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Article

Divergent Responses of Tomato Cultivars with Resistance to Tomato Yellow Leaf Curl Virus as Infected by Meloidogyne javanica

by
Soledad Verdejo-Lucas
1,2
1
Sustainable Plant Protection Program, IRTA, Crta. de Cabrils km 2, 08348 Cabrils, Spain
2
c/Gerona 24, Pl 4 P2, 04002 Almería, Spain
Horticulturae 2023, 9(7), 777; https://doi.org/10.3390/horticulturae9070777
Submission received: 18 June 2023 / Revised: 3 July 2023 / Accepted: 5 July 2023 / Published: 7 July 2023
(This article belongs to the Special Issue Plant-Parasitic Nematodes in Horticultural Crops)
Browse Figure
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Abstract

:
Commercial tomatoes are usually complex F1 hybrids with multiple resistances genes from different wild Solanum species. The response of tomato cultivars with resistance to root-knot nematodes (RKN) and Tomato yellow leaf curl virus (TYLCV) as infected by Meloidogyne javanica was determined in a controlled environment and field conditions. Four treatments were tested, viz. tomato cultivars with (i) RKN resistance alone; (ii) combination of RKN and TYLCV resistance (RKN + TYLCV); (iii) TYLCV resistance alone; and (iv) control (susceptible to the nematode and virus). The RKN-resistant plants effectively suppressed nematode infection and reproduction both in a controlled environment and in field conditions. The RKN + TYLC-resistant plants were less effective (p < 0.001) than the RKN plants in a controlled environment, and their resistance levels were significantly reduced in the field. Nonetheless, the RKN + TYLCV plants supported lower (p < 0.001) nematode infection and reproduction than the susceptible control plants. The TYLCV-resistant plants reduced (p < 0.001) nematode infection and reproduction compared to the susceptible control in a controlled environment and in field conditions. The divergent response of tomato cultivars with resistance to TYLCV via infection by M. javanica can be attributed to the genetic background of the cultivars.

1. Introduction

Root-knot nematodes (RKN: Meloidogyne spp.) are important pathogens for vegetable production worldwide, particularly in protected cultivation because of frequently available host plants, high temperatures under the protected covers, and short fallowing periods between successive crops [1,2].
Plant resistance is an effective and easily adoptable method to control pathogens. Commercial tomato cultivars are usually complex F1 hybrids with multiple resistances genes from different wild Solanum species. The resistance to the nematode is conferred by the single dominant gene Mi-1, which was introgressed from an accession of Solanum peruvianum into S. lycopersicum and is effective against Meloidogyne incognita, Meloidogyne javanica, and Meloidogyne arenaria [3]. Mi-1 resistance is characterized by a hypersensitive reaction that causes cell death, preventing the formation of the feeding site needed for further nematode development. Seven Mi-1 gene homologues, all from the S. peruvianum introgression, are located on the short arm of chromosome 6 [4], but only the Mi-1.2 is functional and confers resistance to RKN [5].
Tomato Yellow Leaf Curl Virus (TYLCV) is a monopartite begomovirus transmitted by the whitefly Bemisia tabaci that can have a devastating effect on tomatoes. Several sources of resistance against this viral disease have been identified in wild Solanum, such as S. chilense (Ty-1, Ty-3, Ty-4, and Ty-6), S. habrochaites (Ty-2), and S. peruvianum (ty-5) [6,7]. The Ty-1 and Ty-3 genes are mapped to chromosome 6, very close to the Mi locus [8,9]. Tomato cultivars with Ty-resistance genes are indeed tolerant rather than resistant to TYLCV because the Ty-mediated resistance results in the systemic infection of the plant with mild to moderate symptoms and low levels of virus accumulation [10]. For the purpose of this study, the term “TYLCV resistance” is used because this is the way seed companies categorized the response of tomato to viral infection.
The Mi- and Ty-1 loci have been introgressed into commercial tomatoes with a double purpose: to decrease damage caused by the nematode and the virus and to reduce final nematode population densities after their cropping. Incorporation of various resistance genes into a single genotype may provide some levels of measurable resistance to another pathogen. For example, the Mi-1 gene, in addition to RKN resistance, also confers resistance to potato aphids (Macrosiphum euphorbiae) [11] and whiteflies (Bemisia tabaci) [12]. Tomatoes with resistance to powdery mildew (Oidium neolycopersici) are also resistant to RKN and aphids [13]. TYLCV-resistant tomatoes are also resistant to Tomato curly stunt virus ToCSV [14] and Tomato mottle virus (ToMoV) [9]. Interactions between the nematode-virus and the plant host may be influenced by the dominance of the genes conferring resistance. The outcome might be an enhancement or reduction of the disease. Severe TYLCV infection was related to high incidence of RKN [15].
Tomato cv. Tyrmes with intermediate resistance to TYLCV but susceptible to RKN decreased M. javanica reproduction under different experimental conditions [16]. Based on this information and previous report [15], experiments were designed to determine the response of tomato cultivars with TYLCV resistance alone and in combination with RKN resistance to nematode infection. Experiments were conducted in a controlled environment and in the field.

2. Material and Methods

The selected tomato cultivars had been described by the seed companies as having high or intermediate resistance to RKN and TYLCV or susceptibility to both pathogens (Table 1).
The experimental design was a factorial 2 × 2. The primary factors were the nematode and the virus, and the secondary factor was the presence or absence of resistance. Four treatments were tested in all experiments, viz. tomato cultivars with (i) RKN resistance alone; (ii) combination of RKN and TYLCV resistance (RKN + TYLCV); (iii) TYLCV resistance alone; and (iv) control (susceptible to the nematode and virus). The RKN-resistant cv. Caramba and the susceptible cv. Durinta were included in all experiments as the standard for resistance and susceptibility, respectively.

2.1. Experiments in a Controlled Environment

Experiments were conducted in a controlled environment to determine the response of tomato cultivars to an initial population density of the nematode. Four experiments were conducted in a growth chamber following similar experimental conditions, plant maintenance, and assessments of nematode infection and reproduction. To circumvent any possible effect due to the cultivar and to check the consistency of the results, six tomato cultivars were tested in the RKN + TYLCV treatment (Cantynflas, Mayoral, Pintyno, Razimo, Rey, and Yanira) and five cultivars in the TYLCV treatment (Birloque, Denis, Tyrmes, Martina, and Verdial) (Table 1). Cultivars were tested as they became available (Table 1) and each cultivar was replicated eight times in experiments 1, 2, and 3, and seven times, in experiment 4.
Tomato seeds were germinated in seed trays containing vermiculite no. 2, and seedlings were transplanted singly into 500-cm3 pots containing steam-sterilized river sand at the third-true leaf stage. Plants were allowed to grow in the growth chamber for one week before they were inoculated with the nematode. An avirulent population of M. javanica (code MJ-05) was used in the experiments. Nematode inoculum was obtained from infected tomato (cv. Roma) roots collected from pot cultures maintained in a glasshouse. Roots were macerated in a 0.5% NaOCl solution in a food blender at ca 1000 rpm for 5 min [17]. The egg suspension was passed through a 74 µm aperture sieve to remove root debris, and the eggs collected on a 25 µm sieve were used as inoculum. Tomato plants were inoculated with 1000 eggs per plant. Aliquots of the egg suspension were added into two holes made in the soil 3 cm apart from the base of the plant. Plants were watered daily as needed and fertilized with a slow-release fertilizer (15% N + 10% P2O5 + 12% K2O + 2% MgO2 + microelements).
Plants were maintained in a growth chamber at 23 ± 2 °C and a photoperiod of 16 h light and 8 h dark. Plants were harvested 49 days after nematode inoculation once they had accumulated 540–589 degree-days, enough to complete one generation of the nematode (base 10 °C). At harvest, shoots were cut at ground level and the root systems were washed free of soil and weighed. Egg masses were stained for ease of counting by immersion of the entire root system into a 0.1 g L−1 erioglaucine solution (Aldrich Chemical Company) [18] for two hours. Eggs were extracted from the entire root system in a 0.5% NaOCl solution for 10 min. The multiplication rate (Pf/Pi) of the nematode was calculated as eggs per plant (Pf) divided by nematode inoculum (Pi). Based on the reproduction index (RI) of the nematode, the resistance level of the cultivars was estimated as eggs/g root on experimental cultivar divided by eggs/g root on susceptible cultivar Durinta × 100 [19]. The level of resistance was categorized as high resistance (RI < 10%), intermediate resistance (10% < RI < 40%), and susceptibility (RI > 40%).

2.2. Field Experiment

The response of tomato cultivars to continuous exposure to high population densities of the nematode was determined in an unheated field plastic house infested with M. javanica. The experiment was conducted from April to July. The soil was a sandy loam with 85.8% sand, 8.1% silt, and 6.1% clay; pH 8.1; 0.9% organic matter (w/w); and 0.40 dS/m electric conductivity. The experimental design was a stratified randomized block due to the uneven distribution of the nematode in the field. Four treatments were tested as previously described: tomato cultivars with (i) RKN resistance alone; (ii) combination of RKN and TYLCV resistance (RKN + TYLCV); (iii) TYLCV resistance alone; and (iv) control (susceptible to the nematode and virus). The RKN + TYLCV treatment included three cultivars, Mayoral, Pintyno, and Razimo. The TYLCV alone included another three cultivars, Birloque, Martina, and Tyrmes (Table 1). The resistant cv. Caramba and susceptible cv. Duritnta were used as controls for reference. Each tomato cultivar was replicated 12 times (4 plants/plot × 3 plots).
Tomato seeds were germinated in seed trays containing vermiculite no. 2, and seedlings at the fourth-true leaf stage were transplanted to plots within each of three blocks. Individual plots consisted of a row of four plants of the respective tomato cultivar that were planted 50 cm apart within the row and 55 cm between rows. Plants were watered through a drip irrigation system, and they were fertilized weekly with a solution consisting of NPK (15-5-30), iron chelate, and micronutrients at rates of 31 kg/ha and 0.9 kg/ha, respectively. Tomato plants were vertically trained. Soil temperatures were recorded daily at 30 min intervals with temperature probes placed in the soil at 15 cm deep. Plants were harvested 93 days after transplanting once they had accumulated 1395 degree-days, sufficient temperature for the nematode to complete two generations.
Composite soil samples were collected before transplanting the tomatoes to determine pre-planting population densities. Individual samples consisted of five cores taken to 25 cm depth with a sampling tube (2.5 cm diameter) per plot. Soil was mixed thoroughly, and nematodes were extracted from 250 cm3 soil subsamples using Baermann trays. Second-stage juveniles were collected 72 h later, concentrated on a 25 μm-pore sieve, and counted. The average initial population densities were 2886 nematodes/250 cm3 soil. Final population densities (Pf) were estimated in rhizosphere soil collected around the roots of individual plants (96 samples). Then, plants were dug from the soil and the disease severity was assessed using a root galling index on a scale of 0 to 10, where 0 = a complete and healthy root system and 10 = plants and roots were dead [20]. Eggs were extracted from 10-g root subsamples from individual plants of each cultivar (96 samples) by blender maceration in a 0.5% NaOCl solution for 10 min [17]. Eggs are expressed per gram of root. The reproduction index (RI) of the nematode was used to estimate the level of resistance as previously described for the experiments in the controlled environment.

2.3. Statistical Analyses

Statistical analyses were performed using the IBM SPSS Statistics package v. 21. The general linear model procedure was used to analyze the data from the experiments conducted in a controlled environment and field condition. Data were expressed as mean ± standard error. Two variables were considered, nematode and virus; each variable had two levels, with or without resistance, which resulted in a factorial experimental design with four treatments. Data from the experiments in a controlled environment were pooled since there was no difference between the four replicated experiments. The dependent variables analyzed were root weight, egg masses/plant, eggs/g root, Pf (eggs/plant), and multiplication rate. For the field experiment, the variables were gall index, eggs/g root, Pf, and multiplication rate. The Bonferroni correction for multiple comparisons was applied when needed to separate means.

3. Results

3.1. Experiments in a Controlled Environment

The resistances to the nematode and virus and their interactions had significant effects on the number of egg masses per plant, eggs/g root, final population densities, and multiplication rate (Table 2). Root weight was lower (p < 0.003) in treatments with RKN resistance (7.73 ± 0.31 g) than in those with no RKN resistance (9.00 ± 0.29 g). Treatments with TYLCV resistance did not differ in root weight.
The analysis of the nematode x virus interaction indicated that egg masses/plant, final population, and the multiplication rate had the lowest (p < 0.001) values in the treatment RKN-alone followed by the RKN + TYLCV, TYLCV alone, and the susceptible control in the last place (Table 3). Eggs/g root were higher (p < 0.001) in RKN + TYLCV than in RKN alone but lower (p < 0.001) than in the susceptible control (Table 3). Treatments RKN + TYLCV and TYLCV alone had similar eggs/g root (Table 3).
Based on the M. javanica RI, 100% of the RKN plants showed high resistance (Figure 1A), 70% of the RKN + TYLCV plants showed high resistance, 23% intermediate resistance, and 7% susceptibility, and 44% of the TYLCV plants expressed high resistance, 45% intermediate resistance, and only 12% susceptibility (Figure 1A).

3.2. Field Experiment

The nematode and the nematode x virus interaction had significant effects on root galling, eggs/g root, and final population (Table 4).
The analysis of the interaction showed that root galling, eggs/g root, and final population were lower (p < 0.001) in the RKN plants than RKN + TYLCV and TYLCV plants that did not differ from each other, and they were followed by the susceptible control plants in the last place (Table 5). In relation to the RI, 92% of the RKN-resistant plants showed high resistance and 8% intermediate resistance and no susceptibility (Figure 1B). Only 8% of the RKN + TYLCV plants expressed high resistance, 33% intermediate resistance, and 58% susceptibility; and 31% of the TYLCV plants showed high resistance, 8% intermediate resistance, and 61% susceptibility (Figure 1B).

4. Discussion

The TYLCV resistance in the tomato cultivars provided opposing responses to nematode infection depending on whether the cultivars had RKN resistance or not. The efficacy of the RKN resistance was consistently reduced in cultivars with combined RKN + TYLCV resistance. The TYLCV resistance alone reduced nematode damage and population increases. All the cultivars included in the treatment provided similar levels of resistance or susceptibility to the nematode, which indicates that the response to the nematode was not cultivar dependent.
In a controlled environment, increased infection and reproduction occurred in the RKN + TYLCV in comparison to the RKN-resistant plants, which made the RKN + TYLCV plants less effective in suppressing the nematode. On the other hand, the TYLCV-resistant plants reduced nematode infection and reproduction compared to the susceptible control. In fact, 89% of the TYLCV plants suppressed nematode infection despite the lack of RKN resistance.
In field conditions, the RKN-resistant plants retained a high level of resistance even under continuous exposure to high population densities, which confirmed the high resistance level of cv. Caramba to the nematode [16]. The resistance genes to the nematode, virus, or to both made the plants more tolerant to nematode damage (root galling), and reduced population increases with respect to the susceptible control. However, the efficacy of the RKN + TYLCV plants in suppressing nematode disease and reproduction was greatly reduced under field conditions; indeed, 58% of these plants responded as susceptible. Cultivar Razymo, described as highly resistant, showed intermediate resistance in the field (RI = 38), whereas cv. Pintyno and Mayoral, described as intermediate resistant, showed susceptibility (RI = 108 and 62, respectively). Consequently, the RKN + TYLCV and TYLCV plants supported similar root galling and nematode reproduction.
The genealogy of the RKN + TYLCV tomatoes was unknown because we tested commercial cultivars but assumed that their resistance was due to background of the cultivars. Further genetic and molecular studies are needed to explain the opposing response of TYLCV-resistant plants to nematode infection in RKN-resistant and susceptible plants. The Ty-1 gene may suppress the expression of the Mi-1 gene resistance, and this hypothesis needs to be tested. The genetic base of TYLCV resistance depends on the introgressed Solanum species and ranges from a single incompletely dominant gene to a polygenic recessive pattern [21,22]. For example, the resistance derived from S. chilense accession LA1969 is conferred by a major incompletely dominant gene (Ty-1 gene) and two or more modifier genes [8]. The RKN resistance is conferred by a single dominant gene (Mi-1) derived from S. peruvianum. The F1 tomato hybrids incorporate several genes from different wild Solanum species and these species often share the same allele for a marker which can lead to false positives. In fact, begomovirus-resistant tomatoes with introgression from S. habrochaites and S. chilense that are susceptible to RKN gave false positives in screenings for RKN resistance with the PCR-based REX-1 marker [23]. The RKN + TYLCV plants may have been developed from a cross between one line carrying Mi and another one carrying Ty-1 or from a cross between a line carrying both Mi and Ty-1 and another line with S. lycopersicum [22]. Therefore, the complexities of the F1 hybrids affect the expression of nematode resistance. Thus, the commercial cultivar, Anastasia, heterozygous for Mi (Mi/mi) and Ty-1 (Ty-1/ty-1) [22], showed susceptibility (RI = 59%) to M. incognita in biological tests (unpublished data). The RKN susceptible (mi/mi) but TYLCV-resistant (Ty-1/Ty-1) tomato SC showed the allele 2 from S. peruvianum for the REX-1 marker [22]. Lines that were homozygous for Ty-1 and did not carry Mi, showed allele 1 (S. lycopersicum allele), allele 2 (S. peruvinum allele), or allele 3 (S. lycopersicum accession LA3473). The PCR-based marker PM3 [23] amplified a fragment of ca 500 bp representing PM3 in cv. Tyrmes but did not do so in the susceptible control Durinta [24], which suggests that Tyrmes may have resistance mediated by the Mi-1 or Mi homologues. Moreover, factors such as a continuous source of high inoculum and the duration of the experiment (two nematode generations in field conditions) significantly lowered the resistance levels of the RKN + TYLCV plants. High continuous population densities reduced the resistance levels of tomato hybrid rootstocks [16]. Tomatoes with intermediate resistance might not provide sufficient nematode control under field conditions but they would perform better than completely susceptible plants. Although continuous cultivation of resistant tomatoes may select virulent individuals within the nematode population able to overcome the resistance [25], the RKN plants retained a high resistance level in the field; therefore, the hypothesis of virulence selection in the RKN + TYLCV plants was rejected.
TYLCV-resistant tomatoes were susceptible to the nematode as previously reported [8,16], but this study demonstrated that they reduced nematode damage and population densities which could be exploited in nematode management programs. The TYLCV disease cannot be effectively controlled with insecticides; therefore, pest advisors encourage growers to plant TYLCV-resistant cultivars in areas where the virus is prevalent. The protective effect of TYLCV resistance against M. javanica infection may lead to reduced yield losses. Nonetheless, where RKN and TYLCV occur simultaneously, effective control of both pathogens is necessary to obtain significant increases in yield [26]. It would be interesting to investigate if nematode-resistant plants affect the tolerance of the TYLCV plants to the viral disease.

5. Conclusions

The combination of RKN resistance and TYLCV resistance in a single genotype reduced the efficacy of the Mi-1 gene in suppressing nematode reproduction. On the contrary, tomatoes with only TYLCV resistance reduced nematode infection and reproduction; therefore, they could be useful in nematode management programs.

Funding

This research received no external funding.

Data Availability Statement

Data will be made available on request.

Acknowledgments

The seeds of the cultivars were kindly provided by the seed companies. Thanks are given to A. Catena for statistical assistance, M. Talavera for reviewing the manuscript, and to M. Blanco, V. Barnes, and O. Jurado for technical assistance in the laboratory and field.

Conflicts of Interest

The author declares no conflict of interest.

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Horticulturae 09 00777 g001 550
Figure 1. Percentage of plants with resistance to root-knot nematode (RKN) and Tomato yellow leaf curl virus (TYLCV) alone and in combination that showed high resistance, intermediate resistance, and susceptibility to Meloidogyne javanica according to the nematode reproduction index (eggs/g root on experimental cultivar divided by eggs/g root on susceptible cultivar Durinta ×100) in (A) a controlled environment, and (B) field conditions.
Figure 1. Percentage of plants with resistance to root-knot nematode (RKN) and Tomato yellow leaf curl virus (TYLCV) alone and in combination that showed high resistance, intermediate resistance, and susceptibility to Meloidogyne javanica according to the nematode reproduction index (eggs/g root on experimental cultivar divided by eggs/g root on susceptible cultivar Durinta ×100) in (A) a controlled environment, and (B) field conditions.
Horticulturae 09 00777 g001
Table
Table 1. Resistances to root-knot nematodes and Tomato yellow leaf curl virus (TYLCV) of tomato cultivars according to the descriptions of the seed companies and experiments where they were tested.
Table 1. Resistances to root-knot nematodes and Tomato yellow leaf curl virus (TYLCV) of tomato cultivars according to the descriptions of the seed companies and experiments where they were tested.
Treatment
(Resistance)		CultivarResistancesExperiments 1
NematodeCaramba, De Ruiter Seeds(HR): Ma, Mi, Mj1, 2, 3, 4, Field
Nematode + VirusYanira, Western Seed(HR): TYLCV/Mi3, 4
Rey, Western SeedTYLCV, Nematodes2, 3, 4
Cantynflas, DiamondTYLCV, Nematodes2, 3, 4
Razymo, Rijk Zwaan(HR): Mi/TYLCV1, Field
Pintyno, Gautier(IR): Ma, Mi, Mj/TYLCV2, Field
Mayoral, De Ruiter Seeds(IR): Ma, Mi, Mj/TYLCV2, Field
VirusTyrmes, Syngenta Seeds(IR): TYLCV1, 3, 4, Field
Martina, Western SeedTYLCV2, 3, 4, Field
Birloque, De Ruiter SeedsTYLCV2, 3, 4, Field
Denis, De Ruiter SeedsTYLCV2
Verdial, Semillas FitóTYLCV 1
Control 2Elvirado, GautierSusceptible1
Durinta, Western SeedSusceptible1, 2, 3, 4, Field
HR: High resistance; IR: Intermediate resistance; Ma, Mi, Mj: Meloidogyne arenaria, Meloidogyne incognita, Meloidogyne javanica. 1 Experiments 1, 2, 3, and 4 were conducted in a controlled environment in a growth chamber. 2 Susceptible to the nematode and the virus.
Table
Table 2. Statistical significance and probability of primary factors, resistance to root-knot nematodes (RKN) and Tomato yellow leaf curl virus (TYLCV), and their interaction, on the infection (egg masses/plant), reproduction (eggs/g root), final population densities (eggs/plant), and multiplication rate (final population/initial population) of Meloidogyne javanica on tomato in controlled conditions in a growth chamber.
Table 2. Statistical significance and probability of primary factors, resistance to root-knot nematodes (RKN) and Tomato yellow leaf curl virus (TYLCV), and their interaction, on the infection (egg masses/plant), reproduction (eggs/g root), final population densities (eggs/plant), and multiplication rate (final population/initial population) of Meloidogyne javanica on tomato in controlled conditions in a growth chamber.
Egg Masses/PlantEggs/g RootFinal PopulationMultiplication Rate
ResistanceF ValueProbabilityF ValueProbabilityF ValueProbabilityF ValueProbability
Nematode (N)62.870.00114.710.00128.970.00177.660.001
Virus (V)26.800.00110.350.00114.650.00145.690.001
N × V38.240.00116.840.00121.040.00158.780.001
Table
Table 3. Infection (egg masses/plant), reproduction (eggs/g root), final population densities (eggs/plant), multiplication rate (final population/initial population) and reproduction index (RI; eggs/g root on experimental cultivar divided by eggs/g root on susceptible cultivar Durinta ×100) of Meloidogyne javanica on tomato cultivars with resistance to root-knot nematodes (RKN) and Tomato yellow leaf curl virus (TYLCV) alone and in combination, inoculated with 1000 eggs per plant in a controlled environment in a growth chamber 49 days after nematode inoculation.
Table 3. Infection (egg masses/plant), reproduction (eggs/g root), final population densities (eggs/plant), multiplication rate (final population/initial population) and reproduction index (RI; eggs/g root on experimental cultivar divided by eggs/g root on susceptible cultivar Durinta ×100) of Meloidogyne javanica on tomato cultivars with resistance to root-knot nematodes (RKN) and Tomato yellow leaf curl virus (TYLCV) alone and in combination, inoculated with 1000 eggs per plant in a controlled environment in a growth chamber 49 days after nematode inoculation.
Resistance Egg Masses FinalMultiplication Plants
RKNTYLCVTreatment/PlantEggs/g RootPopulationRateRI (%)Tested
YesNoRKN1.6 ± 4.3 a42 ± 58 a306 ± 420 a0.17 ± 0.19 a1.8 ± 2.4 a37
YesYesRKN + TYLCV8 ± 14 b496 ± 1750 b2308 ± 6344 b1. 60 ± 2.01 b10.9 ± 16 b87
NoYesTYLCV19 ± 22 c359 ± 713 b4408 ± 8329 c2.18 ± 2.48 c19.0 ± 21 b85
NoNoControl 192 ± 106 d4102 ± 86 c26,603 ± 4384 d16.35 ± 16.62 d 43
Values are mean ± standard error of four experiments, eight replicated plants per cultivar; cultivars tested in each experiment are indicated in Table 1. Values in the same column with different letters indicate statistical differences between treatments according to Bonferroni test (p < 0.001). 1 Susceptible to the nematode and virus.
Table
Table 4. Statistical significance and probability of the primary factors, resistance to root-knot nematodes (RKN) and Tomato yellow leaf curl virus (TYLCV), and their interaction, on root galling (scale 0 to 10), nematode reproduction (eggs/g root), and final population densities (juveniles/250 cm3 soil) of Meloidogyne javanica on tomato in a field plastic house infested with the nematode.
Table 4. Statistical significance and probability of the primary factors, resistance to root-knot nematodes (RKN) and Tomato yellow leaf curl virus (TYLCV), and their interaction, on root galling (scale 0 to 10), nematode reproduction (eggs/g root), and final population densities (juveniles/250 cm3 soil) of Meloidogyne javanica on tomato in a field plastic house infested with the nematode.
Root GallingEggs/g RootFinal Population
F ValuesProbabilityF ValuesProbabilityF ValuesProbability
Nematode (N)50.670.0018.630.0057.120.009
Virus (V)0.780.381.550.220.0070.93
N × V50.670.00113.430.0019.850.002
Table
Table 5. Root galling (scale 0 to 10), nematode reproduction (eggs/g root), final population densities (juveniles/250 cm3 soil), and reproduction index (RI; eggs/g root on experimental cultivar divided by eggs/g root on susceptible cultivar Durinta ×100) of Meloidogyne javanica on tomato cultivars with resistance to root-knot nematodes (RKN) and Tomato yellow leaf curl virus (TYLCV) alone and in combination in a field plastic house infested with the nematode 93 days after transplanting.
Table 5. Root galling (scale 0 to 10), nematode reproduction (eggs/g root), final population densities (juveniles/250 cm3 soil), and reproduction index (RI; eggs/g root on experimental cultivar divided by eggs/g root on susceptible cultivar Durinta ×100) of Meloidogyne javanica on tomato cultivars with resistance to root-knot nematodes (RKN) and Tomato yellow leaf curl virus (TYLCV) alone and in combination in a field plastic house infested with the nematode 93 days after transplanting.
Resistance Plants
RKNTYLCVTreatmentRoot GallingEggs/g RootFinal PopulationRI (%)Tested
YesNoRKN0.67 ± 0.26 a452 ± 216 a1194 ± 881 a3.23 ± 5.3 a12
YesYesRKN + TYLCV4.69 ± 0.32 b10,523 ± 1693 b11,481 ± 19,415 b75 ± 72 b36
NoYesTYLCV4.69 ± 0.46 b9031 ± 1428 b9902 ± 10,454 b61 ± 61 b36
NoNoControl 17.83 ± 0.30 c14,000 ± 2434 c20,756 ± 12,681 c 12
Values are mean ± standard error of 12 plants per cultivar (one cultivar for the resistant and susceptible controls and three cultivars for the RKN + TYLCV and TYLCV-resistant plants). Values in the same column with different letters indicate statistical differences between treatments according to Bonferroni test (p < 0.001). 1 Susceptible to the nematode and virus.
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Verdejo-Lucas, S. Divergent Responses of Tomato Cultivars with Resistance to Tomato Yellow Leaf Curl Virus as Infected by Meloidogyne javanica. Horticulturae 2023, 9, 777. https://doi.org/10.3390/horticulturae9070777

AMA Style

Verdejo-Lucas S. Divergent Responses of Tomato Cultivars with Resistance to Tomato Yellow Leaf Curl Virus as Infected by Meloidogyne javanica. Horticulturae. 2023; 9(7):777. https://doi.org/10.3390/horticulturae9070777

Chicago/Turabian Style

Verdejo-Lucas, Soledad. 2023. "Divergent Responses of Tomato Cultivars with Resistance to Tomato Yellow Leaf Curl Virus as Infected by Meloidogyne javanica" Horticulturae 9, no. 7: 777. https://doi.org/10.3390/horticulturae9070777

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