Cereal Viruses of Importance in Montana

There are several viruses of wheat and barley in Montana that can be economically important. Here we describe the symptoms and control for these diseases.

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THERE ARE SEVERAL ECONOMICALLY IMPORTANT

viruses in Montana cereal grain crops. The principle virus-caused disease is Wheat streak mosaic virus. However, there are additional mite-transmitted viruses, aphid-transmitted viruses and soil-borne viruses that are also important. The purpose of this publication is to describe 1) the principle viruses of importance in cereal crops in Montana, 2) how to recognize virus-infected plants, 3) how viruses move from plant to plant, and 4) how to manage them.

Wheat streak mosaic virus

Wheat streak mosaic (WSM), caused by wheat streak mosaic virus (WSMV), occurs in all wheat-growing regions worldwide and can infect winter and spring wheat, durum, barley, corn, and many other grass species including grassy weeds. Losses in the central Great Plains region of the United States average 2% per year according to estimates from the Kansas Department of Agriculture. WSM was first observed in Montana in 1954 on winter wheat. Since then, there have been major outbreaks of the disease in 1964, 1981, 1993, 1994 and 2016 with losses of greater than 10% statewide. Losses in individual fields can reach 100%.

Symptoms of WSMV infection

Symptoms of WSMV include yellowing of the leaf in a streaked or stippled pattern (Figure 1). Severely infected seedling plants may appear lemon yellow and be confused with nutrient deficiency or cold damage. However, nutrient deficiency is consistent throughout a field or field section, whereas virus diseases are normally patchy. Symptoms often appear first at the edges of a field or near patches of volunteer wheat or downy brome (cheatgrass) and usually do not appear until after spring warm-up and new growth. Rarely, symptoms can appear on winter wheat in the fall.

Winter or spring wheat plants infected at early growth stages become stunted, discolored and rosetted (leaves form a prostrate growth habit). Plants do not use water efficiently (Workneh et. al, 2010). Growth virtually stops and few or no heads are formed. Premature death is also possible. If infection occurs after tillering but before early jointing, grain can be formed. However, florets often are sterile. When wheat is infected at a later growth stage, grain is produced, but test weights may be low. Symptom severity is related to variety, the developmental state of the plant at the time of infection, plant nutrition, air and soil temperature, and the virus strain and/or species involved. Symptoms can be confused with early stages of barley yellow dwarf, nitrogen or sulfur deficiency, winter or frost injury and herbicide injury due to imidazolinones or sulfonylureas. Co-infections with more than one wheat virus may cause more severe symptoms and plant death. Later infections, and adequate but not excessive nitrogen levels may help minimize losses.

FIGURE 1. Leaf symptoms of wheat streak mosaic virus (WSMV) in barley.

FIGURE 2. Wheat curl mites on a wheat leaf. Note the leaf curling (bottom of photo) which protects the mites and creates a favorable microclimate.

Wheat curl mite as a vector of WSMV

WSMV is transmitted by the wheat curl mite (WCM), Aceria tosichella. Another common mite on wheat is the brown wheat mite (Petrobia latens) which vectors barley yellow streak mosaic virus, but does not vector WSMV. The wheat curl mite is not easily seen with the naked eye, but when present in high numbers can make the wheat leaf curl so that the upper surface is rolled inward. Wheat curl mites can be difficult to see but examine a curled leaf with at least a 10X magnifying lens for presence of the small white, cigar-shaped mite (Figure 2). Mites are often easy to find on the youngest fully expanded leaflet of WSMV-infected plants.

Warm fall temperatures and warm, dry spring weather are ideal for mite increase especially on volunteer wheat. Females lay 3-25 eggs, usually about one per day, during their life. Mite populations build rapidly at temperatures between 75-80°F, with a complete life cycle taking approximately 7-10 days at these temperatures. Population growth is slow in cool temperatures (<48 F), and WCM development is very slow and essentially stops at 32°F. WCM tolerate freezing temperatures and can survive over the winter. Reproduction stops at low temperatures but mites can survive freezing temperatures for extended periods, especially when protected within the crown of the plant and insulated by snow cover. The mite survives the winter in the crown of the wheat or grassy weed plants as eggs, nymphs or adults. When infected plants begin growing again in the spring, the eggs hatch and nymphal stages acquire the virus from these plants. The mite vector must acquire the virus from an infected, living plant. The mite feeds with what are known as ‘piercing- sucking’ mouthparts on plant epidermal cells. This creates silvery flecks on the leaf surface where the tissue has been damaged. Mites can only survive on green leaf tissue. This is why destruction of green tissue (elimination of the ‘green bridge’) effectively stops the disease.

Movement of the pathogen and patterns in the field

Yellowing plant symptoms often occur first on field edges, especially those bordering and/or downwind from other infected wheat fields or volunteer wheat. Symptoms also may start in areas bordering rangeland or grassy areas which contain susceptible grass hosts for WSMV such as downy brome (cheatgrass, Bromus tectorum). After appearing on field margins, symptoms may progress toward the middle of the field. Wind dispersal occurs when mites crawl up the tops of host plants and are blown into adjacent areas, often when the plant is drying down due to maturity or herbicide application. Mites are dispersed up to two miles, but ¼ mile is probably more typical. For this reason, do not plant winter wheat next to or downwind to late-maturing corn or spring wheat as these crops can harbor both the wheat curl mite and WSMV. Do not plant spring wheat or barley downwind of infected winter wheat. During hot weather, mites desiccate rapidly and wind dispersal is minimal, but when humidity is high and temperatures are between 50-60, mites can survive multiple days off of a host.

TABLE 1. Capacity of prevalent grassy weeds in Montana to serve as wheat curl mite (WCM) and wheat streak mosaic virus (WSMV) hosts¹.

¹data taken from Somsen 1970, Townsend 1996, Brey 1998, and in Ito 2012

IMPORTANT: When volunteer wheat is sprayed with herbicide, mites sense their host is dying and will move, so avoid spraying volunteer and grassy weeds upwind of susceptible wheat during cool, moist and windy weather. When the weather is hot and dry, it is less likely the mite will survive to find a new host.

As a plant matures, mites migrate to the heads and are found near the glumes. If viable grain shatters before harvest, mites attached to kernels can survive long enough to move onto the sprouting seedlings. However, mites die if insufficient moisture or poor seed-to-soil contact does not allow kernels to germinate within a few days after shattering, or if they do not migrate to other green host plants.

WSMV has been found to be transmitted at low levels (0.2 to 1.5%) in wheat seed in an Australian study (Jones 2005), and is also thought to have moved to Argentina via seed transmission (Stenger and French, 2009). Currently, seed exported to some countries must be tested for WSMV. Crops with a severe infestation of WSMV may contain grain with the virus (seedborne virus), but this virus may or may not be transmitted to the resulting seedlings (seed transmission).

Role of grassy weeds and grasses in virus epidemics

Wheat curl mites and WSMV can both survive in grassy weeds, but neither can survive on/in broadleaf weeds. For grassy weeds to increase the risk of WSMV in cereals, the weed species must both be susceptible to the virus and support WCM populations. Throughout the Great Plains, WSMV incidence is reported in many wild grasses including green foxtail and Persian darnel. In 1995 and from 2008-2009 native and non-native grasses in North- central Montana were surveyed and tested for presence of mites and WSMV (Table 1). Results indicated that downy brome, green foxtail and jointed goatgrass are capable of hosting both the wheat curl mite and WSMV. Western wheatgrass and smooth brome, both perennial grasses, are hosts to the wheat curl mite but not the virus. WSMV was not found in crested wheatgrass or yellow foxtail. The status of prevalent weeds in Montana as WSMV and mite hosts is summarized in Table 1.

Variety tolerance to WSMV infection

No varieties have shown consistent resistance to WSMV, however, some are more tolerant than others. Symptoms in the crop do not necessarily mean there will be a significant yield loss. In field experiments conducted in Bozeman from 2008-2011, where wheat was inoculated with WSMV, winter wheat averaged approximately 15% yield loss and spring wheat and barley averaged approximately 43% yield loss due to WSMV (Tables 2 and 3, Miller et al. 2014).

TABLE 2. Yield loss (%) of winter wheat due to mechanical inoculation with Wheat streak mosaic virus at tillering.

Yield loss: Low < 10%; Medium 10-20%; High 20-30%; Very High 30-40%

Recommended planting dates to avoid WSM

WSM management is based on avoidance of the vector, destruction of the green bridge, and temperature at time of planting. If mite populations increase during the fall because of ideal weather conditions (warm and sunny) and an abundance of volunteer wheat and other grass hosts, massive migration to next year's winter wheat can occur. Volunteer wheat and grassy weeds that are left uncontrolled are a source of mite and virus – they form a ‘green bridge’ to the new crop planted in that field. Destruction of the green leaf material prior to winter wheat seeding will effectively break the disease cycle. Winter wheat is more likely to become infected with WSMV if the mite and virus are present in live (green) tissue, both in the field and in adjacent stubble fields. However, cold fall temperatures reduce the activity of the mite and spread will be lessened. In the same fashion, for spring wheat, early seeding reduces the risk of WSMV infections as temperatures are too cool for mite activity and buildup, and plants are more mature (less susceptible) by the time mite populations grow. Delaying spraying of the stubble fields with glyphosate until spring will result in migrations of the mite to newly planted spring wheat. Volunteer and grassy weed management in August will inhibit the fall and spring infection cycles.

CONTROL SUMMARY

The three most economically feasible methods of controlling WSMV outbreaks are:

• Elimination of the ‘green bridge’ by managing volunteer wheat and grassy weeds in August, 2-3 weeks before planting
• Using tolerant varieties
• Adjusting planting date to avoid colonization by WCM or minimize WCM growth

Winter and spring wheat seeding date as a management tool for WSM is a balancing act of planting early to establish a vigorous plant for yield potential and avoiding the transmission of WSMV by the wheat curl mite. Although planting date is no guarantee to avoid disease, colder fall (i.e. prolonged temperatures at or below freezing) temperatures will minimize mite migration and virus transmission. General guidelines for winter wheat planting date is after September 5 in northern Montana, September 15 in central Montana, and September 20 in southeastern Montana. Fall planting depends on local weather conditions. If it is unseasonably warm when fall planting should begin, it may be necessary to postpone seeding as warm weather keeps mites active for a longer time and wheat may become infected.

Spring wheat crops should be planted as early as possible. Late-seeded spring wheat exposes susceptible seedlings to an active population of mites with the higher temperatures. Spring wheat should not be planted near winter wheat with symptoms of WSM, or near fields of volunteer wheat that were heavily infested with the wheatcurl mite in the previous fall.

TABLE 3. Yield loss (%) of spring wheat and barley due to mechanical inoculation with Wheat streak mosaic virus at tillering.

Yield loss: Low < 10%; Medium 10-20%; High 20-30%; Very High 30-40%; Extremely (Ex.) High >40%

Chemical Control for WCM

No chemicals are registered for wheat curl mite management (Murphy, 2016).

Nitrogen fertilizer impacts

Adding nitrogen to wheat plants increases the reproductive rate of the WCM and plant susceptibility to WSMV. Miller et al. (2015) found that N fertilization increases the reproductive rate of the WCM to the extent that fertilized plants could have 24 times more WCM than would be found on unfertilized plants after six weeks. Also, in a field study in Montana where wheat was mechanically infected with WSMV, Miller et al. (2015) found that as soil nitrate levels rose from 0 ppm to 20 ppm, the probability of WSMV infection rose from 8% to 53%. When nitrate levels increased further to 40 ppm, the infection rate rose to 67%. Therefore, if a field is infested, do not add additional nitrogen. Yield losses due to WSMV eliminate any yield benefit provided by the nitrogen application and cause the disease to spread more than if nitrogen had not been applied.

FIGURE 3. Symptoms of barley yellow streak mosaic virus on barley.

FIGURE 4. Symptoms of barley yellow dwarf virus on wheat. Note purpling and yellow streaks on leaves.

Summary of WSMV Management approaches

• The virus and the mite are dependent on green tissue for their survival. They survive on wheat, barley, oats, corn, rye, and grassy weeds, but volunteer or cultivated wheat is the ideal host for both the virus and the mite. Eliminating the green bridge by destroying volunteer wheat and grassy weeds using herbicides or tillage during August (2-3 weeks before planting) is the most important control method. Herbicides can act slowly on grassy weeds depending on the herbicide mode of action and the conditions at the time of application, so an extended period before planting into the field is critical to eliminate the green bridge. Plants need time to die so they can no longer serve as a pathogen source.
• Fields managed as large blocks rather than strips minimize the field edges that are exposed to mite- infested volunteer wheat or grasses.
• Delayed planting in the fall will minimize exposure of seedlings to mite infestations due to cool temperatures which reduce mite activity.
• There are no pesticides registered for use for WCM control. Imidacloprid has been shown to increase WCM populations and WSMV (Harvey et al. 1998).
• Do not add additional nitrogen to WSMV and mite-infested fields, as fertilization increases mite population growth rate and wheat susceptibility to WSMV infection (Miller et al. 2015).

Other wheat curl mite-transmitted viruses in wheat

Wheat mosaic virus and Triticum mosaic virus

There are two additional wheat curl mite-transmitted viruses present in the U.S. which rarely occur in Montana. When plants are co-infected with WSMV and these viruses, increased yield losses can occur (Byamukama, 2011; Stenger 2007). Changes in management practices in Montana including earlier planted winter wheat next to late-maturing spring cereals, increased corn production, reduced tillage that favors the green bridge and grassy weed production, and a warming climate favoring mite survival and reproduction may increase virus epidemic frequency. The first of these viruses of concern is wheat mosaic virus (WMoV), formerly known as High Plains virus (HPV). WMoV was first identified in corn and WSMV-resistant winter wheat in Kansas in 1993. It is seed transmitted in corn at very low levels. Sweet corn varieties are more susceptible than field corn to WMoV. Because until recently there has been very little corn in the Montana cropping system, this may explain why this virus has not been important here. WMoV was identified for the first time in wheat and barley in central Montana in 2008, suggesting it has been in the state for an extended period of time but was not recognized (Burrows 2009). The second virus is triticum mosaic virus (TriMV), identified in WSMV- resistant winter wheat in Kansas in 2006. It has been identified in Montana but very infrequently and always associated with WSMV infections. Co-infections of two or more of these viruses can cause much more severe symptoms and yield loss than infection by a single virus. Control of these viruses is the same as for WSMV.

FIGURE 5. Wheat soilborne mosaic virus symptoms often occur in low-lying areas.

Brown wheat mite transmitted virus:

Barley yellow streak mosaic virus

Barley yellow streak mosaic virus (BaYSMV) was discovered by scientists from Montana State University working on barley in 1982, and later reported in several western states, Alaska, and Alberta, Canada (Lapierre 2005). Barley plants infested with BaYSMV show chlorotic streaks, stripes, and dashes parallel to the leaf veins and often only on half the leaf (Figure 3). Plants can also have varying degrees of stunting.

Yield losses reaching 100% in individual fields have been reported when barley seedlings are infected with BaYSMV and infested with the brown wheat mite vector, Petrobia latens. The mite’s eggs are the overwintering reservoir of BaYSMV, bridging the virus from summer/ fall to spring plant infections. Destroying the green bridge will reduce mite populations by eliminating a feeding source but mite eggs (red eggs for active populations; white eggs for inactive populations) might survive on standing stubble and under field rocks. Disease incidence and severity are greatest in recrop barley and non-irrigated crops under drought conditions. This virus can also infect wheat to a low extent (less than 10%) when mite populations are high and the wheat is planted next to infected barley. The natural plant host range also includes three grasses, barnyardgrass (Echinochloa crus galli), Persian darnell (Lolium persicum), and green foxtail (Setaria viridis) (Lapierre 2005). No resistant barley cultivars are known, and chemical control for the mite vector is generally not cost effective.

Aphid transmitted viruses: Barley yellow dwarf

Aphid transmitted viruses can occur sporadically in Montana. They are usually associated with aphids migrating from other states rather than aphids overwintering in Montana. These flights change yearly and are hard to predict. The most common aphid transmitted viruses we see are barley yellow dwarf virus (BYDV) and cereal yellow dwarf virus (CYDV). Symptoms include yellowing and/or streaking of leaves and often purpling of the flag leaf and/or stem (Figure 4).

BYDV and CYDV cause barley yellow dwarf (BYD) disease. They are members of the family Luteoviridae and are only acquired in the vector and transmitted to a healthy plant if the aphid has an extended time to feed (more than two hours). Because of that fact, aphids that colonize the plants generally vector this disease rather than aphids that do not colonize cereal grains. The most common vectors in Montana are the greenbug (Schizaphis graminum), the bird cherry oat aphid (Rhopalosiphum padi), the English grain aphid (Sitobion avenae), and the corn aphid (Rhopalosiphum maidis). The Russian wheat aphid (Diuraphis noxia) is not a vector. To identify aphids in your field, you can use the MSU Extension Montguide, Aphids of Economic Importance in Montana (MT200503AG), that can be obtained from MSU Extension Publications, or contact your county Extension agent. The aphid vector(s) can be effectively controlled using an insecticide. If there is already a high number of plants in the field showing symptoms it is likely the infection is nearly 100% and control of aphids at that point is not recommended. In the case of severe virus infection, winter wheat could be destroyed in the fall and replanted to spring crops.

Soilborne viruses

Wheat soilborne mosaic virus (WSbMV) is known to occur sporadically in Montana. This virus is transmitted by Polymyxa named Polymyxa graminis. This organism prefers low-lying wet areas in fields (Figure 5). The virus contaminates fungal structures called zoospores, or swimming spores, and infects a plant during feeding and infection of the vector, Polymyxa. The virus can survive in the soil as an infection of the oospore (fungal reproductive structure) for years. The virus will spread associated with soil on field equipment and via blowing of contaminated soil in the wind.

Control of this virus is very difficult. Resistant or tolerant wheat varieties have been developed by Kansas State University but it is not known how effective they are in Montana. Because of the longevity of the vector in soil, it is not known how effective crop rotation to a non-cereal will be to minimize the disease. Soil fumigation to kill Polymyxa host is an option but is economically prohibitive.

Virus Identification

To get any plant virus identified, contact your local county Extension agent or the Schutter Diagnostic Laboratory. Our website is diagnostics.montana.edu, phone 406-994- 5150, or email diagnostics@montana.edu.

Acknowledgments

Partial research support for developing this publication has been provided by the Montana Wheat and Barley Committee. The wheat virus survey of Montana was funded with grants from subcontracts under the USDA- CSREES IPM Grant number 2007-37620-18152, USDA-Crops at Risk grant number 2008-51100-04461, and USDA-Pest Management Alternatives Program grant number 2012-34381-20120.

For more information

Brey, C. W., Johnson, G. D., and Blodgett, S. L. 1998. Survey of Montana grasses for wheat curl mite (Acari: Eriophyidae), the vector of Wheat streak mosaic virus. Journal of Agricultural Entomology. 15: 173-181.

Burrows, M., C. Thomas, N. McRoberts, R. Bostock, Coop, J. Stack. 2016. Coordination of Diagnostic Efforts in the Great Plains: Wheat Virus Survey and Modelling of Disease Onset. Plant Dis. 100: 1037- 1045.

Burrows, M., Franc, G., Rush, C., Blunt, T., Ito, D., Kinzer, K., Olson, J., O’Mara, J., Price, J., Tande, C., Ziems, A. and Stack, J. 2009. Occurrence of viruses in wheat in the Great Plains region, 2008. Online. Plant Health Progress doi:10.1094/PHP-2009-0706-01-RS.

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