Fungicide Insensitivity in Pulse Crops

Jennifer Bogdan, PAg, CCA

Fungicides have become an essential tool for growing high yielding, top-quality pulse crops in Saskatchewan. However, with increased fungicide use year after year, resistance (insensitivity) within some of the main pulse crop diseases has begun to emerge. Awareness of potential insensitivity issues, in-depth understanding of fungicide groups, proper fungicide use and rotation, and integrated disease management strategies are required in order to delay further development of fungicide insensitivity.

What is Fungicide Insensitivity?

Fungicide insensitivity (resistance) refers to the reduced sensitivity of a pathogen (fungus) to a specific fungicide. This insensitivity is a heritable trait that is passed on to new generations from the few original pathogens that are naturally insensitive within the fungal population (Figure 1).

Pathologists often use the term insensitivity to refer to the resistance of a pathogen to a fungicide. The term resistance is typically reserved to describe the resistance of a host plant to a particular pathogen. In short, insensitivity refers to a pathogen, whereas resistance refers to a plant.

Fungicide Insensitivity in Saskatchewan

Fungicide insensitivity has been reported for Ascochyta blight in chickpeas in Saskatchewan, as well as in North Dakota and Montana. The first report of Group 11 (QoI, strobilurin) insensitive Ascochyta rabiei was in 2003 as part of a baseline study that tested 106 isolates, of which 88 were from Saskatchewan (Gossen and Anderson 2004). One of the Saskatchewan isolates showed cross resistance to both azoxystrobin and pyraclostrobin. A few years later, BASF confirmed Group 11 insensitive A. rabiei in several chickpea fields in southwest Saskatchewan from samples collected in 2006. By this time, it was apparent that a large shift in sensitivity of the A. rabiei population had occurred. In a recent survey of commercial chickpea fields in southern Saskatchewan in 2019, A. rabiei was detected in 33 fields. Group 11 insensitive A. rabiei was present in all 33 (100%) of these fields. Only 8 (24%) of the 33 fields additionally contained Group 11 sensitive (susceptible) A. rabiei (Hubbard 2019).

Ascochyta rabiei isolates have also been tested for sensitivity to chlorothalonil (Group M5) and mancozeb (Group M3), along with pyraclostrobin (Group 11), in a lab setting (Chang et al. 2007). A total of 66 isolates were collected from chickpea fields in southern Alberta in 2003 and 2004. The overall results found 35% of the isolates to be insensitive to chlorothalonil, 53% insensitive to mancozeb, and 24% insensitive to pyraclostrobin.

Some isolates were also found to be insensitive to multiple fungicides: four isolates (6%) were insensitive to all three fungicides, seven isolates (11%) were insensitive to chlorothalonil and mancozeb, three isolates (approximately 5%) were insensitive to chlorothalonil and pyraclostrobin, and seven isolates (11%) were insensitive to mancozeb and pyraclostrobin. This study suggests insensitivity to the Group M fungicides could exist in a lab, depending on the methods used, although this issue has not been reported in the field.

In 2019, BASF collected Anthracnose isolates from targeted (not random), heavily diseased lentil fields in Saskatchewan. Samples came back showing insensitivity to Group 11. The mutation found (G143A) confers cross resistance to all Group 11 chemistries. Survey work is being done in 2020 by a larger industry task force to gain a better understanding of the extent and severity of Group 11 Anthracnose insensitivity.

Researchers in Alberta have studied the sensitivity of Mycosphaerella pinodes in peas to pyraclostrobin (Bowness et al. 2016). In order to develop a baseline sensitivity, they tested 70 unique M. pinodes isolates (40 from Agriculture and Agri-Food Canada in Saskatoon and 30 from the United States Department of Agriculture in Washington). The isolates were all collected prior to 2003, before Group 11 fungicides were registered for use in these areas and so had never been exposed to this fungicide group previously. All 70 isolates were sensitive (susceptible) to pyraclostrobin, thus establishing a true baseline of sensitivity that can be used to monitor future changes in the Mycosphaerella population. The researchers then tested 324 M. pinodes isolates collected from pea fields in Alberta, Saskatchewan, North Dakota, and Washington State in 2010 and 2011. In total, 19 isolates (6%) were insensitive to pyraclostrobin: nine from central Alberta, five from northern Alberta, and five from central and southern Saskatchewan. These results should serve as a warning for industry and growers to ensure the proper use of Group 11, incorporate other disease management strategies, and to continuously monitor the effectiveness of fungicide chemistries.

Fungicide Insensitivity Risk

The risk of developing fungicide insensitivity depends on three main factors: pathogen risk, fungicide risk, and agronomic factors.

1. Pathogen Risk
   Using scientific evidence, experience and reported insensitivity over the past 50 years, the Fungicide Resistance Action Committee (FRAC) has created a classification system for pathogens affecting the major world crop markets. The following factors, based on the biological properties of the pathogen, increase the risk of the pathogen developing insensitivity to a fungicide:
   • Polycyclic (short, multiple disease cycles per season increases the chance of repeated fungicide applications, putting more selection pressure on the pathogen and accelerating genetic changes within the pathogen population)
   • High spore production (higher chance of an insensitive mutant in the population)
   • Spores are dispersed by wind, allowing them to spread to other plants, crops, and regions
   • All crop growth stages can be infected (requires repeated fungicide applications)
   • Presence of a sexual stage in the life cycle (lower risk if asexual stage only)
   • Insensitive pathogen is as competitive as susceptible population (no fitness penalty observed)
   • Pathogen overwinters
   • Insensitivity within the pathogen population has evolved in the past after only a few years of fungicide use

Table 1 categorizes the insensitivity risk of pathogens causing disease in pulse crops in Western Canada.

Source: Fungicide Resistance Action Committee
*Note: C. truncatum that infects lentils was renamed C. lentis in 2014. C. truncatum still exists so it is important to use C. lentis when referring to Anthracnose in lentil

Botrytis cinerea, which causes grey mould, is considered to be one of the most risky pathogens in the world. It is categorized as high risk because it is polycyclic, it releases billions of windblown spores that infect numerous host plants at different growth stages, it can be found everywhere in the world, and it has become insensitive to multiple modes of action within one to two years after their introduction into the marketplace.

Ascochyta rabiei, causing Ascochyta blight in chickpeas, is the most known example of a pathogen showing fungicide insensitivity in Saskatchewan. It has wide genetic diversity, exhibits sexual reproduction, produces high amounts of wind-borne sexual ascospores, and has a polycyclic life cycle. Repeated fungicide applications (as many as 5-6 during a rainy year) are required for blight management each growing season. Within just 2-3 years, the Group 11 fungicides largely lost their effectiveness on Ascochyta blight in chickpeas in the province. However, A. rabiei is classified as medium risk for pathogen insensitivity, not high risk as might be expected. This is because globally, there are not that many reports of Ascochyta insensitivity overall. That being said, a medium risk is still cause for concern, and when a medium risk pathogen like Ascochyta is paired with a high risk fungicide group, such as Group 11, the pathogen-fungicide combination would be considered high risk.

2. Fungicide Risk
   Fungicides are classified as low, medium, or high risk for the development of insensitivity. How a fungicide is categorized is based on its chemical group, mode of action, the insensitivity type of the pathogen, and the properties of the fungicide itself.
   
   Chemical Group
   Based on decades of insensitivity monitoring, the potential for a pathogen to become insensitive to a given fungicide can be fairly accurately predicted by the chemical group to which the fungicide belongs. For example, if a new Group 11 active ingredient is developed, based on the high insensitivity risk of this group, the new active will also be considered a high risk for insensitivity.
   
   When a pathogen becomes insensitive to one fungicide and as a result, also becomes insensitive to another fungicide within the same fungicide group, it is called cross resistant. Active ingredients within the same group all act on the same target site, so when a target site mutation occurs, the pathogen is generally considered to be cross resistant across the entire fungicide group. For Group 11, cross resistance occurs between every active ingredient within the group. For example, a pathogen that is insensitive to pyraclostrobin will also be insensitive to azoxystrobin, picoxystrobin, and trifloxystrobin even if the pathogen has never been exposed to the latter active ingredients. Cross resistance is also shown between all active ingredients of Group 7 (SDHIs) and is generally accepted to occur across Group 3 (DMIs) as well.
   
   When a pathogen becomes insensitive to more than one group of fungicides (i.e. more than one target site), it is said to have multiple resistance. Several distinct mutations are required by the pathogen in order for multiple resistance to occur.
   
   Mode of Action
   Compared to herbicide and insecticide resistance, which can be due to either target site mutations or metabolic resistance, fungicide insensitivity is usually the result of an altered target site in the pathogen. Fungicides that act on a single target site, such as Group 11, have a higher risk of selecting for insensitivity because the pathogen only has to acquire one mutation to render the fungicide ineffective. In comparison, fungicides that act on multiple sites (Group M) have a low insensitivity risk because the pathogen would have to make multiple mutations in order to confer resistance, which is highly unlikely to occur in nature.
   
   Pathogen Insensitivity Type
   Fungicide insensitivity can be quantitative or qualitative. Quantitative insensitivity is controlled by multiple genes and allows the pathogen to become less sensitive to the fungicide, but using higher rates or more applications can still control the disease. Qualitative insensitivity is controlled by a single dominant gene, resulting in the pathogen being completely insensitive to the fungicide and control is no longer achievable. Group 11 and Group 7 insensitivity is typically qualitative.
   
   Fungicide Properties and Persistence
   Generally, systemic fungicides have had more insensitivity issues than contact fungicides. However, this is not always the case. Group 11 fungicides can greatly differ in their systemic abilities. For example, azoxystrobin is highly systemic while trifloxystobin is nearly non-systemic. Yet, all Group 11 actives have had insensitivity issues with various pathogens. The greatest risk for insensitivity is with fungicides that act on a single target site, and many of these products also happen to have systemic properties. Table 2 on page 5 summarizes the insensitivity risk for foliar fungicides used in pulse crops in Western Canada.
   
3. Agronomic Factors
   Of the three components contributing to fungicide insensitivity risk, the agronomic factors, which also include environmental factors, are arguably the most important. Agronomic factors will determine the disease severity in the local geographic area. Without the disease pressure, the use of fungicides would not be necessary and fungicide insensitivity risk would be non-existent.
   
   The most significant agronomic risk factor is the weather. To cause disease, three components are required: the pathogen, the host crop, and the environment. The environment is the primary driving factor causing disease in pulse crops in Saskatchewan since most pathogens are already well-established in pulse-growing areas and pulses are a consistent part of crop rotations on many farms. While the environment may be the most important factor influencing disease, it is also the one that is the least controllable. This is where using best agronomic practices as part of an integrated disease management strategy becomes critical to mitigate the effects of weather on disease development (Table 3, page 6).

Strategies for Fungicide Use

Fungicides should be applied according to a well thought-out plan, taking into account the fungicide group as well as the role the fungicides play in protection of the plant (preventative vs. curative). Preventative fungicides are best used to protect green plant tissue during the early stages of disease development. Curative fungicides can stop fungal infections that have already begun to grow inside of the plant tissue, but typically only those that occurred 24-72 hours before the application, depending on the fungicide used. Curative fungicides cannot erase a lesion or repair any cellular damage that the pathogen has already caused, and like all fungicides, they too should be applied proactively, with prevention in mind.

Source: FRAC

An important concept to understand is the minimum effective dose or critical dose rate. The minimum effective dose is the rate of active ingredient required to effectively control the target pathogen. If the fungicide is a single mode of action product, all of the control (and selection pressure) is attributed to that one mode of action. However, when working with two modes of action that act on the same disease, it is important that each individual mode of action is at a dose rate that could effectively control the pathogen on its own. If the pathogen is insensitive to one mode of action, the other component is solely responsible for the control of the pathogen. Reduced rates can contribute to a shift in the sensitivity of pathogen populations, allowing them to become less sensitive to the active ingredient because of their ability to not be shut down by a critical dose rate.

The fungicide group of most concern when it comes to pathogen insensitivity is Group 11. The insensitivity that has already been reported in common pathogens in lentils and chickpeas has come about from the repeated use of Group 11 applications within the same season, year after year, as well as the general lack of other disease management options. As such, more restrictions on the use of Group 11 and better planning around the timing of these products was needed, but simply switching to another single group, such as Group 7 or Group 3, to use repeatedly would not be sustainable either.

In an effort to curb the use of Group 11s as a solo application, manufacturers began to formulate products with multiple modes of action. The risk of Group 11 insensitivity developing is greatest when fungicides with a single Group 11 active ingredient are used. However, even applying a fungicide with multiple modes of action can eliminate Group 11 sensitive parts of the pathogen population. So while using products with multiple modes of action is a useful strategy from a preventative standpoint, it is not foolproof as fungicide insensitivity will still eventually develop.

Additional care must be taken when choosing a fungicide to use on a known Group 11 insensitive population. If a dual mode of action product containing a Group 11 is used on a Group 11 insensitive pathogen, it is the same as applying a single mode of action product on that pathogen because the Group 11 component will not be effective. In turn, this increases the selection pressure of the non-Group 11 active ingredient on the pathogen population, potentially selecting for multiple resistance. Also, each active ingredient in the multiple mode of action product must exhibit individual control of the target pathogen in order for the product to be truly effective for insensitivity management. For example, fluxapyroxad is included in dual mode of action products registered for Anthracnose in lentils. However, research conducted by North Dakota State University found that fluxapyroxad alone had no activity on Anthracnose in lentils (Wunsch 2013). As a result, any Anthracnose control from these products will come solely from the other active ingredient in the mixture, which again increases selection pressure on the other mode of action. If insensitivity to this other active ingredient already exists in the pathogen population, then Anthracnose control from these products will be very minimal. Therefore, it is important to fully understand the components of any fungicide and to recognize that the vast majority of fungicides used on pulse crops contain Group 3, Group 7, and/or Group 11 chemistries (Table 4).

A number of challenges exist with the current use of fungicides in pulse crops. Fungicide use has been increasing overall and three main fungicide groups (3, 7, and 11) are extensively used. These three modes of action are at medium to high risk of developing pathogen insensitivity. As well, there are very limited non-Group 3, 7, or 11 options for pulse crops. Therefore, proper fungicide stewardship is critical in order to extend the longevity of the main fungicides in the market, even for those classed as medium risk. Based on recommendations from FRAC and key fungicide manufacturers, specific advice for using Group 11, Group 7, and Group 3 fungicides are summarized in Table 5.

Biological Fungicides (Biofungicides)

Biofungicides offer a different, low-risk mode of action that can be used as a complement to traditional fungicides as part of an integrated fungicide program. In addition, certain biofungicides can be used in the off-season to help reduce disease inoculum before and/or after the growing season. Some biofungicides can be applied in the fall, acting on pathogens that could have developed insensitivity to the fungicides used that growing season. Incorporating biofungicides into a fungicide plan may help preserve the longevity of the higher risk fungicide groups and can offer an alternative to pathogen insensitivity that could already be occurring in the field. Table 6 summarizes the biofungicides registered for pulse crops in Western Canada.

Source: Sabine Banniza and Sherrilyn Phelps

Source: FRAC

Source: Saskatchewan Guide to Crop Protection

Key Points for Fungicide Insensitivity

• Fungicide insensitivity is already occurring in Saskatchewan pulse crops. Insensitive populations of Ascochyta blight in chickpeas,
  Anthracnose in lentils, and Mycosphaerella in peas have been documented, and it is possible that other issues exist which have not yet been reported. 
• Many of the pathogens that are routinely sprayed for each year in pulse crops are at a medium-to-high risk of becoming insensitive based on their biological characteristics.
• The three most common fungicide mode of actions used in pulse crops belong to Groups 3, 7, and 11, and are considered medium-to-high risk for insensitivity development. Fungicide insensitivity already occurs in Group 11 in multiple pathogen populations. Although Group 7 insensitivity has not yet been reported in Western Canada, it is at a higher risk of insensitivity because single gene mutations have led to insensitivity in pathogens in other parts of the world.
• Using medium-to-high risk fungicide groups on medium-to-high risk pathogens creates a higher overall risk for insensitivity to develop.
  Employ all available management practices such as Integrated Pest Management (IPM) to mediate agronomic risk factors in order to reduce the insensitivity risk of a particular fungicide-pathogen combination.
• IPM involves controlling the controllables. Incorporate longer crop rotations, select fields carefully, use disease resistant cultivars, pay attention to seed quality, and fertilize adequately.
• Make smart fungicide applications. Scout diligently, and carefully evaluate the need for a fungicide on a field by field basis. Use multiple modes of action when possible and rotate modes of action when making multiple fungicide applications. Preferably only use Group 11  products one time per season (this includes herbicide timing), or no more than two times per season if repeated applications are needed, and do not apply Group 11s alone. Use recommended rates in order to apply an effective dose and follow water volume
  recommendations. Choose correct nozzles and droplet sizes for the best application possible.
• Evaluate fungicide performance. If control is unsatisfactory, contact the appropriate agricultural representative.
• Consider incorporating biofungicides, which offer an alternative mode of action, into the overall disease management plan.

References

• Bowness, R., Gossen, B. D., Chang, K.-F., Goswani, R., Willenborg, C. J., Holtz, M., and Strelkov, S. E. 2016. Sensitivity of Mycosphaerella pinodes to pyraclostrobin fungicide. Plant Dis. 100:192-199.
• Chang, K. F., Ahmed, H. U., Hwang, S. F., Gossen, B. D., Strelkov, S. E., Blade, S. F., and Turnbull, G. D. 2007. Sensitivity of field populations of Ascochyta rabiei to chlorothalonil, mancozeb and pyraclostrobin fungicides and effect of strobilurin fungicides on the progress of ascochyta blight of chickpea. Can. J. Plant Sci. 87:937-944.
• Gossen, B.D., and Anderson, K.L. 2004. First report of resistance to strobilurin fungicides in Didymella rabiei. Can. J. Plant Pathol. 26: 411.
• Hubbard, M. 2019. Saskatchewan survey of Ascochyta blight and root rot in chickpea.
• Wunsch, M. 2013. Management of anthracnose of lentils. North Dakota State University Carrington Research Extension Center.