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Aphid-resistant soybeans are a new option

The risk of abundant populations of soybean aphid Aphis glycines should be high if the insect pest continues to follow its previously established cycle of high numbers every other year. Although soybean aphid numbers followed the pattern and were low in places like Ontario and Ohio in 2008, the numbers did not follow the pattern in all areas of the Midwest.


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In July 2007, an aphid-resistant Rag1 soybean variety had about 200 aphids per plant (left), whereas a similar susceptible variety had about 1500 aphids per plant (right) in US Midwest field trials. The darker colour of the susceptible variety is caused by sooty mould that grew on the honeydew shed by the aphids.        

Photo courtesy of Matthew O’Neal, Iowa State University.


 

The risk of abundant populations of soybean aphid Aphis glycines should be high if the insect pest continues to follow its previously established cycle of high numbers every other year. Although soybean aphid numbers followed the pattern and were low in places like Ontario and Ohio in 2008, the numbers did not follow the pattern in all areas of the Midwest. Large populations occurred in areas of the Dakotas, Nebraska, Minnesota, Iowa, southern Wisconsin and northern Illinois. So researchers are uncertain as to what 2009 holds in terms of soybean aphids.

Entomologists like Tracey Baute of the Ontario Ministry of Agriculture, Food and Rural Affairs, and researchers from Ohio, have not yet noted large numbers of overwintering aphid eggs in their areas in fall 2008 and winter 2009, perhaps pointing to low springtime infestations. However, Baute states that areas such as Michigan, Ohio, Ontario and Quebec are always at risk later in the growing season. “We’re at the end of all the weather systems, so not only do we deal with the soybean aphids we have here that overwinter, but more can blow in on wind currents from states that are west and south of us.”

In addition to the introduction of natural enemies and spraying of insecticide to kill soybean aphids once they surpass established scouting thresholds, plant breeders have been working to develop soybean varieties with some resistance to the insect. To this end, Syngenta Seeds Canada is releasing a 3100 heat unit, aphid-resistant soybean variety for the 2009 growing season, says Don McClure, soybean breeder with Syngenta. This variety contains a gene called Rag1, which occurs naturally in soybean and provides some resistance to the soybean aphid. The Rag1 gene does not affect other insects. 

McClure says that this Rag1-containing soybean variety was planted in Ontario field trials in 2008.  Although soybean aphid pressure was low in Ontario that year, it was an opportunity to evaluate the variety’s agronomic performance. “It still has to yield well and perform well in a grower’s field whether there are aphids or not, and it did that, so we feel pretty comfortable that the variety is a good variety whether we have aphids or not,” says McClure. “Also, we multiplied seedstock seed in 2008. According to the grower, our seed field was more than 60 bushels per acre.”

McClure says that the Rag1 soybean variety will be combined with an insecticide seed treatment, giving two modes of defence against early aphid infestations. In years of high aphid abundance, however, it may still be necessary to spray late in the growing season. “This soybean variety gives growers an opportunity to control a major pest in soybeans, or at least reduces the possibility that they’re going to have to spray large acreages in the summertime with a commercial insecticide. If a grower can control aphids without having to spray the crop, there’s a huge benefit because they’re not affecting the beneficial insects and nontarget insects,” for example, bees and other pollinators and natural enemies of the soybean aphid.

30b
Soybean
aphid populations that surpass the economic threshold of 250 per plant
can also affect soybean yields indirectly by facilitating disease such
as sooty mold. 
Photo courtesy of Matthew O’Neal, Iowa State University.
30c
Despite the development of aphid-resistant soybeans, growers still need to scout their soybean fields. Photo courtesy of Greg Zolnerowich, Kansas State University.
30d 
Growers were forced to cope with plant infestations of this level in 2001 and 2003.
 Growers were forced to cope with plant infestations of this level in 2001 and 2003.


Soybean aphid biotypes
Soon after Rag1 soybean varieties were developed, researchers discovered a soybean aphid biotype that could develop on them. This has caused some people to question whether the soybean aphid is already breaking down the Rag1 resistance. “It is highly unlikely that the soybean aphid is already adapting to Rag1 resistance,” says Dr. Matthew O’Neal, assistant professor and entomologist at Iowa State University. “The plants just have not been present in any extent to provide selection pressure for that to occur.” He says that it is more likely that there were multiple introductions of the aphid or that the aphids that were introduced carried a wider range of genetic variability than would be expected with one introduction, so some individuals already had the traits that allow them to develop on Rag1.

The new soybean aphid biotype was identified in 2006 by researchers from Ohio State University and the University of Illinois. The geographic extent and abundance of this biotype and the possibility of other biotypes are unknown. However, the biotype could cause difficulties for determining areas where Rag1 soybean varieties would be effective.

To address this problem, researchers are trying to determine how many biotypes there are in North America, says Dr. Dechun Wang, associate professor in the Department of Crop and Soil Science at Michigan State University.  “We are planting a set of standard resistant lines in different states to see how many different responses we can see from aphids.” The idea is to group aphids into different biotypes based on their responses to the resistance sources.
In addition, Dr. Andrew Michel, assistant professor at Ohio State University, is attempting to isolate genetic markers that can be used to identify soybean aphid biotypes. He is looking for specific sections of DNA that are linked to the aphid’s ability to survive on Rag1 and other soybean-aphid resistance genes. “I’m analyzing the DNA to look for any sort of diagnostic marker that we could use to differentiate the biotypes. With that information, growers could decide which resistant soybean plant to use on their farms,” says Michel.

Michel’s ultimate goal is to determine the number and distribution of biotypes and whether there are consistent patterns of large-scale migration. “What we need to do first is to get a baseline of what’s going on in one year,” he explains. “Then, we’re going to need to do that again the following year to see how the aphids move. It’s difficult to figure out how the aphid biotypes move without knowing what they are. We need a really good diagnostic tool to track their migration.”

The first soybean aphids for Michel’s research were collected from nine states and Ontario in summer 2008. The aphids are squished and then their DNA is analyzed. “It’s a bit like a blood type; you can take blood and find out if you’re A, AB, B, or O. We want to be able to take an aphid, squish it, get the DNA, and figure out if it’s biotype one, two or three,” says Michel. He is planning to sample more aphid populations in 2009, including ones that colonize specific resistant varieties, to look for markers and migration patterns.

Field experiments with Rag 1 resistance
The good news is that even though aphids can colonize aphid-resistant varieties, there are consistently fewer aphids on the resistant varieties in field experiments with multiple resistant and susceptible soybean varieties. “Often, there are orders of magnitude in difference,” says O’Neal. “There may be 1000 on the susceptible, but only 100 or 200 on the resistant line.”

To measure aphid development, aphid-induced yield loss, and the potential for yield drag associated with Rag1, O’Neal and Iowa State University graduate student Mariana Chiozza compared a Rag1 variety with a susceptible variety in field plots with and without insecticide. They found some unusual results. “Not only did the aphids exceed the economic threshold (250 individuals per plant and increasing), but at times, they exceeded the economic injury level,” says O’Neal. He explains that the economic injury level is the point at which the cost of management equals the loss in yield from the pest. The economic threshold is set lower than the economic injury level so that management can be done before yield loss occurs. “We exceeded the economic injury level on these resistant plants, but the cool thing was, they did not lose as much yield as susceptible plants.”

He also notes that the Rag1 gene does not appear to cause yield drag. “Although the gene might give resistance to aphids, you could imagine that now the plant’s producing something that makes it resistant to aphids and takes away from the yield. But that doesn’t seem to happen.”

Growers who want to plant the new Rag1 varieties this summer will want to know if they should still be scouting and spraying for soybean aphids. The short answer is “yes” to scouting and “possibly” to spraying. “What I’ve been telling our growers is, the Rag1 varieties won’t be aphid free,” says O’Neal. “However, you will be able to be more conservative about the aphid thresholds you use. We’ve developed thresholds for susceptible plants. Now, we have to develop thresholds for resistant plants to give growers a better estimate of when, or even if, they should use an insecticide.” O’Neal will begin work in the summer of 2009 to determine aphid thresholds for resistant soybean varieties.

The great thing about these resistant varieties is that the aphid’s growth is slowed, says O’Neal. “Anything that can slow this down from, for example, an outbreak that occurs over the course of seven days to an outbreak that then might occur over 14 days allows you to get a more timely insecticide application if you need it.” And spraying less insecticide is not only good for the grower, it is good for natural enemies of the aphids, giving them more of a chance to prevent a soybean aphid outbreak by allowing their populations to persist.

O’Neal stresses the fact that a great deal of the funding for soybean aphid research comes from soybean growers through the US soybean checkoff program’s North Central Soybean Research Program. “The growers, through their association, have been incredibly forward-thinking and proactive in dealing with soybean aphid. The association has put up nearly a quarter of a million dollars a year to fund research so that their growers know the best way to manage pests and how well tools like insecticides and host plant resistance will work.” He says that the association also funds extension work by land-grant universities to turn research results into real-world uses. “The growers are very sensitive to the need to be good stewards of these tools. They’re thinking about the long term.”

Other sources of resistance
Several research groups have been testing large collections of genetic resources in soybean germplasm to find other plant introductions that show resistance to the soybean aphid. In addition to Rag1, a Rag2 gene has been identified. Other sources of resistance also have been identified, but the specific genes involved still need to be determined. 
For example, Wang has been testing early maturing soybean germplasm and has identified four plant introductions that show resistance. “Two of them are the type of resistance that interferes with the biology of aphids. We call that type of resistance antibiosis,” he says. The resistance that Wang has identified differs from Rag1 in that it seems to be controlled by two recessive genes, whereas Rag1 resistance involves one dominant gene. 

O’Neal was involved in small-plot field screening of soybean varieties contributed by various breeders to evaluate their performance in resisting aphids. He says that the lines developed by Michigan State University using the resistance sources identified by Wang had the lowest aphid populations across all of the study sites. “We had three levels of performance,” says O’Neal. “We had the susceptible, with the worst performance. Next were all the varieties that had some Rag1 or maybe Rag2. And then there was this Michigan State resistance, which had the best performance. Those differences held up throughout the two years that we did the small-plot screen across six to eight regions.”

Once the various resistance genes have been identified and markers are developed for those genes, soybean breeders can begin to breed them into commercial cultivars. There is also the possibility of combining resistance genes within a soybean variety so that it is harder for aphids to adapt to the resistance. Whether this is possible without yield drag, is necessary for aphid control, and works against all soybean aphid biotypes are some of the questions that will need to be answered, says O’Neal.

It will be very interesting to see how all the pieces of research fit together to tell the story of soybean aphid ecology and to produce new technology and management recommendations. For now, despite the potential advantages of aphid-resistant soybean varieties, O’Neal is unsure how quickly growers will adopt the technology because he says it is still possible to get good yields with susceptible varieties that are scouted and sprayed when necessary. “It comes down to two questions,” he suggests. “Is there enough seed available, and how will it be priced?”


Aphid wars
The only good aphid is not necessarily a dead aphid. “When I talk to growers, before they ask me if they should use resistant varieties, I ask them if they believe the recommendations that we’ve developed about scouting and the 250 per plant threshold,” says Dr. Matthew O’Neal, assistant professor and entomologist at Iowa State University. “I know from five years of research in the field that you don’t need to keep soybeans aphid free. You do need to treat them when an outbreak occurs, but it’s not necessary to keep it free of aphids because you’re going to use inputs that are not going to return anything and, in the long run, you will develop resistance in the aphid to insecticides so that the tools you have now that work really well won’t in the future.”

“Some growers are using insecticide in a preventative approach by applying it before the aphid arrives,” says O’Neal. This is not a good idea. “As a consequence, we’re killing off beneficial insects that eat aphids, making an enemy-free space for the aphid.” Clearly, this can compound the aphid problem.

“It’s always better to have more tools in your toolbox. The more you can throw at this pest in terms of host plant resistance, insecticides, and biological control, the better off you’ll be.” 


Soybean aphid resources for growers
Maps of soybean aphid numbers in scouted fields in Canada and the US are available at http://sba.ipmpipe.org/cgi-bin/sbr/public.cgi. Click on a calendar date to view recent soybean aphid observations; click on a province or state for specific commentary. 
Soybean scouting cards and a map of soybean aphid numbers for Ontario locations are available at http://www.soybean.on.ca/aphids.php


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