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The strawberry (Fragaria x ananassa) has great economic and social importance in the United States, Mexico, Turkey, Poland, Italy, Germany, Russia, including Latin American countries as Chile and Brazil (Coelho Júnior, 2016; OMAIAA, 2017). There are around 4,200 ha of strawberry cultivated areas in Brazil, and the principal producing states are Minas Gerais, Paraná and Rio Grande do Sul (Fagherazzi et al., 2017).
New information on the health benefits of strawberries, such as antioxidant levels, folate, potassium, vitamin C and fiber content, stimulated consumption rates (Garcia et al., 2017). Despite the high added value of the product, broad acceptance by consumers and diversity in the marketing (Fachinello et al., 2011), this crop has a relevant social role in the family farming (Antunes et al., 2007; Lemiska et al., 2014).
The main strawberry production system in Brazil is based on growing under low tunnel (Fagherazzi et al., 2017). Therefore, this crop may be affected by many soil pathogens such as the plant parasitic nematodes Meloidogyne spp. and Pratylenchus spp. (Maas, 1998; Gomes & Cofcewics, 2003). Root-knot nematodes (Meloidogyne spp.) are polyphagous pests and cause great damage in several annual and perennial crops associated to yield losses (Sharma & Fonseca, 2000; Franzener et al., 2005; Lima-Medina et al., 2014). Similarly, root-lesion nematodes (Pratylenchus spp.), the second most important plant-parasitic nematode group for Brazilian agriculture, parasites various crops such as soybeans, oats, corn, millet, sunflower, sugarcane, fruit trees besides other common cultivated plant species (Severino et al., 2010; Ribeiro et al., 2010; Lima-Medina et al., 2014).
Among the control practices for these two plant-parasitic nematode genera, the use of resistant cultivars is one of the most suitable. However, for strawberry, few studies have been performed for Brazilian conditions. Curi et al. (2016) studied the reaction of some strawberry commercial cultivars to Meloidogyne hapla. The authors verified the genetic resistance of Oso Grande and Albion. Similarly, ‘Camarosa’ is resistant to M. enterolobii and M. ethiopica (Somavilla et al., 2006; Freitas et al., 2016) but the reaction of these cultivars to other Meloidgyne species and to Pratylenchus spp. in not known. Considering the pathogenicity of these pests and the scarcity of studies reported on the strawberry, the objective of this work was to evaluate the resistance of eight strawberry cultivars to Meloidogyne and Pratylenchus species related to tropical and subtropical conditions.
MATERIAL AND METHODS
The reaction of eight strawberry cultivars to four root-knot Meloidogyne species and two lesion Pratylenchus species was evaluated at greenhouse conditions. Strawberry seedlings of Festival, Monterrey, Camino Real, San Andreas, Camarosa, Oso Grande, Aromas and Albion cultivars obtained from tissue culture were used to establish this assay. The inoculum of the Meloidogyne and Pratylenchus species was obtained according to the methodology of Hussey & Barker (1973) and Coolen & D’Here (1972), respectively.
One pure population of M. javanica Est J3, M. arenaria Est A2, M. incognita Est I2 and M. hapla Est H2 were maintained on tomato plants (Solanum lycopersicum) cv. Rutgers at greenhouse conditions in order to use as root-knot nematode inoculum. Similarly, pure populations of Pratylenchus zeae and P. brachyurus were maintained on Sorghum bicolor ‘506’ plants to use nematode inoculum.
Strawberry seedlings 30-day old, grown in pots with sterilized soil, were inoculated with 5,000 eggs + second stage juveniles of Meloidogyne arenaria, M. incognita, M. javanica or M. hapla or 1,000 Pratylenchus zeae or P. brachyurus per plant. The experiment was carried out under greenhouse conditions in a completely randomized design with six replications using tomato ‘Rutgers’ and sorghum ‘506’ plants as controls to root-knot and root-lesion nematodes, respectively. A randomized design experiment with six replications of one plant per plot was used.
Ninety days after inoculation, each strawberry plant inoculated with root-knot nematode was evaluated for number of galls in the roots. Subsequently, each root system was processed (Hussey & Barker,1973) to determine the final nematode populations (number of eggs and second stage juveniles) in the different strawberry cultivars. However, to calculate the final population of Pratylenchus species, the roots of different plants were processed by Coolen & D’Herde (1972) method. The reproduction factor (RF= final population / initial population) of each nematode species obtained in each genotype was estimated. Averages of the different variables were compared by Scott-Knott’s clustering test at 5% using the software SASM-Agri (Canteri et al., 2001). The strawberry reaction was determined by the nematode reproduction factor (RF), considering resistant genotypes with RF<1.00, immune with RF= 0.00 and susceptible with RF>1.00 (Oostenbrik, 1966).
RESULTS AND DISCUSSION
Most cultivars were resistant or immune to various nematode species (Table 1). Only ‘Camarosa’ and ‘Oso Grande’ were susceptible to M. arenaria, and the first was susceptible to M. hapla as compared to the susceptible control. Furthermore, the presence of galls on the roots of plants inoculated with Meloidogyne spp. was detected principally of susceptible cultivars (Figure 1). All strawberry cultivars were resistant or immune to P. zeae and P. brachyurus (Table 1). This information is important, because Camarosa is the second most cultivated cultivar in Brazil mainly in soil system production.
Figure 1 Root-systems of strawberry plants exhibiting galls caused by Meloidogyne arenaria (a) and M. hapla (b) at ‘Camarosa’ and M. arenaria at root-system of Oso Grande cultivar (c). Pelotas, Embrapa Clima Temperado, 2017. Foto: Cesar Bauer Gomes.
Table 1 Reaction of strawberry cultivars to different root-knot (Meloidogyne spp.) and root-lesion (Pratylenchus spp.) species of nematodes. Pelotas, Embrapa Clima Temperado, 2018.
| Cultivars | Meloidogyne incognita | Meloidogyne arenaria | Meloidogyne javanica | ||||||
|---|---|---|---|---|---|---|---|---|---|
| galls (no) | RF | R | galls (no) | RF | R | galls (no) | RF | R | |
| Control | 199.16 | 7.11 | S1 | 352.66 | 16.33 | S1 | 345 | 24.13 | S1 |
| Camarosa | 0.00ns | 0.00a* | I | 123.00b | 2.82c | S | 0.00ns | 0.08b | R |
| Oso Grande | 0.00 | 0.00a | I | 105.00b | 2.01c | S | 0.00 | 0.12b | R |
| Monterrey | 0.00 | 0.00a | I | 0.00a | 0.01b | R | 0.00 | 0.04b | R |
| Festival | 0.00 | 0.00a | I | 0.00a | 0.02b | R | 0.00 | 0.12b | R |
| San Andres | 0.00 | 0.21b | R | 0.00a | 0.18b | R | 0.00 | 0.12b | R |
| Aromas | 0.00 | 0.03a | R | 0.00a | 0.14b | R | 0.00 | 0.12b | R |
| Camino Real | 0.00 | 0.00a | I | 7.00c | 0.11b | R | 0.00 | 0.09b | R |
| Albion | 0.00 | 0.00a | I | 0.00a | 0.00a | I | 0.00 | 0.00a | I |
| CV (%) | - | 15.45 | 21.55 | 16.23 | - | 15.13 | |||
| Meloidogyne hapla | Pratylenchus zeae | Pratylenchus brachyurus | |||||||
| galls (no) | RF | R | RF | R | RF | R | |||
| Control | 1150 | 24.39 | S1 | 9.41 | S2 | 7.51 | S2 | ||
| Camarosa | 15.00b | 1.40b | S | 0.88a | R | 0.07b | R | ||
| Oso Grande | 0.00a | 0.10a | R | 0.60b | R | 0.15a | R | ||
| Monterrey | 0.00a | 0.01a | R | 0.00c | I | 0.00b | I | ||
| Festival | 0.00a | 0.01a | R | 0.61b | R | 0.00b | I | ||
| San Andres | 0.40a | 0.01a | R | 0.00c | I | 0.00b | I | ||
| Aromas | 0.00a | 0.17a | R | 0.64b | R | 0.81a | R | ||
| Camino Real | 0.00a | 0.01a | R | 0.00c | I | 0.00b | I | ||
| Albion | 7.40b | 0.25a | R | 0.18b | R | 0.07 | R | ||
| CV (%) | 9.7 | 11.22 | 9.91 | 11.12 | |||||
Means followed by same letters in the column belong to the same group by Scott-Knott test, 5% probability. 1= tomato Rutgers control; 2= sorghum BRS 506 control; R= reaction; RF= reproduction factor; (immune with RF= 0.00 and susceptible with RF>1.00) S= susceptible; I= immune; R= resistant.
In other studies, regarding strawberry genetic resistance to Meloidogyne spp., ‘Camarosa’, ‘Oso Grande’, ‘Aromas’, ‘Camino Real’, ‘Santa Clara’ and ‘Ventana’ were immune to M. enterolobii (Freitas et al., 2016) and the first three cultivars were resistant to M. ethiopica (Somavilla et al., 2006). Pinkerton & Finn (2005), evaluating the reaction of more than 30 strawberry genotypes to M. hapla, observed that most cultivars were resistant to nematode including ‘Camarosa’, which in this study behaved as susceptible.
The reaction of strawberry to root-lesion nematodes observed in this assay was similar to those obtained in other studies with P. penetrans in the USA (Pinkerton & Finn, 2005; Villanueva et al., 2010). The authors observed resistance and tolerance in more than 30 cultivars, including three genotypes evaluated in this experiment as Camarosa, Diamante and Festival. Once there is little information available on the genetic resistance of strawberry to tropical and subtropical Pratyenchus species (P. zeae and P. brachyurus) our results support the need to carry out additional studies on genetic resistance and aggressiveness, using different populations of phytoparasitic nematodes as noted by Loubser & Meyer (1987) and Lima-Medina et al. (2017) in other pathosystems.
Considering the most strawberry cultivars were poor hosts to different Meloidogyne and Pratylenchus species, these results are extremely important for establishing control strategies of these pests, suppressing their populations in the soil. Therefore, the use of resistant strawberry cultivars represents a viable alternative in the implementation of crop rotation systems to the management of these pests, becoming thus an efficient and economic way to reduce nematode populations in infested areas (Carneiro et al., 2000; Ferraz & Freitas, 2004; Lima et al., 2009; Freitas et al., 2016).
Most of the evaluated strawberry cultivars (Festival, Monterrey, Camino Real, San Andreas, Aromas and Albion) are resistant or immune to Meloidogyne spp. and Pratylenchus spp. which confers their status as poor host. In this way these cultivars are an alternative to use in infested areas with these pests.
