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Chilean journal of agricultural research

On-line version ISSN 0718-5839

Chil. j. agric. res. vol.78 no.1 Chillán Mar. 2018

http://dx.doi.org/10.4067/S0718-58392018000100078 

RESEARCH

Response of Capsicum annuum L. var. annuum genotypes to root-knot nematode infection

Renato Silva Soares1 

Edgard Henrique Costa Silva1 

Roberta Luiza Vidal1 

Willame dos Santos Candido2 

Carolina Andrade Franco1 

Francisco José Becker Reifschneider3 

Leila Trevisan Braz1 

1Universidade Estadual Paulista (UNESP), Via de Acesso Prof. Paulo Donato Castellane, Jaboticabal, São Paulo, 14884-900, Brasil.

2Universidade Federal de Goiás, Jataí, Goiás, 75804-020, Brasil.

3Empresa Brasileira de Pesquisa Agropecuária (Embrapa), Secretaria de Relações Internacionais, Brasília-DF, 70770-901, Brasil.

ABSTRACT

Root-knot nematodes are among the main agents that negatively affect the pepper and sweet pepper crop (Capsicum annuum L.), especially Meloidogyne incognita, M. javanica, and M. enterolobii. The objective of this study was to evaluate genotypes of C. annuum L. var. annuum in their response to infection by M. incognita race 3, M. javanica, and M. enterolobii. The experiment was conducted using a completely randomized design arranged in a 27 × 3 factorial scheme with six replicates and each plot consisted of one plant. The experiment was carried out at the UNESP-FCAV in Jaboticabal, Sao Paulo, Brazil. The genotypes were in plastic pots containing an autoclaved mixture of soil, sand, and bovine manure under greenhouse conditions, and they were evaluated for the reproduction index and reproduction factor at 90 d after inoculation. Thirteen genotypes were classified as resistant, based on the reproductive factor, and highly resistant, based on the reproduction index, to M. javanica, while six were resistant and highly resistant materials to M. incognita race 3. No materials resistant to M. enterolobii were identified. The genotypes CNPH 698, CNPH 701, CNPH 702, CNPH 717, and CNPH 718 were simultaneously classified as resistant to M. incognita race 3 and M. javanica based on the reproduction factor.

Key words: Meloidogyne spp.; hot and sweet peppers; reaction; resistance

INTRODUCTION

Sweet pepper (Capsicum annuum L. var. annuum) is among the main vegetable crops in Brazil and is mostly cultivated in a protected environment (Araújo et al., 2009; Oliveira et al., 2009). This type of crop system has allowed the farmer, in addition to better fruit quality, to market the product throughout the year, providing better remuneration (Pinheiro et al., 2014). However, its intensified use has led to an increase in the incidence and severity of soil-borne pathogens, especially root-knot nematodes (Meloidogyne spp.)

Nematodes belonging to the genus Meloidogyne are considered as the most economically important species worldwide (Jones et al., 2013). Symptoms include reduced growth, wilting, and leaf discoloration, which are similar to the symptoms of mineral deficiency. According to Mota et al. (2013), nematodes can also form complexes with other pathogens, such as Fusarium oxysporum, Rhizoctonia solani, and Thielaviopsis basicola.

Farmers use resistant rootstocks to manage the nematodes of the genus Meloidogyne in pepper cropping. Currently, materials that are resistant to Meloidogyne incognita (Kofoid & White) and Meloidogyne javanica (Treub) are species cited by Pinheiro et al. (2014) as the most important for vegetable crops. However, a third species, Meloidogyne enterolobii Yang & Eisenback (sin. Meloidogyne mayaguensis Rammah & Hirschmann) has been gaining importance; it has been found to infect materials resistant to the abovementioned species (Pinheiro et al., 2014).

Due to its great harmful potential, wide range of hosts, and absence of resistant commercial material, M. enterolobii poses a great threat to sweet pepper production (Pinheiro et al., 2013a).

Genetic resistance is considered as the best alternative to control phytonematodes because of the low efficiency of chemical control and the search for sources of vital resistance to breeding programs (Hussain et al., 2014; Liu et al., 2015). However, there are currently no pepper materials, or even rootstocks, that have multiple resistance to the three major species of root-knot nematodes.

Therefore, the objective of the present study was to evaluate genotypes of Capsicum annuum L. var. annuum with respect to their response to infection by M. incognita race 3, M. javanica, and M. enterolobii.

MATERIALS AND METHODS

The experiment was carried out in a protected environment in the Sector of Vegetable Crops and Aromatic Medicinal Plants and Plant Pathology Laboratory, Department of Plant Protection, Universidade Estadual Paulista (UNESP), Agricultural and Veterinary Sciences Faculty (FCAV) in Jaboticabal (21°14'05" S, 48°17'09" W; 614 m a.s.l.), Sao Paulo, Brazil.

We evaluated 24 Capsicum annuum L. var. annuum accessions from the Embrapa Hortalicas germplasm bank (CNPH 146, CNPH 694, CNPH 696, CNPH 697, CNPH 698, CNPH 701, CNPH 702, CNPH 703, CNPH 705, CNPH 707, CNPH 708, CNPH 709, CNPH 712, CNPH 714, CNPH 717, CNPH 718, CNPH 719, CNPH 723, CNPH 726, CNPH 727, CNPH 728, CNPH 729, CNPH 730, and CNPH 731), hot pepper ‘BRS Moema’ (C. chinense Jacq.), and sweet pepper ‘Ikeda’ (C. annuum L.) Tomato (Solanum lycopersicum L.) ‘Santa Cruz Kada’ was used as a standard of susceptibility and to verify the viability of the inoculum.

The experiment was conducted with a completely randomized design, arranged in a 27 × 3 factorial scheme, and included 26 genotypes of Capsicum spp., tomato and three species of root-knot nematodes. Each plot consisted of one plant and six replicates per treatment were performed.

The initial inocula were obtained from subpopulations of M. incognita race 3, M. javanica, and M. enterolobii from the Laboratory of Nematology of the UNESP-FCAV, Campus of Jaboticabal. The morphological characteristics of the perineal pattern (Taylor and Netscher, 1974) and the morphology of the male labial region (Eisenback, 1985) were used to identify the species M. incognita race 3 and M. javanica. For M. enterolobii, the original description of the species was used according to Yang and Eisenback (1983).

The subpopulations were inoculated separately in ‘Santa Cruz Kada’ tomato and kept in the greenhouse for multiplication and maintenance of the inoculum. Approximately 120 d after inoculation, eggs and second-stage juveniles (J2) of the nematode species were extracted separately using the methodology described by Hussey and Barker (1973). The egg population and J2 present in the suspension were estimated with a Peters counting chamber under a photonic microscope. Subsequently, the concentration of this suspension was adjusted to 1000 eggs and second-stage juveniles mL-1.

Seedlings were produced in 128-cell expanded polystyrene trays with commercial substrate (Bioplant, Bioplant Agricola Ltda., Nova Ponte, Minas Gerais, Brazil) and kept in a greenhouse with a sprinkler irrigation system. After 40 d, seedlings were transplanted into 2-L plastic pots containing previously autoclaved (120 °C, 1 atm, 1 h) 1:3:1 soil, sand, and bovine manure mixture. Concomitantly, a 5-mL suspension containing 1000 eggs and second-stage juveniles mL-1 in each pot were inoculated with an automatic pipette; the initial population (Pi) was 5000 eggs and J2.

After 90 d of inoculation, plants were evaluated for nematode response. For this, roots were separated from shoots, washed with water to remove excess adhered mixture, and then weighed on a digital analytical balance. The extraction of Meloidogyne species was performed according to Hussey and Barker (1973). The total number of eggs and J2 (TNEJ) were then quantified by extrapolating the 1 mL count of the suspension into a Peters chamber under a photonic microscope. The TNEJ also corresponded to the final nematode population (Pf). The number of eggs and J2 per gram of root (NEJGR) was calculated by dividing TNEJ by total root weight.

We used the reproduction factor (RF) and the reproduction index (RI) to verify the resistance of C. annuum genotypes to the root-knot nematodes. The RF was determined by dividing the final (Pf) and initial (Pi) population densities: RF = P/Pi . According to Oostenbrink (1966), plants that exhibited RF < 1 were considered resistant to the nematode and were classified as susceptible when RF > 1.

The value of the reproduction index (RI) was calculated by considering the tomato ‘Santa Cruz Kada’ as a pattern of susceptibility in relation to nematode reproduction obtained in Capsicum genotypes. The formula [100 × (NEJGR mean of each genotype/NEJGR mean of the ‘Santa Cruz Kada’ tomato cultivar)] was used. According to the criterion established by Taylor (1967), the degree of resistance was classified as susceptible (S) if RI > 50% of the value obtained for the ‘Santa Cruz Kada’ tomato, slightly resistant (SLR) when RI was between 26% and 50%, moderately resistant (MR) when RI was between 11% and 25%, very resistant (VR) when RI was between 1% and 10% and highly resistant/immune (HR/I) when RI < 1%.

To meet the normality assumptions and error distribution, data were transformed to log (x+5) and then subjected to ANOVA. When significant differences were detected by the F test, these were grouped by the Scott-Knott test at 5% probability. The analyses were performed with the statistical AgroEstat software (Barbosa and Maldonado Júnior, 2015).

RESULTS AND DISCUSSION

The ANOVA detected a significant effect between TNEJ and NEJGR for genotypes of C. annuum and the nematode species M. incognita race 3, M. javanica, and M. enterolobii. There was also a significant difference for the interaction between genotypes of C. annuum and the species of root-knot nematodes (Table 1).

The ‘Santa Cruz Kada’ tomato showed high values of TNEJ and NEJGR, differing significantly by the Scott-Knott test (p < 0.05) to C. annuum genotypes, hot pepper 'BRS Moema', and sweet pepper ‘Ikeda’ (Tables 2 and 3). The reactions represented by the RF were also considered high for the three species of Meloidogyne; they exhibited values > 119.64 (Table 2) and ensured that the environmental conditions made it possible to multiply the inoculum.

The RF classified sweet pepper ‘Ikeda’ as susceptible to M. incognita race 3 and M. enterolobii and resistant to M. javanica (Table 2). Regarding RI, this cultivar showed a susceptible reaction to M. incognita race 3 and M. enterolobii and was highly resistant to M. javanica (Table 3). Peixoto et al. (1999) also observed a susceptible reaction to M. incognita race 3 and resistance to M. javanica for ‘Ikeda’ when evaluating different genotypes of sweet pepper. Bitencourt and Silva (2010), Melo et al. (2011), and Goncalves et al. (2014) also observed susceptibility of ‘Ikeda’ to M. enterolobii.

In studies carried out by Pinheiro et al. (2013a; 2013b), hot pepper ‘BRS Moema’ was resistant to M. javanica and susceptible to M. incognita and M. enterolobii. The same behavior was detected in the present study.

Except for M. enterolobii, the C. annuum genotypes differed for TNEJ and NEJGR, indicating the existence of genetic variability among them for resistance to M. incognita and M. javanica (Tables 2 and 3). For M. enterolobii, all genotypes were considered susceptible by the RF and RI. It was also observed that the RF and RI values for M. enterolobii were generally higher when compared to the other two species, indicating a greater aggressiveness of this species in the pepper crop. The high reproduction rate of M. enterolobii and the wide host range in vegetable crops is reported by Cantu et al. (2009) and Rosa et al. (2015). According to the authors, these factors are evidence of the aggressiveness of the species, which is able to overcome sources of resistance to other root-knot nematodes, such as M. incognita, M. javanica, and M. arenaria.

According to the TNEJ and NEJGR variables for M. incognita race 3, the C. annuum genotypes CNPH 146, CNPH 698, CNPH 701, CNPH 702, CNPH 717, and CNPH 718 showed the lowest values, and these differed from the other materials (Tables 2 and 3). When the reaction of these genotypes based on the RF and RI was considered, they were classified as resistant and highly resistant, respectively, because their values were < 1. The genotypes CNPH 694, CNPH 703, CNPH 719, CNPH 726, CNPH 728, CNPH 729, and CNPH 730 were considered as very resistant and their RI ranged from 1% to 10%. For the moderately resistant reaction, only CNPH 705, CNPH 727, and CNPH 731 were classified in this group. The other genotypes were slightly resistant or susceptible to M. incognita race 3.

Table 1 ANOVA and test of comparison of means of the total number of eggs and second-stage juveniles (TNEJ), reproduction factor (RF), number of eggs and second-stage juveniles per gram of root (NEJGR), reproduction index (RI), and reaction (R) of 25 genotypes of Capsicum annuum, one hot pepper cultivar (BRS Moema) and tomato ‘Santa Cruz Kada’. 

Means followed by the same letter in a column do not differ by the Scott-Knott test at 5% probability; means observed with statistics based on transformed data for log (x+5).

S: Susceptible, RI > 51%; SLR: slightly resistant, 26% < RI < 50%; MR: moderately resistant, 11% < RI < 25%; VR: very resistant, 1% < RI < 10%; HR/I: highly resistant or immune, RI < 1; CV%: coefficient of variance.

*, **Significant at the 0.05 and 0.01 probability levels, respectively.

For the reaction to M. javanica, 13 (54.16%) of the 24 analyzed C. annuum genotypes were considered as resistant and highly resistant based on the RF and RI, respectively (Tables 2 and 3).

Regarding the multiple resistance response to the root-knot nematode species, genotypes CNPH 698, CNPH 701, CNPH 702, CNPH 717, and CNPH 718 were simultaneously classified as resistant and highly resistant to M. incognita race 3 and M. javanica. However, these genotypes were susceptible to M. enterolobii (Tables 2 and 3).

The differences in the responses of the same genotype to M. incognita, M. javanica, and M. enterolobii can be derived from the different specificity of some Me pepper genes that confer resistance to the Meloidogyne species (Pinheiro et al., 2015). Djian-Caporalino et al. (2006) note that resistance to root-knot nematodes in C. annuum is associated with several dominant genes, some of which are specific to certain species or populations (Me4, Mechl, and Mech2) and others are efficient against several Meloidogyne species (Mel, Me3, and Me7).

Table 2 Post analysis of the interactions between genotypes and species of root-knot nematodes for total number of eggs and second-stage juveniles (TNEJ). 

The same lower-case letters in a column and uppercase letters in a row do not differ by the Scott-Knott test (p < 0.05). RF: Reproduction factor; R: resistant; S: susceptible.

*, **Significant at the 0.05 and 0.01 probability levels, respectively. ns:Nonsignificant by F test.

Pinheiro et al. (2013a) report that resistance to M. enterolobii is apparently mediated by genes other than those conferring resistance to M. incognita and M. javanica. Goncalves et al. (2014) verified the inefficiency of the Me7 resistance gene against the action of M. enterolobii, which confers resistance to M. incognita, M. arenaria, and M. javanica and is present in the genotype of C. annuum CM 334.

Resistance to M. enterolobii has been reported in Capsicum genotypes by Oliveira et al. (2009). According to the authors, a line of C. frutescens was identified with simultaneous resistance to M. incognita race 3, M. javanica, and M. enterolobii; however, it is not yet known which genes are related to the resistance to the three nematode species and it is very important to conduct studies on this subject. Goncalves et al. (2014), evaluating accessions of Capsicum spp., identified a C. chinense genotype resistant to M. enterolobii. The authors also affirm that this genotype is also resistant to Pepper yellow mosaic virus (PepYMV), a major pepper virus. However, there are no reports of these genotypes with respect to resistance to M. incognita and M. javanica.

As for the methodologies used, although both the classifications are based on the RI proposed by Taylor (1967) and the classification based on the RF proposed by Oostenbrink (1966), they efficiently discriminate resistant genotypes. The classification based on the RF is best suited for the selection of resistant individuals because it only takes into account the final and initial nematode populations in each studied genotype and selects them in only two classes of reaction (resistant or susceptible). On the other hand, the classification based on the RI considers the proportion of NEJGR, which involves the highly susceptible control. In the present study, tomato ‘Santa Cruz Kada’ was used, which is a genus and species different from the species of Capsicum. Although they belong to the same family, they provide a wider distribution of classes (HR/I, VR, MR, SLR, and S), allowing greater flexibility and low accuracy in the classification (Gomes et al., 2015; Andrade Júnior et al., 2016).

Table 3 Post analysis of interactions between genotypes and root-knot nematode species for number of eggs and second-stage juveniles per gram of root (NEJGR). 

Test F 51.53** 31.10** 0.86ns

The same lower-case letters in a column and uppercase letters in a row do not differ by the Scott-Knott test (p < 0.05).

RI: Reproduction index; S: susceptible, RI > 51%; SLR: slightly resistant, 26% < RI < 50%; MR: moderately resistant, 11% < RI < 25%; VR: very resistant, 1% < RI < 10%; HR/I: highly resistant or immune, RI < 1.

*, **Significant at the 0.05 and 0.01 probability

The characterization of available materials in breeding programs in response to the main pathogens that affect the crop is of extreme importance. However, the use of only genetic resistance to control phytonematodes is not recommended because resistance breakdown has already been reported by high selection pressure (Djian-Caporalino et al., 2011). In this way, management must be integrated and include practices that aim to reduce the nematode population levels (Collange et al., 2011).

CONCLUSIONS

The genotypes of Capsicum annuum L. var. annuum CNPH 146, CNPH 697, CNPH 708, CNPH 702, CNPH 705, CNPH 707, CNPH 712, CNPH 717, CNPH 718, CNPH 727, CNPH 728, and CNPH 728 are resistant based on the reproduction factor, and highly resistant based on the reproduction index to Meloidogyne javanica. For M. incognita race 3, six genotypes (CNPH 146, CNPH 698, CNPH 701, CNPH 702, CNPH 717, and CNPH 718) are resistant and/or highly resistant. The genotypes CNPH 698, CNPH 701, CNPH 702, CNPH 717, and CNPH 718 are simultaneously resistant to M. incognita race 3 and M. javanica. No evaluated C. annuum genotype is resistant to M. enterolobii.

REFERENCES

Andrade Júnior, V.C., Gomes, J.A.A., Oliveira, C.M., Azevedo, A.M., Fernandes, J.S.C., Gomes, L.A.A., et al. 2016. Resistencia de clones de batata-doce a Meloidogyne javanica. Horticultura Brasileira 34:130-136. doi: dx.doi.org/10.1590/S0102-053620160000100020. [ Links ]

Araújo, J.S., Andrade, A.P., Ramalho, C.I., e Azevedo, C.A.V. 2009. Cultivo do pimentão em condições protegidas sob diferentes doses de nitrogênio via fertirrigação. Revista Brasileira de Engenharia Agrícola e Ambiental 13:559-565. doi: dx.doi.org/10.1590/S1415-43662009000500008. [ Links ]

Barbosa, J.C., e Maldonado Júnior, W. 2015. Experimentação Agronómica & AgroEstat: Sistema para análises estatísticas de ensaios agronómicos. 396 p. Universidade Estadual Paulista (UNESP), Jaboticabal, São Paulo, Brasil. [ Links ]

Bitencourt, N.V., e Silva, G.S. 2010. Reprodução de Meloidogyne enterolobii em olerícolas. Nematologia Brasileira 34:181-183. [ Links ]

Cantu, R.R., Wilcken, S.R.S., Rosa, J.M.O., e Goto, R. 2009. Reação de porta enxertos comerciais de tomateiros a Meloidogyne mayaguensis. Summa Phytopathologica 35:216-218. doi:dx.doi.org/10.1590/S0100-54052009000300009. [ Links ]

Collange, B., Navarrete, M., Peyre, G., Mateille, T., and Tchamitchian, M. 2011. Root-knot nematode (Meloidogyne) management in vegetable crop production: The challenge of an agronomic system analysis. Crop Protection 20:1251-1262. doi:doi.org/10.1016/j.cropro.2011.04.016. [ Links ]

Djian-Caporalino, C., Fazari, A., Arguel, M.J., Vernie, T., Vande-Casteele, C., Faure, I., et al. 2006. Root-knot nematode (Meloidogyne spp.) Me resistance genes in pepper (Capsicum annuum L.) are clustered on the P9 chromosome. Theoretical and Applied Genetics 144:473-486. [ Links ]

Djian-Caporalino, C., Molinari, S., Palloix, A., Ciancio, A., Fazari, A., Marteu, N., et al. 2011. The reproductive potential of the root-knot nematode Meloidogyne incognita is affected by selection for virulence against major resistance genes from tomato and pepper. European Journal of Plant Pathology 131:431-440. doi:10.1007/s10658-011-9820-4. [ Links ]

Eisenback, J.D. 1985. Diagnostic characters useful in the identification of the four most common species of root-knot nematodes (Meloidogyne spp.) p. 95-112. In Sasser, J.N. (ed.) North Carolina State University, Raleigh, North Carolina, USA. [ Links ]

Gomes, J.A.A., Junior, V.C.A., Oliveira, C.M., Azevedo, A.M., Maluf, W.R., and Gomes, L.A.A. 2015. Resistance of sweet potato clones to Meloidogyne incognita races 1 and 3. Bragantia 74:291-297. doi:dx.doi.org/10.1590/1678-4499.0454. [ Links ]

Goncalves, L.S.A., Gomes, V.M., Robaina, R.R., Valim, R.H., Rodrigues, R., and Aranha, F.M. 2014. Resistance to root-knot nematode (Meloidogyne enterolobii) in Capsicum spp. accessions. Revista Brasileira de Ciencias Agrárias 9:49-52. doi:10.5039/agraria.v9i1a3496. [ Links ]

Hussain, M.A., Mukhtar, T., and Kayani, M.Z. 2014. Characterization of susceptibility and resistance responses to root-knot nematode (Meloidogyne incognita) infection in okra germplasm. Pakistan Journal of Agricultural Science 51:309-314. [ Links ]

Hussey, R.S., and Barker, K.R. 1973. A comparison of methods of collecting inocula of Meloidogyne spp. including a new technique. Plant Disease Reporter 57:1025-1028. [ Links ]

Jones, J.T., Hargeman, A., Danchin, E.J., Gaur, H.S., Helder, J., Jones, M.G.K., et al. 2013. Top 10 plant-parasitic nematodes in molecular plant pathology. Molecular Plant Pathology 14:946-961. [ Links ]

Liu, B., Ren, J., Zhang, Y., An, J., Chen, M., Chen, H., et al. 2015. A new grafted rootstock against root-knot nematode for cucumber, melon, and watermelon. Agronomy for Sustainable Development 35:251-259. [ Links ]

Melo, O.D., Maluf, W.R., Gonçalves, R.J.S., Gonçalves Neto, A.C., Gomes, L.A.A., e Carvalho, R.C. 2011. Triagem de genótipos de hortaliças para resistência a Meloidogyne enterolobii. Pesquisa Agropecuária Brasileira 46:829-835. doi:dx.doi.org/10.1590/S0100-204X2011000800007. [ Links ]

Mota, F.C., Alves, G.C.S., Giband, M., Gomes, A.C.M.M., Sousa, F.R., Mattos, V.S., et al. 2013. New sources of resistance to Meloidogyne incognita race 3 in wild cotton accessions and histological characterization of the defense mechanisms. Plant Pathology 62:1173-1183. [ Links ]

Oliveira, C.D., Braz, L.T., Santos, J.M., Banzatto, D.A., e Oliveira, P.R. 2009. Resistencia de pimentas a nematóides de galha e compatibilidade enxerto/porta-enxerto entre híbridos de pimentão e pimentas. Horticultura Brasileira 27:520-526. doi:dx.doi.org/10.1590/S0102-05362009000400019. [ Links ]

Oostenbrink, M. 1966. Major characteristics of the relation between nematodes and plants. Mededelingen Landbouw 66:1-46. [ Links ]

Peixoto, J.R., Maluf, W.R., e Campo, V.P. 1999. Avaliação de linhagens, híbridos F1 e cultivares de pimentão quanto á resistência a Meloidogyne spp. Pesquisa Agropecuária Brasileira 34:2259-2265. http://dx.doi.org/10.1590/S0100-204X1999001200013. [ Links ]

Pinheiro, J.B., Boiteux, L.S., Almeida, M.R.A., Pereira, R.B., Galhardo, L.C.S., and Carneiro, R.M.D.G. 2015. First report of Meloidogyne enterolobii in Capsicum rootstocks carrying the Me1 and Me3/Me7 genes in central Brazil. Nematropica 45:184-188. [ Links ]

Pinheiro, J.B., Reifschneider, F.J.B., e Moita, A.W. 2013a. Reprodução de Meloidogyne enterolobii em pimentas Capsicum dos grupos Habanero e Murupi. Nematologia Brasileira 37:61-65. [ Links ]

Pinheiro, J.B., Reifschneider, F.J.B., Pereira, R.B., e Moita, A.W. 2013b. Reprodução de Meloidogyne spp. em Capsicum spp. Nematologia Brasileira 37:20-25. [ Links ]

Pinheiro, J.B., Reifschneider, F.J.B., Pereira, R.B., e Moita, A.W. 2014. Reação de genótipos de Capsicum ao nematoide-das-galhas. Horticultura Brasileira 32:371-375. doi:dx.doi.org/10.1590/S0102-05362014000300022. [ Links ]

Rosa, J.M.O., Westerich, J.N., e Wilcken, S.R.S. 2015. Reprodução de Meloidogyne enterolobii em olerícolas e plantas utilizadas na adubação verde. Revista Ciência Agronómica 46:826-835. doi:dx.doi.org/10.5935/1806-6690.20150071. [ Links ]

Taylor, A.L. 1967. Introduction to research on plant nematology: an FAO guide to the study and control of the plant-parasitic nematodes. 133 p. FAO, Rome, Italy. [ Links ]

Taylor, A.L., and Netscher, C. 1974. An improved technique for preparing perineal patterns of Meloidogyne spp. Nematologica 20:268-269. [ Links ]

Yang, B., and Eisenback, J.D. 1983. Meloidogyne enterolobii sp. (Meloidogynidae), a root-knot nematode parasitizing pacara earpot tree in China. Journal of Nematology 15:381-391. [ Links ]

Received: September 05, 2017; Accepted: January 20, 2018

*Corresponding author (renato_2366@hotmail.com)

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