Introduction

Quinoa (Chenopodium quinoa Willd.) is an important crop in South America because of its high nutritional value and tolerance to external abiotic stress (Jarvis et al., 2008; ^{Verena and Charrondière, 2016}). Its composition has attracted the attention of many scientists owing to its high nutritional value and presence of proteins, lipids, fibers, vitamins, minerals, and essential amino acids; gluten-free nature (^{Navruz-Varli and Sanlier, 2016}; ^{Filho et al., 2017}); tocopherols; and organic acids (^{Pereira et al., 2019}). All these components contribute to food security (Nowak et al., 2016). Peru is one of the main exporters of quinoa worldwide. The Arequipa region achieved a yield of 4.086 kg ha^-1 (Bedoya et al., 2018), increasing its production in the last two decades (Vargas et al., 2015).

The phytosanitary problems that affect quinoa are the kona-kona (Eurysacca quinoa Povolny), cutworms (Copitarsia turbata Herrich & Schäffer), chinch bugs (Epitrix subcrinita Lec.), the green aphid (Macrosiphum euphorbiae Thomas), mildew (Peronospora farinosa Fries), and worldwide economically important nematodes (León et al., 2018). The identified genera of nematodes associated with quinoa crops are Meloidogyne, Nacobbus, Pratylenchus, Helicotylenchus, Mesocriconema, Xiphinema, Dorylaimus, Hemiciclyophora, and Globodera (^{Franco, 2003}; Lima-Medina et al., 2019).

Meloidogyne Göldi, 1887 is a genus that causes problems in the quinoa crop; it also affects other crops such as artichoke, paprika, grapevines, and asparagus. In addition, the agricultural frontier is basically expanded in irrigated soils, where sandy soils and low biological diversity allow a growing population of Meloidogyne spp. (Palomo, 2018). Currently, there are no reports of Meloidogyne in quinoa cultivars for the Arequipa region; therefore, this study aimed to evaluate the response of quinoa cultivars to Meloidogyne arenaria (Neal, 1889) Chitwood, 1949, Meloidogyne incognita (Kofoid and White, 1919) Chitwood, 1949, and Meloidogyne hapla Chitwood, 1949.

Materials and methods

The experiment was conducted in a mesh house with a temperature of 25 °C ± 5 °C at the Phytopathology Laboratory of the Universidad Nacional de San Agustín, Arequipa, Peru (16° 24’ 32” S, 71° 31’ 18” W), from November 2019 to February 2020. The response of five quinoa cultivars (‘Salcedo INIA’, ‘Choclito’, ‘Huariponcho’, ‘Negra Collana’, and ‘Kcancolla’) to M. incognita, M. arenaria, and M. hapla was evaluated.

Quinoa seeds were sown in trays of 200 units with a sterile substrate (Promix^®). Twenty days after emergence, each seedling was transplanted to a bag with 3,000 dm³ of sterilized fine sand. Seven days after transplantation, seedlings were inoculated with pure species of Meloidogyne propagated in tomato (Solanum lycopersicum ‘Rio Grande’).

The quinoa cultivars were inoculated following the method described by ^{Hussey and Barker (1973}) using a dose of 5,000 eggs + juveniles that were distributed in three holes around the plant. The viability of the inoculum was evaluated in tomato plants (‘Rio Grande’) inoculated at the same dose as the quinoa cultivars. Quinoa and tomato cultivars were kept at a temperature of 25 °C ± 5 °C and a humidity of 40 ± 5.

The number of galls (NG), number of nematodes per gram of root (nematodes g⁻¹ root), and the reproduction factor (RF) were evaluated 90 days after inoculation. The number of galls was determined by direct root counting; the extraction of eggs + juveniles was performed using the technique proposed by ^{Hussey and Barker (1973}) and the RF was determined according to the methodology described by Oostenbrink (1996), they were considered immune (RF = 0), resistant (RF <1) and susceptible (RF> 1) species. The number of nematodes per gram of root was estimated by the ratio between the total number of nematodes and the total root mass, in grams, for each repetition.

The experimental design was completely randomized with five quinoa cultivars and three species of Meloidogyne spp., and six replicates were used. Data were subjected to an analysis of variance (ANOVA, p < 0.05) and comparisons were made using the Duncan's test (p < 0.05) using SAS, version 9.0.

Results and discussion

The ANOVA detected a significant effect between nematodes per gram of root (nematodes g⁻¹ root), number of galls (NG) and reproduction factor (RF) for cultivars of quinoa and the nematode species M. arenaria, M. hapla and M. incognita, with a significant difference for the Duncan test (p <0.05).

The RF of M. arenaria and M. hapla was low in most quinoa cultivars; therefore, these were classified as resistant, except for ‘Negra Collana’, which was considered susceptible to M. arenaria with an RF = 1.1 (Table 1). However, for M. hapla, ‘Salcedo INIA’ and ‘Huariponcho’ with an RF = 1.3 and 1. 1, respectively, were considered susceptible (Table 1). Furthermore, the reproduction factor of M. incognita was high in all quinoa cultivars; therefore, all cultivars were classified as susceptible (Table 1) according to ^{Oostenbrink (1966}).

‘Salcedo INIA’, ‘Choclito’, ‘Kcancolla’, and ‘Huariponcho’ were classified as resistant to M. arenaria with an RF = 0.3, 0.4, 0.5, and 0.7, respectively. ‘Salcedo INIA’ showed a lower reproduction rate, which indicates a higher level of resistance, a lower nematodes g⁻¹ root with 436, and the lowest number of galls with 9. Furthermore, ‘Negra Collana’ had the highest reproduction rate, which indicates it is susceptible, with an nematodes g⁻¹ root of 2,301 and an number of galls of 29.5, which although high, was not the highest. ‘Choclito’ had the highest number of galls with 35.8; however, with an RF of 0.4 and an nematodes g⁻¹ root of 609, it was considered resistant (Table 1).

In the case of M. hapla, ‘Salcedo INIA’ showed the highest reproduction rate, RF = 1.26, and thus, it was classified as susceptible to this nematode It also had the highest nematodes g⁻¹ root of 1,997 and a number of galls of 102 ‘Choclito’, with an RF = 0.4, had the lowest reproduction rate and was therefore considered the most resistant; with an nematodes g⁻¹ root of 536 and a higher number of galls (96.17) than that of the ‘Huariponcho’ cultivar (63); considered susceptible, with an RF = 1.1 and an nematodes g⁻¹ root of 1132 (Table 1).

All quinoa cultivars were susceptible to M. incognita. These data coincide and exceed those reported by ^{Asmus et al. (2005}), who indicate that C. quinoa is susceptible to M. incognita race 3 with an RF = 2.6, ‘Huariponcho’ had the highest reproduction rate with an RF = 14.2, being considered as the most susceptible and with the highest nematodes g⁻¹ root of 16,508. These data are similar to those reported by Asmus et al. (2001), where they indicate that the quinoa crop had the highest multiplication of nematodes and its use in infested areas can increase, or at least maintain, the population of Meloidogyne javanica (Treub, 1885) Chitwood 1949. However, ‘Negra Collana’ presented the lowest RF = 2.5 and an nematodes g⁻¹ root of 5,257; therefore, it was considered the least susceptible (Table 1).

In Peru, quinoa species are commonly used in crop rotations for pest management; therefore, knowing the response of different quinoa cultivars to M. incognita, M. arenaria, and M. hapla is essential for researchers and farmers during crop rotation. This study is one of the first to evaluate the response of quinoa cultivars to Meloidogyne spp. Further research regarding the susceptibility and resistance to Meloidogyne spp. is required, as quinoa is of great importance to food security.

Conclusions

All quinoa cultivars were susceptible to M. incognita, ‘Salcedo INIA’ and ‘Huariponcho’ are also susceptible to M. hapla, and ‘Negra Collana’ to M. arenaria. However, ‘Salcedo INIA’, ‘Choclito’, ‘Huariponcho’, and ‘Kcancolla’ are resistant to M. arenaria and ‘Choclito’, ‘Negra Collana’, and ‘Kcancolla’ are resistant to M. hapla.