Ramularia, resistance and ratings rally global experts

Ramularia, resistance and ratings rally global experts

Ramularia leaf spot in barley (caused by the pathogen Ramularia collo-cygni) is widespread throughout the world, reducing both yield and, importantly for malting crops, quality.

It was first noted in Italy in 1893 but only became of economic concern in Europe around the late 1990s, following some high losses in Scottish field crops. The event caused European researchers to take more notice of the disease.

In recent years, ramularia leaf spot has become a greater problem across the whole of the UK, especially as resistance to fungicides has appeared: firstly to strobilurins in 2002, followed by widespread resistance to azoles and SDHIs in 2017.

Limited varietal resistance and the threat of the withdrawal of chlorothalonil, the only active ingredient that remains fully effective on ramularia leaf spot in the UK, are also emerging threats.

For these reasons, AHDB held an international ramularia workshop earlier this month (3–4 October) to bring together researchers, plant breeders, agrochemical companies, agronomists and other experts to share their experiences and theories.

Ramularia workshop summary

People came together from Europe, South America, South Africa, Australia and New Zealand. Presentations were given on all aspects of research and management of ramularia leaf spot – from practical agronomy to complex molecular biology.

***Access presentations, biographies and abstracts***

Its evolution into a problematic disease in the late 1990s coincided with new varieties marketed with better resistance to mildew, which also showed physiological leaf spotting. There were also changes in crop protection, as new fungicides were introduced. Initial research into controlling ramularia leaf spot focused on disease epidemiology, isolating and culturing the fungus, and understanding of losses in yield and quality, as well as fungicide activity and timing. This gave growers an immediate answer for its control and demonstrated to the industry that this disease was a serious threat.

Host, pathogen and environmental interactions

The interaction between ramularia leaf spot and the host plant is complex. In fact, there were initial questions over the impact of the fungus on yield. Recent research shows that when the ramularia leaf spot fungus coexists with the plant before symptom expression, it does not affect yield. It is only when symptoms appear (associated with photodynamic rubellin toxins produced by the fungus), that green leaf area on the upper leaves is lost, and yield and quality are impacted. There are certain conditions that can exacerbate this situation, and the contribution of each of these conditions varies according to location and environment. These conditions include stress due to waterlogging, sunlight duration/intensity, agrochemical inputs, frosts and poor nutrition (this provides an additional challenge when growing low-nitrogen barley for malting).

Physiological stresses, associated with plant development at flowering, are also a trigger. Drought also has a complex interaction – it reduces symptoms but can enhance fungal biomass in the plant.

The role of the rubellin toxins in the development of symptoms and subsequent leaf death is complex and there has been recent evidence that the rubellin toxins may not be totally responsible for disease symptoms. This host-pathogen interaction also needs more investigation.

Ramularia leaf spot is both a seedborne and airborne disease. As a result, reducing levels in the seed does not necessarily prevent disease after flowering.

The pathogen has also been detected in grasses around the world, suggesting it is already ubiquitous worldwide. High homogenicity in a worldwide collection of isolates suggests seed transfer has played a key role in its recent expansion across the globe. Seed transfer could also contribute to the introduction of fungicide resistant isolates to a local population.

The resistance challenge

The R. collo-cygni population is quick to adapt and fungicide resistance has developed rapidly in some areas of the world. In addition, R. collo cygni isolates with mutations conferring fungicide resistance don’t seem to have a fitness penalty, as they do in Zymoseptoria tritici (a close relative that causes septoria tritici disease in wheat). At the workshop, we heard about the recent development of fungicide resistance in Uruguay, Argentina and New Zealand, as well as the story from the UK, France, Germany and Ireland.

Successful varietal breeding for resistance to the disease in the UK has been limited, an issue also experienced around the globe. Thousands of barley lines have been screened with no obvious resistance genes found. Any resistance found is likely to be polygenic (i.e. involving many genes), making it difficult to work with. However, the good news is that it is that ramularia leaf spot resistance genes can be exploited without sacrificing the mlo (mildew resistance) gene, allowing resistance to both these pathogens in the same variety.

Trialling varieties for resistance is also a challenge, as has been found in the UK and New Zealand – two countries that both attempt to produce ramularia disease resistance ratings.

Ramularia leaf spot is an extremely difficult disease to identify and assess, as is it so similar to other biotic and abiotic conditions – such as the spot form of net blotch, old mildew lesions and physiological leaf spotting. Stresses on the crop may also influence the type of symptoms expressed by the pathogen. A potential way to overcome this is to use optical imaging to diagnose ramularia leaf spot symptoms. Alternatively, measuring a reduction in green leaf area is, generally, easier to assess.

But difficulties in assessment are only half of the problem: the large influence of the environment means that varieties perform very differently at different sites – there is a large genotype-by-environment interaction. The influence of different environmental conditions, such as leaf wetness during stem extension (which is linked to high disease epidemics in the UK) on ramularia leaf spot development, is still unclear.

Breeding for varieties that are tolerant and able to coexist with the fungus, rather than resistant to the disease, may be an option. Another example would be to look at canopy architecture and limit the stress from sunlight or to breed earlier-maturing varieties that escape symptom expression. This may lead to lower yields but shouldn’t compromise on quality. Selecting varieties based purely on high green leaf area, without extending maturity, may be a way to select for multi-disease resistance in an efficient way, rather than focusing on specific diseases as we currently do.

Foliar solutions?

Revisiting foliar products that have antioxidant properties aimed at delaying the onset of symptom development could also be an option, as well as the use of elicitors that switch on the resistance genes within the crop. Cover crops that improve soils and fertility or supress any spore release from straw are also being investigated.

Another step would be to take up the strategy used in Uruguay, where micro and macronutrients are applied to the crop early in the season to minimise nutritional stress and ensure good crop growth. Another alternative is to revisit fungicides that may have a limited effect on ramularia leaf spot, for example cyprodinil and sulphur.

If new fungicides come through the pipeline, they are likely to be single site products. These must be used in an integrated programme, with a robust mixing partner to minimise the risk of resistance developing. Chlorothalonil is currently the most effective broad-spectrum fungicide to use in an anti-resistance strategy. Questions over its renewal means we may need to find an alternative, or accept use of lower rates or fewer applications in the future.

The need for action

Without effective management of ramularia leaf spot, cost of production of malting barley will increase as yields and quality will be more volatile and barley will become a riskier crop to grow, leading to a reduction in margins to the grower.

We can see a similar situation occurring with oilseed rape, where poor control of cabbage stem flea beetle is having a major impact, with growers moving away from the crop in high pest pressure situations.

The workshop has increased international collaboration between researchers, agronomists, plant breeders and agrochemical companies. It has resulted in shared ideas, discussion and debate. This is all essential if new integrated measures are to be identified and implemented to maintain the profitability of barley.

Recommended Lists trials

At AHDB, we are looking at our procedures to evaluate varietal resistance in light of the information from this workshop. We will suspend the Recommended List ramularia disease ratings but work to reinstate them as soon as we are able to produce reliable information.

Changes include trials focused on ramularia leaf spot. These will be located in known high-disease pressure areas, with other diseases controlled (as much as possible) and disease assessments made by expert pathologists. Additional susceptible controls will also be included and any known resistant lines. If irrigation is thought to increase the reliability of the trial, this will also be considered.

AHDB’s fungicide performance project also continues to look at the efficacy of current and new products. AHDB also has a programme of research to get a better understanding of resistance mechanisms of plant pathogens to fungicides and how to minimise the development of resistance.

Other options discussed, that have not yet been investigated, include the role of mycorrhizal or antagonistic endophytic fungi and the effect of agronomic approaches (such as no-till).

The workshop highlighted how complex this disease is. We need to find a better strategy to manage it using integrated crop management approaches. We need to revisit our understanding of the epidemiology and the host-pathogen interactions, particularly in relation to the rubellin toxins.

The full genome of R. collo-cygni has been sequenced and is publically available, so we need to use this information to our advantage.

Management of the disease is likely to rely on using many incremental measures as opposed to a single effective measure. We have ourselves a situation where IPM is the only way forward.

It is important to continue sharing experience across the globe. Only through international collaboration will we be able to find solutions to tackle this disease.

Neil Watson from Hutchinsons, who attended the workshop, suggested that holding international workshops may be a good approach to tackle other crop production issues, such as grassweed control and insecticide resistance. AHDB is looking at the potential of this too, watch this space…

More background information on the disease and its symptoms are available ahdb.org.uk/knowledge-library/ramularia

Catherine Garman

Catherine Garman

Catherine is Crop Health & Protection Scientist (Diseases) at AHDB

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