Most common plant parasitic nematodes associated with soybean worldwide.
Plant‐parasitic nematodes are one of the limiting factors for soybean production worldwide. Overall, plant‐parasitic nematodes alone cause an estimated annual crop loss of $78 billion worldwide and an average crop yield loss of 10–15%. This imposes a challenge to sustainable production of food worldwide, since there has been increasing demand for food supply and food security. Unsustainable cropping production systems with monocultures, intensive use of soils and expansion of crops to newly opened areas have intensified problems associated with new pests and diseases. Thus, finding and applying sustainable methods to control diseases associated with soybean are in current need. Over hundred nematode species, comprising fifty genera, have been reported in association with soybean. Of these, the root‐knot nematode Meloidogyne spp., cyst nematode Heterodera glycines, lesion nematode Pratylenchus brachyurus and the reniform nematode Rotylenchulus reniformis are major nematode species limiting soybean production. Here, we report an up‐to‐date literature review on the biology, symptoms, damage and control methods used for these nematodes species. Additionally, unusual and emergent nematode species affecting soybean are discussed.
- lesion nematode
- plant parasitic nematodes
- yield loss
According to the United States Department of Agriculture (USDA), in the 2013/2014 cropping year, USA, Brazil and Argentina accounted for 81.40% of the total world production of soybeans, and China by 64.26% of all world imports. Brazil accounted for the production of 86.27 million tons of soybeans, that is, 44.50% of the Brazilian production of grains with Brazilian average productivity of 3000 kg/ha, which is the second largest producer and processor of grains into meal and oil .
Currently, the rationality of production and the use of alternative fuels derived from biomass, especially bio‐ethanol and vegetable oils, are being increasingly recommended to complement or improve the energy matrices worldwide. Among the producing crops for energy biomass used for biodiesel production features the soybean that is being currently studied as a promising crop for the production of biodiesel. However, in addition to economic feasibility studies including energy efficiency, organization of production system and crop adaptation, it is necessary to take into account policy studies related to diseases and pests in agricultural systems where crops are or will be implemented in order to decrease losses due to pathogen attack.
There has been increasing demand for food supply and food security. Unsustainable cropping production system with monocultures, intensive planting and expansion of crops to newly opened areas has increased problems associated with new pests and diseases. Among these problems, plant parasitic nematodes are one of the limiting factors for soybean production worldwide. Plant parasitic nematodes alone cause an estimated annual crop loss of $78 billion worldwide and an average crop yield loss of 10–15%. Nonetheless, soybean yield loss due to nematode parasitism is quite variable and mostly depends on factors such as nematode species, their population levels, susceptibility of the cultivars, cropping systems, temperatures, time of the year, region and soil factors including soil texture, pH and fertility. The yield loss can reach up to 30–100% in some reported cases [2, 3].
More than 100 nematode species, comprising 50 genera, have been reported in association with soybeans. In Brazil, the species that cause the most damage to soybean are
Since pathogens such as plant parasitic nematodes represent major losses in agricultural systems, especially when the systems are not managed sustainably, the searches for information on the occurrence of nematodes in the production system, population density, species, levels of damage, and monitoring and management of these populations are essential in regions where crops will be implemented.
The goal of this chapter is to report a literature review of main nematode species affecting soybean worldwide and the methods used for their sustainable management in the field. Although there are numerous nematode species associated with soybean, few of them have been continuously reported as major constraint to soybean production worldwide. These include: (i)
|Common name||Species name|
|Soybean cyst nematode|
|Root lesion nematode|
2. Major nematode species affecting soybean
2.1. Root‐knot nematodes (
Root‐knot nematodes (RKN),
In several field surveys for RKN nematodes in main regions of soybean production in Brazil,
In a survey of more than hundreds of soybean fields in USA, it was found  that
Symptoms in the field include yellowing and sub‐development of infested plants. RKN nematodes induce hypertrophy and hyperplasia of infected cells leading to swelling of tissues commonly known as galls. The number and sizes of galls vary depending on the susceptibility of the cultivar, population density and favorable temperatures . RKN‐infected roots change their nutrient and water uptake, leading to decreased yield. Commonly, there are high levels of intraspecific variation within
RKN are endo‐sedentary parasitic nematodes. The second‐stage juvenile (J2) is the infective stage. After RKN hatch from eggs, the J2 migrates through the soil toward suitable root and uses special enzymes and the stylets to force penetration into the vascular cylinder where RKN establish their feeding site by inducing hypertrophy and hyperplasia of a group of cells leading to swelling and formation of giant cells. On this site, nematode goes through three more molting to become a swollen young female. Mature females begin laying eggs in the root, forming mass eggs wrapped in a gelatinous matrix. Each egg mass contains 400–500 eggs on average, and it is formed in the midst of cortical parenchyma or on the surface of the roots. The embryonic development of the nematode results in the first stage (J1) passing through an ecdysis in the egg, followed by the second stage (J2). Adult males do not feed on soybean roots; they leave the root and move freely in the soil until they die .
To control RKN is extremely difficult. Currently, the most effective and environmentally sound way to control RKN is the use of resistant cultivars that stand good yield and have been tested in a particular region where soybeans are planted , the use of tolerant genetic materials and rotation/succession with non‐ and poor host crops [10, 12]. The use of nematicides at planting or via seed treatment is an option. However, they are costly, not very effective, and have side effects to human and to the environment .
Currently, several soybean genotypes have been described as resistant or moderately resistant to
For the 2014/2015 cropping year, the following soybean cultivars were released by Embrapa with reported resistance to
Prior to using resistant soybean cultivar in a certain area, grower should consider the nematode species present in the field, because, although there may be predominance of one species of nematode over another, the presence of mixed populations is very common, which may limit the use of resistant varieties. In addition, in the choice of soybean cultivar, grower must take into consideration the adaptation and yield potential of the cultivar.
However, other control methods for RKN should also be considered. For instance, the use of antagonistic non‐host plants such as
2.2. Soybean cyst nematode (
The soybean cist nematode,
Mature females of soybean cyst nematode retain their eggs inside their bodies after their deaths. The body is formed by a cuticle embedded with polyphenol tanning, resulting in a hard protective structure name cyst which is viable overwintering in the soil for up to 6–8 years. Thus, once the nematode is introduced in soybean fields, it is almost impossible to eliminate it completely. Females can also lay eggs in egg sacs. With stimuli of host root exudate, moisture and temperature, juvenile nematode (J2) hatches from eggs or emerges from cyst and moves freely in the soil. This is the only life stage that is able to infect plant. Following the stimulus of root exudate, J2 can use its stylet and degrading enzymes to penetrate the root and gain access into vascular tissue. There, J2 injects special enzymes that modify and transform a group of cells into specialized feeding sites (nurse cells). Female nematode then becomes lemon shape and eventually breaks through the root tissue and becomes exposed on the root surface. Mature female produces eggs (200–400) either in egg sac or inside the body (cyst) [24, 28]. The cyst then persists in the soil for several years. The entire cycle is completed in 24–30 days depending on optimal conditions, such as moisture and temperature (23–28°C) [26, 28, 29].
Usually, the nematodes can complete three to six generations a year. The cyst nematode reproduces by sexual reproduction (amphimixis), and its genome is characterized by an extremely high diversity, leading to several races of the pathogen. Soybean cyst nematodes can be spread to long distances effectively by means of infested soil particles, farm machinery, vehicles, tools, wind, water and animals among others [29, 30].
Symptoms of soybean cyst nematode can be mistaken for other disease symptoms as well as for management‐associated problems, including iron and other nutrient deficiencies, herbicide toxicity and drought stress . The appearance of cyst nematode symptoms attributed to other causes may lead to non‐detection of the nematode for several years until its population builds up. Soybean infected with cyst nematode appears in the field as irregular patches of stunted, yellowed, less developed plants. Usually, symptoms are more severe in light sandy soils, but it also occurs in heavy soil. The root system infected with soybean cyst nematode is smaller and stunted, and the infection affects nodule formation and decreases nitrogen fixation. In addition, nematode‐infected roots are more prone to soilborne fungi and bacterial pathogen secondary infection. The presence of adult females and cysts attached to soybean roots is typical of soybean cyst nematode infection [25, 26, 29].
Since soybean cyst nematodes can survive inside cysts for several years, once the nematodes have been introduced into soybean field, they are not likely to be easily eradicated. Nonetheless, there are recommended cropping management practices that minimize the problem. For instance, the use of soybean resistant varieties is the most effective way to control this nematode and have been used successfully. Several soybean cultivars have been released, and their sources of resistance come from the parental cultivars PI88788 or the Peking. To avoid breakdown of resistance, it is recommended to use cultivars alternately [11, 29]. It is recommended to use alternately among susceptible and resistant cultivars. For instance, use one susceptible cultivar after two to four years of cultivation with resistant cultivars . In Brazil, most resistant soybean cultivars are specific to races 1 and 3 and are not well adapted to every soybean‐growing region. Besides, due to soybean rust disease, growers are choosing early maturity varieties which are more susceptible to cyst nematode .
Another effective method in controlling soybean cyst nematode is the use of rotation with non‐host crops. Soybean cyst nematode has a narrow host range which facilitates rotation with other non‐host crops. The pathogen levels in the soil significantly decrease, once there is no suitable host for infection. Good examples of non‐host crops are maize, sorghum, oat, alfalfa, rice, cotton, sunflower and castor bean. Rotation for 1 year with one of these crops significantly decreased the population level of cyst nematode, allowing planting of susceptible soybean cultivar in the following cycle .
Although the use of soybean resistant cultivars and crop rotation has worked well, growers should be careful to provide good management practices in soybean areas, including good pH levels and soil fertility in order to maintain the effects of these disease control methods [11, 25, 29]. In summary, the scheme using crop rotation and resistant and susceptible varieties is the best way to manage soybean cyst nematode. For example, the use of maize, resistant soybean cultivar and susceptible soybean cultivar has been one of the best approaches to manage the nematode in the field .
2.3. Root lesion nematode (
Root lesion nematode,
More than 50% of soybean in Brazil are produced in the Cerrado region (vegetation like savanna), with an increase in production over 100% in the central and northeast region . The expansion in areas planted with soybean in the Cerrado region has contributed to intensive agriculture, leading to agronomic challenges, including nematode infection . Among plant parasitic nematodes that infect soybean,
Root lesion nematodes are more common on sandy soils and regions with high temperatures. Eggs are deposited in the roots (cortex) or in the soil. The incubation period ranges from six to eight days at a temperature of 28–30°C. The first molt takes place inside the egg and the other three occur out of the egg. Males and females emerge in 29–32 days. However, at low temperatures the life cycle may be longer. Usually, this nematode occurs in low population in the soil and at high population inside root tissue .
Pathogenicity studies suggested that
In Northern Brazil,
To assess the effect of
Among these economically important crops, maize is the main one used in succession or rotation especially with soybeans. However, this management strategy enables increase in
The use of soybean resistant varieties is probably the best way to control nematode infection, because it is easy, cheap, effective and environmentally safe. Host resistance has been explored. However, no
Seed treatment with nematicides has also been suggested to control
2.4. Reniform nematode (
The reniform nematode,
Sikora et al.  studied
Symptoms caused by
The wide host range of
A promising alternative control to
Considering the host resistance, some soybean varieties are recommended against
Additionally, other sources of resistance have been assessed against
3. Other emerging nematode species threatening soybean production
Lately in Brazil cases of unusual, emergent nematode species affecting soybean fields have been reported. For instance, the nematodes
A new soybean disease named ‘crazy soybean’ is caused by
4. Concluding remarks
This review has shown that there are a significant number of plant parasitic nematodes negatively impacting soybean yield worldwide. Due to intensified land use, monocultures and the use of unsustainable management practices, uncommon nematode species are becoming a new threat to soybean production. This imposes a real challenge to researches to search promptly for new approaches to manage these nematode diseases. Researches and growers should recognize that in fact, nematode diseases negatively impact soybean yield and that sustainable management practices should be considered in order to decrease nematode population level and have a good yield performance. When deciding the management approaches, it is essential to consider them holistically.
Fontana JD, editor. Biodiesel: para leitores de 9 a 90 anos. 1st ed. Curitiba, Brazil: UFPR; 2011. 253 p.
Schmitt DP, Barker KR. Damage and reproduction potentials of Pratylenchus brachuyrusand P. penetranson soybean. Journal of Nematology. 1981; 13(3):327–332.
Barker KR. Introduction. In: Barker KR, Pederson GA, Winhan GL, editors. Plant and Nematode Interactions. Madison, USA: American Society of Agronomy; 1998. pp. 1–120.
Franzener G, Unfried JR, Stangarlin JR, Furlanetto C. Nematoides formadores de galhas e de cisto patogênicos a cultura da soja em municípios do Oeste do Paraná. Nematologia Brasileira. 2005; 29:161–165.
Santana HPE, Comerlato AP, Nasu EGC, Furlanetto C. Variabilidade genética em populações de campo do nematoide de cisto da soja provenientes dos estados do Paraná e Rio Grande do Sul. Tropical Plant Pathology. 2009; 34:261–264.
Dias WP, Ribeiro NR, Lopes ION, Garcia A, Carneiro GES, Silva JFV. Manejo de nematoides na cultura da soja. In: Congresso Brasileiro de Nematologia; 12 de Agosto; Goiânia, Brazil. Goiânia: Sociedade Brasileira de Nematologia. 2007. pp. 26–30.
Furlanetto C, Seifert KE, Fenterseifer CE, Page EC, Davi JJS, Grabouski MMS. Desenvolvimento das culturas de soja, milho e trigo cultivadas em áreas infestadas com o nematoide Tubixaba tuxaua noOeste do Paraná. Tropical Plant Pathology. 2010; 35:295–302.
Karssen G, Moens M. Root‐knot nematodes. In: Perry RN, Moens M, editors. Plant Nematology. Wallingford, UK: CABI Publishing. 2006. pp. 59–90.
Moens M, Perry R, Starr J. Meloidogynespecies‐ a diverse group of novel and important plant parasites. In: Perry RN, Moens M, Star JL, editors. Root‐knot Nematodes. Wallingford, UK: CABI International 2009. pp. 1–17.
Almeida AMR, et al. Doenças da soja. In: Kimati H, et al, editors. Manual de Fitopatologia. São Paulo, Brazil: Ceres; 2005. pp. 569–588.
Dias WP, Garcia A, Silva JFV, Carneiro GES. Nematoides em Soja: identificação e controle. Circular Técnica da Embrapa. 2010; 76:1–8.
Embrapa. Tecnologias de produção de soja na região central do Brasil. Londrina‐Parana, Brazil: Embrapa; 2011. 262 p.
Castro JMC, Lima R, Carneiro RMDG. Variabilidade isoenzimática de populações de Meloidogynespp. provenientes de regiões brasileiras produtoras de soja. Nematologia Brasileira. 2003; 27(1):1–12.
Roese AD, Oliveira RDL, Lanes FF. Reação de cultivares de soja [ Glycines maxL. Merril] a Meloidogyne paranaensis. Nematologia Brasileira. 2004; 28(2):131–135.
Lima EA, Mattos JK, Moita AW, Carneiro RG, Carneiro RMDG. Host status of different crops to Meloidogyne ethiopicacontrol. Tropical Plant Pathology. 2009; 34:152–157.
Garcia MR, Rich R. Root‐knot nematodes in North‐Central Florida soybean fields. Nematropica. 1985; 15(1):43–48.
Fourie H, Mc Donald AH, Loots GC. Plant parasitic nematodes in field crops in South Africa 6: soybean. Nematology. 2001; 3:447–454.
Doucet ME, Pinochet J. Occurrence of Meloidogynespp. in Argentina. Supplemental Journal of Nematology. 1992; 24:765–770.
Dias WP, Asmus GL, Silva JFV, Garcia A, Carneiro GES. Nematoides. In: Almeida AMR, Seixas CDR, editors. Soja: doenças radiculares e de hastes e inter‐relações com o manejo do solo e da cultura. Londrina, Brazil: Embrapa Soja; 2009. pp. 173–206.
Moens M, Perry RN, Starr JL. Meloidogynespecies‐ a diverse group of novel and important plant parasites. In: Perry RN, Moens M, Starr JL, editors. Root Knot Nematodes. Wallingford, UK: CABI International; 2009. pp. 1–18.
Gowen SR. Chemical control of nematodes: efficiency and side‐effects. FAO Plant Production and Protection Paper. 1997; 144:59–65.
Embrapa. Cultivares de soja safra 2014–2015 macrorregiões 4 e 5: regiões Norte e Nordeste do Brasil. Embrapa. 2014;1:1–5.
Embrapa. Cultivares de soja lançamento 2015–2016. Embrapa Soja. 2015;1:1–5.
Santana Gomes SM, Dias‐Arieira CR, Biela F, Cardoso MR, Fontana LF, Puerari HH. Sucessão de culturas no manejo de Pratylenchus brachyurusna soja. Nematropica. 2014; 44(2):1–14.
Riggs RD, Schmitt DP. Soybean cyst nematode. In: Sinclair JB, Backman PA, editors. Compendium of Soybean Diseases. 3rd ed. St. Paul, MN, USA: The American Phytopathological Society; 1989. pp. 65–67.
Dias WP, Silva JFV, Garcia A, Carneiro GES. Biologia e controle do nematoide do cisto da soja ( Heterodera glycines). In: Embrapa Soja, editor. Resultado de pesquisa da Embrapa Soja‐Soja: ecofisiologia, biologia molecular e nematoides. Londrina, Brazil: Embrapa Soja; 2004. pp. 1–48.
Grigolli JFJ, Asmus GL. Manejo de nematoides na cultura da soja. Circular Técnica. 2014; 1:1–19.
Moore WF, Bost SC, Brewer FL, Dun RA, Endo BY, Grau CR, Hardman LL et al. Soybean cyst nematode. Soybean Industry Resources Committee. 1984; 1:1–23.
Tylk G. Soybean cyst nematode [Internet] 1994. [Updated: January 1994]. Available from: http://nematode.unl.edu/scn/scnisu.html
Dias WP, Silva JFV, Carneiro GES, Garcia A, Arias CAA. Nematoides de cisto da soja: biologia e manejo pelo uso da resistência genética. Nematologia Brasileira. 2009; 33(1):1–16.
Ferraz LCCB. Gênero Pratylenchus: os nematoides das lesões radiculares. In: Luiz WC, editor. Revisão Anual de Patologia de Plantas. 1st ed. Passo Fundo: RAPP; 1999. pp. 158–195.
Embrapa Soja. Tecnologias de Produção de Soja. Londrina, Brazil: Embrapa Soja; 2006. 217 p.
De Waele D, Elser A. Migratory endoparasites: Pratylenchusand Radopholusspecies. In: Star JJ, Cook R, Bridge J, editors. Plant Resistance to Parasitic Nematodes. Wallingford, UK: CAB International; 2002. pp. 175–206.
Ribeiro LM, Campos HD, Dias‐Arieira CR, Neves DL, Ribeiro GC. Effect of soybean seed treatment on the population dynamics of Pratylenchus brachyurusunder water stress conditions. Journal of Bioscience. 2014; 30(3):616–622.
Lima FSO, Santos GR, Nogueira SR, Santos PRR, Correa VR. Population dynamics of the root lesion nematode Pratylenchus brachyurusin soybean fields in Tocantins State and its effect to soybean yield. Nematropica. 2015; 45:170–177.
Neves DL, Ribeiro LM, Dias‐Arieira CR, Campos HD, Ribeiro GC. Sobrevivência de Pratylenchus brachyurusem diferentes substratos com baixo teor de umidade. Nematropica. 2012; 42:211–217.
Castillo P, Vovlas N, editors. Pratylenchus(Nematoda: Pratylenchidae): Diagnosis, Biology, Pathogenicity and Management. Leiden: Brill; 2007. 529 p.
Koenning SR, Schmitt DP, Barker KP. Influence of planting date on population dynamics and potential of Pratylenchus brachyuruson soybean. Journal of Nematology. 1985; 17:428–434.
Panorama R. Nematoides- a praga da safra. Panorama Rural. 2010;131:1-2.
Franchini JC, Saraiva OF, Debiase H, Goncalves SL. Contribuição de sistema de manejo do solo para produção sustentável da soja. Circular Técnica. 2007; 46:1–4.
Inomoto MM, Siqueira KMS, Machado ACZ. Sucessão de culturas sob pivô central para controle de fitonematoides: variação populacional, patogenicidade e estimativa de perdas. Tropical Plant Pathology. 2011; 36:178–185.
Rios ADF, Rocha MR, Machado AS, Ávila KAGB, Teixeira RA, Santos LC, Rabelo LRS. Host suitability of soybean and corn genotypes to the lesion caused by nematode under natural infestation conditions. Ciência Rural. 2016; 46:580–584.
Machado ACZ. Host status of some selected Brazilian soybean cultivars to Pratylenchus brachyurus. In: Internacional Congress of Tropical Nematology; 15 de agosto; Maceió, Brazil. Maceió: Sociedade Brasileira de Nematologia; 2009. 1 p.
Bessi R, Sujimoto RF, Inomoto MM. Seed treatment affects Meloidogyne incognitapenetration, colonization and reproduction in cotton. Ciência Rural. 2010; 40(6):1428–1430.
Long DH. Mechanisms for movement of fungicides, nematicides and insecticides from seed coat to target region in cotton production. In: Proceeding of the Beltwide Cotton Conference; June 15; New Orleans. National Cotton Council; 2005. 239 p.
Linford MB, Oliveira JM. Rotylenchulus reniformisnov. gen. n. sp. a nematode parasite of roots. In: Proceeding of the Helminthological Society of Washington; July; Washington; 1940; 7:35–42.
Robinson AF, Inserra RN, Caswell‐Chen EP, Vovlas N, Troccoli A. Rotylenchulusspecies: identification, distribution, host ranges and crop plant resistance. Nematropica. 1997; 27(2):127–180.
Ferraz LCCB, Brown DJF, editors. Nematologia de plantas: fundamentos e importância. 1st ed. Manaus, Brazil: Norma Editora; 2016. 251 p.
Rodriguez‐Kabana R, Gazaway WS, Weaver DW, King PS, Weaver CF. Host suitability of selected tropical legumes and other crops for the reniform nematode, Rotylenchulus reniformis. Nematropica. 1940; 28:195–203.
Nemaplex. Rotylenchulus reniformis. The nematode‐plant expert information system [Internet] 1990. [Updated: February 2008]. Available from: http//:plpnemweb.ucdavis.edu/nemaplex/Taxadata/G116S2.HTML[Accessed: September 2016].
Sikora EJ, Lawrance KS, Murphy J. Survey of plant parasitic nematodes in soybean fields in Alabama. Nematode Management [Internet]. 2010. Available from: http://www.aaes.auburn.edu/comm/pubs/reseacrhreports/09soybeanrr.pdf[Accessed: October 2016].
Asmus GL. Reação de genótipos de soja ao nematoide reniforme. Tropical Plant Pathology. 2008; 33(1):69–71.
Asmus GL, Schirmann MR. Reação de cultivares de soja recomendadas no Mato Grosso do Sul ao nematoide reniforme. Nematologia Brasileira. 2004; 28:239–240.
Favoreto L, Meyer MC, Klepker K, Campos LJM. Ocorrência de Aphelenchoidessp. em plantas de soja com sintomas de soja louca II. In: Congresso Brasileiro de Nematologia; 12 de Agosto; Londrina, Brazil. Sociedade Brasileira de Nematologia; 2016. pp. 81–82.
Maceda A, Silva JF, Dias WP, Santos JM, Soares PLM, Marcondes MC, Lima CG. Ocorrência de Scutellonema brachyurusem soja no Brasil. In: Internacional Congress of Tropical Nematology; August 10; Maceió, Brazil. Maceió: ONTA; 2016. pp. 1–2.
Machado ACZ. Current nematode threat to Brazilian agriculture. Current Agricultural Science and Technology. 2014; 20:26–35.