**9. Race**

Variability in virulence among populations of soybean cyst nematode was recognized by researchers soon after the nematode was discovered in USA. The term race has been adopted by an *ad hoc* committee of the Society of Nematologists to designate the SCN populations differ in their ability to develop on a set of differential soybean cultivars (Table 3). This scheme was developed in 1970 (Golden et al., 1970) and later was refined by (Riggs & Schmitt 1988). The scheme defines 16 possible races. In 2002, HG type was introduced to more adequately define the diversity in virulence phenotypes (Niblack et al., 2002).

Since *H. glycines* was first discovered in North Caroline in 1955. Within the next 6 years, it had been reported in 7 states along the Mississippi river (Riggs, 2004). Today, it has spread to 29 soybean producing states in USA, as far northeast as the state of New Jersey (Riggs,

Fig. 6. Distribution map of *Heterodera glycines* in USA: A: distribution in 1962; B: distribution

The soybeans are the most economic important host for *H. glycines*. It has a broad host range, up to 100 plant species world wide, some selected common hosts are listed in Table 2 (Baldwin & Mundo-Ocampo, 1991), especially some legumes including beans, vetch, clover, and pea. It also attacks many species of weeds (Riggs & Hamblen, 1966). These weeds in the fields must be taken into consideration for any management measures. Some nonhosts are

Variability in virulence among populations of soybean cyst nematode was recognized by researchers soon after the nematode was discovered in USA. The term race has been adopted by an *ad hoc* committee of the Society of Nematologists to designate the SCN populations differ in their ability to develop on a set of differential soybean cultivars (Table 3). This scheme was developed in 1970 (Golden et al., 1970) and later was refined by (Riggs & Schmitt 1988). The scheme defines 16 possible races. In 2002, HG type was introduced to

more adequately define the diversity in virulence phenotypes (Niblack et al., 2002).

**7.2 USA** 

in 2002.

**8. Host** 

**9. Race** 

also listed that may be used in rotation.

2004) (Fig. 6).


Table 2. A list of hosts and nonhosts for *Heterodera glycines*.


A "+" rating is given if the number of females produced by a soybean cyst nematode population on the soybean cultivar is equal to or greater than 10% of the number produced on the susceptible cultivar Lee. If it is less than 10%, a "-" rating is given.

Table 3. Race classification scheme for *Heterodera glycines.* 

Races 1, 2, 3, 4 were described in 1970 (Golden et al., 1970), race 5 in 1979 from Japan (Inagaki, 1979), and race 7 from China (Chen et al., 1988). Today a total 14 races have been reported (Table 4). Only races 12 and 16 have not been reported. USA has the most races. Race 3 is the most common race in the world.

With relative short history of growing soybean (100-200 years), the fact that USA has the highest number of races for the nematode indicates that the races were probably the results of its widespread planting of the resistant cultivars. Argentina (Doucet et al., 2008) and Brazil (Dias et al., 1998) both have a very short history of growing soybean (less than 50 years) have 6, and 9 races respectively. Very likely these races have been imported through seed stocks and on used machinery from several sources in USA. In comparison, the oriental countries, Korea (Kim et al., 1998), Japan (Ichinohe, 1988) and China (Liu et al., 1998) where soybean has been growing for several thousands years, have relative fewer races, because the modern practice of resistant cultivar selection and development is relatively new. Races 8, 11, 13, and 15 have only been found in USA. Lack of race 4 in both Japan and Korean was a surprise.


Table 4. Distribution of races of *Heterodera glycines* in the world

In USA, the most prevalent race for the northern states is the race 3, while the race 6 is the most common race. That difference of variability was noted along the 35 0 N latitude line. Niblack and Riggs (2004) postulated that is likely caused by the history of using different resistant cultivars.

In central China lies between the Yellow and Yangtze rivers which include the province of Shandong, Anhui, Jiangsu, and Henan, and Shanxi, where the soybean may have originated, where the soybeans are planted in the summer and harvested in the fall (short growing season), the most common race is race 4 (Lu et al., 2006), race 3 has not been reported in that region. In northern China includes the province of Heilongjiang, Jilin, Liaoning, and Inner Mongolia where the soybeans are sown in spring and harvested in fall (long growing season) the prevalent race is race 3 and race 4 has only been reported in one case (Dong et al. 2008) (Fig. 7). China is only country that has these 2 races geologically separated. In the

Fig. 7. The race 3 prevalent region and the race 4 prevalent region of *Heterodera glycines* in China

race classification scheme, the race 3 and the race 4 are opposite to each other, all the 4 cultivars are resistant to the race 3 but susceptible to the race 4. The cultivars have their resistant genes rooted in the cultivars collected from the northern region of China where the race 3 is the prevalent. It is likely that these 2 races are the 2 original races and are native to these 2 regions respectively in China, with race 4 is the ancestral to the race 3, since the cradle of the ancient Chinese civilization happened to be in the race 4 region, and ancient Chinese civilization was an agricultural civilization. The north region (race 3 region) was not an ancient agricultural area, rather a nomadic region.

#### **10. Management**

468 Soybean Physiology and Biochemistry

seed stocks and on used machinery from several sources in USA. In comparison, the oriental countries, Korea (Kim et al., 1998), Japan (Ichinohe, 1988) and China (Liu et al., 1998) where soybean has been growing for several thousands years, have relative fewer races, because the modern practice of resistant cultivar selection and development is relatively new. Races 8, 11, 13, and 15 have only been found in USA. Lack of race 4 in both

**Country Races Total Races Dominate Race Argentina 1,3,5,6,9,14 6 3 Brazil 1,2,3,4,5,6,9,10,14 9 3 Canada 1,2,3,5,6 5 3**

**Japan 1,3,5 3 3 Korea 1,3,5,6 4 3 USA 1,2,3,4,5,6,7,8,9,10,11,13,14,15 14 3**

Table 4. Distribution of races of *Heterodera glycines* in the world

**China 1,2,3,4,5,6,7,14 8 3 Northern, 4 Southern**

In USA, the most prevalent race for the northern states is the race 3, while the race 6 is the most common race. That difference of variability was noted along the 35 0 N latitude line. Niblack and Riggs (2004) postulated that is likely caused by the history of using different

In central China lies between the Yellow and Yangtze rivers which include the province of Shandong, Anhui, Jiangsu, and Henan, and Shanxi, where the soybean may have originated, where the soybeans are planted in the summer and harvested in the fall (short growing season), the most common race is race 4 (Lu et al., 2006), race 3 has not been reported in that region. In northern China includes the province of Heilongjiang, Jilin, Liaoning, and Inner Mongolia where the soybeans are sown in spring and harvested in fall (long growing season) the prevalent race is race 3 and race 4 has only been reported in one case (Dong et al. 2008) (Fig. 7). China is only country that has these 2 races geologically separated. In the

Fig. 7. The race 3 prevalent region and the race 4 prevalent region of *Heterodera glycines* in

Japan and Korean was a surprise.

resistant cultivars.

China

#### **10.1 Resistant cultivar**

A search for sources of SCN resistance led to the evaluation of large number of the plant introduction (PI) from among exotic accession in the USDA soybean germplasm collection. Five accessions were selected as parents. The first SCN resistant cultivar "Picket" with Peking as the source for resistance, was breed and released in 1966 in USA (Brim & Ross, 1966), hundreds have been developed for all the Maturity Groups. In 1970, field populations were found readily reproduce on Picket, and Peking. That finding led to the search for another source of resistance. Chosen from USDA soybean germplasm collection, PI 88788 was used for the development of "Bedford" (Hartwig & Epps, 1978). With the widespread deployment of the SCN resistant cultivars, new races emerged. This has been the story for SCN resistant cultivar development in USA. Since the 80s, the soybean seed breeding has been transferred from public institutes to private company. At much later stage, some accessions of the Chinese soybean germplasm collection were identified have resistance. At present, Roundup ready cultivars developed by Monsanto are the most widely used cultivars in USA, and elsewhere.

Relying on few resistant cultivars alone for SCN control had been proven misguided, as the high number and shifting of the races in USA indicated (Young, 1992).

In North America, the basic management tactics of planting resistant cultivars at different fashions, and rotating with non-hosts will continue to be the main methods to manage the SCN problem, even though the tactics face great challenges of the shitting of the nematode races, and of the uneconomical of the non-hosts (Niblack & Chen, 2004).

#### **10.2 Using mutiline cultivars for SCN management**

Probably, it is hard to argue against the fact that monoculture farming has been one of causes for disease and pest epidemics, the best example is without doubt the Irish Potato Famine caused by the potato late blight disease (*Phytophthora infestans*). Recent cases of other invasive alien species such as the Dutch Elm disease also remind us that biodiversity is very important in fighting pests and diseases. The crop biodiversity used to be a norm practice before the modern agriculture (few cultivars, and a few pesticides), each farmer had to grow different kinds of crops for all household needs (grains, vegetable, and others). The usefulness of mixture of multiline cultivars and cultivars mixtures for disease control has been well documented (Mundt, 2002, Wolfe, 1985). The recent successful cases of using multiline cultivars or cultivar mixtures for controlling diseases, such as potato late blight on potato (Garrett & Mundt, 1999), on barley (Wolfe et al. 1981), on rice in China (Zhu et al., 2000) demonstrated that the practical difficulties associated with the mixtures have been overestimated. This concept has not been carefully tested for SCN control. In the few tested cases, the mixtures were not superior to the resistant cultivars in terms of their yield increasing (Young & Hartwig, 1988). More studies are recommended. As Mundt (2002) demonstrated that for biodiversity to be functional, there must be an appropriate match between the resistant genes in a mixture and the virulence genes present in the target pathogens or parasites.

#### **10.3 Cover crop**

Cover crops are commonly used to prevent soil erosion. These crops are usually planted in rotation with primary crops. When the cover crops are incorporated into the soil at the certain stage of the growing season, this practice is being referred as green manure. A major benefit obtained from green manures is the addition of organic matter to the soil, which increases the food supply for macro, and micro organisms in the soil resulting increased biodiversity in soil. There is a lot of information on the benefit effects of soil biodiversity on disease control (Brussaard et al., 2007).

This agriculture practice with certain crops which contain nematicidal compounds is especially interesting. Marigold, especially French marigold (*Tagetes patula*) has been shown reduced the populations in soil of several root-knot nematodes, and root lesion nematodes (Motsinger et al., Ploeg, 2000, Pudasaini, 2007). Castor beans, sesame, Sudan grass, sorghum, and Crucifers have all shown are toxic against plant parasitic nematodes. Among them, plants from Brassica have received considerable attention for their possibility in controlling plant parasitic nematodes by incorporating them into soil (Mojtahedi et al., 1993, Potter et al., 1998). The principle reason is that glucosinolates which exist in these plants convert upon decomposition to isothiocyanates, a group of chemicals proven to have a wide spectrum of biological activities, including nematicidal activity (Brown & Morra 1997), a few these chemicals are volatile, the practice has been referred "Biofumigation". Among these converted isothiocynates, allyl isothiocyanate (AITC) has been proven as being the most toxic against *H. glycines* (Lazzeri et al. 1993). AITC is the decomposition product of allyl glucosinolate (generally called sinigrin), which exists in plants of *Armoracia lapathifolia, Brassica carinata, B. juncea, B. napus, B. oleracea*, and *Peltaria alliacea* (Brown & Morra, 1997). Among them, mustards have been cited most promising, especially the oriental mustard (Brassica juncea) which contains highest concentration of Ally isothiocynate (AITC) in plant (Tsao et al., 2000). AITC toxicity was found highly selective, was highly toxic against J2 of *H. glycines*, but less toxic on

Fig. 8. Effect of particle size of mustard materials on AITC releasing in soil

free-living nematodes, AITC also inhibited the egg hatching of the nematode (Yu et al., 2005). Some materials from this oriental cultivar have been demonstrated effective in reducing population of *Pratylecnhus penetrans* in soil (Yu et al., 2007 a, 2007b).

Recently using mustard such as oil radish, or other mustard related crops as a cover crop for controlling *H. glycines* have tested, but the results have not been conclusive. The potential factors that caused the inconsistency includes: 1) targeted nematode species; 2) mustard varieties; and 3) environmental factors. In another study we found that the particle size had dramatic effect on releasing the AITC in to the soil (Fig. 8). It is likely that with a mustard variety of high AITC concentration, and plant tissue macerated to very fine particles, mustard crops as cover crops for the SCN control can be an effective method.
