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45Russian Journal of Nematology, 2012, 20 (1), 45 - 51
Identification of a novel source of resistance to the root-knot nematode Meloidogyne incognita in
Cucumis
12 3
De-You Ye , Chun-Tao Qian and Chester Kurowski
institute of Vegetables, Gansu Academy of Agricultural Sciences, Lanzhou, 730070, China;
e-mail: ydy_287.my265@yahoo.com.cn 2State Key Laboratory of Crop Genetics and Germplasm Enhancement, Key Laboratory of Southern Vegetable Genetic Improvement, Nanjing Agricultural University, Nanjing, 210095, China 3Harris Moran Seed, 9241 Mace Bld, Davis CA, USA
Accepted for publication 28 December 2011
Summary. Cucumis species germplasm was evaluated for resistance to the root-knot nematode, Melodogyne incognita. The disease index (DI) score for Cucumis hystrix was smaller than for the susceptiple control C. sativus cv. Beijingjietou. Additionally, numerous large galls were found on cv. Beijingjietou, while only a few small galls were found on C. hystrix. Cucumis hystrix infected with M. incognita also had more lateral roots compared to the susceptible control. Furthermore, interspecific progenies derived from the cross between C. hystrix and cv. Beijingjietou had a high level of resistance to M. incognita. Thus, C. hystrix could serve as a valuable M. incognita-resistant source for cucumber improvement. Key words: Cucurbitaceae, gall size, germplasm, interspecific progenies.
Cucumber (Cucumis sativus L., 2n = 2x = 14) is an important vegetable crop that is highly susceptible to the root-knot nematode (Meloidogyne spp.), which causes significant yield losses to cucumber throughout the world (Walters et al., 1993). There are four Meloidogyne species that primarily cause the root-knot disease on a worldwide basis: Meloidogyne incognita, M. arenaria, M. javanica and M. hapla (Fassuliotis, 1982). The southern root-knot nematode, M. incognita, is a major limiting factor in commercial production of cucumber worldwide (Walters & Wehner, 1996). Significant progress has been made in selecting and breeding for resistance to M. arenaria, M. javanica and M. hapla, but no such progress has been made for resistance to M. incognita in cucumber (Walters & Wehner, 1997). Historically, several investigations have indicated that little or no resistance exists in current cultivars and breeding lines of cucumber (Bharali & Phukan, 1996). By contrast, resistance has been discovered in some related Cucumis species, e.g., C. metuliferus, C. anguria, C. ficifolius and C. longipes (Walters et al, 1993). Successful exchange of genes between C. sativus and related wild species is difficult using conventional hybridisation techniques, since the chromosome number of C. sativus is different (n = 7) from most other species
of Cucumis (n = 12) (Dane, 1991). Several attempts have been made to introduce economically important characteristics from wild into cultivated Cucumis species with little success (Chen & Adelberg, 2000). So far, these resistances have not been utilised for cucumber improvement due to the cross incompatibility that exists between the species (Walters & Wehner, 2002).
Cucumis hystrix Chakr. (2n = 2x = 24), is a wild Cucumis species originating in Asia (Kirkbride, 1993; Chen et al, 1995). A successful cross has been made and confirmed between C. hystrix and C. sativus and interspecific Fi hybrids have been obtained between these two species (Chen et al, 1997). This interspecific hybridisation is the first repeatable cross between a cultivated Cucumis species and a wild relative. The fact that there is cross-compatibility between C. hystrix and C. sativus opens a new avenue for cucumber improvement through interspecific hybridisation. The economically important characters of C. hystrix are of great interest to cucumber researchers worldwide.
Genetic resistance is the preferred control strategy in nematode management because it has no harmful effects on human health and the environment (Roberts & May, 1986). Resistant cultivars would suppress or reduce the threat of M. incognita in cucumber production. The objectives of this study are: i) to identify C. hystrix as a potential source of root-knot
nematode resistance; and ii) to evaluate whether or not the resistance from C. hystrix can be transferred to its interspecific progeny with C. sativus.
MATERIALS AND METHODS
Two glasshouse experiments were conducted. The objective of experiment 1 was to identify susceptibility of C. sativus and resistance of C. hystrix to M. incognita. The eight Cucumis genotypes used in this experiment were from the collection of J. F. Chen (Chen et al., 1994). The germplasm evaluated comprised six cucumber cultivars: the Northern Chinese cucumber cv. Beijingjietou, which is well-known for being highly susceptible to M. incognita (Walters & Wehner, 1997); the Southern Chinese cucumber cv. Erzaozi; four C. sativus var. xishuangbannesis cultivars (SWCC8, SWCC9, SWCC10 and SWCC12); plus two wild species of Cucumis (African horned cucumber (2n = 2x = 24), a C. metuliferus line well-known for its high resistance to M. incognita but cross-incompatibility with C. sativus (Deakin et al., 1971) and C. hystrix). This initial experiment was followed by another to evaluate the transmission of resistance from C. hystrix to its interspecific progeny with C. sativus cv. Beijingjietou. Interspecific hybridisation between C. hystrix and C. sativus, and subsequent embryo rescue were performed as described by Chen et al. (1997). The resulting sterile Fi progeny (2n = 19, with genome HC, where H is the genome of C. hystrix, and C is for C. sativus) went through chromosome doubling as previously described by Chen et al. (1998) and dF1 (C. hytivus, 4n = 38, HHCC) was obtained. The BCF1 (3n = 26, HCC/CCH) was obtained by crossing dF1 with the original diploid cucumber parent cv. Beijingjietou.
The original nematode population used for inoculations came from a severely infested plot at Nanjing, Jiangsu province, China. A pure population was established using a single egg mass. Accurate identification of this nematode species was based on female perineal patterns (Hartman & Sasser, 1985), malate dehydrogenase (Mdh) and esterase (Est) phenotypes (Esbenshade & Triantaphyllou, 1985a). The identified species was multiplied on tomato, Solanum lycopersicon Mill. cv. Rutgers, grown in a glasshouse at 20-28°C. Nematode inoculum was prepared in accordance with the technique described by Hussey & Barker (1973). Nematode inoculum concentration was determined from a 1 ml aliquot containing 2000 eggs or second-stage juveniles (J2).
The experiment was conducted in a glasshouse located at Nanjing Agricultural University, Nanjing, China. Seeds were pre-germinated on moist filter
paper in a Petri dish at 28°C. Germinated seeds were sown in 32-cell seeding tray containing sterilised substrate. Seedlings at the two-leaf-stage were transplanted into 30 cm diam. pots (1 seedling/pot) filled with a 2:1 mixture of disinfected sand and soil. Plantlets from in vitro culture were also transplanted into that medium at the same time. Once the seedlings reached the three to four leaf stages, the inoculum was applied at the base of each seedling using a micropipette. The treatments were replicated three times with five plants or plantlets of each genotype per replication and arranged in a completely randomised design. Plants were maintained in the glasshouse at 26±4°C and were fertilised weekly with a commercial nutrient formulation (N:P:K = 20:20:20) and watered daily. The procedures and cultural practices were identical for each experiment conducted in this study.
At 8 weeks after inoculation, plants were removed from the pots, roots were gently washed free of soil before traits evaluation: number of galls and egg masses per root system, average gall size, gall index (GI), egg mass index (EI) and disease index (DI). The number of galls for each root system was counted under a stereoscopic microscope at 10* magnification, after which egg mass counts were made after immersion into Phloxine B solution (0.15 g l-1) for 3 to5 min (Daykin & Hussey, 1985). Average gall size was assessed on a scale of 1 to 3 with 1 = less than 1 mm, 2 = 1-3 mm and 3 = more than 3 mm, based on average gall diameter. Root galling and egg mass production were each assessed on a 0 to 5 scale with 0 = none, 1 = 1-2, 2 = 3-10, 3 = 11-30, 4 = 31-100, and 5 = more than 100 galls (or egg masses) (Hartman & Sasser, 1985). The gall index (GI) and egg mass index (EI) was then counted for each genotype using the formula: GI (EI) = [(no. plants in scale 1*1) + (no. plants in scale 2*2) ... (no. plants in scale 5*5) *100] / [total no. plants examined*5] (Powell et al, 1971). A disease index (DI) was generated to combine both resistance parameters (GI and EI) into a single value di=\/g i=+e i (Kouame et al, 1997). Based on DI values, host reactions were classified as immune (IM), DI = 0.0-1.0; highly resistant (HR), DI = 1.0-2.0; resistant (R), DI = 2.03.0; moderately resistant (MR), DI = 3.0-4.0; moderately susceptible (MS), DI = 4.0-5.0; susceptible (S), DI = 5.0-6.0; and highly susceptible (HS), DI>6.
Data were subjected to analysis of variance using SAS (SAS Inst., Cary, N.C.), and germplasm means were compared using Fisher's least significant difference (LSD) at P = 0.05.
Table 1. Resistance evaluation of Cucumis species, interspecific progeny from cross between C.hystrix and C.sativus to Meloidogyne incognita in greenhouse.
Genotypes or Gall index Egg mass index Disease index Host reaction
Generations (GI) (EI) (DI) (HR)
African horned 1.50ae 0.38a 1.55a HR
C.hystrix 1.38a 0.50a 1.47a HR
Beijingjietou 4.88b 3.88c 6.23d HS
Erzaozi 4.75b 3.75c 6.05d HS
SWCC8 5.00b 2.00b 5.39bc S
SWCC9 4.60b 1.40b 4.81b MS
SWCC10 4.40b 1.60b 4.68b MS
SWCC12 4.80b 1.80b 5.13bc S
Fi(2n) 1.60a 0.80a 1.78a HR
BCFi(3n) 1.80a 0.60a 1.89a HR
dF1(4n) 1.60a 0.60a 1.71a HR
e Significant difference at 0.05. The same letter within the column of GI, EI and DI are not significantly different at 0.05 probability level using Fisher's least significant difference (LSD).
1
S F * ï Vi ^ i p^j JnJ " ' y. . \t • t ♦ f
o C" • f f
m • *
Mtih
Est
Fig. 1. A. Perineal pattern of the female of the Meloidogyne population tested; B. Perineal pattern of the female of Meloidogyne incognita; C. Malate dehydrogenase (Mdh) and esterase (Est) phenotypes of M.javanica (lane 1), M.incognita (lane 2), M. arenaria (lane 3) and Meloidogyne population tested (lane 4).
Fig. 2. Morphological aspects of Cucumis species roots infected by M. incognita. Aspect of the numerous and large sized-galls in the infected roots of the susceptible cv. Beijingjietou (gall diam.>3 mm) (left) and few and small sized-galls in the highly resistant cv. African horned (gall diam.<3 mm) (middle) and in C. hystrix (gall diam.<1mm)(right).
RESULTS
The perineal pattern of the Meloidogyne population tested match previously published descriptions of M. incognita (Jepson, 1987). The dorsal arch is high and squared, the lateral field is indistinct, and the dorsal and ventral striae are not interrupted at this point (Fig. 1A). All of these features for the perineal pattern of the female are similar to M. incognita (Fig. 1B). Enzymatic electrophoresis (malate dehydrogenase (Mdh) and esterase (Est)) was also conducted for the population. Based on the established relationship of Mdh-Est profiles and species of Meloidogyne (Esbenshade & Triantaphyllou, 1985b), the Meloidogyne population used was typical of M. incognita (Mdh-Est phenotype N1-I2) distinct from M. javanica or M. arenaria (Fig. 1C). Both the perineal pattern and enzymatic phenotypes revealed that the Meloidogyne population used in this study was M. incognita.
The evaluated germplasms were broken out into seven classes based on their DI scores (Table 1). None of the genotypes evaluated were considered immune (DI<1) to M. incognita. However, different class reactions were found among the plant species. All C. sativus germplasm genotypes evaluated were moderate to highly susceptible (DI>4) to M. incognita with DI values varying from 4.68 to 6.23. The DI score of cv. Beijingjietou was 6.23, whereas it was only 1.55 for C. metuliferus line Africa horned cucumber. The resistant and susceptible controls behaved as expected. We also discovered C. hystrix exhibited a high level of resistance similar to C. metuliferus line Africa horned cucumber. Furthermore, C. hystrix had smaller DI scores than the susceptible control (P<0.05), and the DI score of C. hystrix was also smaller than the resistant C. metuliferus line Africa horned cucumber (P>0.05).
Subsequently, we focused on three species of Cucumis germplasm: C. sativus cv. Beijingjietou, C. metuliferus line Africa horned cucumber and C. hystrix for further evaluation. For these three species, we found a large difference in the type of galls produced. Three types of galls were observed in susceptible cv. Beijingjietou, while only two gall types were observed in the resistant C. metuliferus line Africa horned cucumber and only one gall type was seen in C. hystrix (Fig. 2). For the susceptible species, 58.1% of the galls were classified in the medium sized-gall category (diameter between 1 and 3 mm); as opposed to 28.6% for C. metuliferus line Africa horned cucumber which displays high resistance. More importantly 29.1% of the galls in cv. Beijingjietou were large with a diameter > 3 mm, whereas this gall type was never observed in C.
metuliferus line Africa horned cucumber and C. hystrix. For C. metuliferus line Africa horned cucumber and C. hystrix, small galls with a diameter < 1 mm were most numerous. In the C. metuliferus line Africa horned cucumber, 71.4% of the galls were classified in this category while all the galls were less than 1 mm in C. hystrix (Fig. 3). The number of lateral roots observed in situ revealed that there were large quantitative differences among these three species. The susceptible C. sativus cv. Beijingjietou only had a few lateral roots while the resistant C. metuliferus line Africa horned cucumber and C. hystrix produced many (Fig. 2). Although the number of lateral roots found on C. metuliferus line Africa horned cucumber and C. hystrix did not differ, both were significantly higher than the susceptible cv. Beijingjietou. There were large differences in the number of egg masses and females among these three species. On C. sativus cv. Beijingjietou, 24 egg masses per root were found, compared to 2 to 3 for C. metuliferus line Africa horned cucumber and C. hystrix. Moreover, egg mass size for the susceptible cv. Beijingjietou was slightly larger than for either C.metuliferus line Africa horned cucumber or C. hystrix. All large galls (diameter > 3mm) each contained 1 to 2 females for the susceptible cv. Beijingjietou, while females were never observed in C. metuliferus line Africa horned cucumber or C. hystrix.
All three interspecific progenies between C. hystrix and C. sativus tested proved to be highly resistant to M. incognita based on their DI scores (Table 1). The DI scores for F1, BCF1 and dF1 were 1.78, 1.89 and 1.71 respectively, and no significant differences were observed among them as well as for the C. hystrix parent (DI = 1.47), although differences were detected among the progenies and the parent C. sativus cv. Beijingjietou (DI = 6.23). In addition, a large difference existed in the number of roots among these three distinct ploidy interspecific progenies. With the exception of the triploid BCF1, which had many roots, the diploid F1 and tetraploid dF1 only had a few roots, which is similar to the C. hystrix parent.
DISCUSSION
Results from this study indicate that no resistance to M. incognita was found in C. sativus, which is in accordance with the earlier results (Walters et al, 1993). However, resistance does exist in C. hystrix. The highly resistant phenotype in C. hystrix was characterised by much smaller sized galls and reduced quantity of galls than in the susceptible C. sativus cv. Beijingjietou. In another experiment, we have confirmed C. hystrix is
80 S 70
S 60
£ 50 1 40
O
■ Beijingjietou M Africa horned
M Cucumis hystrix
I
30 20 10 0
<1 1—3 >3
Gall diameter (mm)
Fig. 3. Distribution of Meloidogyne incognita root galls according to their diameter in three Cucumis species. The same letter on the top of the column is not significantly different at 0.05 probability level using Fisher's least significant difference (LSD).
also resistant to M. arenaria, M. javanica and M. hapla (data unpublished). The findings of this study indicate that C. hystrix may provide a useful source of M. incognita resistance for cucumber breeding programmes. The incorporation of this resistance into cultivated cucumber to control root-knot nematodes would be beneficial to growers, and genetic resistance would contribute to reduced nematicide use. The inheritance of the resistance in C. hystrix, however, remains to be determined. Further investigations are therefore required to gain a clearer understanding of the underlying mechanisms of resistance involved in C. hystrix at both cellular and molecular levels.
Results also revealed that interspecific progenies derived from the cross between C. hystrix and C. sativus have a high level of resistance to M. incognita and the level of resistance was similar to that found in C. hystrix, possibly indicating a common genetic basis for resistance. Pederson & Windham (1989) showed that root-knot nematode resistances may be correlated with chromosome numbers and ploidy level in Trifolium species. In
our study, although chromosome numbers and ploidy level varied among these three interspecific progenies, additional cytogenetics studies are needed to understand whether such a relationship exists. However, large differences for the number in root were observed among the interspecific progenies. This difference in root number may partially explain the different reactions observed due to nematode infection as more roots provided a greater area for root infection (Anzueto et al., 2001). The resistance for interspecific F1 hybrids was introgressed from C. hystrix. This resistance was further transferred to the BCF1 progeny when the dF1 was backcrossed to C. sativus cv. Beijingjietou. The high levels of resistance in the F1 and BCF1 progenies from the crosses possibly indicated that the resistance was inherited in a dominant fashion, and thus C. hystrix can be used in the cucumber improvement.
Meloidogyne-resistance in tomato was introgressed from Solanum peruvianum to S. lycopersicum and is present in all resistant commercial tomato cultivars (Verdejo-Lucas et al,
b
a
2008). Cucumis hystrix showed strong growth and displayed stable resistance to M. incognita under infection in three consecutive years, so it could be used as the source for developing M. incognita-resistant cucumber varieties. However, numerous backcrosses to cucumber and evaluations for M. incognita resistance would be necessary to provide cucumber lines with acceptable horticultural characters and nematode resistance. Currently, we have obtained numerous populations of introgression lines between these two species (Chen et al, 2004). The high frequency of resistant interspecific progenies suggests the possibility of developing near-isogenic lines with resistance to M. incognita. It should also be possible to detect DNA markers linked with resistance to M. incognita and one approach, namely bulk segregate analysis (BSA) (Halden et al, 1997), is currently being pursued.
ACKNOWLEDGEMENT
This research was partially supported by the Key Program (30830079) from the National Natural Science Foundation of China; Cash support from VCO; the '863' Programs (2008AA10Z150); the National Supporting Programs (2006BAD13B06, 2006BAD01A7-5-11, 2008BADB105) from the Ministry of Science and Technology of China.
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De-You Ye1, Chun-Tao Qian, C. Kurowski. Выявление нового источника генетической устойчивости к Meloidogyne incognita у Cucumis.
Резюме. Проведен поиск генов устойчивости к галлообразующим нематодам Melodogyne incognita в геноме огурцов. Индекс заболевания DI для Cucumis hystrix был существенно ниже, чем для восприимчивого контрольного сорта C. sativus cv. Beijingjietou. К тому же, на огурцах cv. Beijingjietou были обнаружены многочисленные крупные галлы, тогда как на C. hystrix обнаружено лишь небольшое количество мелких галлов. Пораженные M. incognita огурцы Cucumis hystrix имели больше боковых корней по сравнению с восприимчивым контролем. Межвидовые гибриды, полученные скрещиванием C. hystrix и cv. Beijingjietou, показали высокий уровень устойчивости к M. incognita. Таким образом, C. hystrix может служить источником ценной устойчивости к M. incognita при селекции огурцов.
