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Agronomy • Rev. Caatinga 33 (4) • Oct-Dec 2020 • https://doi.org/10.1590/1983-21252020v33n401rc   copy

IDENTIFICATION OF PLANT PARASITIC NEMATODES IN TRIPLOID AND TETRAPLOID BANANAS IN BRAZIL

IDENTIFICAÇÃO DE FITONEMATOIDES EM BANANEIRAS TRIPLOIDES E TETRAPLOIDES NO BRASIL

Authorship SCIMAGO INSTITUTIONS RANKINGS

ABSTRACT

Nematodes are important pathogens in banana plants, and the lack of resistant genotypes is the biggest challenge of the banana breeding programs. Little is known on the behavior of banana triploids and tetraploids developed by Embrapa regarding parasitism by plant-parasitic nematodes in field conditions. Embrapa Mandioca e Fruticultura experimental areas, naturally infested in five Brazilian states (Embrapa Acre - Acre, Embrapa Semiárido - Pernambuco, Embrapa Cerrados - Distrito Federal, Palmital - São Paulo and Epagri - Santa Catarina) were evaluated for the distribution and population levels of plant-parasitic nematodes in commercial cultivars and triploid and tetraploid genotypes in the final breeding stage. The root-knot nematodes (Meloidogyne spp.) were the most frequent in roots (40 - 100%) and soil (85.71 - 100%), with a detectable number of juveniles (J2) varying between genotypes (4 - 148 J2.250g-1 roots, and 1 - 110 J2.100 cm-3soil). Four esterase phenotypes were characterized: M. incognita (Est I1 = Rm: 1.0), M. javanica (Est J3 = Rm: 1.0; 1.25 and 1.40 and Est J2 = Rm: 1.0 and 1.40) and M. arenaria (Est A2 = Rm: 1.20 and 1.35), M. javanica (Est J3) was predominant. Meloidogyne javanica and M. incognita were predominant, however mixed infestations between species were found. The occurrence of Meloidogyne spp. was: M. javanica (68.26%), M. incognita (64.73%) and M. arenaria (16.81%). Helicotylenchus multicinctus and Rotylenchulus reniformis was the second most frequent group. Radopholus similis, Scutellonema sp., Criconemoides sp. and Helicotylenchus sp. presented themselves in low frequency and population levels in banana plants.

Keywords:
Musa spp; Occurrence Meloidogyne spp; Helicotylenchus spp; Rotylenchulus reniformis

RESUMO

Nematoides são importantes patógenos em bananeiras, e a inexistência de genotipos com resistência é o maior desafio dos programas de melhoramento genético da cultura. Pouco se conhece sobre o comportamento de bananeiras triploides e tetraploides desenvolvidas pela Embrapa quanto ao parasitismo por fitonematoides em campo. Áreas experimentais naturalmente infestadas da Embrapa Mandioca e Fruticultura em cinco estados brasileiros (Embrapa Acre - Acre, Embrapa Semiárido - Pernambuco, Embrapa Cerrados -Distrito Federal, Palmital - São Paulo e Epagri - Santa Catarina) foram avaliadas quanto a distribuição e níveis populacionais de fitonematoides em cultivares comerciais e genótipos triploides e tetraploides em fase final de melhoramento. Os nematoides das galhas (Meloidogyne spp.) foram os mais frequentes em raízes (40 - 100%) e solo (85,71 - 100%), com número detectável de juvenis (J2) variando entre genótipos (4 - 148 J2.250g-1 raízes e 1 - 110 J2.100 cm-3solo). Quatro fenótipos de esterase foram caracterizados: M. incognita (Est I1 = Rm: 1,0), M. javanica (Est J3 = Rm:1,0; 1,25 e 1,40 e Est J2 = Rm: 1,0 e 1,40) e M. arenaria (Est A2 = Rm:1,20 e 1,35), com predominância de M. javanica (Est J3). Meloidogyne javanica e M. incognita foram predominantes, entretanto infestações mistas entre as espécies foram encontradas. A ocorrência de Meloidogyne spp. foi: M. javanica (68,26%), M. incognita (64,73%) e M. arenaria (16,81%). Helicotylenchus multicinctus e Rotylenchulus reniformis foi o segundo grupo mais frequente. Radopholus similis, Scutellonema sp., Criconemoides sp. e Helicotylenchus sp. se apresentaram em baixa frequência e nível populacional nas bananeiras.

Palavras-chave:
Musa spp; Ocorrência Meloidogyne spp; Helicotylenchus spp; Rotylenchulus reniformis

INTRODUCTION

Bananas rank second in world fruit production, and along with rice, wheat and maize, they are considered the most important food sources worldwide (PERRIER et al., 2011PERRIER, X. et al. Multidiciplinary perspectives on banana (Musa spp.) domestication. Proceedings of the National Academy of Sciences of USA, Washington, v. 108, n. 28, p. 1311-1318, 2011.). India leads in banana production in world rankings, accounting for 26.8% of bananas produced globally, followed by China, with 9.8%; Indonesia, with 6.3%; Brazil, with 5.9%; Ecuador, with 5.5%; and the Philippines, with 5.3% (FAOSTAT, 2017).

Although bananas are the second most produced crop in Brazil, few cultivars are available for commercial exploitation that are resistant or tolerant to pests and diseases. Banana plants are attacked by several plant pathogens, among them plant-parasitic nematodes. The burrowing nematode [Radopholus similis (Cobb, 1893) Thorne, 1949] has been the largest cause of banana crop damage in Brazil, although the root-knot nematodes (species of Meloidogyne Goldi, 1887) and the spiral nematode [Helicotylenchus multicinctus (Cobb, 1893) Golden, 1956] are the most frequent in banana-growing areas, however, little research on the economic losses incurred by banana farms from nematode damage has been conducted at the field level. Measures of chemical control used by large companies are not very applicable to small farmers, who represent the majority of Brazilian banana growers. Therefore, the use of resistant cultivars, either by selection within existing genetic resources or by the generation of new cultivars by hybridization, is considered the most efficient control measure (AMORIM et al., 2011AMORIM, E. P. et al. Quality improvement of cultivated Musa. In: PILLAY, M.; TENKOUANO, A. (Ed.). Banana breeding: progress and challenges. New York: CRC Press, 2011. ch. 13, p. 252-280.).

Since 1995, several diploid, triploid and tetraploid banana genotypes have been evaluated under greenhouse conditions at Embrapa Mandioca e Fruticultura, in Cruz das Almas (BA) and Universidade de Brasília (DF) for resistance to R. similis and Meloidogyne spp. (COSTA; SILVA; ALVES, 1998COSTA, D. C.; SILVA, S. O.; ALVES, F. R. Reação de genotipos de bananeira (Musa spp.) a Radopholus similis e Meloidogyne incognita. Nematologia Brasileira, 22: 49-57, 1998.; COSTA; RIBEIRO; LICHTEMBERG, 2003; COSTA; SILVA; ROCHA, 2000; COSTA, 2004; TEIXEIRA, 2007TEIXEIRA, M. A. Resistência de genótipos de bananeira a Meloidogyne incognita, M. javanica e M. arenaria e variabilidade genética com base em marcadores moleculares RAPD. 2007. 68 f. Dissertação (Mestrado em Fitopatologia: Área de Concentração em nematologia) - Universidade de Brasília, Brasília. 2007.; MONTEIRO, 2011MONTEIRO, J. M. S. Resistência a Radophlolus similis e detecção de nematoides fitoparasitas em bananeiras triploides e tetraploides no Brasil. 2011. 82 f. Dissertação (Mestrado em Fitopatologia: Área de Concentração em nematologia) - Universidade de Brasília, Brasília, 2011.; SANTOS et al., 2010SANTOS, J. R. P. et al. Contrastant banana accessions for resistance to the burrowing nematode, based on molecular markers RAPD. Euphytica, 172: 13-20, 2010., 2013). The main goal of the field trials is to evaluate and validate the genotypes of interest regarding their agronomic and yield characteristics under varying environmental conditions, such as soil conditions, nematode occurrence, and climate. However, little is known about the frequency of plant-parasitic nematodes on triploids and tetraploids banana plants introduced and improved by Embrapa Mandioca e Fruticultura under field conditions. Based on this context, this study aimed to evaluate the occurrence of nematodes associated with the roots and soil of the triploids (AAA and AAB) and tetraploids (AAAA and AAAB) commercials and in the final stage of improvement in different experimental areas planted with banana genotypes of Embrapa Mandioca e Fruticultura.

MATERIALS AND METHODS

Banana Genotypes

In the years 2010/2011, eleven triploids (AAA and AAB) and nineteen tetraploids (AAAA and AAAB) (Table 3) genotypes from the Banana Germplasm Bank of Embrapa Mandioca e Fruticultura were evaluated for occurrence and population levels of plant-parasitic nematodes in five experimental areas, located in units belonging to Embrapa and State Research Institutions (Embrapa Acre - Rio Branco - AC; Embrapa Semiárido -Petrolina - PE; Embrapa Cerrados - Planaltina - DF; Experimental Area of Sustainable Agriculture (Middle Paranapanema Region) - Palmital - SP; Agricultural Research and Rural Extension Company of Santa Catarina/EPAGRI - Luis Alves - SC). The experimental design was a randomized block with three replicates, each block containing six clumps of each genotype, with a spacing of 2.5 m x 3.0 m. The number of genotypes evaluated varied according to the location.

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Table 1
Eleven triploid and nineteen tetraploid genotypes of banana plants from the Embrapa Mandioca e Fruticultura Germplasm Bank were evaluated in five experimental areas located in the states of Acre, Pernambuco, Distrito Federal, São Paulo, and Santa Catarina, Brazil in 2010/2011.
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Table 2
Number and frequency of plant-parasitic nematodes detected per 250 g of roots of banana in samples from different experimental areas of Embrapa Mandioca e Fruticultura, located at Embrapa, Acre State (AC); Embrapa Semiárido, Pernambuco State (PE); Embrapa Cerrados, Federal District (DF) Palmital Middle Paranapanema Region (Sustainable Agriculture), São Paulo State (SP); and Agricultural Research and Rural Extension Company of Santa Catarina/ EPAGRI, State of Santa Catarina (SC) during the years 2010/2011.
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Table 3
Number and frequency of plant-parasitic nematodes detected per 100 cm3 of soil in samples collected in banana plant rhizosphere from different experimental areas of Embrapa Mandioca e Fruticultura, located at Embrapa, Acre State (AC); Embrapa Semiárido, Pernambuco State (PE); Embrapa Cerrados, Federal District (DF); Palmital Middle Paranapanema Region (Sustainable Agriculture), São Paulo State (SP); and Agricultural Research and Rural Extension Company of Santa Catarina/ EPAGRI, State of Santa Catarina (SC) during the years 2010/2011.

Root and soil samples from the rhizosphere of banana genotypes

Samples of roots and soil were collected at a depth of 0 - 20 cm at four core points around the plants of each banana genotype distributed among the three blocks. After collecting individual samples, a composite sample composed of roots (500 g) and one of soil (300 cm3) were obtained by pooling and mixing the individual samples, and these were sent to the Laboratory of Nematology/Plant Quarantine Laboratory of Embrapa Recursos Genéticos e Biotecnologia located in Brasília, DF.

Extraction, quantification and identification of nematodes

For nematode extraction, the root samples were divided into two parts of 250 g. The first part of the roots and the soil (100 cm3) samples were used for extraction of nematodes following the methodologies of Coolen and D’Herde (1972COOLEN, W. A.; D’HERDE. C. J. A method for the quantitative extraction of nematodes from plant tissue. Ghent State Agriculture Research Centre. Belgium: Merelbeke, 1972. 77 p.) and Jenkins (1964JENKINS, W. R. A rapid centrifugal-flotation technique for separating nematodes from soil. Plant Disease Reporter, 48: 692-692, 1964.), respectively. Nematodes extracted from both roots and soil were killed at 60 °C for 1 minute and fixed with 4% FAA (Formaldehyde/Acetic Acid/Ethyl Alcohol). The quantification of the total nematode population was performed using Peter’s glass slide under light microscope. Specimens mounted as semipermanent slides in a drop of formalin 2%, sealed with histologic paraffin (HOOPER, 1990HOOPER, D. J. Extraction and Processing of Plant and soil nematodes. In: LUC, M.; SIKORA, R. A.; BRIDGE, J. (Eds.) Plant Parasitic Nematodes in Subtropical and Tropical Agriculture. Liverpool, UK: CAB International, 1990, ch. 2, p. 45-68.; TIHOHOD, 1993TIHOHOD, D. Nematologia agrícola aplicada. 1 ed. Jaboticabal, SP: FUNEP, 1993. 373 p.; PASCHOAL, et al., 1995PASCHOAL, A. D. et al. Animais de interesse agrícola, veterinário e médico: apontamentos práticos de zoologia e parasitologia. 1. ed. Piracicaba, SP: Centro Acadêmico “Luiz de Queiroz”, 1995. 224 p.) were prepared for microscopy and identified under a light microscope to the genus (MAI, 1975MAI, W. F. Pictorial key to genera of plant-parasitic nematodes. 4th ed. Comstock Pub. Associate. 1975. 219 p.) and species levels (FORTUNER, 1991FORTUNER, R. The Hoplolaimidae. In: NICKLE, W. R. (Ed.). Manual of Agricultural Nematology. New York, NY: Macel Dekker, Inc., 1991. ch. 4, p. 698-719.; JATALA, 1991JATALA, P. Reniform and false root-knot nematodes, Rotylenchulus and Nacobbus spp. In: Nickle. W. R. (Ed.). Manual of Agricultural Nematology. New York, Macel Dekker, p. 509-528, 1991.; LOOF, 1991LOOF, P. A. A. The family Pratylenchidae Thorne, 1949. In: NICKLE, W. R. (Ed.). Manual of Agricultural Nematology. New York, NY: Macel Dekker, Inc. , 1991. ch. 4, p. 363-422.; CARES; ANDRADE, 2006CARES, J. E.; ANDRADE, E. P. Taxonomía do gênero Radopholus. Revisão Anual de Patologia de Plantas, 14: 113-149, 2006.).

The second part of the roots was ground in a blender for 1 minute in water, and the suspension of each sample obtained was inoculated onto tomato plants cv. Santa Cruz, which were maintained in a greenhouse for 45 days for multiplication and identification of the Meloidogyne species. From each sample, 36 females were extracted from tomato roots and submitted to vertical eletrophoresis (ESBENSHADE; TRIANTAPHYLLOU, 1985ESBENSHADE, P. R.; TRIANTAPHYLLOU, A. C. Electrophoretic methods for the study of root-knot nematode enzymes. In: BARKER, K. R.; CARTER, C. C.; SASSER, J. N. (Eds.). An advanced treatise on Meloidogyne Methodology. Raleigh, NC: North Caroline State University Graphics, 1985. v. 2, ch. 8, p. 113- 123.) in a 7% polyacrylamide gel prepared according to Carneiro and Almeida (2001CARNEIRO, R. M. D.; ALMEIDA, M. R. A. Técnica de eletroforese usada no estudo de enzimas dos nematoides de galhas para identificação de espécie. Nematologia Brasileira, 25: 35-44, 2001.). The characterization of Meloidogyne species was based on the revealed esterase phenotypes (CARNEIRO, ALMEIDA, CARNEIRO, 1996CARNEIRO, R. M. D. G.; ALMEIDA, M. R. A.; CARNEIRO, R. G. Enzyme phenotypes of Brazilian isolates of Meloidogyne spp. Fundamental and Applied Nematology, 19: 555-560, 1996.; CARNEIRO, ALMEIDA, QUENÉHERVÉ, 2000). Individual females of M. javanica (Est J3) were used as the standard phenotype.

RESULTS AND DISCUSSION

Using light microscopy, Meloidogyne juveniles (J2), Helicotylenchus, Scutellonema and Criconemoides (MAI, 1975MAI, W. F. Pictorial key to genera of plant-parasitic nematodes. 4th ed. Comstock Pub. Associate. 1975. 219 p.) were morphologically identified to the genus level, whereas Radopholus similis (Cobb, 1893) Thorne, 1949 (LOOF, 1991LOOF, P. A. A. The family Pratylenchidae Thorne, 1949. In: NICKLE, W. R. (Ed.). Manual of Agricultural Nematology. New York, NY: Macel Dekker, Inc. , 1991. ch. 4, p. 363-422.; CARES; ANDRADE, 2006CARES, J. E.; ANDRADE, E. P. Taxonomía do gênero Radopholus. Revisão Anual de Patologia de Plantas, 14: 113-149, 2006.), Rotylenchulus reniformis Linford and Oliveira, 1940 (JATALA, 1991JATALA, P. Reniform and false root-knot nematodes, Rotylenchulus and Nacobbus spp. In: Nickle. W. R. (Ed.). Manual of Agricultural Nematology. New York, Macel Dekker, p. 509-528, 1991.), and H. multicinctus (FORTUNER, 1991FORTUNER, R. The Hoplolaimidae. In: NICKLE, W. R. (Ed.). Manual of Agricultural Nematology. New York, NY: Macel Dekker, Inc., 1991. ch. 4, p. 698-719.) were morphologically identified to the species level; Meloidogyne spp. were identified based on their esterase phenotypes (CARNEIRO, ALMEIDA, CARNEIRO, 1996CARNEIRO, R. M. D. G.; ALMEIDA, M. R. A.; CARNEIRO, R. G. Enzyme phenotypes of Brazilian isolates of Meloidogyne spp. Fundamental and Applied Nematology, 19: 555-560, 1996.; CARNEIRO, ALMEIDA, QUENÉHERVÉ, 2000). The quantification data for nematodes detected in the root and soil samples and the frequencies of each genera/species by experimental area are shown in Tables 2 and 3.

Meloidogyne spp. frequently occurred in root (40 - 100%) and soil (85.71 - 100%) samples across all areas investigated, with the detected number of nematodes varying among banana genotypes in the root (4 to 148 J2.250g-1 roots) and soil (1 to 110 J2.100 cm-3 soil) samples (Tables 2 and 3). In the experimental area of Embrapa Acre, it was observed that the cultivar FHIA 17 stood out from the other evaluated genotypes because of the absence of rootknot nematodes, both in its root and soil samples (Tables 2 and 3). Similar results to those of cv. FHIA 17 were found in the Epagri experimental area, with emphasis on the genotypes PV 7934 and BRS Conquista, where root-knot nematodes were not detected in either the root or soil samples. In the experimental areas of Embrapa Semiárido, Embrapa Cerrados and Palmital, higher population levels of root-knot nematodes were detected, in both the root and soil samples, mainly in the Embrapa Semiárido, where these nematodes were detected in all genotypes and cultivars, with the highest J2 populations occurring in the cultivars FHIA 02 (148 J2.250g-1 roots) and BRS Plantina (126 J2.250g-1 roots and 102 J2.100 cm-3 soil). In the experimental area of Embrapa Cerrados, root-knot nematodes were more abundant in soil than in roots (Tables 2 and 3), with the exception of the rhizosphere soil of the cultivar Japira. In Embrapa Cerrados, root-knot nematodes were not detected in the roots of the YB 4207 and PV 9401 genotypes, or the roots of the Bucanero, Pacovan, FHIA 17 and Maçã cultivars, but were present in all other varieties (Table 2). In the Palmital experimental area, root-knot nematodes were present in the roots and soil of all genotypes and cultivars examined, with the exception of cv. Bucanero, for which root-knot nematodes were absent from roots and present at only a very low population level in soil (1 J2.100 cm-3 soil).

The identification of Meloidogyne species by their esterase phenotypes allowed us to evidence four esterase profiles of the three most common Meloidogyne species previously associated with banana plants: M. incognita (Kofoid and White, 1919) Chitwood, 1949 (I1) one band of esterase activity (Rm:1.0); M. javanica (Treub, 1885) Chitwood, 1949 (J3) three bands (Rm:1.0; 1.25 and 1.40) and (J2) two bands (Rm:1.0 and 1.40) of esterase activity; and M. arenaria (Neal, 1889) Chitwood, 1949 (A2) two bands of esterase activity (Rm:1.20 and 1.35)(Figure 1).

Figure 1
(A) Esterase band patterns (Est) detected for Meloidogyne species and their relative mobility from banana samples collected in areas of experimental fields of Embrapa, Acre State; Embrapa Semiárido, Pernambuco State; Embrapa Cerrados, Federal District; Palmital Middle Paranapanema Region (Sustainable Agriculture), São Paulo State; and Agricultural Research and Rural Extension Company of Santa Catarina / EPAGRI, State of Santa Catarina during the years 2010/ 2011. (B) Polyacrylamide gels (7%) showing patterns of esterase bands for Meloidogyne females in the banana genotypes evaluated in this study. (J3*)M. javanica standard used.

The species M. javanica and M. incognita were predominant. However, mixed infestations of these species were found in Embrapa Acre, Embrapa Cerrados, and Palmital (SP); these sometimes cooccurred with M. arenaria, which showed low incidence (Table 4). Co-infestations only occurred in some cultivars, i.e., FHIA 23, Maçã, Prata Anã, Thap Maeo, Maravilha and Bucanero, and in the genotype PV 7934 (Table 4). Meloidogyne javanica was prevalent across all genotypes, with average values of occurrence in Embrapa Cerrados (91.78%), Palmital (91.74%) and Embrapa Semiárido (67.70%). We note that Meloidogyne javanica comprised 100% of the nematodes occurring on most genotypes in Palmital, except for cv. Pacovan and the genotype YB 4203, which had mixed infections with a predominance of M. incognita. A predominance of M. incognita over M. javanica was observed only at Embrapa Acre (92.31%) and Epagri (74.07%) (Table 4). The results showed that M. javanica was the predominant Meloidogyne species in banana plants, followed by M. incognita and M. arenaria.

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Table 4
Occurrence of Meloidogyne species in different banana genotypes from five experimental areas of Embrapa Mandioca e Fruticultura: Embrapa, Acre State (AC); Embrapa Semiárido, Pernambuco State (PE); Embrapa Cerrados, Federal District (DF); Palmital Middle Paranapanema Region (Sustainable Agriculture), São Paulo State (SP); and Agricultural Research and Rural Extension Company of Santa Catarina / EPAGRI, State of Santa Catarina (SC) during the years 2010/ 2011.

The spiral nematodes Helicotylenchus multicinctus and the reniform nematode Rotylenchulus reniformis were the next most prevalent detected species. The frequency of H. multicinctus in the root samples ranged from 8 to 94.73% and their population sizes ranged from 4 to 26 specimens.250g-1 roots, with the highest prevalences in Palmital-SP. The highest frequencies in soil samples were observed in Palmital-SP (84.21%), Embrapa Acre (84%), and Epagri-SC (70%) with population sizes ranging from 4 to 46 specimens.100 cm-3 soil. For R. reniformis, its frequency was variable, ranging from 8 to 52.63% in the roots and from 4.54% to 100% in soil samples. Rotylenchulus reniformis was most commonly observed among the genotypes in Embrapa Semiárido soils and Palmital roots. Rotylenchulus reniformis population sizes varied among the samples, ranging from 4 to 10 specimens.250g-1 roots and from 11 to 101 specimens.100 cm-3 soil. At Embrapa Semiárido, R. reniformis was detected only in the roots of the genotypes YB 4203 and BRS Platina (Table 2). However, in the rhizosphere soil samples of all genotypes, was detected in large quantities of R. reniformis (Table 3). At Embrapa Cerrados, R. reniformis was only detected in rhizosphere soil samples of the genotype PV 7934.

The burrowing nematode (Radopholus similis) was rare across all experimental areas. It was not detected in the roots of any of the genotypes and was detected in only a few soil samples in Embrapa Acre (20%) and Palmital (10.52%) that were associated with the genotypes Garantida, Thap Maeo, Grande Naine, Tropical, and FHIA 2, ranging in detectable population levels from 1 to 28 specimens.100 cm-3 soil (Table 2 and 3). Other spiral nematodes were also detected in low percentages in the experimental areas of Embrapa Cerrados and Palmital in the roots and soil samples, e.g., Helicotylenchus sp. (15 specimens.250g-1 roots in the PV 7934 genotype), and 5 to 15 specimens.100 cm-3 soil in the Thap Maeo, Grande Naine and Maçã cultivars), and Scutellonema sp. (1 specimen.250g-1 roots and per 100 cm3 of soil in the Caipira, Japira and Thap Maeo cultivars). The ring nematode (Criconemoides sp.) was detected only in soil samples associated with cv. Vitória and the genotype YB 4203 (2 specimens.100 cm-3 soil).

Root-knot nematodes (Meloidogyne spp.) were the most abundant nematodes detected in the roots and soils of the genotypes we studied across all experimental areas, indicating these banana genotypes were good hosts for this nematode and confirming previous reports that banana plants are good multipliers of Meloidogyne spp. (MOREIRA, 1995MOREIRA, R. Como conviver com os nematoides em bananeiras. In: CONGRESSO INTERNACIONAL DE NEMATOLOGIA TROPICAL, 27., 1995, Caldas Novas. Anais... Caldas Novas: ONTA, 1995. p. 186-190.; COSTA et al., 1997COSTA, D. C. et al. Avaliação de danos e perdas à bananeira cv. Nanica, causadas por Meloidogyne incognita na região de Petrolândia-PE. Nematologia Brasileira, 21: 21-21, 1997.; COSTA; SILVA; ALVES, 1998; COSTA; SILVA; ROCHA, 2000; COSTA; RIBEIRO; LICHTEMBERG, 2003; PINTO et al., 2005PINTO, A. C. B. V. et al. Reação de clones de bananeira a Meloidogyne incognita. Nematologia Brasileira, 29: 134-134, 2005.; TEIXEIRA, 2007TEIXEIRA, M. A. Resistência de genótipos de bananeira a Meloidogyne incognita, M. javanica e M. arenaria e variabilidade genética com base em marcadores moleculares RAPD. 2007. 68 f. Dissertação (Mestrado em Fitopatologia: Área de Concentração em nematologia) - Universidade de Brasília, Brasília. 2007.).

In this study the bands patterns of esterase activity detected for M. javanica (Est J3, Est J2), M. incognita (Est I1) and M. arenaria (Est A2), were compatible with the results obtained by Cofcewicz et al. (2004aCOFCEWICZ, E. T. et al. Enzyme phenotype and genetic diversity of root-knot nematode parasitizing Musa in Brazil. Nematology, 6: 85-95, 2004a.). Cofcewicz et al. (2004a) analyzed samples of banana cultivars from different commercial areas (Grande Naine, Prata Anã, Maçã and Pacovan) across several Brazilian regions, and detected the phenotypes of M. javanica J2 (Rm: 1.0 and 1.40) in mixed populations with M. javanica (J3). According to Rajasekhar, Ganguly and Dasgupt (1990)RAJASEKHAR, S. P.; GANGULY, A. K.; DASGUPT, D. R. Effect of some biotic and abiotic factors on the stability of esterase of Meloidogyne incognita and Meloidogyne javanica. Indian Journal of Nematology, 20: 37-43, 1990. and Carneiro, Almeida and Carneiro (1996CARNEIRO, R. M. D. G.; ALMEIDA, M. R. A.; CARNEIRO, R. G. Enzyme phenotypes of Brazilian isolates of Meloidogyne spp. Fundamental and Applied Nematology, 19: 555-560, 1996.), these phenotypes (J2 = Rm: 1.0 and 1.25 and J2 = Rm: 1.0 and 1.40) can be stable or not, being considered atypical patterns, since these populations did not remain stable for a long period in a greenhouse in tomato plants, maintaining only the J3 phenotype after the purification steps. The poor physiological conditions of individual females in banana roots can be considered the reason for the absence of a band in the esterase profile leading to the production of the atypical phenotypes J2 (COFCEWICZ et al., 2004aCOFCEWICZ, E. T. et al. Enzyme phenotype and genetic diversity of root-knot nematode parasitizing Musa in Brazil. Nematology, 6: 85-95, 2004a.). Meloidogyne incognita (I1) identified in the present study, was also observed by Cofcewicz et al. (2004a), but was accompanied by the additional phenotype I2 when they evaluated the occurrence of root-knot nematodes among 25 commercial banana growing areas in Brazil. I2 was absent in this study.

In samples of banana plants, Cofcewicz et al. (2004aCOFCEWICZ, E. T. et al. Enzyme phenotype and genetic diversity of root-knot nematode parasitizing Musa in Brazil. Nematology, 6: 85-95, 2004a.) detected M. javanica, M. incognita, M. arenaria, and Meloidogyne spp. in proportions of 61.7%, 32.2%, 4.3% and 1.8%, respectively, in a study in which samples from 25 areas cultivated with different commercial banana cultivars were evaluated, with a predominance of the cultivars Grande Naine and Pacovan, growing in the main banana producing regions of Brazil, where 20 of them had mixed species populations, and in the other five, single species were identified as M. javanica or M. incognita. In current study, the species described in Cofcewicz et al. (2004a) were present, but the most common species associated with banana triploids and tetraploids were M. javanica (68.26%), M. incognita (64.73%) and M. arenaria (16.81%).

Our evaluation in naturally infested fields demonstrated that the genotypes under consideration are hosts for the root-knot nematodes. However, the suitability of the banana genotypes as root-knot nematode hosts may vary depending on the species of Meloidogyne (CLAUDIO; DAVIDE, 1967CLAUDIO, M. Z.; DAVIDE, R. G. Pathogenicity and identity of root-knot nematodes on five varieties of banana. The Philippine Agriculturist, 51: 241-251, 1967.; DINARDO-MIRANDA; TEIXEIRA, 1996DINARDO-MIRANDA, L. L.; TEIXEIRA, L. A. J. Eficiência hospedeira de oito cultivares de bananeira a fitonematoides. Bragantia, 55: 259-262, 1996.; VILAS BOAS et al., 2002VILAS BOAS et al. Reação de clones de bananeiras (Musa spp.) ao nematoide Meloidogyne incognita (Kofoid & White, 1919) Chitwood, 1949, raça 2. Revista Brasileira de Fruticultura, 24: 690-693, 2002.; COFCEWICZ et al., 2004bCOFCEWICZ, E. T. et al. Reação de cultivares de bananeira a diferentes espécies de nematoides das galhas. Nematologia Brasileira, 28: 11-22, 2004b.; TEIXEIRA, 2007) and the environmental conditions inherent to each location (ARAYA; VARGAS; CHEVES, 1999ARAYA, M.; VARGAS, A.; CHEVES, A. Nematode distribution in roots banana (Musa AAA cv. Valery) in relation to plant height, distance from the pseudostem and soil depth. Nematology, 1: 711-716, 1999.; DAVIDE, 1980; MACSORLEY; PARRADO, 1981MACSORLEY, R.; PARRADO, J. L. Population fluctuations of plant-parasitic nematodes on bananas in Florida. Proceedings of the Florida State Horticultural Society, 94: 321-323, 1981.; KASHAIJA et al., 2004KASHAIJA, I. N. et al. Spatial distribution of roots, nematode populations and root necrosis in highland banana in Uganda. Nematology, 6: 7-12, 2004.; RIBEIRO et al., 2006RIBEIRO, R. C. F. et al. Influência de fatores edáficos sobre a população de M. javanica, Helicotylenchus multicinctus e Radopholus similis em bananeira. In: REUNIÃO INTERNATIONAL DA ASSOCIAÇÃO PARA A COOPERAÇÃO NAS PESQUISAS SOBRE BANANA NO CARIBE E NA AMÉRICA TROPICAL, 17., 2006, Joinvile. Anais... Joinvile: ACORBAT, 2006. p. 813 - 817.). Both species M. javanica and M. incognita were detected, with each species occurring at a rate of up to 100% in certain genotypes. In other genotypes, these two species co -occurred, but in unequal ratios. Likewise, in Palmital (SP), almost all genotypes had isolated infections of M. javanica, but M. incognita was the predominant species only in the cultivar Pacovan and YB 4203 genotype. However, at Embrapa Acre, M. incognita was predominant. Meloidogyne javanica was identified in only three genotypes (Bucanero, Japira and Maçã), while M. arenaria was detected only in the hybrid FHIA 23. One explanation for the variation in the behavior of these species among banana genotypes is that aggressiveness is reported to differ among populations of the same Meloidogyne species (SASSER, HARTMAN, CARTER, 1987SASSER, J. N.; HARTMAN, K. M.; CARTER, C. C. Summary of preliminary crop germplasm evaluations for resistance to root-knot nematodes. 1 ed. Raleigh, NC: Department of Plant Pathology at North Carolina State University, 1987. 88 p.; ROBERTS, 1995ROBERTS, P. A. Conceptual and practical aspects of variability in root-knot nematodes related to host plant resistance. Annual Revue Phytopathology, 33: 199-221, 1995.; BLOK et al., 1997BLOK, V. C. et al. Genetic variation in tropical Meloidogyne spp. as shown by RAPDs. Fundamental and Applied Nematology v. 20, p. 127-133, 1997.). Meloidogyne javanica has been reported as a species with low intraspecific variability. Studies by Cofcewicz et al. (2004aCOFCEWICZ, E. T. et al. Enzyme phenotype and genetic diversity of root-knot nematode parasitizing Musa in Brazil. Nematology, 6: 85-95, 2004a.) with seven M. javanica populations parasitizing banana plants from different regions in Brazil revealed an intraspecific variability of 29.1%, which is still considered low. Even so, it can be hypothesized based on its observed population sizes, that M. javanica populations from Embrapa Semiárido, Embrapa Cerrados, and Palmital, were more aggressive to the banana genotypes than that of Embrapa Acre, whereas the Epagri population exhibited intermediate aggressive behavior. Another factor to be considered in the present study in relation to the behavior of banana genotypes between different locations is the level of natural infestation of these areas by each of the respective nematode species. In some situations, for example, Meloidogyne sp. were observed to be absent in the roots and soil of cultivar FHIA 17 (Embrapa Acre) and genotype PV 7934 (Epagri), while there was non-development of females in the roots of tomato plants that had been inoculated with the suspension of ground roots originating from these genotypes. However, in seemingly similar situations with other cultivars, in which nematodes were not detected in their roots, a large number of female nematodes developed in the roots of tomato plants that had been inoculated with the ground-root slurries of these cultivars; this was the case for the cultivars Grande Naine, Thap Maeo, and others, demonstrating that these nematodes were present, in the form of eggs, in the inoculum. However, for the other locations, the high levels of J2 juveniles in the roots and soil made them readily observable that these banana genotypes are favorable hosts to the root-knot nematodes. Therefore, experiments like this only show the hostability of banana genotypes, and it is not possible to evaluate their resistance or susceptibility to each nematode species.

Among spiral nematodes, H. multicinctus was the one that stood out most in experimental areas, not being detected in Embrapa Semiárido and Embrapa Cerrados experimental areas. An unidentified Helicotylenchus species was detected in Embrapa Cerrados. In Acre, H. multicinctus had already been reported by Cavalcante et al. (2002CAVALCANTE, M. J. B. R. D. et al. Nematoides associados ao amendoim forrageiro e à bananeira no estado do Acre. Fitopatologia Brasileira, 27: 107-107, 2002.) in association with H. dihystera (Cobb, 1893) Sher, 1961 on banana roots (245 specimens.100g-1 roots). In another survey carried out on bananas in Acre, the occurrence (100%) of H. babensae Elmiligy, 1970 was detected (CAVALCANTE; SHARMA; CARES, 2005CAVALCANTE, M. J. B.; SHARMA, R. D.; CARES, J. E. Nematoides associados a genotipos de bananeiras em Rio Branco. Nematologia Brasileira, 29: 91-94, 2005.). According to Costa-Manso et. al. (1994) other species have been reported in association with banana plants in Brazil (H. californicus Sher, 1966, H. cavenessi Sher, 1966, H. crenacauda Sher, 1966, H. erytrinae Zimmermann, 1904 H. flatus Roman, 1965, H. lobus Sher 1966, H. pseudorobustus (Steiner, 1914) Golden, 1956, H. retusus Siddiqi and Brown, 1964 and H. serenus Siddiqi, 1963).

Currently, R. reniformis is not considered a relevant crop pest for banana cultivation, however, it can become an important nematode, due to the increase in its population density in banana rhizosphere. R. reniformis was recovered from soil samples in greater numbers in areas of Embrapa Semiárido, in some soil samples in the Palmital area in São Paulo, and in the rhizosphere soil of the genotype PV 7934 in Embrapa Cerrados. This fact can be explained by the biological nature of the reniform nematode, which completes its life cycle in the soil. It was only observed in the roots of the genotypes BRS Platina and YB 4203 in Embrapa Semiárido and in the genotypes Garantida, Bucanero, FHIA 18, Pacovan, Grande Naine, Prata Anã, YB 4203, Tropical, BRS Platina, PV 9401 and Maçã in Palmital - SP, suggesting this nematode has a greater affinity for these respective banana genotypes. The reniform nematode had previously been reported in the state of Pernambuco in banana roots by Moura (1972MOURA, R. M. Ocorrência em Pernambuco do nematoide Radopholus similis (Cobb) Thorne sobre bananeiras (Musa paradisiaca L.) var. comprida. In: Seminário de Sementes, 3., 1972, Recife. Anais. Recife: Divisão de Produção Vegetal de Recife, 1972. p. 261-262.) and Zem and Lordello (1983ZEM, A. C.; LORDELLO, L. G. E. Estudos sobre hospedeiros de Radopholus similis e Helicotylenchus multicinctus. Nematologia Brasileira, 7: 175-188, 1983.). The results obtained in this study are in agreement with Ritzinger et al. (2007RITZINGER, C. H. S. P. et al. Fitonematoides associados a bananais ‘Pacovan’ sob condição de cultivo irrigado: relação com a produção. Revista Brasileira de Fruticultura, 29: 677-680, 2007.), who detected R. reniformis in a survey of plant-parasitic nematodes in banana plantations located in the irrigated perimeters of the municipalities of Petrolina -PE and Juazeiro-BA, where the authors found a positive correlation between the frequency of R. reniformis and H. multicinctus in roots of the banana cv. Pacovan.

The nematodes found most frequently in banana crops sampled worldwide belong to the genera Helicotylenchus, Meloidogyne and Rotylenchulus (CARLIER; WAELE, D; ESCALANT, 2003CARLIER, J.; WAELE, D.; ESCALANT, J. V. Evaluation of resistance to nematodes. In: VÉZINA, A.; PICQ, C. (Eds.). Global evaluation of Musa germplasm for resistance to Fusarium wilt, Mycosphaerella leaf spot diseases and nematodes. Montpellier, France: INIBAP Technical Guidelines, 2003. v. 7, ch. 4, p. 21-24.). Similar results found in a survey of plant-parasitic nematodes in banana plantations in Brazil reported high frequencies of individuals of these genera (ZEM; lOrDELLO, 1984ZEM, A. C.; LORDELLO, L. G. E. Problemas nematológicos em bananeiras. Anais da Escola Superior de Agricultura Luiz de Queiroz, 41: 93-118, 1984.; NEVES; DIAS; BARBOSA, 2009NEVES, W. S.; DIAS, M. S. C.; BARBOSA, J. G. Flutuação populacional de nematoides em bananais de Minas Gerais e Bahia (anos 2003 a 2008). Nematologia Brasileira, 34: 281-285, 2009.; LIMA et al., 2013LIMA, R. S. et al. Frequencies and population densities of the major phytonematodes associated with banana in the state of Alagoas, Brazil. Nematropica, 43: 186-193, 2013.; VELOZO, 2018VELOZO, A. O. Fitonematoides associados a cultura da bananeira em propriedades rurais do município de Areia - Paraíba. (Monografia de curso de Agronomia). Universidade Federal da Paraíba. Areia, Paraíba. 2018. 35 p.), being specimens of Helicotylenchus the most common among soil samples.

Radopholus similis, the nematode of greatest economic importance for the banana crop, (O’BANNON, 1977O’BANNON, J. H. Worldwide dissemination of Radopholus similis and its importance in crop production. Journal of Nematology, 9: 16-25, 1977.; GOWEN, 1979GOWEN, S. R. Some consideration of problems associated with the nematode pests of banana. Nematropica, 9: 79-91, 1979.; TARTE; PINOCHET, 1981TARTE, R.; PINOCHET, J. Problemas nematológicos del banana: contribuciones recientes a su conocimiento y combate. 1 ed. Panamá: Unión Países Exportadores Banano (UPEB), 1981. 32 p.) was only present at low abundances in this study and only in the experimental areas of Embrapa Acre and Palmital in São Paulo. In Brazil, the species was first reported in banana plantations in the coastal region of São Paulo (CARVALHO, 1959CARVALHO, J. C. O nematoide cavernícola e seu aparecimento em São Paulo. Biológico, 25: 195-198, 1959.), and years later in other Brazilian states by several authors (PEREIRA; FIGUEIREDO JUNIOR; HUSSNI, 1960PEREIRA, H. F., FIGUEIREDO JUNIOR, E. R.; HUSSNI, J. Nematoide cavernícola nos bananais de São Paulo. O Biológico, 26: 27-31, 1960.; SHARMA, 1974aSHARMA, R. D. Nematoide cavernícola atacando a bananeira na Bahia. Ilhéus: Cacau Atualidades, 2: 4 -6, 1974a., b; ZEM, 1978ZEM, A. C.; ALVES, E. J. Nematoides associados a bananeiras no estado do Maranhão. Ciência e Cultura, 30: 13-13, 1978.; ZEM; ALVES, 1978; ZEM; BARREIRA; TEIXEIRA, 1980; ZEM, 1982; HUANG et al., 1982HUANG, C. S. et al. Nematoides fitoparasitos encontrados na Ilha de São Luiz e município de Rosário do estado do Maranhão. In: REUNIÃO BRASILEIRA DE NEMATOLOGIA, 6., 1982, Fortaleza. Anais... Fortaleza: Sociedade Brasileira de Nematologia, 1982. p. 39-39.; ZEM; LORDELLO, 1983, 1984; COSTA-MANSO et al., 1994COSTA-MANSO, E. S. B. G. et al. Catálogo de nematoides fitoparasitos encontrados associados a diferentes tipos de plantas no Brasil. 1 ed., Brasília, DF: Embrapa, 1994. 488 p.). Despite the importance of the species to many banana plantations around the world, studies conducted in Brazil show that R. similis is still sporadic in most growing regions (OLIVEIRA, 2013OLIVEIRA, U. L. C. Fitonematoides associados a bananeiras na região sul e sudoeste da Bahia. 2013. 61f. Dissertação(Mestrado em Produção Vegetal: Área de Concentração em nematologia) -Universidade Estadual de Santa Cruz, Ilheús, Bahia, 2013.). Studies by Cavalcante et al. (2002CAVALCANTE, M. J. B. R. D. et al. Nematoides associados ao amendoim forrageiro e à bananeira no estado do Acre. Fitopatologia Brasileira, 27: 107-107, 2002.) and Cavalcante, Sharma and Cares (2005) in areas planted with different banana cultivars in the state of Acre, did not detect R. similis. According to these author's personal information, the experimental area surveyed in the present study had already been cultivated with banana before the implementation of the current experiment, which may explain the presence of the burrowing nematode in the experimental field at Embrapa Acre.

Other secondary plant-parasitic nematodes of banana plants were also detected in low numbers, such as Criconemoides sp. and Scutellonema sp. Nematodes in the genus Criconemoides have been reported in banana plantations in the state of Acre by Cavalcante, Sharma and Cares (2005CAVALCANTE, M. J. B.; SHARMA, R. D.; CARES, J. E. Nematoides associados a genotipos de bananeiras em Rio Branco. Nematologia Brasileira, 29: 91-94, 2005.) and confirmed by Nogueira et al. (2013NOGUEIRA, S. R. et al. Doenças da Bananeira no Acre. 1. ed. Rio Branco, AC: Embrapa, 2013. 37 p.) in Bonal and Senador Guionard in banana plantation soils. Nematodes of the genera Criconemoides and Scutellonema have also been observed in banana plants (Musa spp., Group AAB) in Nigeria by (SPEIJER; ROTIMI; WAELE, 2001SPEIJER, P. R.; ROTIMI, WAELE, D. D. Plant parasitic nematodes associated with plantain (Musa spp., AAB - group) in Southern Nigeria and their relative importance compared to other biotic constraints. Nematology, 3: 423-436, 2001.). Other banana-related species, as revised by Costa-Manso et al. (1994), with the synonymy of Criconema (C. azani) and Criconemella (C. curvata Raski, 1952, C. onoensis Luc, 1959, C. ornata Raski, 1958, C. peruensiformis (De Grisse, 1967) Luc, 1970 and C. xenoplax Raski, 1952) were reported in Brazil. In Santo Antonio do Amparo (MG), the nematode Criconemella sp. and, in São Vicente Ferrer (PE), the nematode Sculellonema spp. were detected in banana plants by (SOUZA; MAXIMINIANO; CAMPOS, 1999SOUZA, J. T.; MAXIMINIANO, C.; CAMPOS, V. P. Nematoides associados a plantas frutíferas em alguns estados brasileiros. Ciência e Agrotecnologia, 23: 353-357, 1999.). The species Scutellomema magniphasmum Sher, 1965 have been reported to be associated with banana plantations in Malawi in Africa by Saka and Siddiqi (1979SAKA, V. W.; SIDDIQI, M. A. Plant-parasitic nematodes associated with plants in Malawi. Plant Disease Reporter, 63: 945-948, 1979.). Scutellonema brachyurus (Steiner, 1938) Andrássy, 1958 also has been reported in association with banana plants in Brazil (COSTA-MANSO et al., 1994COSTA-MANSO, E. S. B. G. et al. Catálogo de nematoides fitoparasitos encontrados associados a diferentes tipos de plantas no Brasil. 1 ed., Brasília, DF: Embrapa, 1994. 488 p.).

CONCLUSIONS

The nematode genera with the highest frequency and population levels detected in the banana genotypes belong to the genera Meloidogyne, Helicotylenchus and Rotylenchulus. The root-knot nematodes were predominant in all banana genotypes in the experimental areas evaluated. Four esterase phenotypes were characterized for Meloidogyne: M. incognita (Est I1), M. javanica (Est J3 and J2) and M. arenaria (Est A2), predominantly for Meloidogyne javanica (Est J3). In addition to the root-knot nematodes, the spiral nematode (Helicotylenchus multicinctus) and the reniform nematode (Rotylenchulus reniformis) were the most detected in soil samples. Radopholus similis, Scutellonema sp., Criconemoides sp. and Helicotylenchus sp. were plant-parasitic nematodes that showed low frequencies and population levels among banana genotypes.

ACKNOWLEDGEMENTS

The authors thank National Council for Scientific and Technological Development (CNPq) for the scholarship for the senior author, as well as for financial support provided by the grant CNPq Proc. n. 484204/2012-2.

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Publication Dates

  • Publication in this collection
    23 Nov 2020
  • Date of issue
    Oct-Dec 2020

History

  • Received
    31 July 2019
  • Accepted
    08 May 2020
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