The definition of fungicide resistance can often get muddled up in academic arguments over wording such as shifts in sensitivity or insensitivity. However, when fungicides fail to provide the desired control, even when applied at the correct timing and rate in optimum conditions, these arguments often become irrelevant.

Of the major wet-weather cereal diseases that Irish farmers must contend with in 2019, it is difficult to think of one that does not face resistance problems to at least one of the main fungicides families used for its control. Rust diseases are the possible exception, but actions to control them can have major implications for how effective those same fungicides will be on other diseases, such as septoria. So resistance affects them too, but indirectly.

When we think of fungicide resistance today, the three big disease concerns are septoria on wheat and ramularia and net blotch on barley. However, diseases such as rhyncho on barley or eyespot on wheat or barley are not without their issues and improper control could well result in even bigger problems.

Sizing up a new era

We are on the cusp of a new era in crop protection with chlorothalonil revoked and a new wave of chemistry soon to arrive. This makes it important to reflect on where we are now in terms of fungicide resistance, how we have gotten here and what we should learn from these experiences to enhance the longevity of any new chemistries.

However, while we can see new products for the future, we must still somehow get through 2019. It is important to remember that the low disease pressure experienced in 2018 is extremely unlikely in 2019. We should also remember that weather conditions for the critical fungicide timings in winter wheat and barley and spring barley were extremely favourable. This may have given a false sense of security and it is important to remember the impact fungicide resistance can have on disease control.

Fungicides are developed to control fungi and these produce the major diseases of Irish cereal crops. Nearly all of these diseases are extremely specialised and only survive on either wheat or barley. In fact, something such as septoria is so specialised that it will only truly thrive on wheat and would now likely struggle to grow on its original grassy host.

The pressure for resistance

The sole purpose of these fungi is to survive and to pass on their DNA to the next generation. In their natural environment, they achieve this by producing vast quantities of spores, exchanging genetic information through sexual reproduction and by rapidly mutating even in the absence of sex. In doing so, they ensure that at least one of those millions of spores produced will find a susceptible host.

Ramularia control may prove challenging in the absence of a durable contact alternative to chlorothalonil.

Fast forward 40,000 years or so and the grassy plains where these diseases originated and battled to survive are now vast plains of winter wheat or barley. The disease itself has still retained the ability to readily exchange genetic information and mutate readily. However, in most instances it is no longer a battle to find a host, but to overcome the toxic environment we create on these hosts through the application of fungicides. Hence it should come as no surprise that these diseases will find a means of overcoming fungicides; they have been doing this for millennia.

Differences exist in the ability of different diseases to develop resistance. The same can be said of different fungicides. Taking the big three diseases mentioned previously, all three have a medium to high risk of developing resistance. For the fungi, the differences come down to their basic biology, such as their life cycle and ability to mutate and spread spores. The different fungicides also differ in their risk, with strobilurins being regarded as high risk and multi-sites, such as chlorothalonil, being a much lower risk.

These classifications have been confirmed by our recent past. Complete resistance is widespread in Irish septoria and ramularia populations to the strobilurins, and we have incomplete resistance in net blotch. To date, no resistance has been detected to chlorothalonil, even though it has been widely used on wheat and barley.

Azoles have weakened also

When the strobilurins failed to control septoria and ramularia, they were replaced by various azoles and then the SDHIs. The azoles are interesting, in that they are regarded as having single-site activity, yet it has taken both pathogens a considerable period of time to develop resistance. But this has now happened in our current generation of azoles.

The ability of these two fungi to develop resistance to these fungicides demonstrates their ability to adapt. In doing this, they significantly altered the target site for the azole without adversely affecting their biology. Unfortunately, strains with these changes now dominate Irish populations and, as such, the current azoles cannot be relied upon alone to provide sufficient disease control.

The development of the azole Revysol by BASF, which appears not to be affected by the changes in the current populations, shows that there is still scope to target this specific site in these diseases. Whether the diseases take as long to adapt to Revysol as they did with previous azoles remains to be seen.

SDHI issues

Resistance in the SDHIs developed much quicker. While it can be argued that Irish cereal diseases have been exposed to SDHIs for almost as long as the azoles (the first SDHI carboxin was commercialised in the late 1960s), it was after 2011 before most Irish crops received one if not two applications of an SDHI. When this is taken into account, the development of resistance has been much quicker.

Septoria has continued to evolve and develop to overcome the impact of different families of fungicides.

The first isolates of septoria or ramularia with SDHI resistance were found in late 2015. These increased steadily during subsequent seasons and now Irish populations of both diseases are believed to be dominated by resistance.

This is where the definitions of resistance start to get muddled, with phrases such as moderately adapted or moderately resistant being used to describe current populations.

This is partially due to how resistance has developed to the SDHIs. Unlike the azoles or strobilurins, the SDHIs target a protein that is made up of four sub-units (A-D), with the fungicide binding directly to three of these units. Hence, the possibly for resistance to develop resides on three different genes.

As well as this, quite a few different mutations can lead to various changes in the target site, which in themselves can lead to slightly different levels of SDHI binding. For instance, in septoria the mutation which changed H152R on sub-unit C can lead to complete resistance (in the lab this is very difficult to kill with current SDHIs). This was one of the first mutations identified in 2015. However, it seems not to have been highly selected, possibly due to a fitness penalty.

At the same time, other mutations occurred on sub-unit C, independent of each other. These included T79N and N86S. These led to lower levels of resistance, often referred to as moderate, but they have come to dominate the Irish septoria population.

While moderate (we can kill them in the lab with SDHIs, although at significantly higher doses than for sensitive strains), they do have a significant impact on the levels of efficacy achieved by SDHIs alone under field conditions.

Again, like the azoles, there is a new generation of SDHIs in the pipeline which are providing activity against those strains which are affecting SDHIs currently.

The commercial impact of these changes to both the azoles and SDHIs have not yet really been felt. Most fungicide programmes relied on mixtures of azoles plus SDHIs plus chlorothalonil, and rightly so. Each component helps the other, both in terms of efficacy and resistance management.

However, it remains essential to ensure that any weakness in the programme is avoided. This is best done by ensuring correct spray timings to get the most out of the current chemistry. Ensuring good disease control in 2019 depends greatly on this.

Key points

  • Resistance development is real in nature, as organisms fight back against man’s intervention.
  • Diseases differ in their risk of resistance development, as do fungicides.
  • Some diseases now show some form of resistance to most fungicide groups.
  • SDHIs are also now showing resistance development in a number of key diseases.