Insect Resistance in Cucurbits: 1992­98

Susan E. Webb

University of Florida, Central Florida Research and Education Center,
5336 University Avenue, Leesburg, FL 34748

Additional index words. melon, squash, aphids, whiteflies, Aphis gossypii, Bemisia argentifolii, cucumber beetle, squash bug, Anasa tristis

Abstract. Development of cucurbits with resistance to one or more insect pests is essential if we are to reduce our dependence on insecticides for growing these crops. Although very little insect-resistant germplasm has been released, sources of resistance to all major pests have been identified. During the past seven years, research has been reported on the mechanisms of resistance to melon aphid (Aphis gossypii Glover) in muskmelon (Cucumis melo L.) and the associated resistance to transmission of viruses by this aphid; on finding sources of resistance to sweetpotato or silverleaf whitefly (Bemisia sp.), a new and serious pest; and on identifying sources of resistance to cucumber beetles. Recently, resistance to cucumber beetles and bacterial wilt, induced in susceptible plants by the use of plant growth-promoting rhizobacteria, has been reported. In general, however, research on plant resistance to insect pests of cucurbits appears to have declined over the past 10 years. New support and additional research teams are needed to build upon the resources already available, determine how best to use different types of resistance in combination with biological and cultural control methods, identify mechanisms and genes involved in resistance, and make use of advances in biotechnology and genetic engineering in order to overcome barriers to traditional methods of plant breeding.

Host plant resistance to insects has been a valuable tool for managing insect pests in grain crops, alfalfa, and cotton (Stoner, 1996), but has not been nearly as often used in vegetable crops. In a survey of insect-resistant germplasm released in the United States from 1973­87, Smith (1989) found that 61% of 464 releases were in grain crops, but only 13% were in vegetables. Among these, he lists one cultivar and eight parent lines of muskmelon resistant to cucumber beetles. Added to this list should be the three aphid-resistant muskmelon breeding lines released by McCreight et al. (1984). Stoner (1996) found that, of 117 releases between 1988 to early 1994, only 11% were in vegetables and none of these were cucurbits.

Many reasons have been given for the lack of emphasis on host plant resistance as a means of managing insect pests of vegetables in general, including the availability of effective chemical controls, the low tolerance for damage to the plant part to be harvested (Schalk and Ratcliffe, 1976), and the limited market for seed of resistant plants compared with crops such as grains which are grown on a much larger scale (Oelhaf, 1978).

Cucurbits, like many other vegetables, are attacked by a variety of insects [summarized by Robinson (1992) and Dhillon and Wehner (1991)], and the complex of pests will vary depending on geographic location, so varieties resistant to only one or a few insects may have limited usefulness.

Certainly, screening for resistance to insects and identifying mechanisms of resistance to insects can be difficult. Screening methods, both for field and laboratory, including methods of evaluating damage and sampling methods for estimating insect populations, must be developed for each crop. Smith (1989) lists many of the factors that must be considered. Often, natural populations of insects may be too low or unpredictable for field screening, and rearing and release methods must be developed. Because insects may have preferences for one variety or genotype over another, the relative resistance of a variety may change, depending on what is planted near it. This complexity may account for the disparity in the number of reports dealing with disease resistance versus insect resistance. For example, from 1992­98, 41 preliminary reports published in the Cucurbit Genetics Cooperative Reports dealt with dis

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ease resistance, but only eight dealt with insect resistance. Finally, Dhillon and Wehner (1991) suggested that breeding for insect resistance has had low priority because of the limited number of plant breeders working on cucurbits and the many other production problems for which no simple solution, such as insecticides, exists.

Current research

Despite the few examples of releases of insect-resistant cucurbit germplasm in the United States, many sources for resistance to a variety of insect pests of cucurbits have been reported. This literature has been thoroughly reviewed by Robinson (1992), and to a lesser degree, by Stoner (1992), and Dhillon and Wehner (1991), and will not be covered again here. Instead, I will focus on research published after 1991. A number of these papers focus on determining the mechanism and effects of resistance discovered earlier (Chen et al., 1996, 1997a, 1997b; Kishaba et al., 1992a; Shinoda, 1993), several are straightforward reports of screening for resistance (Collins et al., 1994; Hoffman et al., 1996; Simmons and McCreight, 1996), one combines screening and examining a possible mechanism for resistance (Kishaba et al., 1992b), and two involve induced resistance (Zehnder et al., 1997a, 1997b). At least one paper discusses the effects of combining biological control and host plant resistance (Olson et al., 1996). Some of these papers are discussed in more detail below.

Mechanism of aphid resistance and resistance to virus transmission in melon. Building on earlier work by Lecoq et al. (1979, 1980) and Pitrat and Lecoq (1980, 1982), Chen et al. (1997a) studied the mechanism of resistance to virus transmission by Aphis gossypii Glover in melon (Cucumis melo L.), a trait due to a monogenic dominant gene named Vat (Lecoq et al., 1979). The availability of near isogenic lines allowed identification of factors associated specifically with this resistance. Electrical penetration graphs (EPGs) allowed detailed monitoring of stylet penetration behavior. The presence of the Vat gene reduced the duration of intracellular punctures of both Myzus persicae (Sulzer) and A. gossypii, and somewhat reduced the frequency of intracellular punctures (A. gossypii. only). Thus, the authors concluded that behav

ioral traits alone could not account for reduced transmission. Long potential drops associated with successful inoculation of susceptible plants by A. gossypii may account for its more efficient transmission of CMV. The authors suggest that since the Vat gene has no effect on the acquisition of virus (Lecoq et al., 1979), its effect on inoculation must be chemical, perhaps causing interference with release of virus particles from the stylets. It is not clear why this effect should be vector species-specific but not virus-specific.

Chen et al. (1997b) examined the mechanism of resistance to A. gossypii through the use of the near-isogenic lines 'Vedrantais' (susceptible) and 'Margot' (resistant) which were also used in the studies of resistance to virus transmission. Electrical penetration graphs, used to examine behavior of the aphids on resistant and susceptible lines, suggested the presence of a repellent factor in the phloem. Phloem extracts, fed to aphids in sucrose solutions through Parafilm membranes, confirmed the results of EPGs: phloem sap from resistant plants deterred feeding more than sap from susceptible plants. Nitrogenous compounds in phloem sap were analyzed and differences were found in the levels of five of them. Overall, the total protein content of phloem sap was lower in the resistant line as was the rate of exudation. The authors suggest that the phloem-sealing physiology, linked to sulfhydral oxidation processes, of plants carrying the Vat gene is modified, making it difficult for aphids to feed.

Kishaba et al. (1971) described another source of resistance in muskmelon to melon aphid. Subsequent research on mechanisms and evaluation of this resistance for reducing spread of nonpersistently transmitted viruses is reviewed by Kishaba et al. (1992a). Despite the increased movement of aphids on resistant plants found earlier (Kennedy and Kishaba, 1977), they found greatly reduced spread of virus when target plants were all resistant. Virus spread among susceptible plants was high and intermediate when a mixture of susceptible and resistant plants was used (Kishaba et al., 1992a). Many more aphids were needed to transmit virus to resistant plants than were needed to transmit virus to susceptible plants. This resistance can be highly useful for reducing

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virus spread when A. gossypii is the primary vector species, but it may not have much effect when other vectors are more important (Gray et al., 1986).

Field and greenhouse screening to identify insect-resistant germplasm. Even though an understanding of mechanisms is critically important, simple screening can be very useful, both as a first step in identifying sources of resistance, and as a way to identify useful differences in susceptibility among commercially available cultivars. Collins et al. (1994) stated that the germplasm released by McCreight et al. (1984) has had only limited commercial success. They screened currently important muskmelon cultivars and found two with greatly reduced numbers of aphids, Hymark and Sweet Surprise. No information on the genetic background of these varieties was provided, however.

Another screening study identified Cucurbita pepo genotypes that were resistant to, or less preferred by, cucumber beetles, a complex that can include the striped cucumber beetle, Acalymma vittatum (F.); the spotted cucumber beetle, Diabrotica undecimpunctata howardi Barber; western corn rootworm, D. virgifera virgifera LeConte, and northern corn rootworm, D. barberi Smith and Lawrence. Cucurbitacins, which are toxic to many insects, act as a feeding stimulant for cucumber beetles (Chambliss and Jones, 1966; Metcalf, 1986). Genotypes with lower cucurbitacin levels are less preferred by cucumber beetles, but may be more susceptible to other insects (Robinson, 1992). In addition to identifying germplasm that may be used to develop resistant cultivars, Hoffman et al. (1996) also identified some genotypes that were consistently highly preferred by beetles. They suggest that these genotypes could be used as trap crops.

Riley (1995) screened muskmelon cultivars in the field for resistance to silverleaf whitefly, Bemisia argentifolii Bellows & Perring and found evidence for nonpreference (low egg to adult ratio), antibiosis (low pupa to egg ratio), and plant tolerance mechanisms of resistance. Differences among cultivars were most noticeable when whitefly populations were low, however, and tended to disappear when populations were high.

 

Developing a rapid and reproducible method of screening melon germplasm in the greenhouse was the goal of another screening study, this one also aimed at identifying genetic variation for resistance to silverleaf whitefly (Simmons and McCreight, 1996). They concluded that greenhouse tests were useful for evaluating germplasm and possibly for selection of segregating populations. Correlation with field results was not attempted in this study.

In an earlier study, in which screening for resistance and identifying a possible resistance mechanism were reported, Kishaba et al. (1992b) evaluated wild Cucurbita species, selected Lagenaria accessions, and muskmelon accessions for resistance to whitefly. They found that a number of accessions of white-flowered gourd, L. siceraria (Molina) Standley, were resistant. Scanning electron micrographs of the abaxial leaf surface suggested that trichome configuration, rather than simple differences in trichome density, accounted for differences in resistance.

Induced resistance. Wei et al. (1995) found that cucumber plants treated with plant growth-promoting rhizobacteria (PGPR) to induce systemic resistance to disease attracted fewer beetles than untreated plants and suffered less bacterial wilt which is vectored by the beetles. In further work to evaluate effects on beetle populations, Zehnder et al. (1997b) found that cucumber beetle populations were significantly lower on plants treated with PGPR than on plants treated with weekly applications of esfenvalerate insecticide when beetle populations were at their peak. In no-choice tests, beetles carrying the bacterial wilt pathogen, Erwinia tracheiphila, were allowed to feed on cucumber plants. The incidence of bacterial wilt was much lower on PGPR-treated plants, indicating that plants were resistant to infection as well as being less attractive to beetles.

In further work, Zehnder et al. (1997a) conducted choice tests in the greenhouse and analyzed cotyledons from PGPR-treated and untreated plants for cucurbitacin content. They found that feeding damage in choice tests was up to 10-fold lower on PGPR-treated plants. PGPR treatment significantly reduced the concentration of cucurbitacin in cotyledons and this may be the reason why beetles fed less on treated plants.

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Integration of biological control and host plant resistance. Olson et al. (1996) evaluated biological control of squash bug with an egg parasitoid (a scelionid wasp) alone and in combination with host plant resistance. These treatments and control with an insecticide were compared for both a moderately resistant ('Green Striped Cushaw', Cucurbita argyrosperma) and a susceptible ('Jack-O-Lantern', C. pepo) variety. The combination of biological control and resistance was more effective than either measure alone, but the yield from plants in the combination treatment was still much lower than that from plants treated with insecticides.

Future directions

A rough count of papers cited in Robinson (1992) and Stoner (1992) reveals a dramatic decrease over time in the number of papers published in the area of insect and mite resistance to cucurbits. I counted 74 papers published in the 1970s, 55 in the 1980s, and only 18, so far, in the 1990s. My list of papers since 1992, however, was compiled by searching BIOSIS and AGRICOLA and the annual indexes of HortScience and the Journal of the American Society for Horticultural Science, so it is not complete. The preliminary research reports published by the Cucurbit Genetics Cooperative show the same trend. From 1978­82, 15 reports dealing with insect resistance were published. In the past five years (1994­98), only four reports dealt with insect resistance. I suspect that decreases in funding may be responsible, in part. It is difficult to obtain funding for work that may take 12 years or more to yield results (Stoner, 1992), especially if the approach is traditional.

Additional research on host plant resistance to insects is needed, however, to develop sustainable agricultural systems that are less dependent upon insecticides. In Florida, for example, cucurbit growers need ways of controlling pickleworm that will not injure increasingly scarce and expensive bees used for pollination. Different levels and combinations of tolerance, antibiosis, antixenosis may be needed, depending on the cropping system (Kennedy et al., 1987). As stated earlier, varieties that are highly preferred by insects may be useful as trap crops for less preferred cucurbits,

thus enhancing the relative resistance of the less preferred variety. More studies are needed to evaluate the combination of biological and cultural controls and host plant resistance. Absolute immunity to insect damage may not be necessary or desirable; the selection pressure placed on the pest may result in the rapid development of biotypes able to overcome the resistance.

Advances in genetic engineering have resulted in the incorporation of nonhost genes for resistance, such as the genes coding for Bacillus thuringiensis d-endotoxins, into a number of plant species (Stoner, 1996), although not into cucurbits (Robinson, 1992). Other proteins or peptides with insecticidal activity are being sought to control insects not effected by B. thuringiensis proteins (Corbin et al., 1998). Although this method is very appealing in that it appears to be environmentally safe and effective, questions about the risk of insect populations developing resistance to B. thuringiensis toxins have been raised (Stoner, 1996).

As mentioned earlier, sources of resistance to all important insect pests of cucurbits have been described, but not many of these have been utilized (Robinson, 1992). Robinson (1992) points out that much more could be done with these existing sources, although, in some cases, fertile crosses cannot be achieved. Advances in biotechnology may solve some of these problems, but to fully take advantage of gene transfer technologies, the genes responsible for resistance have to be identified. As progress is made in developing molecular markers and in mapping the genomes of cucurbits (Staub, 1995), this may become possible.

Thus, host plant resistance in cucurbits should thus be pursued on several fronts. There is still much to be done by traditional methods. Biotechnological methods should be brought to bear on more difficult problems. The cooperation of entomologists, plant breeders, ecologists, and biochemists will be necessary to identify needs and the best ways of incorporating resistance into sustainable systems. Understanding the mechanisms of resistance may lead to further breakthroughs. The need to fund these efforts for the long term must be recognized. The long-term benefits of host plant resistance will repay the investment many times over.

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Metcalf, R.L. 1986. Coevolutionary adaptations of rootworm beetles (Coleoptera: Chrysomelidae) to cucurbitacins. J. Chem. Ecol. 12:1109­1124.

Oelhaf, R.C. 1978. Organic agriculture: Economic and ecological comparisons with conventional methods. Halstead, New York.

Olson, D.L., J.R. Nechols, and B.W. Schurle. 1996. Comparative evaluation of population effect and economic potential of biological suppression tactics versus chemical control for squash bug (Heteroptera: Coreidae) management on pumpkin. J. Econ. Entomol. 89:631­639.

Pitrat, M. and H. Lecoq. 1980. Inheritance of resistance to cucumber mosaic virus transmission by Aphis gossypii in Cucumis melo. Phytopathology 70:958­961.

Pitrat, M. and H. Lecoq. 1982. Relations génétiques entre les résistances par non-acceptation et par antibiose du melon à Aphis gossypii. Recherche de liaisons avec d'autres gènes. Agronomie 2:503­508.

Riley, D.G. 1995. Host plant resistance in melon cultivars to Bemisia, p. 23­30. In: G.E. Lester and J.R. Dunlap (eds.). Cucurbitaceae '94: Evaluation and enhancement of cucurbit germplasm. Gateway Printing, Edinburg, Texas.

Robinson, R.W. 1992. Genetic resistance in the Cucurbitaceae to insects and spider mites. Plant Breeding Rev. 10:309­360.

Schalk, J.M. and R.H. Ratcliffe. 1976. Evaluation of ARS program on alternative methods of insect control: Host plant resistance to insects. Bul. Entomol. Soc. Amer. 22:7­10.

Shinoda, T. 1993. Callose reaction induced in melon leaves by feeding of melon aphid, Aphis gossypii Glover as possible aphid-resistant factor. Jpn. J. Appl. Entomol. Zool. 37:145­152.

Simmons, A.M. and J.D. McCreight. 1996. Evaluation of melon for resistance to Bemisia argentifolii (Homoptera: Aleyrodidae). J. Econ. Entomol. 89:1663­1668.

Smith, C. M. 1989. Plant resistance to insects: A fundamental approach. Wiley, New York.

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

Stoner, K.A. 1992. Bibliography of plant resistance to arthropods in vegetables, 1977­1991. Phytoparasitica 20:125­180.

Stoner, K.A. 1996. Plant resistance to insects: A resource available for sustainable agriculture. Biol. Agr. Hort. 13:7­38.

Wei, G., C. Yao, G.W. Zehnder, S. Tuzun, and J.W. Kloepper. 1995. Induced systemic resistance by select plant growth-promoting rhizobacteria against bacterial wilt of cucumber and the beetle vectors. Phytopathology 85:1154 (abstr.).

Zehnder, G., J. Kloepper, S. Tuzun, C. Yao, G. Wei, O. Chambliss, and R. Shelby. 1997a. Insect feeding on cucumber mediated by rhizobacteria-induced plant resistance. Entomol. Expt. Appl. 83:81­85.

Zehnder, G., J. Kloepper, C. Yao, and G. Wei. 1997b. Induction of systemic resistance in cucumber against cucumber beetles (Coleoptera: Chrysomelidae) by plant growth-promoting rhizobacteria. J. Econ. Entomol. 90:391­396.

Literature cited

Chambliss, O.L. and C.M. Jones. 1966. Chemical and genetic basis for insect resistance in cucurbits. Proc. Amer. Soc. Hort. Sci. 89:394­405.

Chen, J.-Q., B. Delobel, Y. Rahbé, and N. Sauvion. 1996. Biological and chemical characterisation of a genetic resistance of melon to the melon aphid. Entomol. Expt. Appl. 80:250­253.

Chen, J.-Q., B. Martin, Y. Rahbé, and A. Fereres. 1997a. Early intracellular punctures by two aphid species on near-isogenic melon lines with and without the virus aphid transmission (Vat) resistance gene. Eur. J. Plant. Pathol. 103:521­536.

Chen, J.-Q., Y. Rahbé, B. Delobel, N. Sauvion, J. Guillaud, and G. Febvay. 1997b. Melon resistance to the aphid Aphis gossypii: Behavioural analysis and chemical correlations with nitrogenous compounds. Entomol. Expt. Appl. 85:33­44.

Collins, J.K. ,P. Perkins-Veazie, N. Maness, and B. Cartwright. 1994. Resistance in muskmelon cultivars to melon aphid. HortScience 29:1367.

Dhillon, N.P.S. and T.C. Wehner. 1991. Host-plant resistance to insects in cucurbitsGermplasm resources, genetics, and breeding. Trop. Pest Mgt. 37:421­428.

Gray, S.M., J.W. Moyer, G.G. Kennedy, and C.L. Campbell. 1986. Virus suppression and aphid resistance effects on spatial and temporal spread of watermelon mosaic virus 2. Phytopathology 76:1254­1259.

Hoffman, M.P., R.W. Robinson, M.M. Kyle, and J.J. Kirkwyland. 1996. Defoliation and infestation of Cucurbita pepo genotypes by diabroticite beetles. HortScience 31:439­442.

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Kennedy, G.G. and A.N. Kishaba. 1977. Response of alate melon aphids to resistant and susceptible muskmelon lines. J. Econ. Entomol. 70:407­410.

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Kishaba, A.N., S.J. Castle, D.L. Coudriet, J.D. McCreight, and G.W. Bohn. 1992a. Virus transmission by Aphis gossypii Glover to aphid-resistant and susceptible muskmelons. J. Amer. Soc. Hort. Sci. 117: 248­254.

Kishaba, A.N., S. Castle, J.D. McCreight, P.R. Desjardins. 1992b. Resistance of white-flowered gourd to sweetpotato whitefly. HortScience 27:1217­1221.

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Lecoq, H., G. Labonne, and M. Pitrat. 1980. Specificity of resistance to virus transmission by aphids to Cucumis melo. Ann. Phytopathol. 12:139­144.

McCreight, J.D., A.N. Kishaba, and G.W. Bohn. 1984. AR Hale's Best Jumbo, AR 5, and AR Topmark: Melon aphid-resistant muskmelon breeding lines. HortScience 19:309­310.

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