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Article

Performance of Aubergine Rootstocks against Verticillium dahliae Isolates in Southeastern Spain

by
Carmen María Lacasa
1,
Manuel Cantó-Tejero
2,*,
Victoriano Martínez
1,
Alfredo Lacasa
3 and
Pedro Guirao
2
1
Crop Protection Department, Instituto Murciano de Investigación y Desarrollo Agrario y Medioambiental (IMIDA), C/Mayor s/n, La Alberca, 30150 Murcia, Spain
2
Plant Production and Microbiology Department, E.P.S. Orihuela, University Miguel Hernández (UMH), Carretera de Beniel Km. 3.2, 03312 Orihuela, Alicante, Spain
3
Independent Researcher, 30007 Murcia, Spain
*
Author to whom correspondence should be addressed.
Agronomy 2024, 14(5), 998; https://doi.org/10.3390/agronomy14050998
Submission received: 2 April 2024 / Revised: 22 April 2024 / Accepted: 4 May 2024 / Published: 9 May 2024
(This article belongs to the Topic Agronomy, Soil Health and Climate Change: Challenges and Solutions)
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Abstract

:
Aubergine (Solanum melongena L.) (Solanaceae) is a widespread crop in the Mediterranean basin. Verticillium dahliae is one of the main soil-borne pathogens affecting the aubergine crop. Its control has traditionally been achieved by soil fumigation with chemical disinfectants. Restrictions on the use of chemical fumigants have led to the search for solutions in genetic resistance using rootstocks. In southeastern Spain, aubergines are grafted for the control of V. dahliae. Two Solanum torvum rootstocks (Hugo F1 and Torpedo) and a Solanum melongena hybrid (Javah F1) were tested against five isolates of V. dahliae obtained from grafted (A1 and A2) and ungrafted (Vd8, Vd17 and Vd66) aubergines compared with the susceptible cultivar Larne F1 under controlled conditions. Isolates from grafted plants infected all three rootstocks, with differences observed in the percentage of plants with symptoms and in the disease symptom severity. Three strains isolated from the ungrafted aubergines (Vd8, Vd17 and Vd66) infected Javah F1 rootstock. The Hugo F1 and Torpedo rootstocks showed a high level of resistance to V. dahliae, while Javah F1 was susceptible to the pathogen. The Hugo F1 and Torpedo rootstocks are suitable for mitigating the effects of Verticillium wilt in Mediterranean aubergine crops. Understanding the nature of the resistance from S. torvum could enhance the benefits of grafting or facilitate the introduction of resistance into commercial cultivars.

1. Introduction

Aubergine (Solanum melongena L.) (Solanaceae) is a widespread crop originating in Asia. It is grown outdoors, in tropical and subtropical areas, and in greenhouses all over the world. The main producers are China and India, with a production of 38.2 and 12.7 M t, respectively. Spain is the tenth largest producer of aubergines in the world (276.320 t) and the second largest in Europe after Italy (307.430 t) [1].
Verticillium dahliae and Fusarium oxysporum f. sp. melongenae are the main soil pathogens affecting the aubergine crop in Spain [2,3,4,5]. Verticillium dahliae infects and damages spontaneous, woody and herbaceous crops [6,7,8]. It has a broad pathogenic capacity and a degree of parasitic specialization [8,9]. The symptoms are leaf yellowing, apical wilting, defoliation, reduced growth, the browning of the vascular system and partial or total desiccation of the plant [8,10,11,12]. In the absence of the cultivated host plant, this fungus can persist in the soil in form of microsclerotia for a long time (6 to 14 years) [11,13]. Mild climatic conditions favour the development of the disease and the appearance of symptoms [10,14]. The pathogenic variability of aubergine isolates is high, with different levels of aggressiveness depending on the cultivar [11] and with asymptomatic infectious isolates [4]. In Spain, symptoms of V. dahliae appear on aubergine crops in spring and autumn when temperatures are mild for approximately 3 to 4 weeks. Climate change favours these conditions, so that damage caused by V. dahliae is increasing in aubergine crops in southeastern Spain (Andalucía, Valencia, Murcia and the Islas Baleares), where 94% of Spanish aubergines are produced. In Almería (Andalucía), the importance of Verticillium wilt in aubergines is greater due to the prolongation of the fungal activity period and the increase in the severity of symptoms [4,5].
In crops without sources of resistance, V. dahliae control has traditionally been achieved by reducing the inoculum in the soil prior to planting. Soil fumigation with chemical disinfectants (methyl bromide, chloropicrin or methyl isothiocyanate generators) has been used in horticultural and high-value crops, including aubergine [15].
Restrictions on the use of chemical fumigants have led to the search for solutions in genetic resistance, using rootstocks resistant to the main soil pathogens such as V. dahliae. Some authors have reported high levels of resistance to V. dahliae, F. oxysporum f. sp. melongena and Meloidogyne spp. in Solanum torvum, S. sisymbrifolium and S. incatum and in hybrids of S. lycopersicum with S. hirsutum or with S. habrochaites (Solanaceae) used as tomato rootstocks. However, some S. torvum rootstocks present problems in nursery management, low and irregular germination due to seed dormancy [16] and incompatibility with the aubergine cultivars used. Selections of these species or interspecific hybrids have been evaluated as eggplant rootstocks with different results, sometimes inconsistent, against different pathogens (including V. dahliae) [15,17,18,19,20,21,22,23,24,25].
Solanum torvum seems to be the rootstock that best protects aubergine against soil pathogens, especially Meloidogyne spp. and V. dahliae [17,25,26]. Plants with symptoms of V. dahliae infection were observed in aubergine plants grafted on S. torvum in Mallorca (Spain).
The aim of this work was to evaluate the performance of several commercial rootstocks of aubergine against V. dahliae isolates obtained from grafted and ungrafted aubergine plants.

2. Materials and Methods

2.1. Isolates and Host Plants

Five isolates of V. dahliae were used (Table 1). Two isolates, A1 and A2, were obtained from aubergine plants grafted on the Javah F1 rootstock showing advanced symptoms of Verticillium wilt (reduced growth, leaf yellowing and defoliation). For isolations, stem segments of 2 mm in thickness were cut with a sterilized scalpel from affected plants, and their surface was disinfected by immersion in a solution of sodium hypochlorite at 1% for one minute, followed by two rinses in sterile distilled water (SDW). The washed pieces were dried on sterile filter paper and plated on potato dextrose agar (PDA) medium supplemented with 100 ppm streptomycin sulphate (Sigma Aldrich Company, St. Louis, MO, USA). The plates were incubated at 22 ± 1 °C in the dark for five days. Verticillium spp. were observed to grow out of the vascular bundles. Selected colonies were subcultured on PDA without antibiotics [27]. Vd8, Vd17 and Vd66 isolates were obtained from the mycotheca of the Plant Protection Department of Instituto Murciano de Investigación y Desarrollo Agrario y Medioambiental (IMIDA) and were isolated from aubergine plants grown in greenhouses in Murcia (Spain) showing symptoms of Verticillium wilt. The isolates were identified as V. dahliae on PDA without antibiotics by the absence of yellow or orange pigmentation on the back of the colony, the production of unicellular conidia and microsclerotia [28].

2.2. Production of Inoculum

The inoculum was obtained by blending 18-day-old cultures on PDA with sterile dis-tilled water. The concentration of conidia was determined by a hemacytometer (Neubauer chamber Marienfeld) and adjusted with SDW to 1 × 105 conidia mL−1.

2.3. Susceptibility Assay

Three commercial rootstocks for aubergine with different degrees of resistance to V. dahliae, Hugo F1 (moderate/intermediate resistance), Javah F1 (moderate/intermediate resistance) and Torpedo (high resistance), and one susceptible cultivar (Larne F1) were used in the assay as a control (Table 2). The rootstocks were selected for their favourable nursery behaviour (high germination rates and uniform development), as well as their compatibility with the cultivars commonly grown in the Mediterranean region. The Larne F1 cultivar (aubergine), which is typically cultivated in Spain, was selected as a reference due to its sensitivity to V. dahliae.
The seeds were disinfected with a 1.5% sodium hypochlorite solution for 4 min and then washed several times in SDW before sowing. Seedlings were grown in autoclaved peat (120 °C for one hour) in trays with 150 cells of 25 cm3 each. They were maintained in a growth chamber at 24 ± 1 °C, under a 14:10 (L:D) photoperiod and 60 ± 10% relative humidity.
The plants were transplanted into pots (0.2 L) when they had the first two true leaves. They were grown in an autoclaved peat (Klasmann TS3; Klasmann-Deilmann GmbH, Saterland, Germany) and perlite (Projar, S.A. Co., Valencia, Spain) mixture (2:1) under identical climatic conditions to those described above.
Plants were inoculated seven days after transplanting (3–4 true leaves). Each plant was inoculated with 10 mL of conidial suspension (1 × 105 conidia mL−1), resulting in 1 × 106 conidia per plant [5,11]. A hole (1 cm deep) was made on each side of the plant, and the inoculum was introduced into it. An uninoculated control (10 mL of SDW) was used for each cultivar. For each cultivar and isolate, 15 plants were evaluated. Groups of five plants were replicated three times for each cultivar and isolate. The assay was completed after seven weeks. Two weeks were allowed between each replicate to condition the culture chamber and prepare for the next replicate.
The evaluation was conducted seven weeks after inoculation and involved the measurement of the following parameters.
(1)
Verticillium wilt incidence
At the end of the assay, each plant was tested for the presence or absence of fungal infection by using the methodology by Tello et al. [29]. Four stem samples (1 mm thick sections) were taken from each plant. These were disinfected by immersion in a 1% sodium hypoclorite solution for one minute, rinsed in SDW, dried on sterile filter paper and plated on PDA culture medium. The samples were incubated for a period of five days at a temperature of 22 ± 1 °C, after which they were examined under a microscope for the presence of morphological features and cultural characteristics of V. dahliae. These included the presence of verticillate conidiophores, hyaline conidia and microsclerotia.
The incidence of Verticillium wilt was calculated as the ratio of infected plants to the total number of plants.
(2)
Disease symptom severity
The Verticillium wilt severity of each plant was evaluated according to the following scale: 0 = no symptoms; 1 = chlorosis of the lower leaves; 2 = chlorosis of 30–50% of the leaves; 3 = chlorosis of more than 50% of the leaves; 4 = generalised chlorosis and leaf necrosis and/or wilting of the plant; 5 = death of the plant (Figure 1).

2.4. Statistical Analysis

Statistical analysis of affected plants and disease symptoms was performed by using R, version 4.2.2 [30], and RStudio, version 2022.12.0 [31].
The uninoculated (control) plants showed no symptoms and were excluded from statistical analysis.
(1)
Verticillium wilt incidence
To know the importance of the factors of the affected plants, i.e., Solanum rootstock and V. dahliae isolate, and their interactions, a generalized linear mixed model with binomial distribution and logit link function was fitted, with replication as a random factor. Calculations were performed using the glmer functions of the lme4 software package, version 1.1-34 [32]. The significance of the factors was tested with likelihood ratio tests comparing hierarchically nested models, using the anova function of the stat package [30].
For significant factors, pairwise comparisons of the proportions of affected plants were made by using Fisher’s exact test, with the fisher.multcomp function of the RVAideMemoire package [33].
(2)
Disease symptom severity
Means and medians of the symptoms of the Solanum rootstock and V. dahliae isolate combinations were calculated. Percentile confidence intervals for the medians were calculated by using bootstrap, with the groupwiseMedian function of the rcompanion software package [34].
Symptoms were also analysed by using rank-based non-parametric methods for the analysis of ordinal data in factorial designs [35]. From the midranks of the observations, the non-parametric relative effect of treatment was estimated, and its confidence intervals and the significance of the factors Solanum rootstock and V. dahliae isolate and their interaction were tested with the ANOVA-type statistic by using the rankFD function of the rankFD software package [36,37].
When the main factors Solanum rootstock and V. dahliae isolate and their interactions were significant, pairwise comparisons were made by using the mctp·function of the nparcomp software package [38], with its default settings (Tukey-type contrast, global pseudo-rank estimation method, Fisher asymptotic approximation method and 95% CIs), and a p < 0.05 was adopted as a threshold of statistical significance.

3. Results

3.1. Verticillium Wilt Incidence

There was a highly significant effect of the factors rootstock (LRT(3) = 115.2, p < 0.001) and isolate (LRT(4) = 118.3, p < 0.001). The interaction showed a trend towards significance (LRT(12) = 20.708, p < 0.055) (Table 3).
Multiple comparisons were made with Fisher’s exact test for the different levels of the factors Solanum rootstock and V. dahliae isolate. Since the interaction was close to significance, comparisons were also made for each rootstock–isolate combination (Table 4).
Only plants on the Javah F1 rootstock and Larne F1 cultivar were infected when inoculated with the five isolates. The Javah F1 rootstock exhibited a higher mean proportion of affected plants (0.640) than the Larne F1 cultivar (0.387). However, it only became more susceptible when inoculated with the Vd8 isolate with 100% of plants affected compared with 33.3% of the susceptible cultivar (Table 4).
The mean values of the affected plants show that the S. torvum rootstocks (Hugo F1 and Torpedo) were equally resistant to each other (9.3%) and significantly more resistant than the Larne F1 cultivar and the interspecific rootstock Javah F1, which was the most susceptible (64%).
Differences in the aggressiveness of the isolates were evident when inoculating the Javah F1 rootstock and the Larne F1 cultivar, but not when inoculating the Hugo F1 and Torpedo rootstocks.
Isolates from grafted plants (A1 and A2) were more aggressive (50% and 58.3% of plants affected) than isolates from ungrafted plants, except for isolate Vd8, which was similar in aggressiveness (33.3%) to isolate A1.

3.2. Disease Symptom Severity

The percentage of plants with symptoms was closely related to the percentage of plants from which the pathogen was isolated.
For each combination of plant material and Verticillium isolates, the mean severity index and median are shown in Figure 2.
All cultivars exhibited symptoms on the leaves, except for the Hugo F1 rootstock inoculated with the Vd66 isolate. No plant showed symptoms on 50% or more of its leaves (value 3 on the symptom scale). Yellowing symptoms were observed on the lower leaves of the S. torvum Hugo F1 and Torpedo rootstocks inoculated with isolates Vd66 and Vd8. However, V. dahliae was not isolated from these rootstocks.
The ANOVA-type statistic obtained from the non-parametric analysis of the relative effects shows a significant effect of the factors rootstock and isolate and their interaction on the symptoms (Table 5).
Considering each simple factor independently, significant differences can be observed among all cultivars. The interspecific hybrid rootstock Javah F1 exhibited the highest mean symptom severity (1.827), followed by the Larne F1 cultivar (1.360), the Torpedo rootstock (0.653) and the Hugo F1 rootstock (0.160).
Sixteen days after inoculation, yellowing and wilting symptoms were observed on the basal leaves of the Javah F1 rootstock, with greater prevalence and severity being observed in plants inoculated with isolates A1 and A2. Seven days later, symptoms increased in severity in plants inoculated with isolates A1 and A2, while those inoculated with isolate Vd 8 exhibited only mild symptoms. At this time, plants inoculated with isolates Vd 17 and Vd 66 showed no symptoms.
Grafted plant isolates A1 and A2 induced more severe symptoms (1.45 and 1.433, respectively) compared with ungrafted plant isolates Vd66 and Vd17 (0.55 and 0.6, respectively), although not as severe as Vd8 (0.967).
The interaction effect is shown in Figure 3, where the relative effects for each isolate and cultivar are plotted. All isolates induced similar relative symptom rates in the Solanum rootstocks Hugo F1 and Torpedo. This is not applicable to the susceptible cultivar Larne F1. Isolates from grafted plants resulted in higher symptom levels compared with two isolates from ungrafted aubergines (Vd17 and Vd66). For the interspecific hybrid rootstock Javah F1, only one of the grafted isolates (A1) differed from ungrafted isolates Vd66 and Vd17.

4. Discussion

Five isolates of V. dahliae were inoculated to test the performance of three commercial aubergine rootstocks against a cultivar of aubergine.
Inoculation experiments were conducted to assess the effectiveness of various aubergine rootstocks in controlling Verticillium wilt. The assay results indicate that S. torvum cultivars, Hugo F1 and Torpedo, were effective rootstocks. Only a small percentage of plants (9.3%) were affected by the pathogen and exhibited mild symptoms of chlorosis on the lower leaves at the end of the assay. These rootstocks exhibited resistance when inoculated with isolates from the IMIDA fungus collection and showed low susceptibility when inoculated with isolates from grafted plants. This behaviour is consistent with that obtained by other authors. Zhou et al. [20] reported that S. torvum had a disease rate of 15% and a disease index of 12.5% at the end of the trial. They also found that the first symptoms appeared 5 days later than in susceptible or moderately resistant cultivars, indicating resistance. Cürük et al. [23] reported a 51% reduction in the symptom index (0.983 vs. 2.0) and a 43% reduction in the disease index (1.9 vs. 3.333) in plants grafted on S. torvum compared with ungrafted plants grown on substrates inoculated with 1 × 106 conidia mL−1. Garibaldi et al. [25] found that the onset of symptoms was delayed by five days in S. torvum plants compared with the susceptible variety Black Bell when inoculated with 1 × 107 CFU mL−1 isolates from the rootstock and the variety. At the end of the trial, which was 72 days after inoculation, symptoms were observed in 20–27% of S. torvum plants and 87–100% of Black Bell plants.
The results of the trial indicated that the Javah F1 rootstock was more susceptible than the Larne F1 cultivar. Miles et al. [19] found that the aubergine cultivar Millionaire, when grafted onto the Javah F1, Red Scorpio and Meet rootstocks (S. melongena hybrids), was infected at the same level as the ungrafted cultivar (97–100% of plants).
Isolates obtained from plants grafted onto Javah F1 (A1 and A2) affected more plants of the Larne F1 cultivar and the Javah F1rootstock than those obtained from ungrafted aubergines. They produced more symptoms in sensitive materials than in resistant ones. Xu et al. [11] discovered variations in the pathogenicity and aggressiveness of a group of V. dahliae isolates from aubergine crops. Of the isolates, 25% were classified as strongly virulent (with a disease severity index (DSI) above 45.1 and defoliation), 45% as moderately virulent (with a DSI between 25.1 and 45 and no defoliation) and 30% as weakly virulent (with a DSI below 25 and no defoliation). As in the work by Gómez et al. [5], none of the isolates caused defoliation or plant death. However, 3 of the 12 isolates studied by Xu et al. [11] were defoliants.
The precise origin of S. torvum resistance against V. dahliae remains unclear. Wang et al. [39] proposed that a complex multigene process is involved in the resistance of S. torvum against V. dahliae. This could explain the difference in the behaviour of Hugo F1 and Torpedo, which exhibited a similar percentage of affected plants but displayed differences in the severity of symptoms.
Partial infection of resistant rootstocks and differences in susceptibility between interspecific hybrids and commercial cultivars could be influenced by inoculum density or temperature, as pointed out by Miles et al. [19] when evaluating S. melongena hybrid rootstocks and tomato rootstocks.
The inoculum density used in the experiments (1 × 106 conidia per plant) is similar to that used by other authors: 1 × 107 CFU mL−1 [25]; 0.9 to 2.3 × 106 conidia mL−1 [4]; 1 × 106 conidia mL−1 [11,15,20,23].
However, under natural conditions, performance against the pathogen is more dependent on variations in soil temperature than under controlled conditions. In growing seasons with temperatures unfavourable to the pathogen, rootstock performance is better, disease incidence is generally lower, and grafting provides better quality yield [19,24]. In addition, Zhou et al. [40] observed that the use of S. torvum as a rootstock improved soil health by producing higher levels of oxidoreductases and increased populations of microorganisms (actinomycetes and bacteria) in the rhizosphere of plants.
Grafting is an expensive practice with difficult nursery management, mainly due to heterogeneous seed germination of some S. torvum rootstocks [18]. Seeds of S. torvum germinate slowly, and it may take about 30 days to reach germination, with percentages varying between 15% and 50% [17]. To remedy these shortcomings, some authors consider the breeding of interspecific hybrids of Solanum species [17,21].

5. Conclusions

The selection of lines with better nursery performance must be performed without losing the level of resistance to pathogens. Further research is needed to better understand the interactions between Verticillium dahliae and Solanum torvum, the pathogenic variability of isolates of this fungus and the nature of S. torvum resistance to improve grafting performance or to introduce general or specific resistance into plant material. The S. torvum rootstocks tested could be suitable for mitigating the effects of Verticillium wilt in Mediterranean aubergine crops. Although the results are promising under controlled conditions, fields validation is necessary.

Author Contributions

Conceptualization, C.M.L. and A.L.; methodology, C.M.L. and A.L.; software, P.G.; validation, M.C.-T. and C.M.L. formal analysis, P.G.; investigation, C.M.L. and V.M.; data curation, C.M.L. and M.C.-T.; writing—original draft preparation, C.M.L., A.L., M.C.-T. and P.G., writing—review and editing, M.C.-T. and C.M.L.; visualization, P.G. and M.C.-T.; supervision, C.M.L., A.L. and M.C.-T. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Data Availability Statement

The datasets generated and/or analysed during the current study are available from the corresponding author upon reasonable request.

Conflicts of Interest

The authors declare no conflicts of interest.

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Agronomy 14 00998 g001
Figure 1. Symptom scale to assess infection of aubergine plants by Verticillium dahliae. The numbers represent the level of disease incidence, where 0 = no symptoms; 1 = chlorosis of the lower leaves; 2 = chlorosis of 30–50% of the leaves; 3 = chlorosis of more than 50% of the leaves.
Figure 1. Symptom scale to assess infection of aubergine plants by Verticillium dahliae. The numbers represent the level of disease incidence, where 0 = no symptoms; 1 = chlorosis of the lower leaves; 2 = chlorosis of 30–50% of the leaves; 3 = chlorosis of more than 50% of the leaves.
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Agronomy 14 00998 g002
Figure 2. Severity of disease symptoms for each combination of V. dahliae isolates and Solanum rootstocks and Larne F1 cultivar. Medians and their 95% confidence intervals (in circles and blue lines) and means (black asterisks) are depicted. To facilitate comparisons, the data are organized into facets according to isolates (A) or rootstocks (B). In (A), the term “all” refers to the entire set of isolates for each rootstock, while in (B), it refers to the complete set of rootstocks for each isolate.
Figure 2. Severity of disease symptoms for each combination of V. dahliae isolates and Solanum rootstocks and Larne F1 cultivar. Medians and their 95% confidence intervals (in circles and blue lines) and means (black asterisks) are depicted. To facilitate comparisons, the data are organized into facets according to isolates (A) or rootstocks (B). In (A), the term “all” refers to the entire set of isolates for each rootstock, while in (B), it refers to the complete set of rootstocks for each isolate.
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Figure 3. Relative effects of disease symptoms and their 95% confidence intervals of each combination of Solanum rootstocks and V. dahliae isolates. To facilitate comparisons, the data are organized into facets according to isolates (A) or rootstocks (B). In (A), the term “all” refers to the entire set of isolates for each rootstock, while in (B), it refers to the complete set of rootstocks for each isolate. Within each facet, the letters correspond to multiple comparisons made with all Rootstock:Isolate combinations, except for “all” facets which are made with each single factor. The letters have been simplified to make comparisons within each facet.
Figure 3. Relative effects of disease symptoms and their 95% confidence intervals of each combination of Solanum rootstocks and V. dahliae isolates. To facilitate comparisons, the data are organized into facets according to isolates (A) or rootstocks (B). In (A), the term “all” refers to the entire set of isolates for each rootstock, while in (B), it refers to the complete set of rootstocks for each isolate. Within each facet, the letters correspond to multiple comparisons made with all Rootstock:Isolate combinations, except for “all” facets which are made with each single factor. The letters have been simplified to make comparisons within each facet.
Agronomy 14 00998 g003
Table 1. Verticillium dahliae isolates used in the experiments.
Table 1. Verticillium dahliae isolates used in the experiments.
IsolateOriginDateHost
Vd 8Cartagena (Murcia)February 1984S. melongena cv. Bonica
Vd 17El Palmar (Murcia)May 1988S. melongena
Vd 66Cieza (Murcia)December 1992S. melongena
A1Mallorca (Islas Baleares)June 2012S. melongena grafted on Javah F1 rootstock
A2Mallorca (Islas Baleares)June 2012S. melongena grafted on Javah F1 rootstock
Table 2. Rootstocks used in the experiments.
Table 2. Rootstocks used in the experiments.
Plant SpeciesRootstockCompanyResistance
Solanum torvumHugo F1Akira Seeds1 IR Verticillium sp.
Solanum sp.Javah F1Takii Europe B.V.1 IR Verticillium sp.
Solanum torvumTorpedo Ramiro Arnedo S.A.2 HR Verticillium sp.
Solanum melongenaLarne F1Semillas Fitó S.A.-
1 IR: intermediate resistance. 2 HR: high resistance.
Table 3. Verticillium Wilt Incidence. Generalized linear mixed model fits and analysis of deviance for testing the significance of the factors Solanum rootstock (St) and Verticillium dahliae isolate (Vd) and their interaction.
Table 3. Verticillium Wilt Incidence. Generalized linear mixed model fits and analysis of deviance for testing the significance of the factors Solanum rootstock (St) and Verticillium dahliae isolate (Vd) and their interaction.
Goodness-of-Fit TestAnalysis of Deviance
N 1ModelNpar 5AIC 6Df 7logLik 8Deviance 9TestFactor testedLRT 10Δ dfPr(>Chisq) 11
1St 2 + Vd3 + St:Vd 3 + (1|R 4)21111.6339−34.81369.625
2St 2 + Vd 3 + (1|R 4)9108.3351−45.16690.3331 vs. 2St:Vd20.708120.055
3St 2 + (1|R 4)5218.7155−104.353208.7072 vs. 3Vd118.3744<2.2 × 10−16 ***
4Vd + (1|R 4)6217.5654−102.78205.5592 vs. 4Sc115.2263<2.2 × 10−16 ***
1 N = number of model. 2 St = Solanum rootstock. 3 Vd =Verticillium dahliae isolate. 4 R = replicate. 5 npar = number of model parameters. 6 AIC = Akaike Information Criterion. 7 df = degrees of freedom. 8 logLik = the log-likelihood for the model. 9 deviance = deviance for the model. 10 LRT = likelihood ratio test statistic. 11 Pr(>Chisq) = p-value.
Table 4. Proportion of plants affected and pairwise comparisons using Fisher’s exact test.
Table 4. Proportion of plants affected and pairwise comparisons using Fisher’s exact test.
St 1\Vd 2A1A2Vd17Vd66Vd8Mean
Larne F10.600 ab0.867 a0.067 c0.067 c0.333 bc0.387 B
Hugo F10.267 bc0.200 bc0.000 c0.000 c0.000 c0.093 C
Javah F11.000 a1.000 a0.133 bc0.067 c1.000 a0.640 A
Torpedo0.133 bc0.267 bc0.067 c0.000 c0.000 c0.093 C
Mean0.500 AB0.583 A0.067 C0.033 C0.333 B0.303
1 St = Solanum rootstock and 2 Vd = Verticillium dahliae isolate. Different capital letters indicate significant differences within the mean values of the rootstocks or within the mean values of the isolates with a p-value ≤ 0.05 according to Fisher’s exact test. Different lowercase letters indicate significant differences between rootstock and isolate combinations with a p-value ≤ 0.05 according to Fisher’s exact test.
Table 5. Non-parametric analysis of disease symptoms. ANOVA-type statistic from the relative effect of Solanum rootstocks and V. dahliae isolate and their interaction.
Table 5. Non-parametric analysis of disease symptoms. ANOVA-type statistic from the relative effect of Solanum rootstocks and V. dahliae isolate and their interaction.
ANOVA-Type StatisticStatisticdf1df2p-Value
Rootstock60.72052.6059205.20540
Isolate10.97943.8751205.20540
Rootstock:Isolate1.99559.8844205.20540.036
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Lacasa, C.M.; Cantó-Tejero, M.; Martínez, V.; Lacasa, A.; Guirao, P. Performance of Aubergine Rootstocks against Verticillium dahliae Isolates in Southeastern Spain. Agronomy 2024, 14, 998. https://doi.org/10.3390/agronomy14050998

AMA Style

Lacasa CM, Cantó-Tejero M, Martínez V, Lacasa A, Guirao P. Performance of Aubergine Rootstocks against Verticillium dahliae Isolates in Southeastern Spain. Agronomy. 2024; 14(5):998. https://doi.org/10.3390/agronomy14050998

Chicago/Turabian Style

Lacasa, Carmen María, Manuel Cantó-Tejero, Victoriano Martínez, Alfredo Lacasa, and Pedro Guirao. 2024. "Performance of Aubergine Rootstocks against Verticillium dahliae Isolates in Southeastern Spain" Agronomy 14, no. 5: 998. https://doi.org/10.3390/agronomy14050998

APA Style

Lacasa, C. M., Cantó-Tejero, M., Martínez, V., Lacasa, A., & Guirao, P. (2024). Performance of Aubergine Rootstocks against Verticillium dahliae Isolates in Southeastern Spain. Agronomy, 14(5), 998. https://doi.org/10.3390/agronomy14050998

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