Best management practice for fungicides in the face of resistance

Fungicide resistance – an emerging issue

Unfortunately Australian growers and advisers have become all too familiar with the terminology surrounding herbicide resistance.  In contrast, our knowledge of fungicide resistance is in its ‘infancy’ with the vast majority of growers in the eastern states having little knowledge of how this issue could impact them. In other parts of the world, such as Europe, pathogen resistance to fungicides such as triazoles, strobilurins and SDHIs (succinate dehydrogenase inhibitors) is well recognised, principally as a result of more intensive usage of these agrichemicals. Some of the most problematic cereal pathogens (with regard to resistance issues) are the same diseases that have had a higher profile here in Australia over the last five years: powdery mildew (PM) Blumeria graminis f. sp. hordei in barley, Septoria tritici blotch (STB) caused by the pathogen Zymoseptoria tritici and net form of net blotch (NFNB)—Pyrenophora teres f. teres and spot form of net blotch (SFNB)—Pyrenophora teres f. maculata. In the last two seasons early stage mutations associated with triazole insensitivity (shift whereby the pathogen is less sensitive (more resistant) to the triazole) have been found in the Pyrenophora teres (NFNB) population in Western Australia (WA) and in the Zymoseptoria tritici (STB) population in the eastern states. 

The problems with powdery mildew populations in barley showing triazole insensitivity is well established in WA but now some of the more serious and aggressive mutations have also been found in Victoria. Ninety-eight per cent of the PM samples analysed from a trial site in the southern Victorian high rainfall zone (HRZ) harboured the S509T problematic mutation. This mutation has increased in importance in WA since 2009 and has been associated with more extreme triazole insensitivity that has resulted in poor disease control in the field. 

Will these pathogen mutations influence the field performance of triazole fungicides in the field?

Although reduced field efficacy against powdery mildew with older triazoles, such as tebuconazole (e.g. Folicur®) is recognised in WA this has not been experienced in the eastern states at present. One of the principal reasons for this is that cultivars grown in the eastern states are more resistant to powdery mildew and therefore the mildew population in the eastern states has not been exposed to the same selection pressure since growers are not spraying fungicides for mildew in barley. However, we now know that the same resistant mutations associated with poorer field efficacy are present in the east, and at some stage the frequency and severity of these fungicide mutations could impact on triazole field performance, particularly if the disease became more prominent. With triazoles the shift in pathogen sensitivity is likely to be a gradual process taking years to develop. In effect it is an incomplete form of resistance that develops over time. Strobilurins and SDHIs have developed resistance far quicker as these modes of action are at higher risk of resistance development in the pathogen. With these fungicides, resistance in the pathogen can result from single mutations which potentially influence field performance more quickly; in effect the pathogen can become completely resistant to the fungicide in the field. Since we don’t as yet have known cereal crop pathogen resistance to strobilurins and SDHIs and initial shifts in triazole sensitivity are in their infancy it gives industry the opportunity to review fungicide strategies and use patterns to ensure that we are not using them any more than we need. Now is an excellent stage in the season to ensure that they are used as part of an integrated disease management (IDM) programme where other control measures such as genetic resistance, agronomic and cultural control measures are fully considered.

What can growers do to protect fungicides from the development of resistance?

The more we use fungicides on pathogens that are at a high risk of resistance development, the more likely we are to select for fungicide resistance. The first measure we can consider is a disease management strategy on farm that is based on an integrated disease management (IDM) approach to controlling disease, which makes use of all the tools available to control the disease, not just the fungicides.
 

Integrated disease management

These IDM measures look to reduce disease inoculum before fungicide application is considered. Measures include: 

  • Reducing the intensity of the susceptible crop in the rotation.  For example, increased areas of cereals in the rotation would give rise to increased areas of infected stubbles of diseases such as net blotch, STB, and yellow leaf spot, particularly where cultivars are susceptible to these diseases
  • Using more resistant cultivars, particularly for the early sowings where the crop can be subject to greater infection pressure from stubble borne diseases
  • Reducing disease inoculum by reducing stubble on the surface (burning, grazing, stubble incorporation)
  • Later sowing of cultivars (where they are adapted) that are susceptible to stubble borne diseases such as net blotch, scald, yellow leaf spot and STB
  • Using clean seed sources for stubble borne and seed borne diseases, such as NFNB, which can also be transmitted on the seed
  • Where excess growth from earlier planting allows grazing pre-GS30 it will reduce disease inoculum, although the impact of lax grazing is much less effective than hard grazing.

Many of these tools have to be balanced against other factors such as loss of yield potential with later sowing or soil erosion with stubble management measures. Where the primary inoculum from stubble is windblown over large distances with diseases such as STB, infection can spread from neighbouring paddocks even if some form of stubble management has been practiced in a particular paddock. This is much less the case with yellow leaf spot where initial infection from the stubble is much more local to the paddock itself and wheat on wheat scenarios. 

Anti-resistance measures when using fungicides

Clearly the best way to avoid fungicide resistance is not to use fungicides. However, in an integrated disease management (IDM) approach, when a cultivar’s genetic resistance breaks down or is incomplete, it is imperative that growers and advisers have access to a diverse range of fungicides (in terms of mode of action) for controlling the disease. The main anti-resistance measures in cereal crops that growers can adopt when using fungicides are:

  • To minimise the number of fungicide applications using the same mode of action
  • Avoid repeat applications of the same product and mode of action in the same crop and or year after year, particularly when using strobilurins and SDHIs alone such as the seed treatment fluxapyroxad (Systiva®)
  • Ideally apply no more than one strobilurin or one SDHI in the course of a growing season (the current limit for registered foliar products is two applications of each mode of action in a season)
  • Always mix foliar applications strobilurins or SDHIs with a triazole fungicide (in Australia most of these fungicides products come already formulated with a triazole) using an appropriate rate for both products
  • For most scenarios in Australia, with the exception of Tasmania, two broad spectrum fungicide inputs should be regarded as a maximum in order to control the vast majority of disease outbreaks in susceptible cultivars, with most crops requiring none or one application
  • Although not strictly an anti-resistance strategy in many cases, since all triazoles have the same mode of action, there is emerging evidence to suggest that mutations associated with triazole resistance may be conferring negative cross resistance to other triazoles. This is the case for barley powdery mildew tebuconazole resistant strains and the triazole seed treatment fluquinconazole
  • With SDHI seed treatments that have activity on foliar diseases later in the spring, such as fluxapyroxad (Systiva®), consider foliar fungicide follow ups which have a different mode of action and avoid repeat usage of Systiva® alone in successive years.

Influence of fungicide rate

The vast majority of scientific studies suggest that there is no connection between lower fungicide rates (below label rate) and increased fungicide resistance. In fact, studies suggest the opposite; that increased fungicide rates select for resistance more quickly. Clearly growers and advisers want to control the disease and maximise returns at the minimum cost when they use a fungicide, and fungicide rate is a key efficacy factor, but rates lower than label are not a key factor in the development of fungicide resistance. 

A review of papers studying fungicide resistance (Table 1) clearly indicated that an increased number of sprays, splitting the dose (effectively reducing the rate and increasing the number of sprays) or increasing the dose had the greatest effects in terms of increasing selection for resistance, whilst adding a mix partner of a different mode of action had the greatest impact in terms of decreasing selection pressure. 
 
Table 1: Consequences for resistance (number of studies resulting in increased or decreased resistance risk). (Source: Frank van den Bosch, Annual Review of Phytopathology, 2014)
  Increase selection (resistance) No effect Decrease selection (resistance)
Increase dose 16 1 2
Increase no. of sprays 6 0 0
Split the dose 10 0 1
Add a mix partner 1 6 46

Research into new fungicide active ingredients 

Over the last four years GRDC has not only recognised the need to benchmark the sensitivity of our common pathogens against available fungicide products, but also the need to encourage the registration of new active ingredients for the Australian market. The GRDC New Fungicide Actives project lead by Curtin University (Project CUR00019 and the new bilateral between Curtin/GRDC Program 9) has been working with different target diseases in cereals to generate efficacy data that, combined with manufacturers’ data, might lead to the registration of new fungicides with new modes of action. These research projects are beginning to assist with new product registrations that have good activity on important diseases such as powdery mildew, yellow leaf spot, net blotch, and STB. FAR Australia who has been leading the field research has already identified a number of new fungicide candidates, which are at various stages of development and registration. Though the work has been conducted on a wide range of diseases the results presented here represent just some of the results achieved to date against net blotch, yellow leaf spot, and STB. To recognise commercial sensitivities, where products have not been registered they have been given a treatment number of 1. 

New products for the control of NFNB and SFNB

In barley there are a number of new fungicide products that offer a higher level of NFNB, SFNB, and scald control than the existing standards such as propiconazole (e.g. Tilt®). These new actives take the form of both seed treatments and foliar fungicides. The introduction of the SDHI fluxapyroxad as the seed treatment Systiva® from BASF looks set to be a major step forward (Figure 1 and 2). Previous seed treatments have given partial control of NFNB through controlling infection on the seed, but have lacked systemic activity to give foliar disease control. Systiva® potentially changes the management strategies for controlling NFNB, SFNB, and Scald in susceptible cultivars and situations since this new SDHI has good persistence on foliar diseases. In results from CUR 00019 fungicide activity is evident up to the point that the second fungicide is traditionally applied to barley at awn emergence (GS49) and on occasions through to ear emergence. As such the product has the ability to replace the first fungicide timing which has traditionally been applied at early stem elongation (GS30-31). Where disease pressure dissipates in the second half of the season, due to lack of rainfall and lower crop canopy humidity, there may be no need for a follow up with a foliar fungicide. In addition to Systiva there are new foliar SDHIs which mixed with other fungicide modes of action have good activity on the same stubble borne diseases in barley. Activity of Systiva® seed treatment has also been good on scald - Rhynchosporium secalis. In recent work conducted by the Hart Field site group in South Australia there was a significant reduction in the number of large foci when assessed 121 days after sowing with the use of Systiva® (Table 1).

Bixafen, a SDHI from Bayer CropScience which has been extensively tested under the Curtin University/FAR Australia collaboration, is an example of a SDHI mixed with the triazole prothioconazole (a component of Prosaro®) and is currently undergoing registration in Australia. Figure 1 shows the SFNB control given by this product (proposed trade name Aviator®XPro) applied as two foliar sprays versus two sprays of Tilt®.

Figure 1: Spot form net blotch (SFNB) control using the new SDHIs Fluxopyroxad (Systiva® seed treatment) and the new SDHI foliar fungicide active bixafen mixed with prothioconazole (Aviator Xpro 225EC®) compared to propiconazole applied as a foliar two spray programme in barley (cv. HindmarshA). Meckering WA, 2013.

Figure 1: Spot form net blotch (SFNB) control using the new SDHIs Fluxopyroxad (Systiva® seed treatment) and the new SDHI foliar fungicide active bixafen mixed with prothioconazole (Aviator Xpro 225EC®) compared to propiconazole applied as a foliar two spray programme in barley (cv. Hindmarsh). Meckering WA, 2013.

Yield performance and screenings in these trials correlated with disease control assessments (Figure 2), indicating that products containing new active ingredients offer us new and potentially alternative management tools for barley disease control.

Figure 2: Influence of Spot form of net blotch (SFNB) control on barley yield and quality (cv. HindmarshA). Meckering WA, 2013

Figure 2: Influence of Spot form of net blotch (SFNB) control on barley yield and quality (cv. Hindmarsh). Meckering WA, 2013.
Notes: Tilt 500ml/ha and Aviator®Xpro 300ml/ha (currently undergoing registration & is not commercially available) were applied as foliar sprays twice at GS31 & GS49. Systiva® was applied as a seed treatment alone and was not followed up with a later foliar fungicide. 

Table 2: Per cent scald infection, assessed 25th September. Hart SA (v. Charger sown 27 May).
Treatments
Incidence of scald on leaf layer Hotspot Incidence

Flag
Flag-1
Flag-2
Large Small
1 Nil 20.0 a 40.0 a 33.3 a 4.3 a 0.3 a
2 Systiva® @ 150mL/100kg 3.3 b 36.7 a 23.3 a 0.3 b 1.0 a
5 Tilt 0.5 L/ha @ GS31 + GS49 0.0 b 13.3 a 13.3 a 0.3 b 1.3 a
8 Prosaro® 150 mL/ha @ GS31 + GS49 0.0 b 6.7 a 40.00 a 0.7 b 1.3 a

Mean 5.8
24.2
27.5
1.4
1.0

LSD 10.0
38.1
38.3
2.8
2.5

P Val 0.008
ns
ns
0.031
ns
Data supplied courtesy of the Hart Field Site Group in SA
Large hotspot >10 infected leaves, small hotspot < 10 infected leaves

Adjustments to barley management strategies

The introduction of the fluxapyroxad active as the seed treatment Systiva® provides not only a new fungicide option but an opportunity to have an alternative fungicide strategy to a two spray foliar fungicide approach for susceptible cultivars or high risk rotation positions, such as barley on barley. The use of Systiva® in combination with foliar fungicides is likely to depend on the regional environment and rotation position, disease pressure, and length of growing season. 

Lower rainfall – shorter season environments

In shorter season environments with lower yield potential such as the Wimmera where disease pressure is reduced at later growth stages by warmer and drier conditions Systiva® is likely to be sufficient to give season long disease control where net blotch is the key disease. Under these circumstances whilst the products persistence will have dissipated by ear emergence environmental conditions generally make follow up fungicides far less necessary.

Fungicide resistance risk with SDHIs

SDHIs are at moderate to high risk of fungicide resistance, ensure that they are not over used particularly as a seed treatment with no follow up foliar fungicide of a different mode of action.

Higher rainfall – longer season environments

In longer season scenarios of the HRZ cooler temperatures and higher rainfall later in the spring they typically create greater disease pressure later in the season and a need for greater fungicide persistence. In these scenarios Systiva® seed treatment would need to have a follow up foliar fungicide at awn emergence (GS49) in susceptible cultivars and rotation positions. In addition, in the HRZ, other diseases such as barley leaf rust can become more problematic in the second half of season, and whilst Systiva® has activity it is not as effective against this disease. In these environments a follow up foliar fungicide should also be considered as an important resistance management tool to ensure the value of Systiva® is maintained.

New fungicide performance in wheat

New fungicide active ingredients such as the SDHIs will also have an impact on disease control in wheat as new fungicides become available, particularly against stubble borne diseases such as yellow leaf spot and STB. The foliar fungicide mixture of bixafen and prothioconazole (proposed to be called Aviator®Xpro ɸ) has performed well in trials against both yellow leaf spot and STB (Figure 3a and 3b, 4a and 4b) in the GRDC funded New Actives field trials (CUR00019) lead by FAR. The data illustrates that a number of fungicide products applied in two spray programmes have given superior disease control to tebuconazole applied at the same timings. Although not named at this stage the data shows a number of fungicides that are performing strongly against yellow leaf spot and STB. 

ɸ Currently undergoing registration

Figure 3a and b: Per cent yellow leaf spot infection on flag-1 28 days after two spray programmes of 14 different foliar fungicides and subsequent yield response. (cv. ScoutA) Yorke WA, 2013
Figure 3a and b: Per cent yellow leaf spot infection on flag-1 28 days after two spray programmes of 14 different foliar fungicides and subsequent yield response. (cv. Scout) Yorke WA, 2013

With dry finishes in southern Victoria yield responses to STB control has been variable (and are not presented) however there have been clear indications that a number of new fungicides show good promise for controlling STB, including products such as epoxiconazole (Opus®) which though registered for disease control in wheat has no label claim for STB control currently.

Figure 4a and b: Per cent STB infection on flag-2 26 and 27 days after two spray programmes of 14 different foliar fungicides and subsequent yield response. Westmere VIC, 2013 (cv. EspadaA) and Inverleigh VIC, 2014 (cv. Revenue A).

Figure 4a and b: Per cent STB infection on flag-2 26 and 27 days after two spray programmes of 14 different foliar fungicides; and subsequent yield response. Westmere VIC, 2013 (cv. Espada) and Inverleigh VIC, 2014 (cv. Revenue). 

Genetic resistance – APR genes are a key element of an IDM approach for stripe rust control

A key element of an integrated Disease Management approach is harnessing the value of genetic resistance. A GRDC funded project (FAR 00002) has been examining the value of Adult Plant Resistance (APR) genes for rust control when using newer generation fungicides, such as strobilurins and SDHIs. The work conducted under the Australian Cereal Rust Control Programme (ACRCP) by FAR Australia and Sydney University at Cobbitty has indicated that Adult Plant Resistance (APR) genes both reduce the need for a second fungicide and gives greater flexibility in the timing of a single foliar fungicide. The research work which has compared fungicide programmes on commercial cultivars known to contain either one or two specific APR genes Yr18 and Yr29 has not been able to show significant advantages to newer generation fungicides over the triazole epoxiconazole.

With the wheat cultivar Corack (rated MS for stripe rust) protected by Yr29, despite higher levels of stripe rust earlier in the season, the early fungicide at GS31 gave good protection of the lower canopy (Flag-3 and Flag-2) but did not prevent reinfection of the upper canopy (Flag and Flag-1). The lack of sufficient control in the upper canopy had a greater yield impact than the disease control achieved in the lower canopy, as a result a single flag leaf spray tended to be more effective than an early GS31 spray. However, to effectively control disease and maximise yield both GS31 and GS39 sprays were required (Figure 5). 

Elmore CL Plus has greater resistance to stripe rust (rated MS-MR) and is protected by both Yr18 and Yr29. In this case there was less difference in yield between the GS31 and GS39 fungicide applications since later in the season the upper leaves of Elmore CL Plus appeared more able to protect themselves with the inherent genetic defence conferred by the APR genes. The consequence of this was that Elmore CL Plus showed less response to two fungicides over one and no significant yield differences between a single GS31 and GS39 fungicide timing (Figure 6). 

Figure 5: Influence of fungicide product and timing on grain yield (t/ha) of CorackA under irrigation.  Cobbitty NSW, 2014

Figure 5: Influence of fungicide product and timing on grain yield (t/ha) of Corack under irrigation. Cobbitty NSW, 2014.
Opus - Epz – epoxiconazole 
Radial - Epz + Az – epoxiconazole + azoxystrobin 
F1/14 (experimental fungicide containing a SDHI)
Folicur - Tbz- Tebuconazole 

Figure 6: Influence of fungicide product and timing on grain yield (t/ha) of Elmore CL PlusA under irrigation. Cobbitty NSW, 2014.

Figure 6: Influence of fungicide product and timing on grain yield (t/ha) of Elmore CL Plus under irrigation. Cobbitty NSW, 2014.

Conclusion 

New GRDC research being conducted on integrated disease management and new fungicides in conjunction with the agrichemical manufacturers shows great promise that will result in better disease management in Australian cereal and pulse crops. However, new products with new modes of action are not immune from resistance development, therefore to prolong their activity and that of our existing triazole products we need to use them judiciously and in combination with other control options. 
  
Please note that reference to an agrichemical fungicide in this paper does not constitute a recommendation or that the active ingredient or product referenced carries an approval for control of a specific disease.

Acknowledgements

The research presented in this paper has been made possible by the significant contributions of growers through both trial cooperation and the support of the GRDC, the authors would like to thank them for their continued support.

Contact details 

Nick Poole
23 High St, Inverleigh, VIC 
03 5265 1290

GRDC Project Code: CUR00019, CCDM/GRDC Program 9 and FAR00002,