Clonal Arabica coffee resistant to Meloidogyne paranaensis and damage threshold on plants development

Bárbhara Joana dos Reis Fatobene Wallace Gonçalves Claudio Marcelo Gonçalves Oliveira Oliveiro Guerreiro FilhoAbout the authors

ABSTRACT:

Plants of Coffea arabica Icatu IAC 925 germplasm show resistance to Meloidogyne paranaensis under field conditions, but with variable rates of segregation. One mother plant, IAC 3, of Icatu IAC 925 was evaluated under controlled conditions through the reaction of its clones, obtained by somatic embryogenesis. Reproduction of nematodes in clones were compared with an open-pollinated progeny from the same mother plant, C. arabica cultivar Mundo Novo IAC 515-20, susceptible to nematodes, and Clone IAC 1, also susceptible and obtained by somatic embryogenesis. Open-pollinated progeny showed segregation to resistance and was classified as susceptible according to the reproduction factor. The average number of nematodes (eggs and J2) per gram of roots in clones was eight fold lower than that of open-pollinated progeny, and 51 fold lower than Mundo Novo IAC 515-20. Based on Seinhorst model, IAC 3 clone showed a tolerance limit of 7.7 nematodes per cm3 of soil, while in Mundo Novo the tolerance limit was 3.9 nematodes per cm3 of soil. These results revealed that clonal Arabica coffee nematode-resistant trees represent an alternative to the time consuming and expensive process inherent to conventional breeding strategies.

Keywords:
root-knot nematodes; resistant variety; somatic embryogenesis

Introduction

Root-knot nematodes (RKN) are a serious threat to coffee production worldwide and Meloidogyne paranaensisCarneiro et al. (1996)Carneiro, R.M.D.G.; Carneiro R.G.; Abrantes, M.O.; Santos, M.S.N.A.; Almeida, M.R. A. 1996. Meloidogyne paranaensis n. sp. (Nemata: Meloidogynidae), a root-knot nematode parasitizing coffee in Brazil. Journal of Nematology 28: 177-189. stands out among coffee parasitic species due to its aggressiveness and the losses caused to coffee plantation in Brazil, Guatemala, Hawaii and Mexico (Carneiro et al., 2004Carneiro, R.M.D.G.; Tigano, M.S.; Randig, O.; Almeida, M.R.A.; Sarah, J.L. 2004. Identification, characterization and diversity of Meloidogyne spp. (Tylenchida, Heteroderidae) on coffee from Brazil, Central America and Hawaii. Nematology 6: 287-298.; Lopez-Lima et al., 2014Lopez-Lima, D.; Sánchez-Nava, P.; Carrion, G.; Monteros, A.E.; Villain, L. 2014. Corky-root symptoms for coffee in central Veracruz are linked to the root-knot nematode Meloidogyne paranaensis, a new report for Mexico. European Journal of Plant Pathology 141: 623-629.; Villain et al., 2013Villain, L.; Sarah, J.L.; Hernández, A.; Bertrand, B.; Anthony, F.; Lashermes, P.; Charmetant, P.; Anzueto, F.; Carneiro, R.M.D.G. 2013. Diversity of root-knot nematodes parasiting coffee in Central America. Nematropica 43: 194-206.).

Except for IPR 100 (Sera et al., 2017Sera, T.; Sera, G.H.; Fazuoli, L.C.; Machado, A.C.Z.; Ito, D.S.; Shigueoka, L.H.; Silva, S.A. 2017. IPR 100: rustic dwarf Arabica coffee cultivar with resistance to nematodes Meloidogyne paranaensis and M. incognita. Crop Breeding and Applied Biotechnology 17: 175-179.) and IPR 106 (Ito el al., 2008Ito, D.S.; Sera, G.H.; Sera, T.; Santiago, D.C.; Kanayama, F.S.; Del Grossi, L. 2008. Progenies of coffee with resistance to nematodes MeloidogyneParanaensis and Meloidogyne Incognita race 2. Coffee Science 3: 156-163 (in Portuguese, with abstract in English).), most Coffea arabica L. cultivars are highly susceptible to M. paranaensis. Genetic resistance is the most effective method to cultivate coffee in infested soils (Bertrand and Anthony, 2008Bertrand, B.; Anthony, F. 2008. Genetics of resistance to root-knot nematodes (Meloidogyne spp.) and breeding. p. 165-190. In: Souza, R.M., ed. Plant-parasitic nematodes of coffee. APS Press, St. Paul, MN, USA.). Sources of resistance were identified in C. canephora Pierre ex A. Froehner (Bertrand et al., 2000Bertrand, B.; Peña Durán, M.X.; Anzueto, F.; Cilas, C.; Etienne, H.; Anthony, F.; Eskes, A.B. 2000. Genetic study of Coffea canephora coffee tree resistance to Meloidogyne incognita nematodes in Guatemala and Meloidogyne sp. nematodes in El Salvador for selection of rootstock varieties in Central America. Euphytica 113: 79-86.; Sera et al., 2006Sera, G.H.; Sera, T.; Azevedo, J.A.; Mata, J.S.; Ribeiro Filho, C.; Doi, D.S.; Ito, D.S. Fonseca, I.C.B. 2006. Robusta coffee rootstocks resistants to Meloidogyne paranaensis and M. incognita races 1 and 2. Semina: Ciências Agrárias 27: 171-184.), in wild Ethiopian C. arabica accessions (Anzueto et al., 2001Anzueto, F.; Bertrand, B.; Sarah, J.L.; Eskes, A.B.; Decasy, B. 2001. Resistance to Meloidogyne incognita in Ethiopian Coffea arabica accessions. Euphytica 118: 1-8.; Boisseau et al., 2009Boisseau, M.; Aribi, J.; Sousa, F.R.; Carneiro, R.M.D.G.; Anthony, F. 2009. Resistance to Meloidogyne paranaensis in wild Coffea arabica. Tropical Plant Pathology 34: 38-41.; Fatobene et al., 2017Fatobene, B.J.R.; Andrade, V.T.; Aloise, G.S.; Silvarolla, M.B.; Gonçalves, W.; Guerreiro Filho, O. 2017. Wild Coffea arabica resistant to Meloidogyne paranaensis and genetic parameters for resistance. Euphytica 213: 1-9.), and in C. arabica germplasms derived from introgression of C. canephora genes, such as Timor Hybrid (Bertrand et al., 2001Bertrand, B.; Anthony, F.; Lashermes, P. 2001. Breeding for resistance to Meloidogyne exigua in Coffea arabica by introgression of resistance genes of Coffea canephora. Plant Pathology 50: 637-643.; Salgado et al., 2014Salgado, S.M.L.; Rezende, J.C.; Nunes, J.A.R. 2014. Selection of coffee progenies for resistance to nematode Meloidogyne paranaensis in infested area. Crop Breeding and Applied Biotechnology 14: 94-101.) and in Icatu (Campos and Villain, 2005Campos, V.P.; Villain, L. 2005. Nematode parasites of coffee, cocoa and tea. p. 529-579. In: Luc, M.; Sikora, R.A.; Bridge, J., eds. Plant parasitic nematodes in subtropical and tropical agriculture. CAB International, Wallingford, UK.).

Icatu germplasm results from interspecific hybridization between C. canephora and C. arabica cultivar Bourbon Vermelho. Some plants of this germplasm were resistant to M. paranaensis in our field experiments. Icatu 925 is one of the most promising materials from the plant H4782-7-925. Despite the good performance of plants when compared with C. arabica cultivars, the interspecific origin of Icatu results in resistance segregation in progenies due higher cross-pollination rates in some individuals (Carvalho et al., 1983Carvalho, A.; Costa, W.M.; Fazuoli, L.C. 1983. Self-compatibility, yield, peaberry seed an abnormal seedlings In Icatu coffee populations. Bragantia 42: 157-169 (in Portuguese, with abstract in English).).

Genetic improvement of coffee through traditional methods is hampered because C. arabica is an alloteraploid and perennial species. Thus, clonal propagation of heterozygous genotypes of C. arabica represents an alternative for large-scale multiplication of plants that segregate for the characteristic of interest. Somatic embryogenesis is a valuable alternative to propagate high yielding F1 hybrids (Bertrand et al., 2011Bertrand, B.; Alpizar, E.; Lara, L.; SantaCreo, R.; Hidalgo, M.; Quijano, J.M.; Montagnon, C.; Georget, F.; Etienne, H. 2011. Performance of Coffea arabica F1 hybrids in agroforestry and full-sun cropping systems in comparison with American pure line cultivars. Euphytica 181: 147-158.) and plants resistant to leaf miner Leucoptera coffeella Guérin-Méneville and leaf rust Hemileia vastatrix Berkeley and Broome (Andreazi et al., 2015Andreazi, E.; Sera, G.H.; Faria, R.T.; Sera, T.; Shigueoka, L.H.; Carvalho, F.G.; Carducci, F.C.; Chamlet, D. 2015. Desempenho de híbridos F1 de café arábica com resistência simultânea a ferrugem, mancha aureolada e bicho mineiro. Coffee Science 10: 375-382 (in Portuguese).; Maciel, 2016Maciel, A.L.R.; Rodrigues, F.A.; Pasqual, M.; Carvalho, C.H.S. 2016. Large-scale, high-efficiency production of coffee somatic embryos. Crop Breeding and Applied Biotechnology 16: 102-107.; Mendonça et al., 2016Mendonça, A.P.; Nonato, J.V.A.; Andrade, V.T.; Fatobene, B.J.R.; Braghini, M.T.; Prela-Pantano, A.; Guerreiro Filho, O. 2016. Coffea arabica clones resistant to coffee leaf miner. Crop Breeding and Applied Biotechnology 16: 42-47.).

In this work, we compare M. paranaensis reproduction in clones and sexual progenies of IAC 3, a coffee plant of Icatu IAC 925, as subsidy for the development of a clonal cultivar. We also investigated the effect of initial population levels of M. paranaensis on vegetative growth of IAC 3 and on susceptible control Mundo Novo 515-20.

Materials and Methods

Resistance assessment in greenhouse conditions

The plant IAC 3, of Icatu IAC 925, was selected as mother plant to produce clonal seedlings because it is resistant to M. paranaensis, highly productive and vigorous in infested fields. Clonal seedlings of IAC 3 were obtained via somatic embryogenesis and sexual progenies were obtained by seeds (open pollination). Two susceptible controls were used: C. arabica cultivar Mundo Novo IAC 515-20, obtained from seeds, and Clone IAC 1, an F1 hybrid between the cultivars Icatu Vermelho IAC 4045 and Obatã IAC 1669-20, also propagated by somatic embryogenesis. Clone IAC 1, resistant to the coffee leaf rust and susceptible to M. paranaensis was included to assess the possible effects of somatic embryogenesis in root development, affecting the measurement of nematodes reproduction.

Seedlings obtained by cloning and seeds with two pairs of leaves were transplanted to plastic pots of 500 mL containing a sterile mixture of sand and soil (1:1) fertilized with simple superphosphate and with a controlled release complex fertilizer (NPK 16-8-12). The soil was supplied with amounts of nutrients equivalent to 0.429 kg per m3 of N, 0.567 kg per m3 of P and 0.498 kg per m3 of K.

The identification of M. paranaensis population, collected in Cássia dos Coqueiros, São Paulo State, Brazil, was performed by esterase phenotypes. Afterward, the nematodes were multiplied in pots containing susceptible C. arabica cultivar Mundo Novo IAC 515-20 and susceptible tomato Solanum lycopersicum L. cultivar Santa Cruz.

Inoculums were obtained according to Hussey and Baker (1973)Hussey, R.S.; Barker, K.R. 1973. A comparison of methods of collecting inocula of Meloidogyne spp. including a new technique. Plant Disease Report 57: 1025-1028.. Seedlings of four to six pair of leaves were inoculated with approximately 5,000 eggs and J2 per plant Experiment was arranged in a completely randomized design with 20 replicates and single-plant plots.

Damage to the root systems was evaluated 135 days after inoculation through the damage index (DI) and reproduction factor (RF). DI is scored according to a modified scale of Hussey and Jansen (2002)Hussey, R.S.; Janssen, G.J.W. 2002. Root-knot nematode: Meloidogyne species. p. 43-70. In: Starr, J.L.; Cook, R.; Bridge, J., eds. Plant resistance to parasitic nematodes. CAB International, Wallingford, UK. and Bertrand et al. (2000)Bertrand, B.; Peña Durán, M.X.; Anzueto, F.; Cilas, C.; Etienne, H.; Anthony, F.; Eskes, A.B. 2000. Genetic study of Coffea canephora coffee tree resistance to Meloidogyne incognita nematodes in Guatemala and Meloidogyne sp. nematodes in El Salvador for selection of rootstock varieties in Central America. Euphytica 113: 79-86. where 0 = totally intact root systems; 1 = presence of rare and small swellings in secondary roots; 2 = small swellings of less than 25 % of the root system; 3 = swellings and early necrosis of 25-50 % of the root system; 4 = loss of secondary roots due to necrosis observed in 51-75 % of the root system; and 5 = severe loss of secondary roots greater than 75 % with destruction of the root system. Plants were considered resistant when DI ≤ 2, and susceptible when DI > 2.

Population was estimated by counting nematodes in Peters's slides under a light microscope, quantifying the eggs and juveniles of M. paranaensis. The final population (FP) corresponds to the number of nematodes extracted from the entire roots of each plant. The reproduction factor (RF) was determined according to Oostenbrink (1966)Oostenbrink, M. 1966. Major characteristics of the relation between nematodes and plants. Mededelingen van de Landbouwhogeschool te Wageningen, 66: 1-46..

Number of eggs and J2 per gram of root (NEM) were calculated from the ratio between the size of the final nematode population and fresh root mass to quantify proportionally the number of nematodes per treatment. NEM data were log transformed (log10 (x+1)), subjected to the analysis of variance (ANOVA) and the means were compared by the Scott-Knott test (p < 0.05).

Effect of initial population levels of M. paranaensis on coffee plant development

Seedlings of IAC 3, obtained by somatic embryogenesis, and susceptible control Mundo Novo IAC 515-20, obtained from seeds, were cultivated in a greenhouse in plastic pots of 1.7 L containing a sterile mixture of sand and soil (1:1), fertilized in the same way as the first experiment. Plants with five pairs of leaves were inoculated by the deposition of M. paranaensis suspension (eggs and juveniles) in holes made in the substrate around the plants. The inoculum concentration varied to obtain the initial population levels (Pi) according to the six pre-established treatments (0, 0.7, 1.5, 2.9, 5.9 and 11.8 nematodes per cm3 of soil). The experiment was performed in a completely randomized design with nine replicates and single-plant plots.

After 345 days, the aerial parts of the plants were removed, stored in paper bags and dried in oven (60 ºC) to obtain the top dry weight (TDW). The root system of each plant was washed, the root fresh weight (RFW) was obtained and the nematodes were extracted according to the Hussey and Baker (1973)Hussey, R.S.; Barker, K.R. 1973. A comparison of methods of collecting inocula of Meloidogyne spp. including a new technique. Plant Disease Report 57: 1025-1028.. The final population (FP) and reproduction factor (RF) was estimated according the same procedures described for the first experiment.

The RFW data were analyzed according to the nonlinear model proposed by Seinhorst (1965), based on the equation: Y=m+(1m) .ZPiT.; in which, Y is the ratio of the estimated variable for plant growth in an initial population density of the nematode (PI) divided by the value obtained in the control plant; m is the minimum yield of the plant obtained under high population densities of the nematode; Z is a constant less than 1 (Z < 1); Pi is the initial population density of the nematode and T is the tolerance limit. For the Seinhorst analysis, we used the SeinFit software, DOS version, developed by Viaene et al. (1997)Viaene, N.M.; Simoens, P.; Abawi, G.S. 1997. Seinfit, a computer program for the estimation of the Seinhorst equation. Journal of Nematology 29: 474-477.. Additionally, the experimental data were submitted to the principal component analysis (PCA) using Statistica 11 software. In the PCA, the reduction of top dry weight (RTDW) was obtained from the relation between the value of each treatment by the experimental control, according the equation: RTDW = 100-(TDWt/TDWc)*100, where TDWt is the top dry weight of a treatment and TDWc is the top dry weight of the control.

Results

Resistance assessment in greenhouse conditions

Progeny IAC 3 was considered susceptible to M. paranaensis according RF, on average, with a resistance segregation rate of 50 % (Table 1), but its NEM was six fold lower and statistically different from the susceptible control Mundo Novo IAC 515-20. Conversely, clone IAC 3 revealed a reduced mean of RF and NEM and, as expected, all replicates were resistant to M. paranaensis (%R=100). Susceptible control Mundo Novo IAC 515-20, obtained by seeds, and Clone IAC 1, propagated by somatic embryogenesis, showed high RF means and 100 % of susceptible plants (Table 1).

Table 1
Damage index (DI), number of eggs and J2 per gram of roots (NEM), reproduction factor (RF), phenotype and percentage of resistant plants according reproduction factor (% R) in coffee trees inoculated with Meloidogyne paranaensis.

Effect of initial population levels of M. paranaensis on coffee plant development

The reproduction factor for each inoculum density tested in both coffee seedlings are presented in Table 2. With the increase of nematode density, there was a reduction in RF. For example, in Mundo Novo, the RF value at the lowest density was 44.1, while at the highest nematode density, this value was 1.2; thus, regardless of the Pi level, Mundo Novo was considered susceptible. Conversely, IAC 3 was considered resistant, as RF was 0.35 at the lowest density and 0.06 at the highest.

Table 2
Effect of Meloidogyne paranaensis initial population (Pi) on the root fresh weight (RFW) of coffee plants Mundo Novo and IAC 3, final nematode population (FP), reproduction factor (RF) and plant phenotype, 345 days after inoculation.

The results obtained with the Seinhorst nonlinear model (Figure 1) showed that Mundo Novo plants, adjusted the equation as follows: Y=0.250+(0.75).1Pi-3.9. The value found for the tolerance limit (T) was 3.9 nematodes per cm3 of soil; therefore, plants began to suffer damage caused by M. paranaensis at this population density. There was also a reduction of 75 % of RFW (m = 0.250), demonstrating the severity of damages caused by M. paranaensis in C. arabica cv Mundo Novo.

Figure 1
Relationship between Meloidogyne paranaensis initial population (Pi) and the root fresh weight of coffee plants IAC 3 and Mundo Novo IAC 515-20, 345 days after inoculation.

Conversely, for plants from clonal seedlings IAC 3, the equation was as follows: Y=0.900+(0.10).1Pi-7.7, where T was 7.7 nematodes per cm3 of soil, and the m value was 0.900, indicating that IAC 3 RFW was only reduced by an average of 10 % in response to nematode infection, clearly demonstrating that IAC 3 plants were more tolerant to nematode attack than Mundo Novo.

According to PCA (Figure 2), 90 % of the total variability is explained by the axes ‘varietal resistance’ (60 %) and ‘vegetative development’ (30 %) of plants. Varietal resistance was explained by DI, FP, NEM and RF variables and vegetative development, by RFW, TDW and RTDW variables.

Figure 2
Principal component analysis. Varietal resistance (60 %) and vegetative development (30 %) of plants from clone IAC 3 and cultivar Mundo Novo IAC 515-20 inoculated with 0.74, 1.47, 2.9, 5.9 and 11.8 nematodes per cm3 of soil and relationship among damage index (DI), root fresh weight (RFW), final population (FP), number of nematodes, eggs and J2 per gram of root (NEM), reproduction factor (RF), top dry weight (TDW) and reduction of top dry weight (RTDW) variables.

Regardless of the initial level of the inoculum, coffee trees of clone IAC 3 form a cluster to the left of the X axis, revealing a high level of varietal resistance to nematode M. paranaensis (Figure 1). The cultivar Mundo Novo IAC 515-20 presented high mean values of the variables DI, FP, NEM and RF, susceptible to M. paranaensis. However, influence of the initial level of inoculum on the vegetative development of the plants was lower when inoculated with 5.9 and 11.8 nematodes per cm3 of soil (Figure 2).

Discussion

Coffea arabica is an autogamous and tetraploid species with self-fertilization rate of about 90 % (Carvalho and Krug, 1949Carvalho, A.; Krug, C.A. 1949. Agents of pollination of coffee flower (Coffea arabica L.) Bragantia 9: 11-24. (in Portuguese, with abstract in English).) and its cultivars are commercially propagated by seeds. Breeding programs aim to select uniform cultivars for all agronomic traits; however, it is a lengthy procedure that involves several selection cycles. This process is more complex when it involves the resistance genes introgression of diploid and allogamous species, such as C. canephora. Therefore, genetic resistance of IAC 3 to M. paranaensis found in segregating progenies could be immediately explored using clonal coffee trees. Multiplication of resistant plants via somatic embryogenesis is a promising tool for large-scale production, shortening the time to obtain a resistant cultivar, besides eliminating the fixation step of resistance genes. In field conditions, coffee clones from seeds have similar performance of traditional seedlings and do not have limitations for commercial use (Etienne and Bertrand, 2001Etienne, H.; Bertrand, B. 2001. Trueness-to-type and agronomic characteristics of Coffea arabica trees micropropagated by the embryogenic cell suspension technique. Tree Physiology 21: 1031-1038.).

Despite the higher production cost, aggregated value of clonal seedlings resistant to RKN may compensate farmer's investment in infested areas. To address this question, several works have been conducted to increase efficiency of somatic embryogenesis protocols and to reduce production costs of clonal seedlings (Etienne et al., 2012Etienne, H.; Bertrand, B.; Montagnon, C.; Bobadilla Landey, R.; Dechamp, E. 2012. An example of successful technology transfer in micropropagation: the multiplication of Coffea arabica by somatic embryogenesis. Cahiers Agricultures 21: 115-24.; Etienne et al., 2013Etienne, H.; Bertrand, B.; Georget, F.; Lartaud, M.; Montes, F.; Dechamp, E.; Verdeil, J.L.; Barry-Etienne, D. 2013. Development of coffee somatic and zygotic embryos to plants differs in the morphological, histochemical and hydration aspects. Tree Physiology 33: 640-653.; Maciel et al., 2016Maciel, A.L.R.; Rodrigues, F.A.; Pasqual, M.; Carvalho, C.H.S. 2016. Large-scale, high-efficiency production of coffee somatic embryos. Crop Breeding and Applied Biotechnology 16: 102-107.).

Considering the analysis of the effect of initial population levels of M. paranaensis on IAC 3 and Mundo Novo development, several greenhouse experiments have shown the relationships between coffee and Meloidogyne spp based on the Seinhorst model. Vovlas and Di Vito (1991)Vovlas, N.; Di Vito, M. 1991. Effect of root-knot nematodes Meloidogyne incognita and M. javanica on the growth of coffee (Coffea arabica L.) in pots. Nematologia Mediterranea 19: 253-258. reported that the tolerance limit was two eggs per cm3 of soil of M. javanica and M. incognita, on C. arabica cultivar São Tomé. Also, Zhang and Schmitt (1995)Zhang, F.; Schmitt, D.P. 1995. Relationship of Meloidogyne konaensis population densities to coffee growth. Plant Disease 79: 446-449. demonstrated that the shoot and root growth of C. arabica cultivars SL28, Guatemalan, Mundo Novo, Bourbon Vermelho and Guadalupe were suppressed by M. konaensis. The authors calculated the threshold to be a little less than 10 eggs per plant. Di Vito et al. (2000)Di Vito, M.; Crozzoli, R.; Vovlas, N. 2000. Pathogenicity of Meloidogyne exigua on coffee (Coffea arabica L.) in pots. Nematropica 30: 55-61. observed the reduction in the seedling of São Tomé caused by M. exigua. The tolerance limit for the variable shoot weight was 1.2 eggs and J2 per cm3 of soil. However, there is paucity of information regarding the relationship of M. paranaensis population densities to coffee growth.

For Souza and Bressan-Smith (2007), threshold levels can only demonstrate the potential of damage caused to seedlings under greenhouse conditions and cannot be used to predict any damage to coffee production in the field. However, our results showed that clonal seedlings (IAC 3) were actually more tolerant to M. paranaensis attack than Mundo Novo plants. IAC 3 demonstrated a tolerance limit of 7.7 nematodes per cm3 of soil (equivalent to a Pi of 13090 nematodes per plant), while in Mundo Novo IAC515-20 the tolerance limit was 3.9 nematodes per cm3 of soil (equivalent to a Pi of 6588 nematodes per plant). Thus, IAC 3 clone showed higher level of tolerance as it resisted nematode attack better than Mundo Novo plants.

If threshold levels (Figure 1) are considered only for studies conducted in greenhouse conditions, the PCA results reveal that the clonal seedlings are always resistant to M. paranaensis regardless of the initial nematode population in the soil (Figure 2). This resistance reaction of young plants of Clone IAC 3 to high nematode population levels is of outstanding practical importance, since coffee growers rarely adopt practices to reduce nematode population levels in infested soils before planting.

Acknowledgments

The authors are grateful to Consórcio Brasileiro de Pesquisa e Desenvolvimento do Café (CBP and D-Café) (project 002.06.10.014.00.03: Evaluation of coffee plants resistant to Meloidogyne spp. in infested areas of São Paulo State.); Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for research fellowship (OGF CNPq DT 308.634/2016-0); Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) for scholarship (BJRF FAPESP 2010/15416-0) and Dra. Mirian Perez Maluf for helpful comments and suggestions.

References

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Publication Dates

  • Publication in this collection
    May-Jun 2019

History

  • Received
    06 Dec 2017
  • Accepted
    06 Feb 2018
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