cucurbits and current distribution of Didymella bryoniae.

Table 3.

Distribution of host and pathogen also may have influenced susceptibility to gummy stem blight in Citrullus. Fourteen Citrullus colocynthis accessions from Iran (seven accessions), Afghanistan (three accessions), Egypt (two accessions), Morocco (one accession), and Cyprus (one accession) were very susceptible to D. bryoniae (Levi et al., 2001). Because C. colocynthis is a desert species, and most of the accessions were collected from countries with arid climates, it is very unlikely that colocynth has been exposed to D. bryoniae in nature (Table 3; Fig. 1). On the other hand, citron (C. lanatus var. citroides), which originated in central Africa where D. bryoniae occurs, was less susceptible than both C. colocynthis and C. lanatus var. lanatus (Levi et al., 2001). In field evaluations, one cultivar of citron also was less susceptible to gummy stem blight than two watermelon cultivars (Keinath, 2010). It is possible, however, that citron and Cucurbita spp. always were inherently less susceptible to gummy stem blight than other taxa without natural selection occurring over time.

In summary, the earliest reports of D. bryoniae were from Bryonia spp. in Europe in the second half of the 19th century. By the early 20th century, D. bryoniae had been found on most commonly cultivated cucurbits on both sides of the Atlantic Ocean. Currently, D. bryoniae is part of the global movement of plant products and pathogens, because it travels from continent to continent on and in seed. Because the fungus is well adapted to cucurbits, it is able to rapidly colonize host tissue and reproduce abundantly. Thus, it is ideally suited to continue to plague cucurbits grown in humid environments.

Literature Cited

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Contributor Notes

This material is based on work supported by NIFA/USDA under project number SC-1700294. Keynote address presented 15 Nov. 2010 at Cucurbitaceae 2010, Charleston, SC.Technical Contribution No. 5900 of the Clemson University Experiment Station.e-mail tknth@clemson.edu.
  • ArnyC.RoweR.C.1991Effects of temperature and duration of surface wetness on spore production and infection of cucumbers by Didymella bryoniaePhytopathology81206209

    • Search Google Scholar
    • Export Citation
  • AveskampM.M.de GruyterJ.WoudenbergJ.H.C.VerkleyG.J.M.CrousP.W.2010Highlights of the Didymellaceae: A polyphasic approach to characterise Phoma and related pleosporalean generaStud. Mycol.65160

    • Search Google Scholar
    • Export Citation
  • BoughallebN.El MahjoubM.Abad-CamposP.Pérez-SierraA.García-JiménezJ.ArmengolJ.2007First report of gummy stem blight caused by Didymella bryoniae on grafted watermelon in TunisiaPlant Dis.91468

    • Search Google Scholar
    • Export Citation
  • BrownM.E.HowardE.M.KnightB.C.1970Seed-borne Mycosphaerella melonis on cucumberPlant Pathol.19198

  • BurdonJ.J.ThrallP.H.2009Coevolution of plants and their pathogens in natural habitatsScience324755756

  • ChesterF.D.1891Notes on three new or noteworthy diseases of plantsBull. Torrey Bot. Club18371374

  • ChiuW.F.WalkerJ.C.1949Physiology and pathogenicity of the cucurbit black-rot fungusJ. Agr. Res.78589615

  • CorlettM.1981A taxonomic survey of some species of Didymella and Didymella-like speciesCan. J. Bot.5920162042

  • de NeergaardE.1989aHistological investigation of flower parts of cucumber infected by Didymella bryoniaeCan. J. Plant Pathol.112838

  • de NeergaardE.1989bStudies of Didymella bryoniae (Auersw.) Rehm: Development in the hostJ. Phytopathol.127107115

  • FarrD.F.RossmanA.Y.2010Fungal databases. Systematic Mycology and Microbiology Laboratory, ARS, USDA6 May 2010<http://nt.ars-grin.gov/fungaldatabases/index.cfm>.

    • Search Google Scholar
    • Export Citation
  • GrossenbacherJ.G.1909A Mycosphaerella wilt of melons. New York (Geneva) Agr. Expt. Sta. Tech. Bull9193229

  • KagiwataT.1970Brown heart rot of the cucumber by Mycosphaerella melonis (Pass.) Chieu et Walker, and its controlRev. Plant Prot. Res.39497

    • Search Google Scholar
    • Export Citation
  • KeinathA.P.1995Fungicide timing for optimum management of gummy stem blight epidemics on watermelonPlant Dis.79354358

  • KeinathA.P.1996Spread of Didymella bryoniae from contaminated watermelon seed and transplants in greenhouse and field environments6572PandalaiS.G.Recent research developments in plant pathologyVol. 1Research SignpostTrivandrum, India

    • Search Google Scholar
    • Export Citation
  • KeinathA.P.2008Survival of Didymella bryoniae in infested muskmelon crowns in South CarolinaPlant Dis.9212231228

  • KeinathA.P.2009Sensitivity to azoxystrobin in Didymella bryoniae isolates collected before and after field use of strobilurin fungicidesPest Manag. Sci.6510901096

    • Search Google Scholar
    • Export Citation
  • KeinathA.P.2010Susceptibility of cucurbit species to gummy stem blight and their suitability for reproduction by Didymella bryoniae. Cucurbitaceae 2010 Proc25

    • Search Google Scholar
    • Export Citation
  • KirkP.M.CannonP.F.MinterD.W.StalpersJ.A.2008Dictionary of the fungi10th EdCAB InternationalWallingford, UK

    • Export Citation
  • LeeD.-H.MathurS.B.NeergaardP.1984Detection and location of seed-borne inoculum of Didymella bryoniae and its transmission in seedlings of cucumber and pumpkinPhytopathol. Z.109301308

    • Search Google Scholar
    • Export Citation
  • LeviA.ThomasC.E.KeinathA.P.WehnerT.C.2001Genetic diversity among Citrullus lanatus and Citrullus colocynthis accessionsGenet. Resources Crop Evol.48559566

    • Search Google Scholar
    • Export Citation
  • NgaN.T.T.GiauN.T.LongN.T.LübeckM.ShettyN.P.de NeergaardE.ThuyT.T.T.KimP.V.JørgensenH.J.L.2010Rhizobacterially induced protection of watermelon against Didymella bryoniaeJ. Appl. Microbiol.109567582

    • Search Google Scholar
    • Export Citation
  • NovakS.J.MackR.N.1995Allozyme diversity in the apomictic vine Bryonia alba (Cucurbitaceae): Potential consequences of multiple introductionsAmer. J. Bot.8211531162

    • Search Google Scholar
    • Export Citation
  • PickersgillB.2007Domestication of plants in the Americas: Insights from Mendelian and molecular geneticsAnn. Bot. (Lond.)100925940

  • PunithalingamE.HollidayP.1972Didymella bryoniaeCMI description of pathogenic fungi and bacteria. No. 332. Commonwealth Mycol. Inst., Kew, UK

    • Search Google Scholar
    • Export Citation
  • RobertV.StegehuisG.StalpersJ.2005The MycoBank engine and related databases6 May 2010. <http://www.mycobank.org/>.

    • Export Citation
  • RobinsonR.W.Decker-WaltersD.S.1997CucurbitsCAB InternationalNew York, NY

    • Export Citation
  • SchenckN.C.1968Epidemiology of gummy stem blight (Mycosphaerella citrullina) on watermelon: Ascospore incidence and disease developmentPhytopathology5814201422

    • Search Google Scholar
    • Export Citation
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  • SitterlyW.R.1969Effect of crop rotation on cucumber gummy stem blightPlant Dis. Reptr.53417419

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