Soybean Cyst Nematode, Heterodera glycines (Ichinohe, 1952) (Chromadorea: Rhabdita: Heteroderidae)

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Introduction

The nematode Heterodera glycines, known as soybean cyst nematode (SCN) (Figure 1), is the most economically damaging pest of soybean crops in the United States and around the world (Hunt, 2008; Yu, 2011; Zhou et. al., 2017; The SCN Coalition, 2023). Members of the Heteroderidae family belong in the order Rhabditida; most are plant parasitic while some are insect parasites. They are obligate parasites that attack different species of crops and weeds. The word heteros in Greek means ‘other’, deras ‘skin’ (Siddiqi, 2000). Heteroderidae are divided into two groups, cyst and cystoid, based on morphological alterations in their skin (Nemaplex, 2023). The cyst group are unique in that the female skin changes, transforming into a hardened cyst that protects her eggs. Unlike many plant parasites, there may be little to no aboveground evidence of an infestation with H. glycines (Constantino, 2021). They are incredibly damaging to the agricultural economy and impossible to eradicate once established. With proper management, it is possible to minimize H. glycines populations and maximize yield.

Distribution

Heterodera glycines is largely found in places where soybeans are grown commercially. Ichinohe first reported Heterodera glycines in Japan in 1915 (Riggs, 1977), though some sources reference material from 1952. It may have been previously identified and grouped as H. schachtii, which was reported in the 1880s (Ferris, 2023). As soybeans first originated in China, it is assumed that H. glycines originated there as well (Yu, 2011).

After escaping mainland China, soybean cyst nematode spread rapidly from Asia to other parts of the world through trade, wind, and animal migration. Currently, this pest is found in several countries throughout Africa, Asia, North and South America (Yu, 2011; Mesa-Valle, 2020). It also has a limited distribution in Europe, being found in 3 soybean fields in Italy in 2000 (Manachini, 2000) and 1 field each in 2018 and 2020 (Perin et al., 2021). In the United States, it is concentrated in the Midwest, Mid-South, and Southeast. H. glycines was first recognized in North Carolina in 1954 (Schmitt, 1991). Since then, it has spread to more than twenty-five states, including Florida (Figure 2).

Description

Heterodera glycines is a nematode that differs in morphological appearance among growth stages. They appear similar to other species in the Heterodera schachtii group. The body length of H. glycines 2nd-stage juveniles is 375–540 m with a stylet of 22.0–26.0 m. The tail measures between 40.0–61.0 m and the hyaline tail part is 21.0–33.0 m (EPPO, 2018). Stylet knobs are concave anteriorly (Figure 3). Second-stage juveniles have a vermiform shape with a sharp taper at the tail and a slight taper in the head region. The head appears offset with 3–4 annules (Figure 4). The lateral field continues to have four incisures and the tail rounded.

Males have a rounded tail and regular, annulated cuticle. The head has 4–5 annules and four incisures in the lateral field. Their stylet is stout with lateral knobs protruding anteriorly. The gubernaculum is present. Spicules are well formed and ventrally curved.

Females have a lemon shape and a neck that projects (Figure 5). They are white to light yellow and turn more yellow as they mature. The cysts are also shaped like a lemon with a projecting cone and neck. They are approximately 340–920 m long and 320–610 m wide. Females have reticulate ridges along their bodies with no annulation or lateral incisures. There is a prominent sub-crystalline layer. The head skeleton is hexaradiate. Females contain an egg sac that resembles a gel-like grid which holds 200–500 eggs. Their stylet is narrower with knobs that project at an angle, posteriorly. Young, sedentary females have coiled ovaries that are paired, opening posteriorly through the vulva. The vulva is enclosed by the semifenestrae, which has thin walls and a crescent shape. Bullae are distributed below the well-developed underbridge and are elongated and pronounced. In young cysts, the vulval region remains intact. When the female matures, the body wall changes from yellow to a brown cyst that encases the eggs after death. As the cyst ages, the wall becomes thin and divides, exposing an open fenestra divided by a vulval bridge (Figure 6). These are called ambifenestrate (EPPO, 2018).

Life Cycle and Biology

The life cycle of H. glycines lasts between 3–4 weeks, should conditions be favorable (Davis and Tylka, 2021). In H. glycines, the cyst serves as a survival or overwintering structure that contains eggs. They undergo J1 molt to J2 inside the egg (Figure 7). At this point, they hatch from the egg using both a stylet and protein enzymes that help dissolve the egg wall (Gardner, 2017).

Hatching is a response to chemical signaling from host plants (Giesler and Wilson, 2011). Once hatched, soybean cyst nematodes use their stylet to pierce a host plant’s root and move intra- and intercellularly toward the vasculature. Inside the vasculature, the parasite excretes effector proteins which cause a syncytium to form (Figure 8) so that the plant will nourish the parasite continuously as it loses its motility (Koenning, 2004; Gheysen and Mitchum, 2011). Inside of the syncytium, H. glycines undergoes three more molts at which point male and female adults will emerge.

SCN reproduce sexually (Koenning, 2004). Males take on a vermiform body type and exit the root to find a female for mating at which point it completes its life cycle. The female are pyriform and remain stationary. After sexual differentiation, the female begins to swell with eggs until her posterior bursts from the root and can be seen on the exterior of the host root (Figure 7) (Chowdhury et. al., 2022). Eventually the female dies; her body darkens to a brown color and hardens, encasing the eggs inside. At this point, the cysts fall off into the soil and eggs inside the cyst remain dormant until environmental cues begin the cycle again (i.e., temperature, seasonality, food resources, host plant chemical signaling) (Davis and Tylka, 2021).

Symptoms and Diagnosis

It can be difficult to diagnose an infestation since aboveground symptoms mimic many other plant ailments. Plants may not exhibit symptoms if the infection rate is low. When H. glycines have high populations within agricultural systems, plants could have chlorosis or stunted growth (Figure 9) (Musil, 2016). Often, there are no above ground symptoms and the only indication of infestation is decreased yield. Yield losses of more than 30% are possible with no visible symptoms present (Allen et. al., 2017). Belowground, lemon-shaped female cysts may be visible on roots as signs of infection and are much smaller than nitrogen-fixing soybean nodules (Figure 10). These cysts can be visible with the naked eye or more readily with a hand lens, so can be used as a preliminary diagnostic tool.

It is important to watch fields closely to detect H. glycines infestation early. Aside from monitoring yield, assessing H. glycines in soil or root samples is necessary. The presence of H. glycines can be confirmed by extracting and quantifying H. glycines juveniles from soil using routine extraction for a variety of nematodes, such as that performed in the UF/IFAS Nematode Assay Lab. As described above, checking for cysts on gently washed plant roots (Chen et. al., 2021) is another way to confirm the presence of H. glycines. However, these methods do not always provide an accurate measurement of the severity of H. glycines infestation. In regions where H. glycines is common, quantifying cysts or eggs released from cysts from a soil sample is the recommended method for H. glycines quantification. The HG type test is also an important H. glycines diagnostic tool (Niblack et al., 2002). This test quantifies the reproduction of H. glycines from a given field on various soybean lines that serve as the sources for H. glycines resistance in commercial soybean cultivars (Niblack et al., 2002). This is an important tool for selecting a resistant soybean cultivar to grow in a given field as explained further under "Host Resistance" in the “Management” section. Professional diagnostic clinics in areas where H. glycines is common routinely provide services for HG type testing and quantification of cysts or eggs from soil.

Hosts

The primary host is soybean. Anywhere in the United States soybeans are grown, H. glycines is often present. However, H. glycines attacks several members of crops, primarily from the Fabaceae family, both ornamental and edible species, although plants from a number of other families are also hosts (EPPO, 2008; Rocha et. al., 2021). Several broadleaf species such as field pennycress, common mallow, Canada thistle, common cocklebur have been reported as potential hosts in the Midwest (Johnson et. al., 2008; Venkatesh et. al., 2000; Creech et. al., 2007; Poromarto et. al., 2015). Table 1 highlights some soybean cyst nematode hosts, roughly in order of prevalence.

For crop managers it is important to know which weeds are hosts to H. glycines. Practices such as cover cropping or intercropping could potentially exacerbate the problem if a host of H. glycines is selected. Particularly in warmer regions, if winter annual weeds (hosting H. glycines) are left in crop fields, they could also increase H. glycines populations into the spring when crops are sown. This would perpetuate H. glycines life cycle through resource amplification.

Economic Importance

H. glycines is the most devastating parasite to soybean producers. It is estimated that total losses from H. glycines between 1996 and 2016 were $95.48 billion dollars (Bandara et. al., 2020). As of 2020, economic losses from H. glycines are approximately $1.5 billion each year (The SCN Coalition, 2021). H. glycines causes double the losses of all other individual diseases, comparatively on soybean crops in the United States (Allen et. al., 2017). When cultivars that are susceptible to H. glycines are selected, crop yield can decrease 60% (Hershman, 2015). In the United States, there are more than 70 million acres planted with soybean (USDA-NASS, 2023). The US is the foremost producer of soybeans globally. Soybeans comprise 90% of the US oilseed production sector (USDA-ERS, 2022). Losses in yield can be devastating to both profits and global supply chain demand.

Management

There are several categories of management practices currently utilized among growers and agricultural managers, although not each technique will be applicable in every situation. Agricultural managers may choose the best practices tailored for their needs. Some of these management practices can include: Prevention, Sanitation, Crop Rotation, Host Resistance, Nematicides, Biocontrols, and Cultural Practices.

Prevention: H. glycines persists in the soil indefinitely once it becomes established. Therefore, prevention is the best method of management. Soybean cyst nematode quarantine restricts movement of the pest from infected sites, which has been effective in certain states such as California (CDFA, 2021).

Sanitation: Closely related to prevention, sanitation practices are used to limit the movement of H. glycines since redistribution is thought to rely largely on human intervention. For example, tillage practices relocate cysts as they move soil within a field (Mangel, 2023). Soil carried on equipment can also transport H. glycines among fields, so cleaning equipment between fields can limit spread from mechanization (Ferris, 2023).

Crop Rotation: Once established in a field, current management practices involve managing this parasite to minimal numbers for maximum yield. Crop rotation with nonhost crops is part of an integrated pest management strategy to accomplish this. Since SCN is an obligate parasite, crop rotation with nonhost varieties prohibits it from reaching maturity and producing progeny (Davis and Tylka, 2021). Some nonhost crops include alfalfa, barley, canola, clover, corn, cotton, forage grasses, oats, rye, sorghum, tobacco, and wheat (Wrather and Mitchum, 2010).

Host Resistance: Another useful practice is planting resistant varieties. A single soybean line, PI 88788, has long been the predominant source of resistance in commercial soybean cultivars (Tylka, 2022). A few other sources of resistance, namely Peking, are also available in some soybean cultivars (Tylka, 2022). Because of the reliance on PI 88788-derived resistance, H. glycines populations have shifted increasingly such that populations from many fields can readily reproduce on PI 88788 cultivars (Tylka, 2022). In those fields, cultivars with PI 88788 resistance will have reduced efficacy. For this reason, rotating sources of resistance is important to delay population shifts in fields where this has not occurred. Furthermore, conducting HG type testing, as described above, is important for selecting a resistant cultivar that will be effective against the H. glycines population in a given field, particularly in areas with a history of this nematode in soybean production.

Nematicides: Some growers prefer to use nematicides to control H. glycines. Many nematicides provide temporary control; however, some are less effective due to the rapid growth cycle of H. glycines. In addition, nematicides cannot control H. glycines through the entire growing season, and infestation populations may be higher at the end of the season even with treatment (Tylka, 1994). Further information on management tips for H. glycines can be found in the UF/IFAS EDIS on nematode management in Florida soybean (Grabau, 2023).

Biocontrol: An alternative to chemical usage is biological control. Certain bacteria, fungi, and predatory nematodes can destroy H. glycines. It is important to note that only a few species are available for commercial applications, although there is continued research and progress in this field.

Cultural Practices: Controlling annual, winter weeds that host H. glycines reduces population density and subsequent pest pressure on profitable crops (Niblack and Tylka, 2008). Lastly, ensuring that plants have optimal nutrients and water will help to maintain yield and prevent susceptibility from stress. When plants are healthy and thriving, they are better able to resist infection and maintain yield.

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