Skip to main content
NCBI home page
Journal of Nematology logoLink to Journal of Nematology
. 2007 Dec;39(4):327–332.

Effects of the Mi-1, N and Tabasco Genes on Infection and Reproduction of Meloidogyne mayaguensis on Tomato and Pepper Genotypes

J A Brito 1, J D Stanley 1, R Kaur 2, R Cetintas 3, M Di Vito 4, J A Thies 5, D W Dickson 6
PMCID: PMC2586510  PMID: 19259507

Abstract

Meloidogyne mayaguensis is a damaging root-knot nematode able to reproduce on root-knot nematode-resistant tomato and other economically important crops. In a growth chamber experiment conducted at 22 and 33°C, isolate 1 of M. mayaguensis reproduced at both temperatures on the Mi-1-carrying tomato lines BHN 543 and BHN 585, whereas M. incognita race 4 failed to reproduce at 22°C, but reproduced well at 33°C. These results were confirmed in another experiment at 26 ± 1.8°C, where minimal or no reproduction of M. incognita race 4 was observed on the Mi-1-carrying tomato genotypes BHN 543, BHN 585, BHN 586 and ‘Sanibel’, whereas heavy infection and reproduction of M. mayaguensis isolate 1 occurred on these four genotypes. Seven additional Florida M. mayaguensis isolates also reproduced on resistant ‘Sanibel’ tomato at 26 ± 1.8°C. Isolate 3 was the most virulent, with reproduction factor (Rf) equal to 8.4, and isolate 8 was the least virulent (Rf = 2.1). At 24°C, isolate 1 of M. mayaguensis also reproduced well (Rf ≥ 1) and induced numerous small galls and large egg masses on the roots of root-knot nematode-resistant bell pepper ‘Charleston Belle’ carrying the N gene and on three root-knot nematode-resistant sweet pepper lines (9913/2, SAIS 97.9001 and SAIS 97.9008) carrying the Tabasco gene. In contrast, M. incognita race 4 failed to reproduce or reproduced poorly on these resistant pepper genotypes. The ability of M. mayaguensis isolates to overcome the resistance of tomato and pepper genotypes carrying the Mi-1, N and Tabasco genes limits the use of resistant cultivars to manage this nematode species in infested tomato and pepper fields in Florida.

Keywords: Capsicum annuum, bell pepper, resistance, root-knot nematodes, Solanum lycopersicum, sweet pepper

Meloidogyne mayaguensis was first reported in the continental US in 2002 (Brito et al., 2004). This nematode is of special interest because of its ability to overcome root-knot nematode resistance genes in some economically important crops. Populations of M. mayaguensis from Côte d'lvoire and Burkina Faso (Fargette et al., 1996), Senegal (Duponnois et al., 1995) and Cuba (Rodríguez-Hernández et al., 2001; Rodríguez et al., 2003) have been reported to overcome the Mi-1 gene in tomato (Solanum lycopersicum L.) cultivars and other unidentified root-knot nematode resistance genes in soybean (Glycine max (L.) Merrill) ‘Forrest’ and sweet-potato (Ipomoea batatas (L.) Lam.) ‘CDH’ (Fargette, 1987).

The Mi-1 gene confers resistance in tomato to the three most common warm-climate root-knot nematodes species, M. arenaria, M. incognita and M. javanica (Williamson, 1999). No information is available on the ability of M. mayaguensis to reproduce on root-knot nematode-resistant pepper (Capsicum annuum L.) cultivars. Sources of genetic resistance in pepper to M. arenaria, M. hapla, M. incognita and M. javanica were found in two wild lines of Capsicum chinense and one of Capsicum frutescens (Di Vito and Saccardo, 1979, 1982; Di Vito et al., 1991). Several single dominant genes in pepper, including the N gene (Di Vito et al., 1993b; Fery et al., 1998; Thies and Fery, 2000), the Me-1 and Me-3 genes (Hendy et al., 1985; Castagnone-Sereno et al., 2001; Djian-Caporalino et al., 2001) and the Tabasco gene in pepper lines such as line 89422 (Di Vito and Saccardo, 1986), 9913/2, SAIS 97.9001 and SAIS 97.9008 (M. Di Vito and F. Saccardo, unpub. data), also confer resistance to the three major root-knot nematode species (Di Vito et al., 1993a). The dominant N gene in bell pepper ‘Charleston Belle’ confers resistance to M. arenaria races 1 and 2, M. javanica (Thies and Fery, 2000) and M. incognita (Di Vito et al., 1993b; Fery et al., 1998). Two dominant genes in wild line 56–547/7 of C. chacoense and line 46–530/7 of C. chinense and a recessive gene in PI 159237 and PI 159256 of C. annuum (Di Vito and Saccardo, 1986) confer resistance to M. javanica and M. arenaria, respectively (Di Vito et al., 1993b).

The instability of the root-knot nematode resistance genes in both tomato and pepper at high soil temperature limits their usefulness to manage Meloidogyne spp. in vegetable-production in warm climates. Although the Mi-1 gene in tomato is not stable at high soil temperatures (Dropkin, 1969; Ammati et al., 1986; Haroon et al., 1993), this has not been a problem in processing tomato in California (J. O. Becker, UC Riverside, pers. comm.). A recent report in Florida also showed that tomato with the Mi-1 gene greatly suppressed root galling by M. javanica in both fall and spring tomato crops grown under polyethylene mulch (Rich and Olson, 1999). Similarly, galling caused by root-knot nematode was greatly reduced by the N gene in fall and spring bell pepper crops grown under polyethylene mulch (Thies et al., 2008).

The resistance to root-knot nematodes conditioned by some unidentified genes in pepper was stable at high soil temperatures (Djian-Caporalino et al., 2001). The wild lines 24, 28 and 56 of C. chinense, 32 of C. chacoense, 79 of C. frutescens and 92–3 of C. annuum, resistant to the Italian populations of M. incognita, M. javanica and M. arenaria (Di Vito et al., 1991), maintained their resistance at a very high soil temperature (38°C) (Di Vito et al., 1995; Di Vito and Saccardo, 1996). The resistance conferred by the N gene in bell pepper ‘Charleston Belle’ was only partially lost at soil temperatures of 28 to 32°C under controlled conditions (Thies and Fery, 1998). The objectives of this study were to (i) determine whether M. mayaguensis from Florida is able to overcome the Mi-1-mediated resistance in tomato, the N gene in bell pepper ‘Charleston Belle’ and the Tabasco gene in three pepper lines; and (ii) determine the virulence of seven isolates of M. mayaguensis to a root-knot nematode-resistant tomato cultivar.

Materials and Methods

Nematode source: Meloidogyne mayaguensis and M. incognita isolates were originally collected from field populations in Florida. The nematode species were identified using morphometrics, perineal patterns and esterase and malate dehydrogenase phenotypes. A single egg mass isolate from each field population was reared on tomato ‘Rutgers’ in separate greenhouses. The isolates of M. mayaguensis were: isolate 1 (DPI: N01–304–15B) and isolate 2 (N01–283–14B) collected from unidentified ornamental plants from Broward and Palm Beach Counties, respectively; isolate 3 (N02–341–4B) obtained from tomato from Hendry County; isolate 4 (N02–817–8B) from cape honeysuckle (Tecomaria capensis (Thunb.) Spach) from Palm Beach County; isolate 5 (N03–282–1B) from basil (Ocimum sp.) from Martin County; isolate 6 (N04–503–2B) from tomato from Hendry County; isolate 7 (N04–681–3B) from trumpet flower (Brugmansia sp.) from Alachua County; and isolate 8 (N04–1180–4B) from bottle brush (Callistemon citrinus (Curtis) Skeels) from Nassau County. The isolate of M. incognita race 4 was originally isolated from tobacco (Nicotiana tabacum L.), Green Acres Research Farm, University of Florida, Alachua County, FL.

Tomato tests: The reproduction of M. mayaguensis and M. incognita race 4 on resistant and susceptible tomato genotypes was compared in three experiments. Experiments 1 and 2 were conducted with M. mayaguensis isolate 1 and Mi-1-l-carrying tomato genotypes BHN 585 and BHN 586 under constant environmental temperatures of 22 and 33°C, respectively, in growth chambers (Walker et al., 1993) with 60% RH. Experiment 3 was conducted at 26 ± 1.8°C in a growth room also with M. mayaguensis isolate 1 and four Mi-1-l-carrying tomato genotypes (Table 1). In experiment 4, the reproduction of seven M. mayaguensis isolates on Mi-1-carrying tomato cultivar ‘Sanibel’ was evaluated at 26 ± 1.8°C in a growth room. Thirty-day-old seedlings grown in vermiculite (Grace Canada, Ajax, Ontario) were transplanted individually into 10- (growth chambers) or 15-cm-diam. (growth room) clay pots containing pasteurized soil. Five days after transplanting, each seedling was inoculated with 2,500 (exp. 1, 2) or 5,000 eggs (exp. 3, 4). Inoculum was dispensed into four holes (1.5-cm deep) around the plant base using a micropipette. Seedlings were arranged in a completely randomized design with four (exp. 1, 2) or six replicates (exp. 3, 4). Plants were watered daily with equal amounts of water and fertilized weekly with Peters Professional 20–20–20 (United Industries, St. Louis, MO). Experiments 1–2 and 3–4 were evaluated 39 and 60 d after inoculation (DAI), respectively. Root systems were harvested, washed gently, stained (Thies et al., 2002) and then rated for nematode reproduction with a gall index (GI) and an egg mass index (EMI), using a 0 to 5 scale (Taylor and Sasser, 1978). Eggs were extracted from the entire root systems using the NaOCl method (Hussey and Barker, 1973) as modified by Boneti and Ferraz (1981). Nematode reproduction was assessed by calculating the reproduction factor (Rf = Pf/Pi), where Pi = initial inoculum level and Pf = final egg recovery (Sasser et al., 1984). Egg mass index, Rf and eggs per gram of roots (exp. 4 only) were used to assess the effectiveness of resistance genes on the reproduction of M. mayaguensis and M. incognita.

Table 1.

Root-knot nematode-resistant tomato and pepper genotypes used in this study.

graphic file with name 327tbl1.jpg

Open in a new tab

Pepper tests: Four root-knot nematode-resistant pepper genotypes (Table 1) were compared with the root-knot nematode-susceptible ‘Keystone Resistant Giant’ pepper in a growth chamber (Walker et al., 1993) at 24°C in two experiments. Meloidogyne mayaguensis (isolate 1) and M. incognita race 4 were used in this study. Each seedling (35-d-old) growing in a clay pot (10-cm-diam.) was inoculated with 2,500 eggs. Treatments were set up in a completely randomized design. Plants were watered daily and fertilized as described for the tomato studies. Root systems were harvested at 45 DAI. Reproduction factor, GI and EMI were determined as described above.

Statistical analysis: Data from nematode EMI, GI and Rf were subjected to AN OVA using JMPIN (SAS Institute Inc., Cary, NC), and treatment means were separated by Tukey's HSD test at P ≤ 0.05. Gall index and EMI data from tomato and pepper tests were transformed by √x+1 to equalize the error variances prior to analysis of variance. Untransformed data are presented in the tables.

Results

Tomato tests: Isolate 1 of M. mayaguensis reproduced on the susceptible tomato cultivar and on both the Mi-1-carrying tomato genotypes BHN 585, BHN 586 at 22 and 33°C (Table 2). There also was reproduction at 26 ± 1.8°C on ‘Sanibel’ (Tables 3, 4), BHN 543, BHN 585 and BHN 586 (Table 3). Meloidogyne incognita reproduced well on the Mi-1-carrying tomato genotypes at 33°C, but there was no or minimal reproduction at 22°C (Table 2). The Rf of M. mayaguensis (isolate 1) on Mi-1 tomatoes at 22 and 33°C was higher than that of M. incognita (Table 2). Similar results were observed at 26 ± 1.8°C; M. incognita reproduced poorly on the Mi-1-carrying tomatoes, and the Rf values varied from 0.1 to 0.2 (Table 3). The average Rf of M. mayaguensis (isolate 1) on the Mi-1-carrying tomatoes ranged from 7.4 on BHN 585 to 15.0 on BHN 586 at 22°C and from 8.7 to 9.9 on BHN 585 and BHN 586 tomatoes at 33°C, respectively (Table 2). However, at 26 ± 1.8°C, BHN 543 and BHN 585 tomatoes supported more M. mayaguensis reproduction (P<0.05) than ‘Sanibel’ tomato (Table 3). The Rf of this nematode isolate ranged from 85.5 on ‘Sanibel’ to 157.9 on BHN 585 (Table 3). All root-knot nematode-resistant tomato genotypes were susceptible (Rf ≥ 1) to M. mayaguensis (isolate 1) regardless of the temperature (Tables 2, 3).

Table 2.

Reproduction factor (Rf), egg mass (EMI) and gall indices (GI) of meloidogyne mayaguensis (isolate 1) and M. incognita race 4 on two Mi-1-carrying tomato cultivars and the susceptible tomato ‘Rutgers’ at 22 and 33°C, experiments 1 and 2.

graphic file with name 327tbl2.jpg

Open in a new tab

Table 3.

Reproduction factor (Rf), egg mass (EMI) and galling indices (GI) of Meloidogyne mayaguensis (isolate 1) and M. incognita race 4 on four Mi-1-carrying tomato cultivars and the susceptible tomato ‘Rutgers’ at 26 ± 1.8°C in experiment 3.

graphic file with name 327tbl3.jpg

Open in a new tab

Table 4.

Reproduction factor (Rf), eggs per gram of roots, galling (GI) and egg mass indices (EMI) of seven isolates of Meloidogyn mayaguensis on Mi-1 carrying ‘Sanibel’ and susceptible ‘Rutgers’ tomatoes under growth room conditions at 26 ± 1.8°C in experiment 4.

graphic file with name 327tbl4.jpg

Open in a new tab

Isolate 1 of M. mayaguensis produced higher egg mass and galling indices on the Mi-1 tomato genotypes at 22°C (Table 2) and at 26 ± 1.8°C in experiment 3 than M. incognita (Table 3). There were no differences (P > 0.05) in the EMI and GI (Table 2) between both nematodes at 33°C, except that M. mayaguensis (isolate 1) had higher EMI (EMI = 5.0) and GI (GI = 4.8) on BHN 585 tomato than M. incognita (GI = 3.8; EMI = 3.8) (Table 2). Conversely, there were no differences of the Rf, EMI and GI on the susceptible ‘Rutgers’ tomato inoculated with either nematode regardless of the temperature, except for M. mayaguensis, which had higher reproduction (Rf = 47.3) than M. incognita (Rf = 4.7) at 33°C (P<0.05) (Tables 2, 3).

Seven isolates of M. mayaguensis evaluated in experiment 4 were virulent to Mi-1-carrying ‘Sanibel’ tomato; however, isolate 3 was the most virulent (Rf = 8.4), and isolate 8 was the least (Rf = 2.1) (Table 4). All these isolates produced similar number of eggs per gram of roots (P > 0.05) on ‘Sanibel’ tomato (Table 4), but all isolates had higher Rf, eggs per gram of roots and EMI on ‘Rutgers’ than ‘Sanibel’ tomato (P < 0.05) (Table 4). The difference in the Rf values between experiment 3 and 4 (Tables 3, 4) might be due to the different M. mayaguensis isolates used in these experiments and smaller root systems obtained in experiment 4 (data not shown).

Pepper tests: Meloidogyne mayaguensis (isolate 1) had a higher Rf and produced more egg masses and galls (P < 0.05) on all the root-knot nematode-resistant pepper genotypes than M. incognita race 4 (Table 5). Meloidogyne mayaguensis had a higher Rf (79.9) on the N-carrying bell pepper ‘Charleston Belle’ than on the susceptible ‘Keystone Resistant Giant’ (Rf = 34.4). Meloidogyne incognita did not induce any root galls, and no egg mass formation was observed on ‘Charleston Belle’ bell pepper, while M. mayaguensis produced visible galls and numerous, large egg masses on ‘Charleston Belle’ (Table 5) and the pepper lines. Very few galls and egg masses were observed in all pepper lines inoculated with M. incognita race 4 (Table 5). Meloidogyne mayaguensis reproduced equally (P> 0.05) on the three root-knot nematode-resistant pepper lines 9913/2, SAIS 97.9001 and SAIS 97.9008, whereas M. incognita reproduced poorly (Table 5). The Rf values of M. mayaguensis on the pepper lines ranged from 51.4 on SAIS 97.9008 to 29.1 on SAIS 97.9001, whereas the EMI values ranged from 4.3 to 4.8 on SAIS 97.9001 and 9913/2, respectively (Table 5). The GI values ranged from 3.5 to 4.8 on SAIS 97.9001 and 9913/2, respectively. Based on Rf values, all root-knot nematode-resistant pepper genotypes were susceptible to M. mayaguensis and resistant to M. incognita race 4 (Tables 5).

Table 5.

Reproduction factor (Rf), egg mass (EMI) and galling (GI) indices of Meloidogyne mayaguensis (isolate 1) and M. incognita race 4 on root-knot nematode resistant peppers and a susceptible cultivar ‘Keystone Resistant Giant’ at 24°C in two separate experiments.

graphic file with name 327tbl5.jpg

Open in a new tab

Discussion

The isolates of M. mayaguensis from Florida were able to overcome the resistance of the Mi-1 gene in four tomato genotypes, the N gene in the bell pepper ‘Charleston Belle’ and the Tabasco gene in pepper lines. All these genes confer resistance to M. arenaria, M. incognita and M. javanica. The results of this study indicated that M. mayaguensis from Florida reproduced well at 22, 26 ± 1.8 and 33°C on Mi-1 gene-carrying tomato and at 24°C on root-knot nematode-resistant pepper genotypes, whereas M. incognita reproduced well at 33°C and had little or no reproduction at 22°C when inoculated on the same genotypes. These results confirm previous studies that have reported the instability of the Mi-1 gene to M. incognita at high soil temperatures (Dropkin, 1969; Ammati et al., 1986). It is worth mentioning that the soil temperatures in the experiments carried out in the growth chambers were monitored manually at different intervals during the duration of the experiments. The difference between the soil and environmental temperatures within each growth chamber during these studies was negligible.

Isolate 1 of M. mayaguensis reproduced well on the Mi-1 resistance gene in ‘Sanibel’, BHN 543, BHN 585 and BHN 586 tomato genotypes and the N resistance gene in bell pepper ‘Charleston Belle’, as well as the Tabasco gene in pepper lines 9913/2, Sais 97.9001 and Sais 97.9008. All the root-knot nematode-resistant tomato and pepper genotypes evaluated were susceptible to M. mayaguensis isolate 1 and resistant to M. incognita race 4. Both nematodes produced similar EMI and GI and reproduced well on the susceptible ‘Rutgers’ tomato and ‘Keystone Resistant Giant’ pepper used as control. This is the first report of M. mayaguensis breaking the resistance of root-knot nematode resistance genes in bell pepper and sweet pepper; however, virulent isolates of M. arenaria and M. incognita have been reported to overcome the resistance conferred by gene Me-3 in pepper line HDA149 (Castagnone-Sereno et al., 2001). Likewise, virulent isolates of M. incognita collected in Uruguay reproduced on Mi-l-carrying tomato ‘Nikita’ and on root-knot nematode-resistant peppers ‘Atlante’, ‘Carolina Wonder’ and Charleston Belle' (Piedra Buena et al., 2005). In contrast, the Me-1 resistance gene in the pepper line HDA330 has been reported to be effective against M. incognita virulent isolates (Castagnone-Sereno et al., 2001); however, no data is available on the reproduction of M. mayaguensis on Me-1-carrying peppers.

Eight isolates of M. mayaguensis used in this study were virulent to the Me-1-carrying ‘Sanibel’ tomato; however, seven of eight isolates produced more egg masses, more eggs per gram of root and had a higher Rf on the susceptible ‘Rutgers’ than on ‘Sanibel’ tomato. These differences may indicate that the Mi-1 gene has a negative effect on the ability of these M. mayaguensis isolates to reproduce on Me-1-carrying resistant tomato genotypes. Meloidogyne mayaguensis isolate 1, however, reproduced at similar levels on the susceptible and resistant tomato genotypes, as well as on susceptible and resistant pepper genotypes, except on ‘Charleston Belle’ pepper. These results suggest that there is not only variability in the virulence among the isolates of M. mayaguensis but also among root-knot nematode resistance genes regarding to their effectiveness to reduce M. mayaguensis reproduction. The reproduction of other isolates of M. mayaguensis in Me-1-carrying tomato has been reported in countries in Africa, the Caribbean basin and South America. Populations of M. mayaguensis have been found reproducing on the Me-1-carrying ‘Rossol’ tomato in Côte d'lvoire and Burkina Faso (Fargette et al., 1996), on ‘Guadajira’ tomato in Cuba (Rodríguez et al., 2003) and ‘Viradoro’ tomato in Brazil (Guimarães et al., 2003).

The use of root-knot nematode resistance genes to manage Meloidogyne species in tomato and pepper production in Florida may provide another alternative to pre-plant fumigation with methyl bromide or other fumigants. However, depending on the extent of M. mayaguensis' distribution in the state, results of our study indicate that M. mayaguensis would most likely pose a disease problem where these root-knot nematode-resistant plant genotypes are deployed.

Footnotes

This study was supported by funding from T-STAR, USDA-CSREES 2005–34135–15895. We thank Maria L. Mendes and Renato N. Inserra for their valuable suggestions and for reading the manuscript.

This paper was edited by Isgouhi Kaloshian.

Literature Cited

  1. Ammati M, Thomason IJ, McKinney HE. Retention of resistance to Meloidogyne incognita in Lycopersicon genotypes at high soil-temperature. Journal of Nematology. 1986;18:491–495. [PMC free article] [PubMed] [Google Scholar]
  2. Brito JA, Powers TO, Mullin PG, Inserra RN, Dickson DW. Morphological and molecular characterization of Meloidogyne mayaguensis isolates from Florida. Journal of Nematology. 2004;36:232–240. [PMC free article] [PubMed] [Google Scholar]
  3. Boneti JIS, Ferraz S. Modificação do método de Hussey & Barker para extração de ovos de Meloidogyne exigua de raízes de cafeeiro. Fitopatologia Brasileira. 1981;6:553. [Google Scholar]
  4. Castagnone-Sereno P, Bongiovanni M, Djian-Caporalino C. New data on the specificity of the root-knot nematode resistance genes Mel and Me3 in pepper. Plant Breeding. 2001;120:429–433. [Google Scholar]
  5. Di Vito M, Saccardo F. Resistance of Capsicum species to Meloidogyne incognita . Root-knot nematode (Meloidogyne species) systematics, biology and control. In: Lamberti F, Taylor CE, editors. New York: Academic Press; 1979. pp. 455–456. [Google Scholar]
  6. Di Vito M, Saccardo F. Response of Capsicum to root-knot nematodes (Meloidogyne spp.) Capsicum Newsletter. 1982;1:70–71. [Google Scholar]
  7. Di Vito M, Saccardo F. Zaragoza: Spain; 1986. Response of inbred lines of Capsicum to root-knot nematodes (Meloidogyne spp.) Proceedings of the VIth EUCARPIA meeting on genetics and breeding on Capsicum and eggplant; pp. 119–123. [Google Scholar]
  8. Di Vito M, Saccardo F. Citrus and Vegetable Magazine; 1996. Resistance of pepper to root-knot nematodes (Meloidogyne spp.): Present and future; pp. 55–56. [Google Scholar]
  9. Di Vito M, Saccardo F, Errico A, Zema V, Zaccheo G. Genetics of resistance to root-knot nematodes (Meloidogyne spp.) in Capsicum chacoense, C. chinense and C. frutescens . Journal of Genetics and Breeding. 1993a;47:23–26. [Google Scholar]
  10. Di Vito M, Saccardo F, Zaccheo G. Response of lines of Capsicum spp. to Italian populations of four species of Meloidogyne . Nematologia Mediterranea. 1991;19:43–46. [Google Scholar]
  11. Di Vito M, Saccardo F, Zaccheo G. Response of new lines of pepper to Meloidogyne incognita, M. javanica, M. arenaria and M. hapla . Afro-Asian Journal of Nematology. 1993b;3:135–138. [Google Scholar]
  12. Di Vito M, Zaccheo G, Catalano F, Oreste G. Budapest: Hungary; 1995. Effect of temperature stability of resistance to root-knot nematodes (Meloidogyne spp.) Proceedings of the IXth EUCARPIA meeting on genetics and breeding on Capsicum and eggplant; pp. 230–232. [Google Scholar]
  13. Djian-Caporalino C, Pijarowski L, Fazari A, Samson M, Gaveau L, O'Byrne C, Lefebvre V, Caranta C, Palloix A, Abad P. High-resolution genetic mapping of the pepper (Capsicum annuum L.) resistance loci Me3 and Me4 conferring heat stable resistance to root-knot nematodes (Meloidogyne spp.) Theoretical and Applied Genetics. 2001;103:592–600. [Google Scholar]
  14. Dropkin VH. The necrotic reaction of tomatoes and other hosts resistant to Meloidogyne. Reversal by temperature. Phytopathology. 1969;59:1632–1637. [Google Scholar]
  15. Duponnois R, Mateille T, Gueye M. Biological characteristics and effect of two strains of Arthrobotrys oligospora from Senegal on Meloidogyne species parasitizing tomato plants. Biocontrol Science and Technology. 1995;5:517–525. [Google Scholar]
  16. Fargette M. Use of esterase phenotype in the taxonomy of the genus Meloidogyne. 2. Esterase phenotypes observed in West African populations and their characterization. Revue de Nématologie. 1987;10:45–56. [Google Scholar]
  17. Fargette M, Phillips MS, Blok VG, Waugh R, Trudgill DL. A RFLP study of relationships between species, isolates and resistance-breaking lines of tropical species of Meloidogyne . Fundamental and Applied Nematology. 1996;19:193–200. [Google Scholar]
  18. Fery RL, Dukes PD, Thies JA. ‘Caroline Wonder’ and ‘Charleston Belle’: Southern root-knot nematode resistant bell peppers. HortScience. 1998;33:900–902. [Google Scholar]
  19. Guimarães LMP, Moura RM, Pedrosa EMR. Parasitismo de Meloiodgyne mayaguensis em diferentes espedies botanicas. Nematologia Brasileira. 2003;27:139–145. [Google Scholar]
  20. Haroon SA, Baki AA, Huettel RN. An in vitro test for temperature sensitivity and resistance to Meloidogyne incognita in tomato. Journal of Nematology. 1993;25:83–88. [PMC free article] [PubMed] [Google Scholar]
  21. Hendy H, Pochard E, Dalmasso A. Inheritance of resistance to Meloidogyne chitwood (Tylenchida) in 2 lines of Capsicum annuum. Study of homozygous progenies obtained by androgenesis. Agronomie. 1985;5:93–100. [Google Scholar]
  22. Hussey RS, Barker KR. A comparison of methods of collecting inocula of Meloidogyne spp., including a new technique. Plant Disease Reporter. 1973;57:1025–1028. [Google Scholar]
  23. Piedra Buena A, Díez-Rozo MA, Bello A, Robertson L, López-Pérez JA, Escuer M, De León L. Comportamiento de Meloidogyne incognita sobre tomate pimiento resistente en Uruguay. Nematropica. 2005;35:111–120. [Google Scholar]
  24. Rich JR, Olson SM. Utility of Mi-gene resistance in tomato to manage Meloidogyne javanica in North Florida. Journal of Nematology. 1999;31:715–718. [PMC free article] [PubMed] [Google Scholar]
  25. Rodríguez MG, Sánchez L, Rowe J. Host status of agriculturally important plant families of the root-knot nematode Meloidogyne mayaguensis . Nematropica. 2003;33:125–130. [Google Scholar]
  26. Rodríguez-Hermández MG, Sanchez L, Arocha Y, Peteira B, Solórzano E, Rowe J. Identification and characterization ofMeloidogyne mayaguensis from Cuba. Nematropica. 2001;31:152. (Abstr.). [Google Scholar]
  27. Sasser JN, Carter CC, Hartman KM. Raleigh, NC: North Carolina State University Graphics; 1984. Standardization of host suitability studies and reporting of resistance to root-knot nematodes. [Google Scholar]
  28. Taylor AL, Sasser JN. Raleigh, NC: North Carolina State University Graphics; 1978. Biology, identification and control of root-knot nematodes (Meloidogyne spp.). Cooperative Publication of the Department of Plant Pathology, North Carolina State University and U.S. Agency for International Development. [Google Scholar]
  29. Thies JA, Dickson DW, Fery RL. Stability of resistance to root-knot nematodes in ‘Charleston Belle’ and ‘Carolina Wonder’ bell pepper in a sub-tropical environment. HortScience. 2008;43:188–190. [Google Scholar]
  30. Thies JA, Fery RL. Modified expression of the N gene for the southern root-knot nematode resistance in pepper at high soil temperatures. Journal of the American Society for Horticultural Science. 1998;123:1012–1015. [Google Scholar]
  31. Thies JA, Fery RL. Characterization of resistance conferred by N gene to Meloidogyne arenaria races 1 and 2, M. hapla, and M. javanica in two sets of isogenic lines of Capsicum annuum L. Journal of the American Society for Horticultural Science. 2000;125:71–75. [Google Scholar]
  32. Thies JA, Merrill SB, Corley EL. Red food coloring stain: New, safer procedures for staining nematodes in roots and egg masses on root surfaces. Journal of Nematology. 2002;34:179–181. [PMC free article] [PubMed] [Google Scholar]
  33. Walker TJ, Gaffney JJ, Kidder AW, Ziffer AB. Florida reach-in environmental chambers for Entomological Research. American Entomologist. 1993;39:177–182. [Google Scholar]
  34. Williamson VM. Plant nematode resistance genes. Current Opinion in Plant Biology. 1999;2:327–331. doi: 10.1016/S1369-5266(99)80057-0. [DOI] [PubMed] [Google Scholar]

Articles from Journal of Nematology are provided here courtesy of Society of Nematologists

RESOURCES