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Reaction of common bean genotypes to Heterodera glycines

Reação de genótipos de feijoeiro comum a Heterodera glycines

ABSTRACT

The soybean cyst nematode (Heterodera glycines) may result in a significant economic impact on bean cultivation. This study aimed to evaluate the reaction of 55 common bean genotypes from the Embrapa Arroz e Feijão core collection to the race 3/HG type 0 of H. glycines. Among the genotypes evaluated, 34 were considered resistant to the cyst nematode, and, in addition to showing a lower population of females in the roots, also reduced the fecundity of H. glycines.

KEYWORDS:
Phaseolus vulgaris ; nematoide de cisto; resistência genética

RESUMO

O nematoide de cisto da soja (Heterodera glycines) pode resultar em impacto econômico significativo no cultivo de feijão. Objetivou-se avaliar a reação de 55 genótipos de feijão comum da coleção nuclear da Embrapa Arroz e Feijão à raça 3/Tipo HG 0 de H. glycines. Dentre os genótipos avaliados, 34 foram considerados resistentes ao nematoide de cisto, os quais, além de apresentarem menor população de fêmeas nas raízes, também reduziram a fecundidade de H. glycines.

PALAVRAS-CHAVE:
Phaseolus vulgaris ; cyst nematode; genetic resistance

INTRODUCTION

Common bean (Phaseolus vulgaris L.) has agricultural, nutritional, social and economic importance, being cultivated in several countries (Uebersax et al. 2022UEBERSAX, M. A.; CICHY, K. A.; GOMEZ, F. E.; PORCH, T. G.; HEITHOLT, J.; OSORNO, J. M.; KAMFWA, K.; SNAPP, S. S.; BALES, S. Dry beans (Phaseolus vulgaris L.) as a vital component of sustainable agriculture and food security: a review. Legume Science, v. 5, n. 1, p. 155-155, 2022.). Brazil is the second largest producer in the world (FAO 2022FOOD AND AGRICULTURE ORGANIZATION OF THE UNITED NATIONS (FAO). Statistics Division. Countries by commodity: beans, dry. 2022. Avalaible at: https://www.fao.org/faostat/en/#rankings/countries_by_commodity. Access on: Jan. 21, 2024.
https://www.fao.org/faostat/en/#rankings...
), with 3 million tons in just over 2.7 million ha (Conab 2023COMPANHIA NACIONAL DE ABASTECIMENTO (Conab). Acompanhamento da safra brasileira de grãos. Brasília, DF: Conab, 2023.). The highest yield comes from the third harvest, partly due to the use of high technologies, inputs and irrigation in the central plateau of Brazil, in the Cerrado (Brazilian Savanna) region (Silva & Wander 2018SILVA, O. F. da; WANDER, A. E. Caracterização e avaliação econômica do sistema de cultivo de feijãocomum irrigado no Cerrado: o caso da cultivar BRS Estilo. In: TÔSTO, S. G.; BELARMINO, L. C.; CASTRO, G. S. A.; MANGABEIRA, J. A. de C.; SILVA, O. F. da (ed.). Caracterização e avaliação econômica de sistemas de produção e cultivo de grãos em biomas brasileiros. Brasília, DF: Embrapa, 2018. p. 47-68.).

Several species of nematodes are reported to cause diseases in common bean, including Meloidogyne javanica (Treub 1885) (Chitwood 1949), M. incognita (Kofoid & White 1919) Chitwood (1949) and Pratylenchus brachyurus (Godfrey 1929) (Freire & Ferraz 1977FREIRE, F. C. O.; FERRAZ, S. Nematoides associados ao feijoeiro, na Zona da Mata, Minas Gerais, e efeitos do parasitismo de Meloidogyne incognita e M. javanica sobre o cultivar “Rico 23”. Revista Ceres, v. 24, n. 1, p. 141-149, 1977., Abawi & Widmer 2000ABAWI, G. S.; WIDMER, T. L. Impact of soil health management practices on soilborne pathogens, nematodes and root diseases of vegetable crops. Applied Soil Ecology, v. 15, n. 1, p. 37-47, 2000., Bonfim Junior et al. 2021BONFIM JUNIOR, M. F.; INOMOTO, M. M.; ARAÚJO FILHO, J. V. Phytonematodes infesting common bean fields in Brazil, and pathogenicity tests with Pratylenchus brachyurus. Arquivos do Instituto Biológico, v. 88, e00312020, 2021.). However, host ability studies of common bean to Heterodera glycines (Ichinohe 1952) have showed that most cultivars are susceptible to the nematode (Noel et al. 1982NOEL, G. R.; JACOBSEN, B. J.; LEEPER, C. D. Soybean cyst nematode in commercial snap beans. Plant Disease, v. 6, n. 6, p. 520-522, 1982., Jain et al. 2019JAIN, S.; POROMARTO, S.; OSORNO, J. M.; MCCLEAN, P. E.; NELSON, B. D. Genome wide association study discovers genomic regions involved in resistance to soybean cyst nematode (Heterodera glycines) in common bean. PloS One, v. 14, n. 2, e0212140, 2019., Dias et al. 2023DIAS, W. P.; WENDLAND, A.; CARNEIRO, G. E. S.; OLIVEIRA FILHO, F. G.; LOPES, I. O. N. L. Reaction of common bean genotypes to plant parasitic nematodes. Pesquisa Agropecuária Tropical, v. 53, e74717, 2023.). Although this nematode is mainly known for causing yellow dwarfism in soybean, some bean lines have behaved as more susceptible than soybean (Melton et al. 1986MELTON, T. A.; JACOBSEN, B. J.; NOEL, G. R. Effects of temperature on development of Heterodera glycines on Glycines max and Phaseolus vulgaris. Journal of Nematology, v. 18, n. 4, p. 468-474, 1986.).

The cyst nematode has been considered an emerging pest in common bean crops in many regions, such as the midwestern USA (Shi et al. 2021SHI, A.; GEPTS, P.; SONG, Q.; XIONG, H.; MICHAELS, T. E.; CHEN, S. Genome-wide association study and genomic prediction for soybean cyst nematode resistance in USDA common bean (Phaseolus vulgaris) core collection. Frontiers in Plant Science, v. 12, e624156, 2021.). Symptoms such as plant yellowing and stunting were observed in common bean (Yan et al. 2017YAN, G. P.; PLAISANCE, A.; CHOWDHURY, I.; BAIDOO, R.; UPADHAYA, A.; PASCHE, J.; MARKELL, S.; NELSON, B.; CHEN, S. First report of the soybean cyst nematode Heterodera glycines infecting dry bean (Phaseolus vulgaris L.) in a commercial field in Minnesota. Plant Disease, v. 101, n. 2, p. 391-391, 2017.); however, the recognition of this nematode as the cause of crop losses usually occurs late in the season, since the symptoms are visible only at the end stage of the crop. At this time, it is impossible to eradicate the nematode due to its survival mechanisms, since the cysts produced by H. glycines remain viable in the soil for many years (Sato et al. 2019SATO, K.; KADOTA, Y.; SHIRASU, K. Plant immune responses to plant parasitic nematodes. Frontiers in Plant Science, v. 10, e1165, 2019., Shaibu et al. 2020SHAIBU, A. S.; LI, B.; ZHANG, S.; SUN, J. Soybean cyst nematode-resistance: gene identification and breeding strategies. The Crop Journal, v. 8, n. 6, p. 892-904, 2020.).

The proper management of this nematode is performed by integration techniques that aim to reduce the pathogen population. Both crop rotation with non-host species and resistant cultivars are the most suitable measures to reduce H. glycines populations in the growing area (Ferraz et al. 1999FERRAZ, S.; VALLE, L. A. C.; DIAS, C. R. Utilização de plantas antagônicas no controle do nematoide de cisto da soja (Heterodera glycines Ichinohe). In: SOCIEDADE BRASILEIRA DE NEMATOLOGIA. O nematoide de cisto da soja: a experiência brasileira. Jaboticabal: Artsigner, 1999. p. 25-53., Yan & Baidoo 2018YAN, G.; BAIDOO, R. Current research status of Heterodera glycines resistance and its implication on soybean breeding. Engineering, v. 4, n. 4, p. 534-541, 2018.). The use of resistant cultivars allows the cultivation of the crop of interest, does not incur in additional costs or environmental harm, and enables the production in large areas (EPPO 2008EUROPEAN AND MEDITERRANEAN PLANT PROTECTION ORGANIZATION (EPPO). Heterodera glycines: procedures for official control. OEPP/EPPO Bulletin, v. 38, n. 1, p. 410-413, 2008.). Nevertheless, in 2011, Singh & SchwartzSINGH, S.; SCHWARTZ, H. Review: breeding common bean for resistance to insect pests and nematodes. Canadian Journal of Plant Science, v. 91, n. 2, p. 239-250, 2011. considered that the breeding of common bean plants for resistance to cyst nematode was practically nonexistent, what indicates a lack of studies for this species.

So far, there are few studies evaluating the reaction of bean genotypes to H. glycines. Abawi & Jacobsen (1984)ABAWI, G. S.; JACOBSEN, B. J. Effect of initial inoculum densities of Heterodera glycines on growth of soybean and kidney bean and their efficiency as hosts under greenhouse conditions. Phytopathology, v. 74, n. 12, p. 1470-1474, 1984. showed that the evaluated bean and soybean cultivars did not differ in terms of cyst nematode development. On the other hand, Smith & Young (2003)SMITH, J. R.; YOUNG, L. D. Host suitability of diverse lines of Phaseolus vulgaris to multiple populations of Heterodera glycines. Journal of Nematology, v. 35, n. 1, p. 23-28, 2003. concluded that P. vulgaris genotypes differed in their host suitability to different isolates of H. glycines. Similarly, Poromarto & Nelson (2009)POROMARTO, S. H.; NELSON, B. D. Reproduction of soybean cyst nematode on dry bean cultivars adapted to North Dakota and northern Minnesota. Plant Disease, v. 93, n. 5, p. 507-511, 2009. described a variation in susceptibility for 24 bean cultivars evaluated in Iran. Most of the cultivars evaluated by Heydari et al. (2010)HEYDARI, R.; POURJAM, E.; MAAFI, Z. T.; SAFAIE, N. Comparative host suitability of common bean cultivars to the soybean cyst nematode, Heterodera glycines, in Iran. Nematology, v. 12, n. 3, p. 335-341, 2010. were considered susceptible or moderately susceptible to the HG type 0 populations. In the USA, of 317 lines from the USDA collection, only a small percentage was considered resistant (Jain et al. 2019JAIN, S.; POROMARTO, S.; OSORNO, J. M.; MCCLEAN, P. E.; NELSON, B. D. Genome wide association study discovers genomic regions involved in resistance to soybean cyst nematode (Heterodera glycines) in common bean. PloS One, v. 14, n. 2, e0212140, 2019.). Later, a new study showed that, from the USDA core collection, out of 315 accessions, only 15 were resistant. In Brazil, a histological study revealed that both resistant and susceptible cultivars developed syncytium (Becker et al. 1999BECKER, W. F.; FERRAZ, S.; SILVA, E. A. M. da. Alterações histopatológicas em raízes de feijoeiro comum (Phaseolus vulgaris) infectadas por Heterodera glycines. Nematologia Brasileira, v. 23, n. 1, p. 34-46, 1999.). Becker & Ferraz (2004)BECKER, W. F.; FERRAZ, S. Efeito da concentração inicial de inóculo do nematoide Heterodera glycines no desenvolvimento do feijoeiro comum. Agropecuária Catarinense, v. 17, n. 2, p. 89-93, 2004. demonstrated that the nematode inoculum concentration may interfere with the development of bean and soybean plants. According to Dias et al. (2023)DIAS, W. P.; WENDLAND, A.; CARNEIRO, G. E. S.; OLIVEIRA FILHO, F. G.; LOPES, I. O. N. L. Reaction of common bean genotypes to plant parasitic nematodes. Pesquisa Agropecuária Tropical, v. 53, e74717, 2023., among 81 bean genotypes evaluated, only 7 were considered resistant to H. glycines.

The planting of susceptible host species such as common bean can increase the nematode population in the area and lead to a decline in crop yield. For that reason, the plantings in areas previously cultivated with crops such as soybean represent a greater risk of yield loss by allowing a nematode population increase (Noel et al. 1982NOEL, G. R.; JACOBSEN, B. J.; LEEPER, C. D. Soybean cyst nematode in commercial snap beans. Plant Disease, v. 6, n. 6, p. 520-522, 1982.). Furthermore, a large part of bean cultivation, especially in the third crop (also known as winter crop, which is grown between the months of April and October in Brazil), occurs in central Brazil (Silva & Wander 2018SILVA, O. F. da; WANDER, A. E. Caracterização e avaliação econômica do sistema de cultivo de feijãocomum irrigado no Cerrado: o caso da cultivar BRS Estilo. In: TÔSTO, S. G.; BELARMINO, L. C.; CASTRO, G. S. A.; MANGABEIRA, J. A. de C.; SILVA, O. F. da (ed.). Caracterização e avaliação econômica de sistemas de produção e cultivo de grãos em biomas brasileiros. Brasília, DF: Embrapa, 2018. p. 47-68.), where the presence of high populations (Dias et al. 2004DIAS, W. P.; SILVA, J. F. V.; GARCIA, A.; CARNEIRO, G. E. S. Biologia e controle do nematoide de cisto da soja (Heterodera glycines Ichinohe). In: SARAIVA, O. F.; LEITE, R. M. V. B. de C. (org.). Resultados de pesquisa da Embrapa Soja - 2003: ecofisiologia, biologia molecular e nematoides. Londrina: Embrapa Soja, 2004. p. 10-13., Dias et al. 2009DIAS, W. P.; SILVA. J. F. V.; CARNEIRO, G. E. S.; GARCIA, A.; ARIAS, C. A. A. Nematoide de cisto da soja: biologia e manejo pelo uso da resistência genética. Nematologia Brasileira, v. 33, n. 1, p. 1-17, 2009.) and diversity (Moreira et al. 2020MOREIRA, J. A. A.; TAVARES, M. C.; ARAÚJO, F. G.; MENEZES, I. P. P. Genetic diversity of soybean cyst nematode (Heterodera glycines) populations in southeastern Goiás state, Brasil. Australian Journal of Crop Science, v. 17, n. 7, p. 1162-1170, 2020.) of H. glycines is frequent.

Thus, this study aimed to assess the reaction of 55 common bean genotypes belonging to the Embrapa Arroz e Feijão core collection to Heterodera glycines, race 3/HG type 0.

MATERIAL AND METHODS

The experiments were carried out under greenhouse conditions (16°35’52.1”S and 49°16’53.5”W), from January to April 2020. A completely randomized design was used, with six replications, in which the experimental unit consisted of a plastic cup (500 mL) containing one plant. Fifty-five common bean genotypes (of Mesoamerican origin) from the Embrapa Arroz e Feijão core collection were tested (Table 1). As a susceptibility standard to verify the inoculum viability, the Brasmax Desafio RR soybean cultivar was used. The 55 genotypes were divided into 3 experiments, with 25 genotypes tested in the first one (sowing on Jan. 13, 2020), 13 in the second (sowing on Jan. 20, 2020) and 17 in the third (sowing on Mar. 09, 2020).

Table 1
Description of common bean (Phaseolus vulgaris) accessions belonging to the Embrapa Arroz e Feijão core collection used for the study of host ability to Heterodera glycines.

Initially, 2 seeds were sown per cup containing a substrate composed of soil and sand (1:1, v/v), previously autoclaved. The plants were fertilized with 3 g of Osmocote (15 % of N, 9 % of P and 12 % of K) at the time of sowing. At 8 days after planting, thinning was performed, leaving 1 seedling cup−1.

The H. glycines inoculum was obtained by multiplying a population extracted from soil field samples collected in Rio Verde (Goiás state, Brazil), previously characterized as race 3 or HG type 0. The cysts were collected from the soil throughout the suspension in 2 L of water and subsequently sieved using a 20-mesh sieve (0.84 mm) coupled to a 100-mesh sieve (0.149 mm). The cysts retained in the 100-mesh sieve were collected and transferred to a 100-mesh sieve (0.149 mm) coupled to a 500-mesh sieve (0.025 mm), for the eggs extraction. The cysts were macerated using a test tube and applying little water jets, releasing the eggs and juveniles from the inside of the cysts. The eggs and second stage juveniles (J2) were collected from a 500-mesh sieve (0.025 mm) and counted under a light microscope with the aid of a Peters slide. The inoculum was calibrated for 1,000 eggs + J2 per milliliter.

The inoculation was performed at 8 days after sowing, using 4 mL of calibrated suspension per plant, totalling 4,000 eggs + J2 per plant, divided into two holes (3 cm deep) opened on each side of the plant stem, using an automatic pipette. Irrigation was performed daily. The cups were kept immersed in sand over metal benches to reduce the variation in temperature within the cups.

Evaluations were performed at 38 days after inoculation. The plants were taken to the laboratory and submitted to the evaluation of vegetative variables such as fresh root and shoot mass, and nematological variables such as number of females per root, number of females per 10 g of roots and number of eggs per female.

The root system was carefully removed from the cups and placed in a 20-mesh sieve (0.84 mm) coupled to a 100-mesh sieve (0.149 mm) and washed with strong jets of water for the female release. The roots and shoots of each plant were weighed on a digital scale and later discarded. The females collected on the 100-mesh sieve were transferred to 100-mL beakers with water (Zamboni et al. 2019ZAMBONI, A. C.; SILVA, S. A. da; FERRAZ, L. C. C. B. Métodos em nematologia agrícola. Piracicaba: Sociedade Brasileira de Nematologia, 2019.). The contents of each beaker were poured into filter paper coupled with a small, screened gutter (Andrade et al. 1995ANDRADE, P. J. M.; ASMUS, G. L.; SILVA, J. F. V Um novo sistema para detecção e contagem de cistos de Heterodera glycines recuperados de amostras de solo. Fitopatologia Brasileira, v. 20, supl., p. 358, 1995.). Then the filter paper was transferred to an acrylic plate (10 × 30 cm) for female counting under a stereoscopic microscope (15x magnification), thus determining the number of females and, later, the number of females/10 g of roots.

Ten females from each sample were randomly removed and placed in a beaker (50 mL) with water, then transferred to a 100-mesh sieve (0.149 mm) coupled to a 500-mesh sieve (0.025 mm) and macerated with a glass test tube according to the aforementioned methodology, allowing the release of eggs and J2. The suspension was quantified with the aid of a Peters slide under an optical microscope (50x magnification), thus obtaining the number of eggs + J2 per female. The genotypes resistance to the nematode was determined by the reproduction factor (RF), which was calculated by the ratio between the final (Fp) and the initial population (Ip) of the nematode of each plot (RF = Fp/Ip). According to Oostenbrink (1966)OOSTENBRINK, M. Major characteristics of the relation between nematodes and plant. Mededelingen Landbouwhogeschool, v. 66, n. 4, p. 1-46, 1966., genotypes that present FR < 1.0 are considered resistant.

The obtained data were submitted to non-parametric statistical analysis, using the Kruskal-Wallis test, followed by the post-hoc test (Bonferroni test), and medians were compared at 5 % of probability by the RStudio version 4.1. 3 statistical software (R Core Team 2016R CORE TEAM. R: a language and environment for statistical computing. Vienna: R Foundation for Statistical Computing, 2016.). Statistical tests were performed among bean genotypes, and the Brasmax Desafio RR soybean cultivar was used to verify the inoculum viability.

RESULTS AND DISCUSSION

In the first experiment (Table 2), there was no statistical difference among the treatments for the variables evaluated. All bean accessions tested in this experiment were resistant to Heterodera glycines. The values referring to the reproduction factor (FR) were not subjected to statistical analysis and ranged from 0.07 to 0.66 among the bean accessions (Figure 1). Although no plant prevented the nematode from multiplying (FR = 0), the FR was low for the entire group tested.

Table 2
Reaction of 25 common bean accessions from the Embrapa Arroz e Feijão core collection to Heterodera glycines, at 38 days after inoculation, in the experiment 1.

Figure 1
Reproduction factor of Heterodera glycines on common bean accessions from the Embrapa Arroz e Feijão core collection. A) experiment 1; B: experiment 2; C: experiment 3. All codes are reduced to the last 5 numbers, excluding “BGF00”, for a higher image quality.

For all the accessions tested (Table 2), the nematological variables showed lower values than those observed in soybean (susceptible standard), although it was not included in the statistical analysis. The lower number of eggs/female in the bean accessions, when compared to soybean, shows that the H. glycines fecundity is also affected when they feed on these bean genotypes. This suggests that the nematode has a greater fecundity when it parasitizes soybean. Despite the common bean being an alternative host, it does not offer the same conditions for its development.

All genotypes tested in the second experiment (Table 3) behaved as resistant to the nematode, with FR values ranging from 0.00 to 0.53 (Figure 1). The BGF0005484 genotype showed the lowest root fresh mass, when compared to BGF0006141, which had the highest values for this variable. In addition to the lower root fresh mass, BGF0005484, BGF0011347 and BGF0012685 showed a significantly lower shoot fresh mass, if compared to the BGF000641 genotype.

Table 3
Reaction of 13 common bean accessions from the Embrapa Arroz e Feijão core collection to Heterodera glycines, at 38 days after inoculation, in the experiment 2.

Regarding the nematological variables (Table 3), BGF0012685 presented the highest values for number of females and number of females/10 g of roots (25 and 340, respectively), concerning most of the genotypes studied. While the lowest values for these two variables were observed for the BGF0011360 genotype, 0.33 females and 5.92 females/10 g of roots were related to the BGF0012685, BGF0005887 and BGF0006497 genotypes. Interestingly, this genotype also presented the lowest number of eggs/female, when compared to the BGF0011367 and BGF0006141 genotypes, even when showing an RF = 0, being considered an immune genotype to H. glycines, concerning the Oostenbrink’s classification.

In the experiment 3 (Table 4), 17 genotypes were tested and only BGF0015908 behaved as resistant. However, it did not differ from the other plants, in relation to root and shoot fresh mass. The nematode density (females/10 g of roots) in this genotype differed only from BGF0014855. The RF varied among the bean genotypes from 0.6 to 7.02 (Figure 1). The variable eggs/female showed a statistical difference among the genotypes, but the difference was not detected in the post-hoc test.

Table 4
Reaction of 17 common bean accessions from the Embrapa Arroz e Feijão core collection to Heterodera glycines, at 38 days after inoculation, in the experiment 3.

Although the results for soybean were not included in the statistical analyses, in the experiments 1 and 3 the total number of eggs/female was higher for soybean than in common bean genotypes, what did not occur in the experiment 2, in which only the value of the BGF0011367 genotype exceeded the control. The total number of females was lower for the common bean than in soybean, for all three experiments. This shows that the common bean, even being an alternative host for the soybean cyst nematode, offers conditions for its development, but it is not a better host than soybean. Regarding the variation observed in the nematode female populations, it is important to highlight that these are different bean genotypes. In addition, such variation is inherent in studies with nematodes (Acharya et al. 2021ACHARYA, K.; YAN, G.; PLAISANCE, A. Effects of cover crops on population reduction of soybean cyst nematode (Heterodera glycines). Plant Disease, v. 105, n. 4, p. 764-769, 2021., Pinheiro et al. 2021PINHEIRO, J. B.; SILVA, G. O.; MACÊDO, A. G.; JESUS, J. G.; RAULINO, L.; MAGALHÃES, C. C.; BISCAIA, D.; MELO, R. A. C.; SILVA, P. P.; NASCIMENTO, W. M. Population dynamics of the nematodes Heterodera glycines and Pratylenchus brachyurus in a succession crop of soybean and chickpea. Agronomía Colombiana, v. 39, n. 3, p. 337-342, 2021.).

The Oostenbrink’s (1966)OOSTENBRINK, M. Major characteristics of the relation between nematodes and plant. Mededelingen Landbouwhogeschool, v. 66, n. 4, p. 1-46, 1966. criterion for classifying genotypes, in terms of resistance to nematodes, is the simplest way, because it has only three classes, being susceptible for plants with RF ≥ 1.0, resistant with RF < 1.0 and showing immunity with RF = 0. In the present study, only one inoculum density was used; however, in general, there is an increase in the nematode penetration and reproduction in the plant roots as the inoculum increases up to a certain limit. So, it is desirable to carry out further studies increasing the inoculum concentrations in order to confirm their resistance under higher inoculum pressure (Abawi & Jacobsen 1984ABAWI, G. S.; JACOBSEN, B. J. Effect of initial inoculum densities of Heterodera glycines on growth of soybean and kidney bean and their efficiency as hosts under greenhouse conditions. Phytopathology, v. 74, n. 12, p. 1470-1474, 1984., Becker & Ferraz 2004BECKER, W. F.; FERRAZ, S. Efeito da concentração inicial de inóculo do nematoide Heterodera glycines no desenvolvimento do feijoeiro comum. Agropecuária Catarinense, v. 17, n. 2, p. 89-93, 2004., Araújo et al. 2019ARAÚJO, F. G.; SILVA, J. O.; BARBOSA, K. A. G.; MOREIRA, J. A. A.; ROCHA, M. R. Life cycle of Heterodera glycines in resistant and susceptible soybean. Journal of Agricultural Science, v. 11, n. 2, p. 449-506, 2019.).

Differently from what was proved by Abawi & Jacobsen (1984)ABAWI, G. S.; JACOBSEN, B. J. Effect of initial inoculum densities of Heterodera glycines on growth of soybean and kidney bean and their efficiency as hosts under greenhouse conditions. Phytopathology, v. 74, n. 12, p. 1470-1474, 1984., in the present study the nematode reproduction in susceptible bean genotypes was always lower than that of susceptible soybean. These authors observed that the reproduction did not differ between susceptible cultivars of both crops.

Stricter criteria for classifying genotypes are important at an early stage of the breeding program, so that the best genotypes are selected and resistance genes identified. Becker et al. (1999)BECKER, W. F.; FERRAZ, S.; SILVA, E. A. M. da. Alterações histopatológicas em raízes de feijoeiro comum (Phaseolus vulgaris) infectadas por Heterodera glycines. Nematologia Brasileira, v. 23, n. 1, p. 34-46, 1999. observed that the nematode developed syncytium in two bean cultivars (“Ouro” and “L-2300”, susceptible and resistant, respectively); however, the development of syncytium in the resistant cultivar was not complete.

As observed in the experiment 3, in which most accessions behaved as susceptible, Smith & Young (2003)SMITH, J. R.; YOUNG, L. D. Host suitability of diverse lines of Phaseolus vulgaris to multiple populations of Heterodera glycines. Journal of Nematology, v. 35, n. 1, p. 23-28, 2003. demonstrated that common bean lines could be hosts as good as soybean. This is what happened with the G122 bean genotype, which proved to be a host as good as the Lee 74 soybean cultivar, recommended as a susceptibility standard in the HG type test and race test. The study also reported a large variation in the genotypes’ hostability in relation to the race of the nematode population.

Contrary to what was observed in the present study, Poromarto & Nelson (2009)POROMARTO, S. H.; NELSON, B. D. Reproduction of soybean cyst nematode on dry bean cultivars adapted to North Dakota and northern Minnesota. Plant Disease, v. 93, n. 5, p. 507-511, 2009. reported that all 24 bean cultivars evaluated allowed the normal development of H. glycines females (HG type 0) under greenhouse conditions, representing a potential threat to dry bean in northern North Dakota and northern Minnesota. In this same sense, Heydari et al. (2010)HEYDARI, R.; POURJAM, E.; MAAFI, Z. T.; SAFAIE, N. Comparative host suitability of common bean cultivars to the soybean cyst nematode, Heterodera glycines, in Iran. Nematology, v. 12, n. 3, p. 335-341, 2010., studying the 11 most used bean cultivars in Iran, showed that most cultivars were susceptible or moderately susceptible to populations of HG Type 0 of H. glycines.

According to Mizobutsi et al. (2012)MIZOBUTSI, E. H.; FERRAZ, S.; MIZUBUTI, E. S.; DIAS-ARIEIRA, C. R.; RIBEIRO, R. C. Viabilidade e sobrevivência do inóculo de Heterodera glycines raça 3 no solo. Tropical Plant Pathology, v. 37, n. 3, p. 223-226, 2012., the H. glycines inoculum, race 3, produced in bean is less viable in the soil than that produced in soybean, since the development of the nematode is directly related to the formation of a viable feeding site that guarantees the development and support of female in its reproductive stage for a new cycle to be generated. This does not occur in the resistant and susceptible bean cultivars studied by the authors, indicating that there is a nutritional restriction in alternative hosts of the nematode, such as the common bean. This fact impacts the development of the nematode as well as the nutrition of the adult female, which affects the viability of eggs produced and causes population reduction in the next cycle.

The results of Mizobutsi et al. (2012)MIZOBUTSI, E. H.; FERRAZ, S.; MIZUBUTI, E. S.; DIAS-ARIEIRA, C. R.; RIBEIRO, R. C. Viabilidade e sobrevivência do inóculo de Heterodera glycines raça 3 no solo. Tropical Plant Pathology, v. 37, n. 3, p. 223-226, 2012. showed that the J2 penetration was low in L2300 (resistant) and Ouro (susceptible) bean cultivars, when compared to susceptible soybean (cv. FT-Cristalina). This phase is dependent on energy reserves that come from the accumulation of lipids during embryonic development, which, in turn, depends on the female’s good nutrition. The same occurred in relation to female survival, which was lower in L2300, cv. Gold, and soybean. Thus, the use of resistant bean cultivars or those that have a low reproduction factor can be good alternatives in the management of the nematode. Furthermore, it shows the need to identify the resistance mechanisms that may be present in resistant genotypes.

It is important to point out that in the present study the genotypes were tested only for the race 3 (HG Type 0) of the nematode; but under field conditions, there are other races that may prevail among those existing in the area, and genotypes resistant to a certain race may be susceptible to others. Jain et al. (2019)JAIN, S.; POROMARTO, S.; OSORNO, J. M.; MCCLEAN, P. E.; NELSON, B. D. Genome wide association study discovers genomic regions involved in resistance to soybean cyst nematode (Heterodera glycines) in common bean. PloS One, v. 14, n. 2, e0212140, 2019., through phenotyping tests, reported 86 bean accessions from the USDA common bean core collection as resistant to HG type 0. Shi et al. (2021)SHI, A.; GEPTS, P.; SONG, Q.; XIONG, H.; MICHAELS, T. E.; CHEN, S. Genome-wide association study and genomic prediction for soybean cyst nematode resistance in USDA common bean (Phaseolus vulgaris) core collection. Frontiers in Plant Science, v. 12, e624156, 2021., who also worked with these accessions, identified that of these only 59 accessions were resistant to the HG type 0 (race 6). As this HG type may correspond to race 3 or 6, it is possible that the 86 accessions were tested for race 3. Later, evaluating 81 common bean genotypes in Brazil, Dias et al. (2023)DIAS, W. P.; WENDLAND, A.; CARNEIRO, G. E. S.; OLIVEIRA FILHO, F. G.; LOPES, I. O. N. L. Reaction of common bean genotypes to plant parasitic nematodes. Pesquisa Agropecuária Tropical, v. 53, e74717, 2023. observed that only seven of them were considered resistant to the race 1 of the soybean cyst nematode.

In any case, those genotypes that proved to be susceptible, regardless of the HG type, should be discarded for future studies and focus on the resistant ones. Even those genotypes that behave as resistant must be subject of further studies to confirm the resistance and to investigate the mechanisms and genes involved. It is also important to continue phenotyping tests in order to evaluate the whole Embrapa Arroz e Feijão core collection with a view to identify sources of resistance to this nematode and other species.

CONCLUSIONS

Among the 55 bean accessions evaluated, 34 were resistant to Heterodera glycines. The accessions that proved to be resistant, in addition to presenting a lower population of females in the roots, also reduced the fecundity of the nematode, an important aspect in its hostability.

ACKNOWLEDGMENTS

The authors thank the Embrapa Arroz e Feijão for providing the seeds of the common bean genotypes; the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for the productivity fellowship to the first author; and the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (Capes) for the master’s degree scholarship and postdoctoral fellowship to the second and third authors, respectively.

REFERENCES

  • ABAWI, G. S.; JACOBSEN, B. J. Effect of initial inoculum densities of Heterodera glycines on growth of soybean and kidney bean and their efficiency as hosts under greenhouse conditions. Phytopathology, v. 74, n. 12, p. 1470-1474, 1984.
  • ABAWI, G. S.; WIDMER, T. L. Impact of soil health management practices on soilborne pathogens, nematodes and root diseases of vegetable crops. Applied Soil Ecology, v. 15, n. 1, p. 37-47, 2000.
  • ACHARYA, K.; YAN, G.; PLAISANCE, A. Effects of cover crops on population reduction of soybean cyst nematode (Heterodera glycines). Plant Disease, v. 105, n. 4, p. 764-769, 2021.
  • ANDRADE, P. J. M.; ASMUS, G. L.; SILVA, J. F. V Um novo sistema para detecção e contagem de cistos de Heterodera glycines recuperados de amostras de solo. Fitopatologia Brasileira, v. 20, supl., p. 358, 1995.
  • ARAÚJO, F. G.; SILVA, J. O.; BARBOSA, K. A. G.; MOREIRA, J. A. A.; ROCHA, M. R. Life cycle of Heterodera glycines in resistant and susceptible soybean. Journal of Agricultural Science, v. 11, n. 2, p. 449-506, 2019.
  • BECKER, W. F.; FERRAZ, S. Efeito da concentração inicial de inóculo do nematoide Heterodera glycines no desenvolvimento do feijoeiro comum. Agropecuária Catarinense, v. 17, n. 2, p. 89-93, 2004.
  • BECKER, W. F.; FERRAZ, S.; SILVA, E. A. M. da. Alterações histopatológicas em raízes de feijoeiro comum (Phaseolus vulgaris) infectadas por Heterodera glycines. Nematologia Brasileira, v. 23, n. 1, p. 34-46, 1999.
  • BONFIM JUNIOR, M. F.; INOMOTO, M. M.; ARAÚJO FILHO, J. V. Phytonematodes infesting common bean fields in Brazil, and pathogenicity tests with Pratylenchus brachyurus. Arquivos do Instituto Biológico, v. 88, e00312020, 2021.
  • COMPANHIA NACIONAL DE ABASTECIMENTO (Conab). Acompanhamento da safra brasileira de grãos. Brasília, DF: Conab, 2023.
  • DIAS, W. P.; SILVA, J. F. V.; GARCIA, A.; CARNEIRO, G. E. S. Biologia e controle do nematoide de cisto da soja (Heterodera glycines Ichinohe). In: SARAIVA, O. F.; LEITE, R. M. V. B. de C. (org.). Resultados de pesquisa da Embrapa Soja - 2003: ecofisiologia, biologia molecular e nematoides. Londrina: Embrapa Soja, 2004. p. 10-13.
  • DIAS, W. P.; SILVA. J. F. V.; CARNEIRO, G. E. S.; GARCIA, A.; ARIAS, C. A. A. Nematoide de cisto da soja: biologia e manejo pelo uso da resistência genética. Nematologia Brasileira, v. 33, n. 1, p. 1-17, 2009.
  • DIAS, W. P.; WENDLAND, A.; CARNEIRO, G. E. S.; OLIVEIRA FILHO, F. G.; LOPES, I. O. N. L. Reaction of common bean genotypes to plant parasitic nematodes. Pesquisa Agropecuária Tropical, v. 53, e74717, 2023.
  • EUROPEAN AND MEDITERRANEAN PLANT PROTECTION ORGANIZATION (EPPO). Heterodera glycines: procedures for official control. OEPP/EPPO Bulletin, v. 38, n. 1, p. 410-413, 2008.
  • FERRAZ, S.; VALLE, L. A. C.; DIAS, C. R. Utilização de plantas antagônicas no controle do nematoide de cisto da soja (Heterodera glycines Ichinohe). In: SOCIEDADE BRASILEIRA DE NEMATOLOGIA. O nematoide de cisto da soja: a experiência brasileira. Jaboticabal: Artsigner, 1999. p. 25-53.
  • FOOD AND AGRICULTURE ORGANIZATION OF THE UNITED NATIONS (FAO). Statistics Division. Countries by commodity: beans, dry. 2022. Avalaible at: https://www.fao.org/faostat/en/#rankings/countries_by_commodity. Access on: Jan. 21, 2024.
    » https://www.fao.org/faostat/en/#rankings/countries_by_commodity.
  • FREIRE, F. C. O.; FERRAZ, S. Nematoides associados ao feijoeiro, na Zona da Mata, Minas Gerais, e efeitos do parasitismo de Meloidogyne incognita e M. javanica sobre o cultivar “Rico 23”. Revista Ceres, v. 24, n. 1, p. 141-149, 1977.
  • HEYDARI, R.; POURJAM, E.; MAAFI, Z. T.; SAFAIE, N. Comparative host suitability of common bean cultivars to the soybean cyst nematode, Heterodera glycines, in Iran. Nematology, v. 12, n. 3, p. 335-341, 2010.
  • JAIN, S.; POROMARTO, S.; OSORNO, J. M.; MCCLEAN, P. E.; NELSON, B. D. Genome wide association study discovers genomic regions involved in resistance to soybean cyst nematode (Heterodera glycines) in common bean. PloS One, v. 14, n. 2, e0212140, 2019.
  • MELTON, T. A.; JACOBSEN, B. J.; NOEL, G. R. Effects of temperature on development of Heterodera glycines on Glycines max and Phaseolus vulgaris. Journal of Nematology, v. 18, n. 4, p. 468-474, 1986.
  • MIZOBUTSI, E. H.; FERRAZ, S.; MIZUBUTI, E. S.; DIAS-ARIEIRA, C. R.; RIBEIRO, R. C. Viabilidade e sobrevivência do inóculo de Heterodera glycines raça 3 no solo. Tropical Plant Pathology, v. 37, n. 3, p. 223-226, 2012.
  • MOREIRA, J. A. A.; TAVARES, M. C.; ARAÚJO, F. G.; MENEZES, I. P. P. Genetic diversity of soybean cyst nematode (Heterodera glycines) populations in southeastern Goiás state, Brasil. Australian Journal of Crop Science, v. 17, n. 7, p. 1162-1170, 2020.
  • NOEL, G. R.; JACOBSEN, B. J.; LEEPER, C. D. Soybean cyst nematode in commercial snap beans. Plant Disease, v. 6, n. 6, p. 520-522, 1982.
  • OOSTENBRINK, M. Major characteristics of the relation between nematodes and plant. Mededelingen Landbouwhogeschool, v. 66, n. 4, p. 1-46, 1966.
  • PINHEIRO, J. B.; SILVA, G. O.; MACÊDO, A. G.; JESUS, J. G.; RAULINO, L.; MAGALHÃES, C. C.; BISCAIA, D.; MELO, R. A. C.; SILVA, P. P.; NASCIMENTO, W. M. Population dynamics of the nematodes Heterodera glycines and Pratylenchus brachyurus in a succession crop of soybean and chickpea. Agronomía Colombiana, v. 39, n. 3, p. 337-342, 2021.
  • POROMARTO, S. H.; NELSON, B. D. Reproduction of soybean cyst nematode on dry bean cultivars adapted to North Dakota and northern Minnesota. Plant Disease, v. 93, n. 5, p. 507-511, 2009.
  • R CORE TEAM. R: a language and environment for statistical computing. Vienna: R Foundation for Statistical Computing, 2016.
  • SATO, K.; KADOTA, Y.; SHIRASU, K. Plant immune responses to plant parasitic nematodes. Frontiers in Plant Science, v. 10, e1165, 2019.
  • SHAIBU, A. S.; LI, B.; ZHANG, S.; SUN, J. Soybean cyst nematode-resistance: gene identification and breeding strategies. The Crop Journal, v. 8, n. 6, p. 892-904, 2020.
  • SHI, A.; GEPTS, P.; SONG, Q.; XIONG, H.; MICHAELS, T. E.; CHEN, S. Genome-wide association study and genomic prediction for soybean cyst nematode resistance in USDA common bean (Phaseolus vulgaris) core collection. Frontiers in Plant Science, v. 12, e624156, 2021.
  • SILVA, O. F. da; WANDER, A. E. Caracterização e avaliação econômica do sistema de cultivo de feijãocomum irrigado no Cerrado: o caso da cultivar BRS Estilo. In: TÔSTO, S. G.; BELARMINO, L. C.; CASTRO, G. S. A.; MANGABEIRA, J. A. de C.; SILVA, O. F. da (ed.). Caracterização e avaliação econômica de sistemas de produção e cultivo de grãos em biomas brasileiros. Brasília, DF: Embrapa, 2018. p. 47-68.
  • SINGH, S.; SCHWARTZ, H. Review: breeding common bean for resistance to insect pests and nematodes. Canadian Journal of Plant Science, v. 91, n. 2, p. 239-250, 2011.
  • SMITH, J. R.; YOUNG, L. D. Host suitability of diverse lines of Phaseolus vulgaris to multiple populations of Heterodera glycines. Journal of Nematology, v. 35, n. 1, p. 23-28, 2003.
  • UEBERSAX, M. A.; CICHY, K. A.; GOMEZ, F. E.; PORCH, T. G.; HEITHOLT, J.; OSORNO, J. M.; KAMFWA, K.; SNAPP, S. S.; BALES, S. Dry beans (Phaseolus vulgaris L.) as a vital component of sustainable agriculture and food security: a review. Legume Science, v. 5, n. 1, p. 155-155, 2022.
  • YAN, G. P.; PLAISANCE, A.; CHOWDHURY, I.; BAIDOO, R.; UPADHAYA, A.; PASCHE, J.; MARKELL, S.; NELSON, B.; CHEN, S. First report of the soybean cyst nematode Heterodera glycines infecting dry bean (Phaseolus vulgaris L.) in a commercial field in Minnesota. Plant Disease, v. 101, n. 2, p. 391-391, 2017.
  • YAN, G.; BAIDOO, R. Current research status of Heterodera glycines resistance and its implication on soybean breeding. Engineering, v. 4, n. 4, p. 534-541, 2018.
  • ZAMBONI, A. C.; SILVA, S. A. da; FERRAZ, L. C. C. B. Métodos em nematologia agrícola. Piracicaba: Sociedade Brasileira de Nematologia, 2019.

Publication Dates

  • Publication in this collection
    27 May 2024
  • Date of issue
    2024

History

  • Received
    02 Feb 2024
  • Accepted
    22 Mar 2024
  • Published
    12 Apr 2024
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