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2010 Plant Management Network.
Accepted for publication 2 December 2009. Published 15 March 2010.


Evaluation of Northern-Grown Crops as Hosts of Soybean Cyst Nematode


Susilo H. Poromarto and Berlin D. Nelson, Department of Plant Pathology, North Dakota State University, Fargo, ND 58108-6050


Corresponding author: Berlin D. Nelson. berlin.nelson@ndsu.edu


Poromarto, S. H., and Nelson, B. D. 2010. Evaluation of northern-grown crops as hosts of soybean cyst nematode. Online. Plant Health Progress doi:10.1094/PHP-2010-0315-02-RS.


Abstract

Sixty-two cultivars/varieties of thirteen crops grown in the northern Great Plains were evaluated for suitability as hosts of the soybean cyst nematode (SCN; Heterodera glycines Ichinohe) (HG type 0) using soybean Lee 74 as the susceptible host. “Cone-tainers” with autoclaved sand were infested with 2,000 eggs placed into a 2-cm × 1-cm hole and then a 3-day-old germinated seed was placed in the hole. “Cone-tainers” were placed in sand in plastic pots immersed in a water bath at 27°C in the greenhouse. Plants were harvested after 30 days, and females were extracted and counted. A female index (FI = the average number of females on the test plant divided by the average number of females on soybean Lee 74 times 100) was calculated for each cultivar to assess host suitability to the nematode. FIs ≥ 10 indicated a suitable host. Canola, clover, lentil, and sunflower were nonhosts (no evidence of reproduction), while borage, camelina, chickpea, crambe, cuphea, field pea, nyjer, and safflower were poor hosts for SCN with FIs less than 8. Lupines were the only suitable host with FIs of 42 to 57. This is the first report of reproduction of SCN on chickpea, crambe, cuphea, and nyjer.


Introduction

North Dakota and northern Minnesota have diverse cropping systems that differ from the corn-soybean system common in much of the North Central United States. In addition to the traditional planting of small grains, potato, sugar beet, and dry bean, other crops such as soybean, canola, field pea, sunflower, and lentil have been integrated into the cropping systems in the past 30 years and there has been a dramatic increase in hectares of those crops. North Dakota, for example, was ranked number one in production of canola (Brassica napus L.), field pea (Pisum sativum L.), sunflower (Helianthus annuus L.), and lentil (Lens culinaris Medik.) in the United States in 2008 with values of 250, 112, 307, and 29 million dollars, respectively (10). In addition, specialty crops being grown commercially, or under investigation for production include borage (Borago officinalis L.), clover (Trifolium sp. and Melilotus sp.), camelina (Camelina microcarpa Andrz. ex DC.), chickpea (Cicer arietinum L.), crambe (Crambe maritima L.), cuphea (Cuphea viscosissima Jacq.), lupines (Lupines albus L.), nyjer (Guizotia abyssinica (L.f.) Cass), and safflower (Carthamus tinctorius L.).

Soybean is the principal oilseed crop in North Dakota and northern Minnesota with over 1.6 million hectares in the area. Soybean is now grown throughout the eastern half of North Dakota and throughout much of the northern part of Minnesota in the Red River Valley and areas bordering the Valley. Soybean cyst nematode (SCN) (Heterodera glycines Ichinohe) is a major pathogen of soybean that occurs in most soybean production areas in the United States (11,27). SCN was first reported in North Dakota in 2003 (2) and the nematode is currently found in two southeastern counties, Richland and Cass. SCN is also found in several Minnesota counties directly to the east of the infested counties in North Dakota. To date, only HG type 0 (12) has been identified in infested fields in North Dakota (2). SCN will continue to expand northward into counties where the majority of the aforementioned crops are grown.

Management of SCN includes crop rotation with nonhosts to help reduce egg population densities (11). The suitability of potential rotation crops as hosts for SCN, therefore, is important to understand. Furthermore, it is necessary to know which crops might be adversely affected by SCN as there are susceptible hosts other than soybean (13,16). Not all the crops grown in North Dakota and northern Minnesota have been extensively evaluated as hosts for SCN. For example, there were no reports we could find indicating the host suitability of camelina, crambe, cuphea, or safflower to SCN.

The extensive host range studies of Riggs and Hamblen (17,18) indicated an important consideration when examining a species for reproduction of SCN: within a species, cultivar/variety can be an important factor in determining the amount of reproduction on the roots. For example, Riggs and Hamblen (17) evaluated numerous plant introductions of pea and found types that were immune, resistant, and susceptible. Poromarto and Nelson (13) tested 24 cultivars of dry bean and found resistant to highly susceptible types. Numerous published studies, however, examining reproduction of SCN on different species of plants used only one or a few cultivars/varieties of the crops tested (5,8,19,20,23,25).

The objectives of this study were to: (i) evaluate reproduction of SCN on the roots of various crop cultivars commercially grown or being tested in the North Dakota and northern Minnesota area; and (ii), if new suitable hosts were identified, to assess the ability of eggs produced on those hosts to hatch and reproduce on susceptible soybean.


Crop Genotype and Planting

Sixty two cultivars/varities from thirteen crops were tested for suitability as hosts for SCN in the greenhouse (Table 1). The crops were: borage, camelina, canola, chickpea, clover (T. hybridum L., T. pretense L., T. repens L. and M. officinalis L.), crambe, cuphea, field pea, lentil, lupines, nyjer, safflower, and sunflower. The soybean cultivar Lee 74 was used as a susceptible control in all tests (12). Each crop was evaluated in separate experiments.


Table 1. Reproduction of soybean cyst nematode on crops grown in North Dakota and northern Minnesotax.

Crop Cultivar Exp. 1 Exp. 2 Avg.
Borage
(Borago officinalis L.)
1. Purple Borage 36/552 25/658 31/605
2. White Borage 0/552 5/658 3/605
Camelina
(Camelina microcarpa
Andrz. ex DC.)
1. Blaine Creek 1/438 2/515 2/477
2. Boha 1/438 1/515 1/477
3. Calena 1/438 3/515 2/477
4. Celine 2/438 2/515 2/477
5. Ligena 1/438 1/515 1/477
6. Suneson 3/438 5/515 4/477
Canola
(Brassica napus L.)
1. Crusher 0/327 0/791 0/559
2. Gladiator 0/327 0/791 0/559
3. Hudson 0/327 0/791 0/559
4. HyClass 601 0/327 0/791 0/559
5. Hylite 0/327 0/791 0/559
6. Marksman 0/327 0/791 0/559
7. Patriot 0/327 0/791 0/559
8. Proseed 2013 0/327 0/791 0/559
9. Rider 0/327 0/791 0/559
10. Skyhawk 0/327 0/791 0/559
Chickpea
(Cicer arietinum L.)
1. Anna 0/105 6/579 3/342
2. Siera 0/105 0/579 0/342
Clover
(Trifolium sp.
and Melilotus sp.)
1. Aliske Clover
(T. hybridum L.)
0/552 0/458 0/505
2. Red Clover
(T. pretense L.)
0/552 0/458 0/505
3. Sweet Clover
(M. officinalis L.)
0/552 0/458 0/505
4. White Clover
(T. repens L.)
0/552 0/458 0/505
Crambe
(Crambe maritima L.)y
1. Belann 52/610 18/342 35/476
2. Carmen 27/610 13/342 20/476
3. Indy 22/610 19/342 20/476
4. Meyer 55/610 17/342 36/476
5. Prophet 39/610 16/342 28/476
Cuphea (Cuphea viscosissima Jacq.) 0/552 18/658 9/605
Field pea
(Pisum sativum L.)
1. Admiral 0/105 0/579 0/342
2. Eclipse 0/105 0/579 0/342
3. Majoret 0/105 1/579 0/342
4. Miami 0/105 0/579 0/342
5. Mozart 0/105 0/579 0/342
6. Striker 0/105 0/579 0/342
Lentil
(Lens culinaris Medik.)
1. Crimson 0/105 0/579 0/342
2. Merrit 0/105 0/579 0/342
3. Pennell 0/105 0/579 0/342
4. Redberry 0/105 0/579 0/342
5. Rich Lea 0/105 0/579 0/342
6. Sovereign 0/105 0/579 0/342
Lupines
(Lupines albus L.)
1. 10018-98-1 131/458 210/331 171/395
2. 8145-94-1 204/458 246/331 225/395
3. Lupro 2085 144/458 212/331 178/395
4. 8130-94-1 130/458 202/331 166/395
5. LU206 140/458 257/331 199/395
Nyjer
(Guizotia
abyssinica
(L.f.) Cass.)
1. Early bird 0/552 0/658 0/605
2. Early bird-50 0/552 0/658 0/605
3. Unknown 1/552 2/658 2/605
Safflower
(Carthamus tinctorius L.)
1. Fincl 1/438 1/515 1/472
2. Montola 2003 4/438 3/515 4/472
3. Nutrasaft 2/438 1/515 2/472
Sunflower
(Helianthus annuus L.)
1. H 288 0/533 0/542 0/536
2. Proseed 9130 0/533 0/542 0/536
3. Myc 7350 0/533 0/542 0/536
4. Myc 8c841 0/533 0/542 0/536
5. Car 270 0/533 0/542 0/536
6. 8031 0/533 0/542 0/536
7. P 386 0/533 0/542 0/536
8. DM-2 0/533 0/542 0/536
9. S-37 0/533 0/542 0/536

 x Plants inoculated with Heterodera glycines HG type 0 and incubated at 27C for 30 days. The data presented are the number of females produced on the test crop over the number produced on Lee 74, the susceptible soybean check. The right column is the average of the two experiments. There were four replications in each experiment.

 y All crambe cultivars had significantly (P ≤0.001) fewer females than Lee 74.


Seeds were surface disinfected with 1.0% NaOCl for one minute, rinsed with water, and germinated on seed germination paper (Anchor Paper, St. Paul, MN) for three days. Healthy seedlings of uniform size were transplanted into a 2 × 1-cm hole in autoclaved river sand in individual plastic “Cone-tainers” Type SC10 Super Cell (3.8-cm diameter, 21-cm depth, 164-ml volume; Stuewe & Sons, Inc., Corvallis, OR). “Cone-tainers” were placed in autoclaved sand in 30.5-cm diameter × 30.5-cm depth plastic pots (Cambro, Huntington Beach, CA) immersed in a water bath at 27  3°C in the greenhouse. Plants were grown for 30 days under natural and supplemental light using high pressure sodium lamps (1,000 E/m²/s) for 16 h/day. Plants were watered daily as needed to maintain the sand at field capacity. At 14 and 21 days after planting, plants were fertilized with 3 ml of a solution of Peters Hydro-Sol 5-11-26 (W.R. Grace & Co.-Conn., Fogelsville, PA; at the rate of 20 ml of Peters in 980 ml of water).


SCN Source, Inoculation, and Evaluation

Soil naturally infested with SCN was collected from a soybean field in Richland Co., ND. The population of SCN was identified as HG type 0 following the methods of Niblack et al. (12). The indicator lines and female index (FI) for the HG type classification were as follows: PI 548402, FI 0.1; PI 88788, FI 0.6; PI 90763, FI 0.1; PI 437654, FI 0.2; PI 209332, FI 0.1; PI89772, FI 0.1; PI548316, FI 6.5; Lee 74 FI 100 (average female number/plant of Lee 74 = 570).

The general methods of Niblack et al. (12) to inoculate plants were followed with some modifications. The egg source was directly from Lee 74 soybean inoculated with eggs from the soil and grown in the greenhouse under the same conditions as previously described. Cysts were extracted from soil or roots with an 18-mesh (1 mm) sieve (VWR Scientific, West Chester, PA) nested over a 60-mesh (250 m) sieve. Cysts were crushed with a Wheaten Potter Elvehjen Tissue Grinder (55 ml capacity) (VWR Scientific, West Chester, PA) and eggs were collected on a 200-mesh (75 m) nested over a 500-mesh (25 m) sieve. A suspension of eggs in distilled water was prepared and adjusted to 1,000 eggs/ml. As the seedling was transplanted into the sand, a suspension of 2,000 eggs was placed in the planting hole and the seedling was covered with sand. Watchdog 450 Data loggers with soil temperature sensors (Spectrum Technologies, Inc., Plainfield, IL) were used to monitor the temperature of the sand in the “Cone-tainers.” Temperatures in the sand among experiments averaged 27  1°C, but temperature variations of 3 to 4°C were recorded almost daily.

Females of SCN were collected from the roots of individual 30-day-old plants. Plants were extracted from the “Cone-tainers” and the root-sand masses were soaked in water. The females were washed off the roots and sieved from the water/sand mix of the root soakings using the previously described sieves. Females from each plant were counted with a dissecting microscope. Roots were also examined with the dissecting microscope to insure mature females were removed.


Infecting Soybean with Eggs from Crambe and Purple Borage

Eggs of SCN produced on crambe and purple borage were inoculated onto soybean to determine if they would result in the same number of females per plant as eggs produced on soybean. Females produced on soybean Lee 74, the five crambe cultivars, and purple borage were collected and the eggs extracted as previously described. Lee 74 plants were then immediately inoculated with 2,000 eggs per plant from each of the five crambe cultivars, purple borage, and Lee 74 and grown as previously described. After 30 days, females on Lee 74 were extracted and counted. In addition, the average number of eggs per female produced on the crambe cultivars, purple borage, and Lee 74 was determined. Females from each plant were crushed and the eggs collected as previously described. Egg numbers were counted with an American Optical One-Ten microscope (Buffalo, NY) and the average number of eggs per female was calculated.


Experimental Design and Analysis

The data from the reproduction on the various crops were not analyzed for most crops since the primary purpose was only to detect reproduction and in most cases there was no or little reproduction. However, a female index (FI) (FI = the average number of females on the test plant divided by the average number of females on the susceptible soybean Lee 74 times 100) was calculated to assess host suitability (12).

For all experiments, the design was a randomized complete block with 4 replications (one plant per replication) and all experiments were repeated once. In the experiments with crambe and those infecting soybean with eggs from crambe and purple borage, the data from individual experiments were analyzed separately by analysis of variance (ANOVA) with SAS (SAS Institute Inc., Cary, NC) and variances were compared between repeated experiments. The data were then combined over experiments and analyzed by ANOVA. Least significant differences (Fishers protected F test, α = 0.05) were calculated following significant (P ≥ 0.05) F tests.


Discussion and Conclusions

With soybean, an FI of greater than 10 is considered a suitable host (12), therefore that standard was used in this research to separate a poor host from a suitable host. The terms suitable host and susceptible host are used throughout the literature on SCN, but we chose to use suitable host in our research since susceptible host implies there is an effect of SCN on the growth of the host and such information is not available from most host range studies with SCN. Canola, the four clovers, lentil, and sunflower were nonhosts of SCN in this study since there was no evidence of reproduction on roots in experiments where the susceptible soybean had high numbers of females (Table 1). Field pea cultivars could also be considered a non-host since only one cultivar in one experiment had an average of one female on the roots. Borage, camelina, chickpea, crambe, cuphea, nyjer, and safflower were poor hosts for SCN with FIs less than 8 (Table 1). This is the first report we are aware of where chickpea, crambe, nyjer, and safflower were directly inoculated with eggs of SCN. White lupine was the only crop tested that was a suitable host with an FI > 10.

Canola, oilseed rape, and sunflower were previously tested as hosts of SCN. Venkatesh et al. (23) tested one canola cultivar against three races of SCN by direct inoculation and found no reproduction of this nematode. Warnke et al. (25) evaluated one cultivar of oilseed rape and found that penetration of roots by J2 (second stage juveniles) occurred but there was no development of mature females. They also reported that the roots of rape stimulated egg hatch. Sortland and MacDonald (20) directly inoculated a sunflower cultivar with SCN race 5 and reported no females developed. Both canola and sunflower were evaluated in greenhouse and field tests as rotation crops for SCN management and there was no evidence that populations of SCN were increased by these crops (9,20,24). Miller et al. (9) in field studies at three locations in Minnesota reported those two crops reduced SCN egg population density during the season compared with a susceptible soybean. However, Jackson et al. (6) in Missouri reported that canola increased the number of SCN eggs when used as a rotation crop in one year but not a second year of a field study. Wong and Tylka (26) reported that wild sunflower was a nonhost of SCN and reduced SCN egg numbers in infested soil in greenhouse and field experiments.

Clover has been tested for SCN host suitability in numerous studies. Riggs and Hamblen (18) reported that red and white clover were nonhosts, but a few females developed on several sweet clover plant introductions. No females were observed on sweet clover or the other three clover species in our study. Although the majority of clover species in Melilotus and Trifolium are nonhosts or poor hosts (17,18), Riggs and Hamblen (18) reported there were plant introductions of at least 7 clover species within those genera that were susceptible to SCN with an FI greater than 10. Riggs (15) reported that the white clover cultivar Ladino and other species of clover such as Rose clover (Trifolium hirtum All.) were penetrated by J2, but there was no further development of the nematode. In contrast, other species of clover, such as Trifolium vesiculosum Savi and Crimson clover, T. incarnatum L., were not penetrated by J2 (15). Red clover is penetrated by J2, but the nematode does not mature into adults (8,19). Red clover appears to have various effects on SCN, from stimulating hatching of eggs (1,6,8,14,19) to reducing population densities in soil (6,8,9).

The genus Lens, which includes lentils, has not been adequately tested as a host for SCN. Riggs and Hamblen (18) evaluated one plant introduction of lentil and reported no reproduction of SCN. That is the only previous report on lentil that we found. Chickpea also has not previously been evaluated as a host, but our study indicates it is a poor host. Although all 6 cultivars of lentil were nonhosts in our study and a few females developed on chickpea, it is noteworthy to mention that lentil and chickpea are hosts of H. ciceri which occurs in the Mediterranean Basin (3,4)

In most studies where pea was evaluated as a host, it has been primarily with one or two cultivars and there was no evidence that those cultivars were susceptible to SCN (5,9,15,20,24). However, Riggs and Hamblen (17) in their extensive study of hosts in the Leguminosae showed that out of 199 plant introductions of P. sativum, five were rated as susceptible to SCN, 132 allowed some reproduction, and the rest were immune. Riggs (15) demonstrated SCN J2 will not penetrate some pea cultivars while penetration will occur in others, but the nematode will not continue to develop. In our study, six pea cultivars were evaluated and SCN only formed mature females on one, Majorete, but the number of females was less than 1% of those on the susceptible soybean Lee 74.

Borage was reported as a susceptible host (FI 19) by Riggs and Hamblen (18) but only one type was evaluated. The average FIs for purple and white borage in our study were only 5 and 0.5, respectively. Apparently within the species there are resistant and susceptible borage types. Since there was limited information on borage as a host of SCN and there was a report that some types are susceptible hosts, the effectiveness of eggs produced on purple borage as inoculum for soybean was investigated. The number of females on the Lee 74 plants that were inoculated with eggs produced on purple borage plants was significantly lower (P > 0.05) than the number of females on Lee 74 plants inoculated with eggs produced on Lee 74 (Table 2). The mean number of SCN females per Lee 74 plant was 211 and 367 when eggs originated from purple borage and Lee 74, respectively. Apparently J2 from females produced on purple borage are less capable of infecting soybean or the eggs have reduced hatching compared to eggs formed on soybean. The average number of eggs per female produced on purple borage, however, was not significantly (P < 0.05) different from the number produced on Lee 74 (Table 2).


Table 2. Number of eggs per soybean cyst nematode female produced
on crambe and purple borage and number of females formed on Lee 74
soybean inoculated with eggs produced on crambe and purple borage.w

Cultivarx Eggs/femaley Females on Lee 74z
Lee 74 (soybean) 292 367a
Belann (crambe) 284 357a
Carmen (crambe) 274 313a
Prophet (crambe) 282 320a
Meyer (crambe) 284 338a
Indy (crambe) 276 320a
Purple Borage 276 211b

 w Plants inoculated with Heterodera glycines HG type 0 and incubated at
27C for 30 days. Data represent means from two experiments each
with four replications combined for analysis.

 x Lee 74 is the susceptible soybean for comparison.

 y Analysis of variance indicated no significant (P = 0.05) difference in
numbers of eggs per female.

 z Lee 74 was inoculated with 2,000 eggs/plant produced on the respective
cultivars in the left hand column. Means followed by the same letter are
not significantly different (Fishers least significant difference, α = 0.05).


All six cultivars of camelina and the three varieties of nyjer were poor hosts for SCN with FIs averaging less than 1. One cuphea type and three cultivars of safflower were evaluated and they were also poor hosts, with FIs < 2. We found no previous reports of the direct inoculation of camelina, cuphea, nyjer, or safflower with eggs of SCN. Warnke et al. (24), however, grew camelina in SCN-infested soil for evaluation as a rotation crop in a greenhouse study and there was no evidence of an increase in egg population density, indicating there was no reproduction. Safflower is reported to contain nematicidal polyacetylenes (7).

All white lupine cultivars were suitable hosts, with FIs ranging from 42 to 57. Although lupines have been reported as a host for SCN (18), the cultivars tested here had not previously been evaluated. Riggs and Hamblen (18) reported that from 38 species or cultivars of Lupinus, 17 were immune, 13 were resistant, and 8 were susceptible. Riggs (15) reported that several white lupine cultivars were susceptible with FIs greater than 10.

This is the first report of reproduction of SCN on crambe. All crambe cultivars had significantly (P ≤ 0.001) fewer females than Lee 74, and the average FIs ranged from 4 to 8 (Table 1). These five crambe cultivars, therefore, would be considered resistant compared to Lee 74. There were no significant differences (P > 0.05) in numbers of females among the five crambe cultivars in the combined data (Table 1). There were also no significant (P > 0.05) differences in the average number of eggs/female produced on the five crambe cultivars and Lee 74 (Table 2). As with borage, the eggs produced on crambe were tested as inoculum on soybean. There were no significant (P > 0.05) differences in the number of females on the Lee 74 plants that were inoculated with eggs produced on crambe compared to Lee 74 plants inoculated with eggs produced on Lee 74 (Table 2). Crambe is known to contain glucosinolate compounds that are thought to play a role in defense against pests (21,22).

Although eight of the crops evaluated were poor hosts, if they were grown in areas with SCN, especially in rotation with soybean, reproduction of SCN on these crops under field conditions should be evaluated. Until such data are available, the potential role these crops might play in crop rotations and SCN biology will be in question. In addition, there may be cultivars/varieties within those crops, especially crambe, that are better hosts for SCN. Fortunately, with the exception of dry bean (13) and white lupines, all the traditional crops and apparently most of the specialty crops grown or being considered for production in North Dakota and northern Minnesota are poor hosts for SCN.


Acknowledgments

The authors wish to thank the North Dakota Soybean Council and the State Board of Agricultural Research and Education for financial support of this research. We also thank our many colleagues who provided seed of the various crops.


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