Beet western yellows virus (synonym: Turnip yellows virus) and green peach aphid in canola

GRDC and SAGIT project codes: DAS00151, CES00001, CES00002, DAV0119, S1114

Take home messages

• Beet western yellows virus (BWYV, syn. Turnip yellows virus) is widespread throughout grain growing areas of Australia.
• Early BWYV infection in canola can cause seed yield losses of up to 46%, decrease seed oil content and increase seed erucic acid and glucosinolate contents.
• Wild radish weeds and volunteer canola are the most important reservoirs but perennials such as lucerne and many weeds species are also infected.
• Epidemics are likely to occur when aphids are present early in the season (green bridge prior to seeding, warm temperatures).
• Integrated management strategies have been devised for BWYV in canola.
• Green peach aphid (GPA), the main vector for BWYV, has a high prevalence of resistance to insecticides. Growers should implement resistance management strategies for insecticides including neonicotinoids.

Background

Widespread infestations of green peach aphids (GPA) (Myzus persicae) during autumn and winter of 2014 contributed to an outbreak of Beet western yellows virus (BWYV, syn. Turnip yellows virus) in southern Australia. Canola crops across the lower and mid north regions of South Australia, the Eyre Peninsula, western Victoria and some parts of NSW have been severely affected by the virus.

The severity of the current BWYV outbreak is possibly due to a combination of the following factors:

• summer rainfall which resulted in a ‘green bridge’ of weed hosts of BWYV and aphids,
• the early start to the season and early sowing,
• very mild autumn conditions which contributed to early (and extended)  levels of aphid activity through till late June,
• crop management practices,
• the prevalence of insecticide resistance in GPA (particularly to pyrethroids, organophosphates, carbamates); and
• the low proportion of canola seed treated with imidacloprid (Gaucho®) in some areas.

In South Australia, canola crops in the lower and mid north were the most severely impacted, followed by the South Australian/Victorian Mallee, and some yield loss from BWYV infection has also occurred in canola crops on Eyre Peninsula.

BWYV is an aphid-borne virus that causes yield and quality losses in canola crops.  It also infects other crop and pasture species including mustard, chickpea, faba bean, field pea, lentil, lupin, lucerne, medic and subterranean clover.  BWYV is found widespread throughout southern and eastern Australia.

BWYV infection causes reddening, purpling or yellowing of lower leaves of canola plants.  Plants infected early (well before flowering) are often pale and stunted and these plants produce few flowers or seeds.  Symptoms are milder and stunting is lacking with late infection. In late infections there is minimum effect on yield.  Leaf symptom type and severity differ depending on plant age at infection, environmental conditions and the canola variety involved.  Symptoms of BWYV in canola can be confused with those caused by nutrient deficiencies, water-logging or other plant stresses that cause yellowing, reddening or purpling of lower leaves.

BWYV is not seed-borne and survives from one growing season to the next in over-summering canola, broad-leafed weed species, and perennial legume pastures. BWYV is spread by several aphid species that colonise canola including GPA which is the principle vector.  The virus infects the phloem cells in a plants’ vascular system but not its other tissues.  BWYV is transmitted persistently, i.e. once an aphid feeds on the phloem cells of an infected plant, it acquires the virus. When the infective aphid probes the phloem of a healthy plant, it infects the plant and continues transmitting BWYV for the rest of its life.

BWYV observations in South Australia 2014

Reports of failing canola crops started in mid-June, initially in South Australia from the lower north and Mallee regions. Entire paddocks were affected with purple/yellow leaves at the rosette stage followed by complete leaf loss. At the same time GPA was reported as widespread and in high numbers (> five per leaf on every plant). Symptomatic plants were submitted by agronomists to VIC DEPI Horsham and tests identified BWYV in 100% of these early samples. While it was not possible to separate losses from direct feeding damage and losses caused by virus infection, it is apparent that virus infection had an impact on crop growth and yield. Aphids would not have caused purple/yellow leaves and in the absence of virus, crops may have recovered once aphid population numbers dropped in winter.

By mid-September agronomists and researchers across southern Australia had submitted samples from 618 canola crops for BWYV of which 57% were positive.  290 of these samples were from South Australia where 86.55% of samples were positive (Table 1). Over 90 weed samples were also submitted for testing from South Australia and results demonstrated the wide host range for BWYV (Table 2).

Table 1. Incidence of BWYV in canola for South Australian regions in 2014 determined by virus testing of plant material at Horsham VicDEPI.

Table 2. Incidence of BWYV virus in weed species sampled by agronomists in and around South Australian canola crops in 2014 determined by virus testing of plant material at Horsham VicDEPI.

Other weeds tested as uninfected - Barley grass, bedstraw, charlock, dandelion, geranium, London rocket, Medic, ryegrass, soursob, sowthistle, wild oats, short fruited turnip, capeweed, vetch

*A negative result in the table below does not infer that these species are not hosts of BWYV.

Crop management influenced the severity of BWYV infection and while observations made in 2014 are summarised here, these still need to be confirmed via the management survey being undertaken within the GRDC project DAS00151.

Stubble treatment:

Milder symptoms were observed where canola was sown into standing stubble despite high infection rates at mid-season. This is because aphids prefer to land on bare earth and most likely they did not move into crops in standing stubble until after the vulnerable rosette stage.

Crop Density:

Milder symptoms were observed where the crop was denser. As above, aphids prefer to land on bare earth and most likely they did not move into denser crops until after the vulnerable rosette stage.

Sowing date: 

Milder symptoms occurred in later sown crops. This is linked to the timing of aphid flights when crops are at the most vulnerable stage.

Weed control:

Severe symptoms were observed where weed control was closely followed by sowing. This practice provided the opportunity for aphids to move directly from the dying weeds to the emerging crop. Milder symptoms were observed if there was a 10-14 day break between weed control and sowing.

Seed dressings:

Milder symptoms occurred in crops treated with seed dressings containing neonicotinoids (e.g. imidacloprid, Gaucho®) despite high infection rates at mid-season. These seed dressings probably delayed the infestation by GPA and allowed the canola seedlings to grow beyond the rosette stage before virus infection occurred.

Varieties:

Observations in commercial crops found that the variety Stingray often did not display symptoms of BWYV infection.  Disease assessment and plant sampling for virus testing were conducted at the Roseworthy NVT trial on 6^th August 2014. The data had a high degree of variability but there were significant differences in expression of virus symptoms and % infection rate (Table 3). In particular the variety Stingray showed minimal virus symptoms (3.3% leaf area diseased (LAD)) in this trial and had a relatively low % infection rate (30%) but data from one interstate trial had higher infection rates for Stingray. Further data is required to confirm this result.

Table 3: Results of visual assessment of virus symptoms (% leaf area diseased of lower canopy) and BWYV virus testing (% infection rate) at Roseworthy NVT trial, rated and sampled on 6^th August 2014. Virus tests were conducted at Horsham Vic DEPI. Different letters indicate significant differences (P<0.001).

Yield loss observations:

There were no trials of infected and uninfected plots for yield comparisons and hence the information below is based on observations from experienced agronomists.

Yield loss from BWYV infection ranged from 75% loss to negligible effects across South Australia.

• A small percentage of crops (10-15%) only yielded 500-600 kg/ha down from an average of 2-2.5 t/ha.  These were the crops infested at a very early stage in the lower north, as well as a few crops in the Mallee region and around Lock on Eyre Peninsula.
• 50-60% of crops in the lower and mid north region of South Australia and a lower percentage on Eyre Peninsula had yields of 1-1.1 kg/ha i.e. 50% of normal yield. Possibly half these yield losses are due to diamondback moth and half due to virus. Diamondback moth was reported to be more numerous in crops that had been sprayed earlier with insecticides for the control of GPA and other establishment pests, possibly due to the insecticides having killed off the beneficial insects. Frost and waterlogging also affected some crops. These crops had extensive symptoms of virus but continued to grow throughout the season although yield was affected.
• 20-25% of crops in the lower and mid north, and a higher percentage on Eyre Peninsula, did not get infected with virus, and yielded  approximately 2 t/ha.

BWYV studies in Western Australia

Methodology

Studies on BWYV in canola in Western Australia began in 1998, with extensive surveys of canola crops, broad-leafed weeds and volunteer canola plants across the grainbelt.  These surveys were done over-winter and over-summer, and completed over a four year period.  Other studies were undertaken during the same period and subsequently to determine the occurrence of BWYV in grain legume crops, vegetable brassica crops, additional weeds and native plants. 

Seed yield and quality losses caused by BWYV infection were quantified in field experiments over two years.  Plants infected with BWYV and infested with GPA were introduced to plots of canola to provide sources of infection.  Seed dressing and/or foliar insecticide were applied at different times to manage the virus incidence in plots, and eliminate aphid feeding damage as a cause of losses.  Virus levels were monitored by laboratory testing and plots harvested.  Effect on canola yield and quality (oil, glucosinolate and erucic acid content) were evaluated.  For three further years, additional field experiments examined the effectiveness of neonicotinoid seed dressings applied at recommended rates in supressing BWYV spread in canola.  

Different canola genotypes were examined for their responses to infection with BWYV in field and glasshouse experiments.  Genotypes were exposed to infection with BWYV spread by GPA.  Virus infection was monitored by laboratory testing and genotypes evaluated for sensitivity and susceptibility to infection. 

In pot experiments, BWYV infective aphids were placed on canola plants grown from seed treated with insecticide seed dressing.  Aphid populations and virus infection were monitored and compared with untreated control plants.

Epidemiological information and meteorological data was gathered to better understand the environmental conditions that favour BWYV epidemics.

Results and discussion

From surveys of canola crops in WA, BWYV was found to be the predominant virus infecting these crops with wild radish (Raphanus raphanistrum) and volunteer canola being identified as major virus reservoirs.  Interestingly, over-summer surveys of weeds found BWYV infecting four other weed species including wild melon (Citrullus lanatus), fleabane (Conzya spp.), stinkweed (Navarrentia squarrosa) and blackberry nightshade (Solanum nigrum).  In addition seven aphid species were also found over-summering on weeds.  In other surveys, BWYV was also found infecting other crop or pasture species including mustard, vegetable brassicas, chickpea, faba bean, field pea, lucerne, medic and subterranean clover.  Some native plant species were also infected.  BWYV is also found widespread elsewhere in southern and eastern Australia.

From field trials when canola plants became infected by GPA very early and the BWYV incidence in crops reached 96-100%, overall seed yield losses were up to 46%.  For every 1% increase in the level of BWYV in a canola crop, there was a 6-12kg/ha decline in yield resulting from formation of fewer seeds.  BWYV infection diminished seed quality by decreasing oil content and increasing erucic acid and glucosinolate levels. If the crop becomes infected late, spread was much less and yield and quality losses were minimal.

From field and glasshouse experiments, several canola genotypes (including varieties Tranby and Trigold) were found with useful infection resistance to BWYV.   However, given the often rapid turn-over of canola varieties, continued evaluation of new varieties and identification of additional parental lines of BWYV resistant varieties is required.

In field experiments, use of recommended rates of imidacloprid applied commercially often gave relatively poor BWYV control. In glasshouse experiments, use of imidacloprid seed dressing applied commercially was also only partially effective due to not covering all seeds.   Care must be used to avoid development of imidacloprid resistance in GPA from unnecessary or inappropriate use of this neonicotinoid chemical group. 

The extent of BWYV spread in canola crops and the resulting yield losses varied between years, growing seasons, rainfall zones, and geographic regions. High rainfall before the growing season starts favoured ‘green bridge’ formation and enabled green peach aphid populations to build-up and spread BWYV before sowing time. A substantial ‘green bridge’ before sowing starts favoured early aphid arrival and consequently widespread early BWYV infection of canola crops. This information was used to develop a forecasting model for BWYV in canola used in WA. The WA BWYV model was found not suitable for South Australia and Victoria possibly due to adverse weather conditions during the growing season (frost, temperature and rainfall) that affect the aphid numbers and virus infection. Dr Moin Salam of DAFWA is developing a BWYV forecasting model suitable for South Australian and Victorian conditions.  

2014 GPA Resistance Studies

Methodology

Approximately 50 GPA samples were collected by researchers, advisers and growers in autumn-spring 2014, and subsequently screened for insecticide resistance. These populations spanned NSW, Victoria and SA. 

DNA testing by cesar was carried out using TaqMan assays to screen: (i) the kdr and/or super-kdr mutations that confer resistance to pyrethroids, (ii) the MACE mutation that confers resistance to carbamates, and (iii) the overproduction of one of two closely related carboxylesterases (E4 and FE4) that confers resistance to organophosphates. In each case, 20 individual aphids from each population were screened.

Results and discussion

Testing revealed widespread resistance to the three chemical groups tested. Following DNA tests, aphids from all populations were found to be resistant to synthetic pyrethroids, including bifenthrin and alpha-cypermethrin, and to carbamates, including pirimicarb. The use of these insecticides is not expected to provide control against these GPA populations in most field situations. The mechanism of resistance to pyrethroids is also likely to render these products ineffective as an anti-feed.

The story for organophosphates, such as dimethoate and chlorpyrifos, is more complex. The amplified carboxyl-esterase mechanism leads to organophosphate resistance in GPA. This mechanism is unusual because it is regulated by DNA methylation, and can be ‘switched on’ in response to pesticide exposure. As a result, aphid populations can quickly adapt to survive organophosphates, even though they may have recently been effective. Following DNA tests, all aphid populations tested were found to contain resistance at the esterase genes. Aphids from these populations are expected to have a moderate level of resistance (5-20-fold) to organophosphates.

The field efficacy of organophosphates remains uncertain. Some control may be achieved against populations found to be ‘resistant’, although the use of organophosphate insecticides is risky and may not be effective (particularly if the population has been exposed to insecticides already this season). When faced with GPA populations with known resistance to organophosphates, growers are advised to spray test strips within paddocks to determine field efficacy.

Management of BWYV and GPA

An integrated disease management approach using control measures that operate in different ways is needed to control BWYV and GPA in canola crops:

• Control wild radish weeds and canola volunteers.  This helps to minimise potential aphid and virus infection sources near the crop.
• Allow a 7-14 day period between weed control and sowing the crop. This reduces the transfer of aphids from weeds directly onto the seedling crop.
• Manipulate sowing dates. Avoid exposure of young canola seedlings to peak aphid flights by delayed sowing.
• Sow at high seeding rates.  High plant density helps diminish the rate of virus spread and speeds up canopy closure resulting in lower aphid landing rates.
• Sow varieties with infection resistance.  Some varieties will only become infected at low levels, while others have moderate resistance to BWYV infection. Growers need to be aware that such varietal differences do exist.
• Sow into standing stubble to reduce aphid landings. This will reduce the likelihood of virus infection as aphids will prefer to land elsewhere.
• Use insecticide seed dressings. Insecticide seed dressing applied effectively can provide early control of GPA at the vulnerable seedling growth stage.  However, to achieve effective control application must ensure that sufficient insecticide sticks to each seed. 
• Observe appropriate use of foliar insecticides for control of aphids to avoid exacerbating insecticide resistance issues and to protect beneficial insects, including predators and foraging honey bees.

Conclusion

Wild radish (Raphanus raphanistrum) and volunteer canola are the most important reservoirs but perennials such as lucerne and some native legumes are also infected.  Early BWYV infection can cause seed yield losses of up to 46%, decrease seed oil content and increase seed erucic acid and glucosinolate contents.  Infection resistance was identified in some Australian varieties and imidacloprid seed dressing can be effective in controlling BWYV if coverage is adequate. 

Identify the risk of potential of BWYV epidemics prior to sowing and use appropriate management strategies.

In many cases in 2014, growers were unable to achieve adequate control of GPA populations due to the prevalence of insecticide resistance. High levels of resistance to carbamates and pyrethroids are now confirmed to be widespread across Australia. Moderate levels of resistance to organophosphates have been observed in many populations, and there is evidence that resistance to neonicotinoids (e.g. imidacloprid) is evolving. Growers and advisers should implement resistance management strategies for GPA. Further information can be found at the following sites:

• http://ipmguidelinesforgrains.com.au/ipm-information/resistance-management-strategies/
• Resistance Management Strategy for the Green Peach Aphid, GRDC Fact Sheet
  

Acknowledgements

Bill Kimber, Helen de Graaf, Kym Perry and Ken Henry (SARDI): Industry meetings and survey of management practices affecting BWYV in canola.

Michelle Russ and Marzena Krysinska-Kaczmarek (SARDI): Preparation of virus samples.

Siobhan de Little and Anthony van Rooyen (cesar): GPA resistance testing.

Katherine Hollaway (Vic DEPI): Map of BWYV incidence from virus testing (www.eXtensionAUS.com.au).

Murray Sharman (QDAFF): PCR tests to confirm identity of Turnip Yellows Virus.

Sam Holmes (Holmes Farm Consulting): Assistance with GRDC and SAGIT Project applications.

All the growers, advisers and other industry people who submitted plant and aphid samples for testing.

References

Coutts, B.A., Hawkes, J.R. and Jones, R.A.C. (2006) Occurrence of Beet western yellows virus and its aphid vectors in over-summering broad-leafed weeds and volunteer crop plants in the grainbelt region of south-western Australia. Australian Journal of Agricultural Research 57:975-982.

Coutts, B.A. and Jones, R.A.C. (2000) Viruses infecting canola (Brassica napus) in south-west Australia: incidence, distribution, spread and infection reservoir in wild radish (Raphanus raphanistrum). Australian Journal of Agricultural Research 51:925-936.

Coutts, B.A., Webster, C.G. and Jones, R.A.C. (2010).  Control of Beet western yellows virus in Brassica napus crops: infection resistance in Australian genotypes and effectiveness of imidacloprid seed dressing. Crop and Pasture Science 61:321-330.

Jones, R.A.C., Coutts, B.A., and Hawkes, J.R. (2007) Yield-limiting potential of Beet western yellows virus in Brassica napus. Australian Journal of Agricultural Research 58:788-801

Maling, T., Diggle, A.J., Thackray, D.J., Siddique, K.H.M. and Jones, R.A.C. (2010). An epidemiological model for externally acquired vector-borne viruses applied to Beet western yellows virus in Brassica napus crops in a Mediterranean-type environment. Crop and Pasture Science 61:132-144.

UminaP.A., Edwards, O., Carson^, P., van Rooyen^, A. and Anderson, A. (2014). High levels of resistance to carbamate and pyrethroid chemicals widespread in Australian Myzus persicae (Hemiptera: Aphididae) populations. Journal of Economic Entomology 107: 1626- 1638.

Other resources:

• https://www.youtube.com/results?q=groundcover+TV+15
• www.eXtensionAUS.com.au

Contact details

Brenda Coutts
brenda.coutts@agric.wa.gov.au

Paul Umina
pumina@unimelb.edu.au

Jenny Davidson
Jenny.Davidson@sa.gov.au