Reaction of sugarcane genotypes to root-knot nematode parasitism (Meloidogyne javanica and Meloidogyne incognita)

ABSTRACT

Root-knot nematodes (Meloidogyne spp.) can cause a reduction up to 50% in the production of sugarcane (Saccharum spp.). Genetic resistance is considered an important component in the management of nematodes. Therefore, the aim of this study was to evaluate the susceptibility of 12 sugarcane genotypes when subjected to parasitism by Meloidogyne javanica and Meloidogyne incognita under controlled conditions in a plant growth chamber. Four experiments were carried out in randomized blocks with 12 treatments and four replicates for M. javanica and three replicates for M. incognita. The treatments were the sugarcane genotypes: RB966928 (susceptibility pattern), RB026842, RB036168, RB036145, RB036065, RB966229, RB036066, RB036068, RB046209, RB036163, RB036153, and RB036059. Each repetition consisted of a 2-L pot with previously autoclaved substrate (1:1 of sand and soil), and a pre-sprouted seedling was transplanted. From pure populations of M. javanica and M. incognita, approximately 2,000 eggs and eventual J₂ were inoculated per pot. After 120 days, the final population of nematodes in the root and soil was counted using an optical light microscope and Peters slide, and the reproduction factor (RF) was calculated. Plants that presented RF < 1 were considered resistant, and plants that presented RF > 1 were considered susceptible. Among the 12 genotypes evaluated, 66% were susceptible to parasitism by M. javanica. The genotypes RB046209, RB036163, RB036153, and RB036059 were classified as resistant to M. javanica parasitism. For the species M. incognita, the susceptible genotypes represented 75% of the total, and the resistant genotypes were RB036163, RB036153, and RB036059.

Keywords
Saccharumspp.; nematode; genetic resistance; susceptibility; resistant

INTRODUCTION

Sugarcane (Saccharum spp. L. hybrid) is a semi-perennial monoculture adapted to tropical and subtropical climates (MORAIS et al., 2015). Sugarcane plants cultivated commercially are mostly hybrids resulting from the backcrossing of several Saccharum species, mainly S. officinarum and S. spontaneum (FIGUEIREDO, 2010). They are versatile crops that generate several products and by-products, especially sugar and ethanol (MORAIS et al., 2015).

Currently, Brazil is the largest sugarcane producer in the world, followed by India, China, Thailand, Pakistan, and Mexico (FAO, 2020). With a planted area of 8,127.7 hectares, Brazil produced 572,874.9 tons in the 2022/23 harvest. However, crop production can be affected by environmental weather conditions, such as drought and frost, and by weeds, pests, diseases, among others (CONAB, 2022).

Diseases in the sugarcane crop caused by nematodes are of great importance because they can reduce production by up to 50% in highly susceptible cultivars with high nematode population levels (DINARDO-MIRANDA, 2005). Among the nematodes that affect crop production in Brazil, the root-knot nematodes Meloidogyne javanica (Treub) (Chitwood 1949) and M. incognita (Kofoide & White) (Chitwood 1949) stand out. The average reduction in productivity caused by M. javanica and M. incognita in susceptible cultivars is 20% and 40%, respectively (DINARDO-MIRANDA, 2005).

The genus Meloidogyne comprises the most important phytonematodes in the world (JONES et al., 2013). The characteristic symptoms of nematodes of the genus Meloidogyne are root thickenings called galls. They are formed because of cellular hypertrophy and hyperplasia in the vascular cylinder (JONES et al., 2013; FERRAZ, 2018). However, galls on the sugarcane root system, when formed, are rare and small. They are predominantly found at the tips of roots and are therefore difficult to detect (DIAS-ARIEIRA et al., 2010b; FERRAZ; BROWN, 2016). Other symptoms that can be observed in sugarcane fields are changes in the agronomic characteristics of cultivars, such as internode length, tiller height, and stem thickness (FERRAZ; BROWN, 2016).

Among the methods for phytonematode control in sugarcane, cultural (BERRY et al., 2011; SANTANA-GOMES et al., 2019), biological (CARDOZO; ARAÚJO, 2011; FERREIRA et al., 2017; MAZZUCHELLI et al., 2020), chemical (DINARDO-MIRANDA et al., 2008; DIAS-ARIEIRA et al., 2010a), and genetic resistance (DINARDO-MIRANDA et al., 1995; DIAS-ARIEIRA et al., 2010a; DINARDO-MIRANDA; FRACASSO, 2010; SILVA et al., 2012; SILVA et al., 2016; BELLÉ et al., 2017; THOMAZELLI et al., 2020) stand out. The application of biological and chemical products has shown low efficiency, mainly because the period of action of the product after application is very short compared with the fast life cycle of nematodes (FERREIRA et al., 2017), and the number of nematodes tends to return at high levels after 90 to 120 days after chemical or biological treatment (SILVA et al., 2016). In addition, the semi-perennial characteristic in which the sugarcane field can be grown for several years with little disturbance to the soil facilitates the increase in the nematode population in just two or three cultivation cycles, which makes cultural management difficult and results in a decline in productivity in subsequent harvests (JAYAKUMAR; GANAPATHY, 2020).

The use of resistant cultivars is an efficient, non-polluting, and cost-effective control measure. In Brazil, genotypes were tested for root-knot nematode parasitism resistance in the states of Pernambuco (SILVA et al., 2012; SILVA et al., 2016), São Paulo (DINARDO-MIRANDA et al., 1995; DINARDO-MIRANDA; FRACASSO, 2010; THOMAZELLI et al., 2020), Paraná (DIAS-ARIEIRA et al., 2010a), and Rio Grande do Sul (BELLÉ et al., 2017), demonstrating differences in the resistance/susceptibility of the genotypes in relation to the root-knot nematode.

The Inter-University Network for the Development of the Sugar-Energy Sector (RIDESA) breeding program plays an important role in the development of sugarcane genotypes aimed at increasing productivity, in addition to the search for disease-resistant genotypes (DAROS et al., 2016). Testing genotypes for nematode parasitism resistance is a complementary and indispensable strategy for this program. Therefore, the objective of this study was to evaluate the reaction of 12 sugarcane genotypes from RIDESA to the parasitism of M. javanica and M. incognita.

MATERIAL AND METHODS

This study consisted of four experiments. The first and second experiments (E1 and E2) were carried out from September 2020 to January 2021, and the third and fourth experiments (E3 and E4), from November 2020 to March 2021. The experiments were conducted in a plant growth chamber (Fitotron, Instalafrio) under controlled conditions (28°C ± 2), at the Plant Science and Plant Protection, Universidade Federal do Paraná (UFPR). RIDESA produced the pre-sprouted seedlings in Paranavaí, PR, Brazil, at the RIDESA/UFPR experimental station.

The experiments were conducted in a randomized block design for operational reasons in the evaluation of the experiments, with 12 treatments consisting of the following sugarcane genotypes: RB966928, RB026842, RB036168, RB036145, RB036065, RB966229, RB036066, RB036068, RB046209, RB036163, RB036153, and RB036059. Based on the results obtained from DIAS-ARIEIRA et al. (2010b) and BELLÉ et al. (2017), genotype RB966928 was considered as the susceptibility standard.

Experiments E1 and E3 evaluated the resistance of cultivars to M. javanica parasitism and had four replications. Experiments E2 and E4 evaluated the resistance of the genotypes to the parasitism of M. incognita with three replications. Each replicate consisted of a 2-L vase with soil previously autoclaved at 120° C for 1 hour, in a 1:1 proportion of sand and soil.

Pre-sprouted 80-day-old seedlings were transplanted into pots. After seven days of transplanting, they were fertilized with 50-120-100 kg·ha^-1 (N-P-K), as recommended by PAULETTI and MOTTA (2019), for the average expected productivity of plant cane, thus totaling 0.11 g of urea, 0.29 g supertriple, and 0.17 g KCl per pot. Twenty days after transplantation, each pot was inoculated with approximately 2,000 eggs and any J2 from the pure population of M. javanica and M. incognita, which were produced in tomato plants of the Santa Clara cultivar kept in a greenhouse for 60 days.

The suspensions of M. javanica and M. incognita specimens were obtained using the centrifugal flotation technique in sucrose solution (COOLEN; D’HERDE, 1972). The suspension was calibrated and applied by depositing 1 mL of the suspension containing the eggs and any J2 of M. javanica and M. incognita in three equidistant holes around the plants with a depth of 4 cm previously made with the aid of a Falcon tube. To test the viability of the inoculum, the same amount was inoculated into 25-day- old ‘Santa Clara’ tomato seedlings susceptible to Meloidogyne. Four replicates were performed for each species.

One hundred and 20 days after inoculation, the plants were removed from the pots, and the roots were collected, washed, and placed on absorbent paper to remove excess water. They were weighed and cut into fractions of 2 to 5 cm. A 5-g sample taken from random spots of clean roots was separated and destined for nematode extraction. Root fragments were processed in a blender and floated in sucrose (COOLEN; D’HERDE, 1972). When preparing the soil for extraction, the contents of the pots were poured into a tray, homogenized, and 50 cm³ of the soil was removed at random spots. The aliquot was subjected to extraction following JENKINS’ (1964) method.

Using a Peters chamber, the number of eggs and J2 in the roots and soil was counted under an optical light microscope at 40x magnification. To obtain the final population, the nematodes counted in the 5-g root suspension were multiplied by the total mass of the root system and added to those in the soil. The reproduction factor (RF) was evaluated using the initial and final population ratio (RF = final population/initial population). The reactions of the sugarcane genotypes were classified according to the RF value, considering resistant plants that presented RF < 1 and susceptible plants with RF > 1 (OOSTENBRINK, 1966).

The data from the experiments were submitted to tests of normality and homogeneity of variance, in a 12 × 2-factorial scheme, with the first factor being the genotypes and the second factor being the experiment time (repetition) for each evaluated species. Analysis of variance (ANOVA) was performed, followed by the Scott-Knott’s test at a 5% probability level using R software version 4.0.4 (R Core Team).

RESULTS

The inoculum was proven viable, presenting in tomato plants an average RF of 3.62 (standard deviation = 1.4) for M. javanica and 6.61 (standard deviation = 3.2) for M. incognita.

There was no significant interaction between the factors genotypes and repetition of experiments, and there was no effect of experiment time. The two experiments for each species of root-knot nematodes were grouped.

Regarding M. javanica parasitism, genotypes RB966928, RB026842, RB036168, RB036145, RB036065, RB966229, RB036066, and RB036068 showed susceptibility (RF > 1). On the other hand, the RB046209, RB036163, RB036153, and RB036059 genotypes were classified as resistant (RF < 1) (Table 1). The RB966928 genotype, used as a susceptibility standard, showed the highest reproduction factor for M. javanica, with RF = 3.46, whereas the RB046209 genotype presented the lowest reproduction factor (0.49) (Table 1).

Table 1
Final population and reproduction factor of Meloidogyne javanica and Meloidogyne incognita and reaction of the different sugarcane genotypes to nematodes

Genotype	Meloidogyne javanica				Meloidogyne incognita
	FP	RF	R#		FP	RF	R
RB966928	6,920.16* a	3.46***	S		3,746.15**** a	1.87	S
RB026842	5,627.87** a	2.81	S		6,511.57 a	3.25	S
RB036168	4,938.66 a	2.46	S		3,027.38 a	1.51	S
RB036145	4,278.24 a	2.13	S		3,453.07 a	1.72	S
RB036065	3,675.00 a	1.83	S		2,154.33 a	1.07	S
RB036229	3,649.57 a	1.82	S		3,782.55 a	1.89	S
RB036066	2,808.27 b	1.40	S		2,379.31 a	1.18	S
RB036068	2,377.95 b	1.18	S		2,058.09 a	1.02	S
RB046209	996.64 b	0.49	R		2,432.44 a	1.21	S
RB036163	1,873.35 b	0.93	R		1,913.44 a	0.95	R
RB036153	1,905.58 b	0.95	R		1,506.14 b	0.75	R
RB036059	1,252.75 b	0.62	R		472.72 b	0.23	R
CV	69.96%				93.84%

• ^*
  Means followed by the same line do not differ in the column by the Scott-Knott’s test at 5%;
• ^**
  untransformed data;
• ^***
  average of four repetitions;
• ^****
  average of three repetitions;
• coefficient of variation; FP: final population; RF: reproduction factor = final population/initial population (Pi = 2,000); R^#: reaction; S: susceptibility (RF > 1); R: resistance (RF < 1).

Regarding M. incognita parasitism, nine of the genotypes (RB966928, RB026842, RB036168, RB036145, RB036065, RB966229, RB036066, RB036068 and RB046209) tested showed susceptibility (RF > 1). Genotypes RB036163, RB036153, and RB036059 were classified as resistant (RF < 1) (Table 1). Genotype RB026842 showed the highest RF (3.25), and genotype RB036059 had the lowest RF value (0.23).

DISCUSSION

In this study, variation in the reaction of 12 sugarcane genotypes was observed when subjected to parasitism by M. javanica and M. incognita. These results are essential to help direct the choice of genotype to be used in the management of sugarcane in areas infested by root-knot nematodes.

Meloidogyne javanica is a widely spread species in sugarcane areas. In northwest Paraná, it is the predominant species, with an incidence of 46% in the areas sampled by SEVERINO et al. (2010). In a survey in the three mesoregions of the state of Paraná, in 2020, Meloidogyne spp. was frequent in 70% of the root samples (MARTINHA et al., 2022). In addition, NOVARETTI (1995) found that eight individuals per gram of roots indicate a high population density and can cause damage to the crop. In a study carried out in Paraná, in which the reaction of sugarcane genotypes with the acronyms RB and CTC to the parasitism of M. javanica and M. incognita was tested. DIAS-ARIEIRA et al. (2010b) observed that the evaluated genotypes showed susceptibility to both species. As in this study, the species M. javanica showed higher RF values.

The RB046209, RB036163, RB036153, and RB036059 genotypes tested in this study showed promising results regarding resistance to M. javanica. However, it is important to emphasize that this behavior can vary in the field. For example, in experiments carried out in different regions with variation in temperature, humidity, and soil type, DINARDO-MIRANDA et al. (2019) found that the reproduction and development of nematodes are directly affected by temperature, and soil moisture, which also interfere with dormancy, diapause, and the nematode life cycle.

Another experiment by DINARDO-MIRANDA et al. (1995) tested 18 genotypes in areas naturally infested by M. javanica and observed that all provided reproduction of the nematode. However, 12 genotypes were considered susceptible. Different reproduction rates may, in part, be associated with the genetic factor of the host, conferring resistance or susceptibility, as well as with the genetic characteristics of nematode populations. Nematodes that reproduce by mitotic parthenogenesis, such as M. javanica, can adapt quickly and overcome host resistance (CASTAGNONE-SERENO, 2006). This was observed in studies by BELLÉ et al. (2017), who evaluated the reaction of RB group genotypes to M. javanica and found that all genetic materials tested were susceptible to the root-knot nematode. As in the present study, the RB966928 genotype has been identified in several studies as a good host for M. javanica (BELLÉ et al., 2017; DIAS-ARIEIRA et al., 2010b; DINARDO-MIRANDA et al., 2019).

Regarding the M. incognita species, the RB036163, RB036153, and RB036059 genotypes showed resistant behavior. In Brazil, in addition to these genotypes, the CTC-17 genotype and RB041443 have already been reported to be resistant to M. incognita (DIAS-ARIEIRA et al., 2010b). However, SILVA et al. (2016), when testing 23 genotypes, found that all were susceptible to M. incognita.

Research carried out in other countries has proven the susceptibility of sugarcane genotypes to root-knot nematodes. In Nigeria, SALAWU (1992) evaluated the reaction of 12 genotypes to M. incognita and observed that all materials behaved as highly susceptible, even those in which shoot and root masses were high.

DIAS-ARIEIRA et al. (2010a) point out that, although the evaluation method by the RF presents some limitations, it is the most viable for use in sugarcane, since in this host the formation of visible galls does not always occur, which makes it difficult to use scales based on the number of galls or egg mass.

This study demonstrated the presence of resistant genotypes to M. javanica and M. incognita. Genotypes with susceptible reactions can be used preferentially in areas without the presence of the nematode. These results are essential to help both genetic improvement programs in the development of genotypes and to direct the use of these genotypes in areas infested or not with root-knot nematodes.

CONCLUSIONS

Among the 12 genotypes evaluated, 34% were resistant to M. javanica parasitism, whereas the M. incognita species resistant genotypes represented 25% of the total.

Genotypes RB036163, RB036153, and RB036059 showed resistant behavior in both species.

ACKNOWLEDGEMENTS

We thank Rede Interuniversitária para o Desenvolvimento do Setor Sucroenergético (RIDESA) for supplying the plant material and the Programa de Melhoramento Genético da Cana-de-açúcar at Universidade Federal do Paraná for providing the structure for conducting the experiments.

• Peer Review History: Double-blind Peer Review.

• FUNDING

  Coordenação de Aperfeiçoamento de Pessoal de Nível Superior
  https://doi.org/10.13039/501100002322
  Finance Code: 001
  Conselho Nacional de Desenvolvimento Científico e Tecnológico
  https://doi.org/10.13039/501100003593
  Grant No: 30664/72021-4

• ETHICAL APPROVAL

  Not applicable.

AVAILABILITY OF DATA AND MATERIAL

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

REFERENCES

• BELLÉ, C.; KULCZYNSKI, S.M.; KUHN, P.R.; DONINI, L.P.; GOMES, C.B. Reaction of sugarcane genotypes to parasitism of Meloidogyne javanica and Pratylenchus zeae Revista Caatinga, v.30, n.2, p.530-535, 2017. https://doi.org/10.1590/1983-21252017v30n229rc
  » https://doi.org/10.1590/1983-21252017v30n229rc
• BERRY, S.D.; RHODES, R.; FOSTER, J.; RISEDE, J.-M.; ANTWERPRN, R.V. The effect of cover crops on plant parasitic nematodes of sugarcane. International Journal of Pest Management, v.57, n.4, p.363-375, 2011. https://doi.org/10.1080/09670874.2011.621984
  » https://doi.org/10.1080/09670874.2011.621984
• CARDOZO, R.B.; ARAÚJO, F.F. Multiplicação de Bacillus subtilis em vinhaça e viabilidade no controle da meloidoginose, em cana-de-açúcar. Revista Brasileira de Engenharia Agrícola e Ambiental, v.15, n.12, p.1283-1288, 2011.
• CASTAGNONE-SERENO, P. Genetic variability and adaptive evolution in parthenogenetic root-knot nematodes. Heredity, v.96, n.4, p.282-289, 2006. https://doi.org/10.1038/sj.hdy.6800794
  » https://doi.org/10.1038/sj.hdy.6800794
• CONAB - Companhia Nacional de Abastecimento. Acompanhamento da safra brasileira Cana-de-açúcar, safra 2022/23. Brasília: CONAB, 2022. Available from: http://www.conab.gov.br Access on: Nov. 9, 2022.
  » http://www.conab.gov.br
• COOLEN, W.A.; D’HERDE, C.J. A method for the quantitative extraction of nematodes from plant tissue Ghent: State Nematology and Entomology Research Station, 1972.
• DAROS, E.; ZAMBON, J.L.C.; OLIVEIRA, R.A. Programa de Melhoramento Genético da Cana-de-Açúcar da UFPR: 25 anos de pesquisa Curitiba: UFPR, 2016.
• DIAS-ARIEIRA, C.R.; SANTANA, S.M.; ARIEIRA, J.O.; RIBEIRO, R.C.F.; VOLK, L.B.S. Efeito do carbofurano na população de nematoides e no rendimento da cana-de-açúcar em solos arenosos do Paraná. Nematologia Brasileira, v.34, n.2, p.118-122, 2010a.
• DIAS-ARIEIRA, C.R.; SANTOS, D.A.; SOUTO, E.R.; BIELA, F.; CHIAMOLERA, F.M.; CUNHA, T.P.L.; SANTANA, S.M.; PUERARI, H.H. Reação de variedades de cana-de-açúcar aos nematoides-das-galhas. Nematologia Brasileira, v.34, n.4, 2010b.
• DINARDO-MIRANDA, L.L. Manejo de fitonematoides em cana-de-açúcar. Jornal Cana, v.5, p.64-67, 2005.
• DINARDO-MIRANDA, L.L.; FRACASSO, J.V. Spatial and temporal variability of plant-parasitic nematodes population in sugarcane. Bragantia, v.69, p.39-52, 2010. Suppl. https://doi.org/10.1590/S0006-87052010000500006
  » https://doi.org/10.1590/S0006-87052010000500006
• DINARDO-MIRANDA, L.L.; FRACASSO, J.V.; MIRANDA, I.D. Damage caused by Meloidogyne javanica and Pratylenchus zeae to sugarcane cultivars. Summa Phytopathologica, v.45, n.2, p.146-156, 2019. https://doi.org/10.1590/0100-5405/187782
  » https://doi.org/10.1590/0100-5405/187782
• DINARDO-MIRANDA, L.L.; NOVAETTI, W.R.T.; MOELLI, J.L.; NELLI, E.J. Comportamento de variedade de cana-de-açúcar em relação a Meloidogyne javanica em condições de campo. Nematologia Brasileira, v.19, p.60-66, 1995.
• DINARDO-MIRANDA, L.L.; PIVETTA, J.P.; FRACASSO, J.V. Influência da época de aplicação de nematicidas em soqueiras sobre as populações de nematoides e a produtividade da cana-de-açúcar. Bragantia, v.67, n.1, p.179-190, 2008. https://doi.org/10.1590/S0006-87052008000100022
  » https://doi.org/10.1590/S0006-87052008000100022
• FAO - Food and Agriculture Organization. Base de dados Faostat Agriculture FAO, 2020. Available from: http://www.fao.org/faostat/en/#rankings/countries_by_commodity Access on: Oct. 16, 2021.
  » http://www.fao.org/faostat/en/#rankings/countries_by_commodity
• FERRAZ, L.C.C.B. Nematoides. In: AMORIM, L.; REZENDE, J.A.M.; BERGAMIN FILHO, A. (eds.). Manual de Fitopatologia: Princípios e Conceitos 5th. Ed. São Paulo: Agronomica Ceres, 2018. v.1, chap.13, p.195-211.
• FERRAZ, L.C.C.B.; BROWN, D.J.F. Nematologia de plantas: fundamentos e importância Manaus: Norma, 2016.
• FERREIRA, R.J., SOARES, P.L.M.; CARVALHO, R.B.; SANTOS, J.M.; BATISTA, E.S.P.; BARBOSA, J.C. Bacillus species for controlling root-knot nematodes in development in sugar cane. Nematropica, v.47, n.2, p.106-113, 2017.
• FIGUEIREDO, P. Breve história da Cana-de-açúcar e do papel do Instituto Agronômico no seu estabelecimento no Brasil. In: DINARDO-MIRANDA, L.L.; VASCONCELOS, A.C.M.; LANDELL, M.G.A. (eds.). Cana-de-açúcar Campinas: Instituto Agronômico, 2010. p.31-45.
• JAYAKUMAR, J.; GANAPATHY, S. Resistance of sugarcane clones against root knot nematode, Meloidogyne incognita and lesion nematode, Pratylenchus zeae Journal of Entomology and Zoology Studies, v.8, n.4, p.45-48, 2020.
• JENKINS, W.R.A. Rapid Centrifugal: Flotation technique for separating nematodes from soil. Plant Disease Reporter, v.48, n.9, p.692, 1964. Available from: https://babel.hathitrust.org/cgi/pt?id=chi.098078550&view=1up&seq=186. Access on Oct. 18, 2020
  » https://babel.hathitrust.org/cgi/pt?id=chi.098078550&view=1up&seq=186
• JONES, J.T.; HAEGEMAN, A.; DANCHIN, E.G.J.; GAUR, H.S.; HELDER, J.; JONES, M.G.K.; KIKUCHI, T.; MANZANILLA-LÓPEZ, R.; PALOMARES-RIUS, J.E.; WESEMAEL, W.M.L.; PERRY, R.N. Top 10 plant-parasitic nematodes in molecular plant pathology. Molecular Plant Pathology, v.14, n.9, p.946-961, 2013. https://doi.org/10.1111/mpp.12057
  » https://doi.org/10.1111/mpp.12057
• MARTINHA, D.D.; SILVA, M.C.C.; MACEDA, A.; HAHN, M.H.; CALEGARIO, R.F.; RUARO, L.; OLIVEIRA, R.A.; DUARTE, H.S.S. Survey of nematodes associated with sugarcane in the State of Paraná. Arquivos do Instituto Biológico, v.89, e00332021, 2022. https://doi.org/10.1590/1808-1657000332021
  » https://doi.org/10.1590/1808-1657000332021
• MAZZUCHELLI, R.C.L.; MAZZUCHELLI, E.H.L.; ARAUJO, F.F. Efficiency of Bacillus subtilis for root-knot and lesion nematodes management in sugarcane. Biological Control, v.143, 104185, 2020. https://doi.org/10.1016/j.biocontrol.2020.104185
  » https://doi.org/10.1016/j.biocontrol.2020.104185
• MORAIS, L.K.; CURSI, D.E.; SANTOS, J.M.; SAMPAIO, M.; CÂMARA, T.M.M.; SILVA, P.A.E.; BARBOSA, G.V.; HOFFMANN, H.P.; CHAPOLA, R.G.; JÚNIOR, A.R.F.; GAZAFFI, R. Melhoramento genético da cana-de-açúcar Brazil: Embrapa Tabuleiros Costeiros, 2015. 38p. Available from: https://ainfo.cnptia.embrapa.br/digital/bitstream/item/142119/1/Doc-200.pdf Access on Oct. 18, 2021.
  » https://ainfo.cnptia.embrapa.br/digital/bitstream/item/142119/1/Doc-200.pdf
• NOVARETTI, W.R.T. Pathogenicity and control of sugarcane nematodes in Brazil. Nematropica, v.25, p.92-99, 1995.
• OOSTENBRINK, R. Major characteristics of the relation between nematodes and plants. Mededeelingen der Landbouw-Hoogeschool, Wageningen, v.66, n.4, p.1-46, 1966.
• PAULETTI, V.; MOTTA, A.C.V. (Eds.). Manual de adubação e calagem para o estado do Paraná 2nd. Ed. Curitiba: Cubo, 2019. v.1.
• SALAWU, E.O. Effect of Meloidogyne incognita and Heterodera sacharia singly and combined on the growth of sugarcane. Nematology Mediterranea, v.20, p.187-188, 1992.
• SANTANA-GOMES, S.M., DIAS-ARIEIRA, C.R.; BIELA, F.; RAGAZZI, M.; BALDISERA, S.S.; SCHWENGBER, R.P. Planting different crops in succession to manage Pratylenchus zeae in sugarcane. Nematropica, v.49, n.1, p.63-70, 2019.
• SEVERINO, J.J.; DIAS-ARIEIRA, C.R.; TESSMANN, D.J. Nematodes associated with sugarcane in sandy soils in Paraná, Brazil. Nematropica, v.40, n.1, p.111-119, 2010.
• SILVA, A.P.; PEDROSA, E.M.R.; CHAVES, A.; MARANHÃO, S.R.V.L.; GUIMARÃES, L.M.P.; ROLIM, M.M. Reação de variedades de cana-de-açúcar ao parasitismo de Meloidogyne incognita e M. enterolobii Revista Brasileira de Ciências Agrárias, v.7, p.814-819, 2012. Suppl. Available from: http://www.agraria.pro.br/ojs32/index.php/RBCA/article/view/v7isa2276/914 Access on Oct. 18, 2021
  » http://www.agraria.pro.br/ojs32/index.php/RBCA/article/view/v7isa2276/914
• SILVA, M.S.; BANDEIRA, A.A.; MARANHÃO, S.R.V.L.; CARVALHO, R.M.; PEDROSA, E.M.R. Comportamento de genótipos RB de cana-de-açúcar ao parasitismo dos nematoides das galhas. Revista Brasileira de Ciências Agrárias, v.11, n.2, p.73-79, 2016. https://doi.org/10.5039/agraria.v11i2a5368
  » https://doi.org/10.5039/agraria.v11i2a5368
• THOMAZELLI, G.S.; VIDAL, R.L.; VIZENTINI, L.R.; NASCIMENTO, D.D.; SOARES, R.S.; MAMMANA, A.F.; FERREIRA, R.J.; SOARES, P.L.M. Immunity of sugarcane cultivars to Meloidogyne enterolobii Bioscience Journal, Uberlândia, v.36, n.6, p.1984-1989, 2020. https://doi.org/10.14393/BJ-v36n6a2020-47972
  » https://doi.org/10.14393/BJ-v36n6a2020-47972

Edited by

Associate Editor: Silvia Galleti https://orcid.org/0000-0002-0745-5716

Publication Dates

• Publication in this collection
  10 Nov 2023
• Date of issue
  2023

History

• Received
  27 Dec 2022
• Accepted
  29 Aug 2023