Journal o f Nematology 20(3):392-395. 1988.

© T h e Society of Nematologists 1988.

Complete Characterization of the Race Scheme for

Heterodera glycines 1
R. D. RIGGS 2 AND D. P. SCHMITT~
Abstract: One hundred thirty-eight isolates o f Heterodera glycines from nine states in the United
States, People's Republic o f China, and Indonesia were tested on the four standard soybean race
differentials. A total of 12 variants were found, including the five races described previously. T h e
seven variants that did not correspond to one o f the described races and reports from other areas
of populations that could not be classified are evidence that the present race classification system
needs to be fully characterized. Eleven additional races are described; this expands the total to 16
races, the maximum possible using the four prescribed differentials and a + or - rating for each.
The seven new races are designated as 6, 9, 10, 13, 14, 15, and 16. This complete characterization
of the race scheme will allow for immediate communication o f the discovery of the remaining four
races plus the identification o f previous undescribed races.
Key words." Heterodera glycines, race, soybean, soybean cyst nematode.

Heterodera gIycines Ichinohe, the soybean
cyst nematode (SCN), was first observed in
the United States in North Carolina (15)
in 1954. Resistance to SCN was readily
available and incorporated into commer-
cial soybean (Glycine max (L.) Merr.) (10).
Within 5 years of commercial use of resis-
tance, physiological variation was reported
in SCN (9). Other variants, based on mat-
uration of SCN females on differential soy-
bean cultivars, were reported (8,12). Phys-
iological strains of SCN were reported from
Japan (13), and Miller (6) differentiated 11
groups. A procedure for separating races,
using four differentials and a susceptible
standard, was established in 1970 (2). Four
races were named at that time, and race 5
was added in 1979 (3). Sixteen races were
possible with this scheme, but the lack of
characterization of them has led to diffi-
culty in communication among breeders,
researchers, and others working with SCN.
Many populations from Arkansas (7), Flor-
ida (4), Indiana (1), Iowa (16), Minnesota
(5), and North Carolina (11) are not races
1-5.
Our objective is to designate the re-
Received for publication 15 January 1987.
t Approved for publication by the directors of the Arkansas
Agricultural Experiment Station and the North Carolina Ag-
ricultural Research Service.
Professor, Department of Plant Pathology, University of
Arkansas, Fayettevil/e, AR 72701.
s AssociateProfessor, Department of Plant Pathology, North
Carolina State University, Raleigh, NC 27695.
392
maining 11 races in the scheme proposed
by Golden et al. (2).
MATERIALS AND METHODS
One hundred thirty-eight isolates of SCN
were collected from farms in Arkansas,
Florida, Illinois, Kentucky, Mississippi,
North Carolina, Texas, Virginia, and Wis-
consin in the United States and Indonesia
and People's Republic of China. T h e 67
samples obtained by the University o f Ar-
kansas were each divided and placed in two
15-cm-d clay pots containing fine sand. T w o
'Lee' soybean seedlings were transplanted
into each pot and allowed to grow 6 weeks
to increase the population. Cysts were ob-
tained by a roiling and sieving method,
broken in a blender, and sieved (250-#m-
pore) to remove unbroken cysts (7). Each
isolate was tested using the original pre-
scribed soybean differentials 'Pickett', 'Pe-
king', PI 88788, and PI 90763 (2). Lee was
the standard against which female matu-
ration on each differential was measured.
Seeds of the soybean differentials were ger-
minated in vermiculite and transplanted
singly into 7.5-cm-d clay pots when coty-
ledons opened. Each cultivar or line was
transplanted into three pots. Plants were
inoculated 2 days later with 4,000 eggs and
second-stage juveniles in a 10-ml suspen-
sion. All plants were grown in a green-
house at 25-30 C. Thirty days after inoc-
ulation, cysts and females were collected
and counted. Each pot was processed by
 Race S c h e m e f o r H. glycines: Riggs, Schmitt 393

TABLE 1. Isolates o f Heterodera glycines tested in each race a n d r a n g e o f indices on each differential.

Isolates Indices range

in race
(no.) Pickett Peking PI88788 PI90763
Race AR NC AR NC AR NC AR NC AR NC

1 2 12 4-7 0.7 1 0-3 20-52 22-185 0-0.3 0-4

2 14 24 43-209 11-288 10-48 12-251 10-143 11-366 0-7 0-7
3 6 3 0-8 1 0-3 0-4 0-2 0-6 0-0.4 0-3
4 12 15 21-810 17-319 10-132 17-193 10-261 1 2 - 1 0 4 10-109 12-123
5 9 8 11-97 11-78 0-6 0-5 12-120 12-98 0-3 0-3
6 7 3 12-57 15-33 0-6 0-3 0-2 2-8 0-3 2-3
7 -- 1 0 4 73 13
8
9 6 2 44-110 14-47 12-33 10-21 0-6 2-6 1-8 21
10 1 -- 1 3 21 13
11
12
13
14 0 1 27-209 63 15-84 14 0-5 8 10-42 19
15 1 1 25 15 4 0 42 12 19 14
16 -- 1 4 14 100 27

AR = Arkansas. NC = North Carolina. - - indicates this race was not found.

washing and r u b b i n g the roots to f r e e the replications d e t e r m i n e d the i n d e x o f the

females and cysts, suspending the soil and
n e m a t o d e s in water, and sieving the sus-
pension t h r o u g h nested 8 5 0 - # m - p o r e and
250-/~m-pore sieves.
S o m e o f the 71 isolates collected f r o m
N o r t h Carolina fields were increased on
' L e e 68' soybean; in others, the differen-
tials were seeded directly in the infested
soil. Infested field soil was divided and
m i x e d in equal portions with e n o u g h sand
to fill 15 7.5-cm-d pots. Soil with isolates
increased o n L e e 68 was m i x e d and placed
in 15 7.5-cm-d pots. At 30 days a f t e r trans-
planting, n e m a t o d e s were r e m o v e d f r o m
the roots with a high pressure stream o f
water and collected on a 250-#m-pore sieve.
At each location the i n d e x (I), as used
by G o l d e n et al. (2), was calculated as fol-
lows:
Average number of
females and cysts
f r o m differential
I= x 100
Average number of
females and cysts
from Lee
Each differential was given a + o r - r a t i n g
based on I. T h e i n d e x for each replication
was calculated, and the a v e r a g e o f t h r e e
differential. T h e i n d e x was r o u n d e d to the
nearest whole n u m b e r unless it was less
t h a n 0.5. An I --- 10 was assigned a + a n d
an I < 10 was assigned a - . T h i s is an
a r b i t r a r y b r e a k i n g point based on the as-
sumption o f G o l d e n et al. (2) that if as m u c h
as 10% m a t u r a t i o n o c c u r r e d the popula-
tion would readily increase o n that differ-
ential.
R E S U L T S AND D I S C U S S I O N
T h e 138 isolates were s e p a r a t e d into 12
distinct groups using the f o u r soybean dif-
ferentials ( T a b l e 1). O f the isolates tested
in Arkansas and N o r t h Carolina, respec-
tively, 3% and 17% were race 1, 21% and
34% were race 2, 9% and 4% were race 3,
18% and 21% were race 4, and 13% a n d
11% were race 5. Sixty-four p e r c e n t o f t h e
isolates tested in Arkansas fit into races 1 -
5, as did 87% o f those tested in N o r t h Car-
olina. T h i s means 36% o f the isolates tested
in Arkansas and 13% o f those tested in
N o r t h Carolina, o r 25% o f the total pop-
ulations tested, did not fit these 5 races. In
a 1 9 8 5 - 8 6 survey in N o r t h Carolina, 23%
did not fit (11).
Based on the + and - ratings, t h e r e were
33 isolates in seven g r o u p s that did not fit
Please r e p l a c e p a g e 394 o f J O N v o l u m e 20 No. 3 with this p a g e
394 Journal of Nematology, Volume 20, No. 3, July 1988

TABLE 2. Full e x p a n s i o n o f r a c e classification for versa. In these cases t h e m e a n I was used

Heterodera glycines u s i n g t h e h o s t d i f f e r e n t i a l s as de-
to classify the race. T h e SCN r a c e cate-
s c r i b e d by G o l d e n et al. (2).
gories a r e artificial, b e i n g b a s e d on rela-
Reaction on differential
tionships established by r e s e a r c h e r s . Iso-
lates with I ~ 10 m a y b e h a v e in the field
Race Pickett Peking PI 88788 PI 90763
as o n e race o r a n o t h e r d e p e n d i n g on the
1 m -- -I- --
e n v i r o n m e n t . A s o y b e a n cultivar p l a n t e d
2 + + + -
in a field causes shifts in the g e n e f r e q u e n c y
3 . . . .

4 + + + + o f the isolates (14).

5 + - + - S C N is e x t r e m e l y variable genetically,
6 + - - - a n d these additional r a c e designations a r e
7 - - + +
8 - - - +
n e e d e d so the variants can b e classified.
9 + + - - T h e c o m p l e t e c h a r a c t e r i z a t i o n o f the race
10 + - - + s c h e m e to 16 will e n a b l e p l a n t b r e e d e r s to
11 - + + -
identify resistance to specific races if b r o a d
12 - + - +
13 - + - -
resistance c a n n o t be found. T h e r a c e clas-
14 + + - + sification system n e e d s to b e i m p r o v e d , a n d
15 + - + + r e s e a r c h is u n d e r w a y to d e t e r m i n e which
16 - + + +
p a r a m e t e r s should b e used. Until such a
+ = Number of females and cysts recovered was 10% or system is devised, h o w e v e r , utilization o f
more of the number on Lee cultivar.
- = Number of females and cysts recovered was less than the r a c e s c h e m e r e c o m m e n d e d h e r e i n will
10% of the number on Lee. enable researchers, extension personnel,
a n d o t h e r advisors to c o n t i n u e t h e p r o g r e s s
in o n e o f the d e s c r i b e d races ( T a b l e 1). t h a t has a l r e a d y b e e n m a d e . I n fact, all
T w e n t y - e i g h t o f the isolates w e r e in t h r e e c u r r e n t cultivars with S C N resistance h a v e
g r o u p s o f n e a r equal size a n d f o u r g r o u p s b e e n d e v e l o p e d using t h e r a c e s c h e m e o f
w e r e r e p r e s e n t e d by e i t h e r o n e o r two iso- G o l d e n et al. (2). T h e additional r a c e de-
lates. T o a c c o m m o d a t e these a n d o t h e r iso- scriptions should m a k e the c u r r e n t system
lates t h a t do n o t fit in t h e five d e s c r i b e d m o r e useful.
races, the race s c h e m e n e e d s to include all
LITERATURE CITED
16 o f the races t h a t are possible w h e n using
f o u r differentials a n d a + a n d - r a t i n g 1. F a g h i h i , J . , J . M. Ferris, a n d V. R. Ferris. 1985.
( T a b l e 2). Based on this classification, 10 I n d i a n a p o p u l a t i o n s o f s o y b e a n cyst n e m a t o d e . J o u r -
nal o f N e m a t o l o g y 17:495 (Abstr.).
isolates w e r e race 6, 1 was r a c e 7, 8 w e r e 2. G o l d e n , A. M., J. M. Epps, R. D. Riggs, L. A.
race 9, 1 was race 10, 10 w e r e race 14, 2 Duclos, J. A. Fox, a n d R. L. B e r n a r d . 1970. T e r -
w e r e race 15, a n d 1 was race 16 ( T a b l e 1). m i n o l o g y a n d i d e n t i t y o f infraspecific f o r m s o f t h e
s o y b e a n cyst n e m a t o d e (Heterodera glycines). P l a n t Dis-
In the recent survey in N o r t h Carolina (11),
ease R e p o r t e r 5 4 : 5 4 4 - 5 4 6 .
eight distinct g r o u p s w e r e f o u n d . O f 156 3. I n a g a k i , H. 1979. R a c e status o f five J a p a n e s e
isolates, 23% would b e classified race 6, 9, p o p u l a t i o n s ofHeterodera glycines. J a p a n e s e J o u r n a l o f
or 15. Nematology 9:1-4.
4. L e h m a n , P. S., a n d R. A. D unn. 1987. Distri-
Isolates fitting the descriptions for races
b u t i o n of F l o r i d a p o p u l a t i o n s o f t h e s o y b e a n cyst
6, 8, a n d 9 w e r e r e p o r t e d earlier (7) b u t n e m a t o d e w i t h p r e v i o u s l y u n d e s c r i b e d g e n e t i c vari-
w e r e n o t given a r a c e n u m b e r . Isolates with ation. P l a n t Disease 7 1 : 6 8 - 7 0 .
the criteria o f r a c e 6 w e r e r e p o r t e d f r o m 5. M a c D o n a l d , D. H., G. R. N oe l , a n d W. E.
L u e s c h e n . 1980. S o y b e a n cyst n e m a t o d e , Heterodera
I n d i a n a (1) a n d race 5 o r 15 f r o m Min-
glycines in M i n n e s o t a . P l a n t Disease 6 4 : 3 1 9 - 3 2 1 .
nesota (5). Isolates fitting criteria f o r races 6. Miller, L. I. 1970. D i f f e r e n t i a t i o n o f e l e v e n iso-
9 a n d 14 w e r e r e p o r t e d in a survey o f Flor- lates as races of t h e s o y b e a n cyst n e m a t o d e . P hyt o-
ida p o p u l a t i o n s (4). p a t h o l o g y 6 0 : 1 0 1 6 (Abstr.).
7. Riggs, R. D., M. L. H a m b l e n , a n d L. Rakes.
T h e r e was v a r i a t i o n a m o n g replications, 1981. Infra -s pe c i e s v a r i a t i o n in r e a c t i o n t o hos t s in
a n d in certain tests o n e replication was as- Heterodera glycines p o p u l a t i o n s . J o u r n a l o f N e m a t o l -
signed a + , t h e o t h e r two a - , a n d vice ogy 1 3 : 1 7 1 - 1 7 9 .
 R a c e S c h e m e f o r H. glycines: Riggs, Schmitt 3 9 5

8. Riggs, R. D., D. A. Slack, and M. L. Hamblen.
1968. New biotype of soybean cyst nematode. Ar-
kansas Farm Research 17(5):11.
9. Ross, J. P. 1961. Physiological strains of Het-
erodera glycines. Plant Disease Reporter 46:766-769.
10. Ross, J. P. and C. A. Brim. 1957. Resistance
of soybeans to the soybean cyst nematode as deter-
mined by the double-row method. Plant Disease Re-
porter 41:923-924.
11. Schmitt, D. P,, and K. R. Barker. 1988. In-
cidence of plant-parasitic nematodes in the Coastal
Plain of North Carolina. Plant Disease 72:107-110.
12. Smart, G. C., Jr. 1964. Physiological sti'ains
and one additional host of the soybean cyst nematode,
Heterodera glycines. Plant Disease Reporter 48:542-
543.
13. Sugiyama, S., K. Hiruma, J. Miyahara, and K.
Kohuhun. 1968. Studies on the resistance of soybean
varieties to soybean cyst nematode. II. Differences of
physiological strains of the nematode from Kerawana
and Kikyogahara. Japanese Journal of Breeding 16:
206-212.
14. Triantaphyllou, A. C. 1975. Genetic structure
of races of Heteroderaglycines and inheritance of ability
to reproduce on resistant soybeans. Journal of Nema-
tology 7:356-364.
15. Winstead, N. N., C. B. Skotland, andJ. N. Sas-
ser. 1955. Soybean-cyst nematode in North Carolina.
Plant Disease Reporter 39:9-11.
16. Zirakparvar, M. E., and D. C. Norton. 1981.
Population characteristics ofHeterodera glycines in Iowa.
Plant Disease 65'.807-809.

N o t e : A f t e r this m a n u s c r i p t h a d b e e n s u b m i t t e d t o t h e p r i n t e r , t h e a u t h o r s w e r e
m a d e a w a r e o f t h e f o l l o w i n g a b s t r a c t . C h e n , P. H., D. S. Z h a n g , a n d S. Y. C h e n . 198?.
F i r s t r e p o r t o n a n e w p h y s i o l o g i c a l r a c e (race 7) o f s o y b e a n cyst n e m a t o d e (Heterodera
glycines). J o u r n a l o f t h e C h i n e s e A c a d e m y o f A g r i c u l t u r a l S c i e n c e s 2 0 : 9 4 (Abstr.). T h e
authors have adjusted their race designations accordingly.