Fungicide resistant wheat powdery mildew – mildewcide success at Malinong

Take home messages

• Fungicide resistance surveys indicate increasing levels of QoI fungicide resistance and saturation of the mutation associated with DMI fungicide reduced sensitivity.
• DMI and QoI fungicides failed to reduce wheat powdery mildew at Malinong in 2023.
• Mildewcide products reduced wheat powdery mildew to manageable levels at Malinong.
• The application of group 11 QoI fungicides increased the frequency of resistance mutation G143A at the QoI target at three trial sites where resistance was present at low levels prior to fungicide application.
• APVMA permits have been issued for the use of Legend® (quinoxyfen) (PER93197), Vivando® (metrafenone) (PER93198) and Talendo® (proquinazid) (PER93216) for the control of wheat powdery mildew. These products have provided high levels of powdery mildew control in wheat trials from 2020–2023, when applied prior to development of severe infection.

Background

Similar to 2022, wheat powdery mildew (WPM) was widespread across south-eastern Australia in the 2023 season. It was easily identified in most wheat growing regions, expanding its area of incidence compared with historical occurrence. There are a range of interacting factors that have caused this, including the predominance of SVS varieties grown in most regions over a long period of time, conducive environmental conditions for developing large crop canopies and for disease development, and inoculum source carrying over from previous seasons.

Difficulty achieving high levels of disease control with what were considered robust and well-timed fungicides is continuing to be reported in many regions. Fungicide resistance testing, funded by SAGIT project TC120 and GRDC project TRE2204-001RTX, has revealed resistance to group 11 (QoI) and reduced sensitivity to group 3 (DMI) fungicides as an important factor in these control failures. GRDC project TRE2204-001RTX continues to quantify the extent and speed of resistance development across the regions and identify management strategies for WPM, given resistance development.

Method

Fungicide resistance paddock survey

A field survey to determine frequencies of the mutations G143A at CytB (Qol fungicide resistance) and Y136F at Cyp51 (DMI reduced sensitivity) was undertaken in 2022. This included 145 paddocks sampled across SA and Vic, including the Eyre Peninsula, SA Mallee and Upper SE of SA. An additional 51 paddocks, predominantly from the Yorke Peninsula, were sampled in 2023. However, results from these resistance tests were not available at the time of publication. The 2022 and 2023 samples add to the database of 73 paddocks sampled from the Yorke Peninsula and Mid North SA in 2021 and NE Vic and southern NSW in 2020.

Field trials

Small plot trials were established at three locations in 2023, at Wards Hill and Malinong, SA and Katamatite, Vic. These trials investigated post-emergent fungicide efficacy, pre-emergent fungicide efficacy, fungicide timing and varietal resistance interactions. A moderate to high level WPM infection occurred at Malinong (fungicide efficacy and variety resistance trials) in 2023 and this paper primarily focuses on these results. Very low levels of WPM infection occurred at the Wards Hill and Katamatite sites in 2023.

Fungicide efficacy trials

The fungicide efficacy trial at Malinong was sown to ScepterA wheat on 9 May 2023. The fungicide treatments shown in Table 1 were applied at GS32 (2nd node) on 17 July 2023 and GS41 (flag leaf sheath extending) on 21 August 2023. Product rates were selected based on maximum label rate, unless specified otherwise. Wheat powdery mildew was scored as pustule counts on 21 August and 20 September 2023. Twelve middle tillers were selected from each plot and pustules were counted on the stem, flag-3 and flag-2 on 21 August and flag and flag-1 on 20 September. Statistical analysis was conducted using the transformation 1-1/sqrt(pustule count + 1) using mixed linear models in R. Where large pustules occurred or merged, a count of 1 was given for each 2mm2 of pustule area. Septoria assessments were conducted by estimating the leaf area infected on the flag and flag-1 of the same tillers as for the WPM assessment. Plant samples were collected from selected treatments to determine changes in frequencies of the G143A at CytB and Y136F at Cyp51 mutations in response to fungicide application.

Variety trial

The variety trial at Malinong was sown on 9 May 2023 and compared six wheat varieties: Valiant (VS), Scepter (SVS), Mace (MSS), Grenade CL Plus (MS), Calibre (S) and Brumby (R). Three fungicide strategies were applied to Valiant, Scepter, Mace and Grenade CL Plus. Fungicide strategy 1 was only applied to Calibre and Brumby. Depending on the strategy the fungicide treatments were applied on the following dates: GS32 on 17 July, GS41 on 21 August and GS55 on 20 September 2023.

• Strategy 1 = Epoxiconazole 125^h @ 500mL/ha GS32
• Strategy 2 = Epoxiconazole 125^h @ 500mL/ha GS32 fb Maxentis^® @ 600mL/ha GS41
• Strategy 3 = Epoxiconazole 125^h @ 500mL/ha GS32 + Vivando^k @ 300mL/ha fb Maxentis @ 600 mL/ha + Vivando @ 300mL/ha GS41 fb mildewcide at GS55

^hEpoxiconazole 125 label rate for powdery mildew is 250mL/ha, 500mL/ha is maximum label rate for wheat for control of leaf rust, stripe rust and Septoria nodorum blotch. It has been applied standalone in this trial for research and demonstration purposes.

^kVivando applied under APVMA permit PER93198. This permit states to apply at or before BBCH31 and reapply 21–28 days after the first application and no later than BBCH61.

Wheat powdery mildew and Septoria assessments were conducted as outlined in the fungicide efficacy trial above.

Both trials were harvested for grain yield on 21 December.

Results and discussion

Wheat powdery mildew fungicide resistance survey

The mutation frequency for Y136F at Cyp51 is a gateway mutation that indicates reduced sensitivity to group 3 fungicides. It does not infer that the DMI fungicides will be ineffective, but the pathogen may be less sensitive. From the paddock survey of 145 samples collected in 2022 from the Eyre Peninsula, SA Mallee, Upper Southeast and Victoria, the incidence of this mutation averaged 98.6% (data not shown). This shows the Y136F mutation is near saturation within the WPM population. The survey results also revealed there is little geographical trend in the Y136F mutation frequency. For example, the minimum mutation frequency value of 57% was sampled at a site near Nundroo. However, a paddock approximately 14km away had a value of 98%.

Mutation frequency for G143A at CytB confers resistance to group 11 QoI fungicides such as azoxystrobin. For the samples collected in 2022, there was a geographical trend for the mutation to increase in frequency from the west to the east (Figure 1). The highest values were sampled in higher rainfall areas in Victoria (mean 64%, range 23–100%), which also corresponds with where detections of the G143A mutation were first discovered in Australia in 2016. Surprisingly, the mutation was detected at moderate frequencies in the SA Mallee (mean 18%, range 0–43%), where use of strobilurin fungicides has historically been low, which suggests that the resistance has not developed locally in the Mallee but moved there over time from an area with the resistance mutation. The Upper SE also had moderate to high mutation frequencies (mean 26%, range 0–71%). Mutation frequency was lower on the EP (mean 3.4%, range 0–50%), indicating that the strobilurins may still provide useful activity in many paddocks in that region. However, the mutation is still present in 6% of paddocks sampled on the EP at moderate levels. This will increase with strobilurin use. Despite the overall trend of declining resistance mutation from east to west, higher levels of resistance were detected in the northern YP region in 2021 (mean 33%, range 2–90%). This may be due to the high levels of WPM present on the northern YP over the last 5-10 years resulting in greater selection for the resistant mutation.

Figure 1. Frequency of wheat powdery mildew G143A mutation at CytB for survey paddocks sampled 2022 (circles) and 2021 (triangles).

Field trials – wheat powdery mildew fungicide resistance and post-emergent fungicide performance

Mutation frequency for Y136F at Cyp51 was high at all survey locations in 2022 averaging 99% (data not presented). Data presented in Table 1 shows the application of any standalone DMI fungicide did not reduce WPM infection compared to the control. However, it is important to note that tebuconazole and Proviso® (prothioconazole) are not registered for control of WPM when applied alone. When the three DMI fungicides tebuconazole, prothioconazole and Opus® (epoxiconazole) were combined, a 60% reduction in WPM was achieved at the early assessment. However, control is below expectation for such a robust treatment.

Septoria tritici blotch impacted the trial site, with some treatments providing better control than others. Within the standalone DMI treatments, greater levels of Septoria control were generally related to higher WPM pustule counts and this needs to be considered when interpreting results.

The group 11 QoI fungicides did not reduce WPM infection compared to the control (Table 1). Azoxystrobin applied alone is not registered in wheat but has been included in this trial as a demonstration and provided no control of WPM. Where azoxystrobin was applied in combination with a DMI active (Amistar® Xtra, Tazer® Xpert and Maxentis®), no additional control of WPM was achieved compared to where the DMI mix partner was applied alone. The fungicide Opera® contains the QoI fungicide pyraclostrobin (plus the DMI epoxiconazole) and similar to the dual active products containing azoxystrobin, this product provided no control of WPM at Malinong in 2023.

The group 7 SDHI fungicides are the only other registered fungicide group for WPM control in wheat. In this trial, Aviator® Xpro® was applied at maximum label rate. As observed in previous trials, the SDHI component in Aviator Xpro, bixafen, provided no additional control compared to the DMI mix partner prothioconazole (Trengove et al. 2022).

Table 1: Wheat powdery mildew (pustule number), Septoria tritici blotch (% Flag-1 % infection) and grain yield of ScepterA wheat in the fungicide efficacy trial at Malinong, SA, 2023. WPM data has been transformed for analysis, fungicide treatments sharing the same letter within a column are statistically similar.

^cAzoxystrobin (Mirador® 625) is registered in wheat only when mixed with a DMI mix partner. It has been applied standalone in this trial for research and demonstration purposes.

^gTebuconazole applied alone is not registered for the control of wheat powdery mildew. It has been applied standalone in this trial for research and demonstration purposes.

^hOpus (Epoxiconazole 125) label rate for powdery mildew is 250mL/ha, 500mL/ha is maximum label rate for wheat for control of leaf rust, stripe rust and Septoria nodorum blotch. It has been applied standalone in this trial for research and demonstration purposes.

^fProviso (prothioconazole) is not registered in wheat when applied stand alone. It has been applied standalone in this trial for research and demonstration purposes.

^jTalendo applied under APVMA permit PER93216.

^ILegend applied under APVMA permit PER93197.

^mOpera label rate for powdery mildew is 500mL/ha, 1000mL/ha is maximum label rate for wheat for control of leaf rust. It has been applied standalone in this trial for research and demonstration purposes.

As a result of the dry spring, WPM infection reduced significantly after the last assessment and grain yield results were mostly unaffected by the presence of WPM (Figure 2). Grain yields ranged from 5.1–6.3t/ha, with Septoria being the largest contributor to grain yield loss. This highlights the importance of managing all diseases present and is the reason mildewcide products should always be applied with a robust fungicide package to target other diseases.

Figure 2. The impact of WPM (left, y = 0.0122x + 5.7841, R² = 0.0282) and Septoria tritici blotch (right, y = -0.014x + 6.165, R² = 0.6775) on grain yield. Diseases were assessed on 20 September at Malinong SA in 2023.

Response to single season selection pressure in group 11 resistance

Mutation frequency for G143A at CytB ranged from 1.2% to 24% in the control across four trial sites in 2022 (Table 2). The results also show treatments containing the group 11 fungicide azoxystrobin generally increased this frequency across the sites. This is expected, where the continual use of group 11 QoI fungicides maintains selection pressure on the population. This finding is also consistent with previous results from Bute in 2021, where treatments including azoxystrobin increased mutation frequency from 19% to 49% (Trengove et al. 2022).

Table 2: Frequency of G143A mutation at CytB (conferring resistance to group 11 QoI fungicides) in four fungicide trials, 2022. Letters denote treatments that are significantly different with the same column.

^cAzoxystrobin (Mirador® 625) is registered in wheat only when mixed with a DMI mix partner. It has been applied standalone in these trials for research and demonstration purposes.

^gTebuconazole applied alone is not registered for the control of wheat powdery mildew. It has been applied standalone in these trials for research and demonstration purposes.

Samples collected from selected treatments in 2023 are being analysed and are expected to show a similar increase to the other sites where group 11 fungicides have been applied.

Mildewcides - permits and summary of trial performance

The APVMA has issued permits for three fungicides for the control of powdery mildew in wheat. Legend and other registered products with 250g/L quinoxyfen (group 13, PER93197), Talendo (group 13, PER93216) and Vivando® (group U8, PER93198) are currently able to be used for WPM control until 31 July 2024. These products represent two fungicide modes of action not previously registered for use in wheat in Australia.

Critical use comments that are common to all three of these permits include:

• Apply as a protectant only
• Do not apply more than 2 applications per crop
• Apply in accordance with the current CropLife Fungicide Resistance Management Strategy.

Critical use comments specific to each permitted fungicide are detailed in Table 3.

Table 3: Critical comments for permitted products Legend (PER93197), Talendo (PER93216) and Vivando (PER93198) for control of powdery mildew in wheat.

The products Legend and Talendo were included in the product efficacy trial at Malinong in 2023 and provided high levels of WPM control where other products failed. Vivando was included in the variety trial at Malinong and provided excellent control in SVS or better varieties. These results are consistent with previous trials where these products were applied prior to WPM establishing in the canopy. Performance of the permitted products varied across six trials, with timing of application relative to disease build up considered a very important factor in performance (Table 4).

Mildewcide permit product performance was lower when the WPM was established prior to fungicide application. This occurred at Bute in 2020 and at Malinong in 2022 (Table 4). Wheat powdery mildew was first detected at GS14 at Bute in 2020 and was already at moderate levels before fungicide application at GS32. Moderate control was achieved in this instance. Similarly, at Malinong in 2022, WPM infection was well established in the trial prior to fungicide application at GS39, in this case no effective control was achieved with these products.

The mildewcide products performed well at Bute in 2021 and 2022, all but eliminating the WPM infection (Table 4). This is similar to the control achieved at Malinong in 2023. In these four trials, the WPM infection did not develop until after the first fungicide application. This highlights the importance of using these permitted mildewcide products as protectants only.

Table 4: Performance of permitted products against WPM in trials at Bute and Malinong on wheat varieties rated SVS, letters denote significant differences within a column.

Varietal resistance to wheat powdery mildew

A number of wheat varieties performed similarly at Malinong, despite their variation in WPM resistance ranking. This is in contrast to previous seasons where WPM infection has generally followed the resistance ratings closely, with MS performing better than MSS which performed better than SVS (Trengove et al. 2021, Trengove et al. 2022, Trengove et al. 2023). At Malinong in 2023, the VS variety Valiant had the highest WPM infection. Both Mace (MSS) and Grenade CL Plus (MS) did not perform any better than the SVS variety Scepter (Figure 3). Anecdotal reports from growers and consultants in the area also observed this in paddocks. There has potentially been some breakdown of resistance or local pathotypes that are more virulent on those varieties. However, more research in the area is required to understand this further.

The newer variety Calibre, rated S, has consistently performed better than the rating suggests. In all previous trials at Bute, it has performed similarly to Mace or Grenade CL Plus. In this season, it has outperformed those two varieties significantly, with minimal WPM infection following a single application of epoxiconazole, which failed to control WPM in the adjacent product efficacy trial. The levels of WPM infection on Calibre over the last three seasons indicate that the S rating is not appropriate for this variety.

Brumby was released with an R rating and, prior to 2023, was generally performing at that level. The rating in the 2024 South Australian crop sowing guide has been revised to R/S, to indicate an S rating to a rarer strain of WPM which is likely present at the Malinong site. In the 2023 Malinong trial, Brumby performed similarly to Calibre and there were several reports of WPM infection in Brumby at low levels around the area and on the Yorke Peninsula.

The variety Valiant, rated VS, had the highest level of WPM infection under all three fungicide strategies. This includes Strategy 3 which received two applications (prior to WPM assessment) of the mildewcide Vivando and was only able to reduce the pustule number to the level observed in Strategy 1 and 2 for Scepter, Mace and Grenade CL Plus. Vivando was able to provide high levels of WPM control in Scepter, Mace and Grenade CL Plus (Figure 3). These results highlight the pressure VS varieties are putting on fungicides and fungicide resistance development. Varieties rated VS should be avoided in areas where WPM is a concern.

Figure 3. Wheat powdery mildew infection (21 August 2023) and grain yield for Malinong variety × fungicide trial, lower- and upper-case letters denote significant differences P<0.005 for WPM infection and grain yield respectively. Fungicide strategies are described in the methodology.

Acknowledgements

The research undertaken as part of this project is made possible by the significant contributions of growers through both trial cooperation and the support of the GRDC, the author would like to thank them for their continued support. PER93197, PER93216 and PER93198 are a result of SAGIT and GRDC investments, field studies and regulatory, and the support of Grain Producers Australia (GPA) as the permit holder. The research input during this project from Nick Poole, Ben Morris and Tara Garrard is gratefully acknowledged.

References

Trengove S, Sherriff S, Bruce J, Lopez Ruiz F (2021) Management of powdery mildew on fungicide resistant wheat. 2021 GRDC Adelaide Grains Research Update.

Trengove S, Sherriff S, Bruce J, Lopez Ruiz F, Dodhia K (2022) Fungicide resistant wheat powdery mildew – management and resistance testing. 2022 GRDC Online Grains Research Update.

Trengove S, Sherriff S, Bruce J, Lopez Ruiz F, Dodhia K, Poole N, Morris B (2023) Fungicide resistant wheat powdery mildew – update on management and resistance testing. 2023 GRDC Bendigo Grains Research Update.

Contact details

Sam Trengove
Trengove Consulting
Bute SA 5560
samtrenny34@hotmail.com