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Mapping Wheat Powdery Mildew Across Europe

Research reveals complex dynamics of wheat powdery mildew populations in Europe.

Fabrizio Menardo, J. Jigisha, J. Ly, N. Minadakis, F. Freund, L. Kunz, U. Piechota, B. Akin, V. Balmas, R. Ben-David, S. Bencze, S. Bourras, M. Bozzoli, O. Cotuna, G. Couleaud, M. Cseplo, P. Czembor, F. Desiderio, J. Dörnte, A. Dreiseitl, A. Feechan, A. Gadaleta, K. Gauthier, A. Giancaspro, S. L. Giove, A. Handley-Cornillet, A. Hubbard, G. Karaoglanidis, S. Kildea, E. Koc, Z. Liatukas, M. S. Lopes, F. Mascher, C. McCabe, T. Miedaner, F. Martinez-Moreno, C. F. Nellist, S. Okon, C. Praz, J. Sanchez-Martin, V. Sarateanu, P. Schulz, N. Schwartz, D. Seghetta, Solis Martel

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Table of Contents

Over the past two decades, the speed of DNA sequencing technology has greatly advanced the field of molecular epidemiology. This technology allows researchers to study the genetic makeup of pathogens in real-time, which is essential for understanding and controlling human diseases. A prime example of this was during the COVID-19 pandemic, where researchers sequenced many viral genomes weekly to track the virus's spread, monitor new variants, and help create vaccines.

Importance in Agriculture

Pathogens don't just threaten human health-they also severely impact agriculture, causing significant crop losses annually. For instance, microbial pathogens are responsible for around 20% loss in major crops like wheat. Even before the advent of whole genome sequencing, researchers recognized that understanding the Genetics of plant pathogens could enhance disease control measures. The combination of these genetic studies with advanced sequencing techniques has sparked renewed interest in using pathogen information to manage pests better and breed resistant crops.

Genomic data has been key in examining various agricultural diseases, such as olive quick decline syndrome in Italy and the recent outbreaks of wheat blast in countries like Zambia and Bangladesh. While knowledge about these pathogens has improved, gaps still exist regarding their biology, including how far a pathogen can spread in one season and how connected different epidemics are across regions. Unfortunately, answering these basic questions often lacks enough evidence.

Focus on Wheat Powdery Mildew

This study looks closely at wheat powdery mildew in Europe and the Mediterranean, which is a crucial region for global wheat production. Powdery mildew, caused by the fungus Blumeria graminis forma specialis tritici (Bgt), attacks wheat's leaves, stems, and spikes. Although it can be found wherever wheat is grown, it tends to thrive in cooler, humid climates-common in Northern Europe.

Currently, powdery mildew is managed using chemical Fungicides and by developing resistant wheat varieties. However, Bgt Populations are increasingly showing resistance to fungicides, and new resistant varieties often only provide a temporary solution. The longevity of genetic resistance depends on both how pathogens evolve and the mechanisms behind the resistance.

Bgt is known to reproduce both sexually and asexually, but recent genomic studies suggest that sexual reproduction may not happen often. Furthermore, available data indicates that European Bgt samples are largely uniform, implying a single interconnected population across the continent. However, these studies are based on limited samples from different decades.

Research Goals

Here, we aim to address some unresolved questions about wheat powdery mildew by conducting a comprehensive sampling of Bgt populations over two consecutive years, 2022 and 2023, followed by whole genome sequencing. We wish to show how population Genomics and molecular epidemiology can provide essential insights into pathogen biology and inform control strategies.

Methodology

Sampling and Sequencing

To understand the dynamics of wheat powdery mildew epidemics in Europe, we organized an extensive sampling campaign over two growing seasons. We collected 276 new Bgt strains from over 90 locations across 20 countries in Europe and the Mediterranean. These samples were then sequenced, and we combined our new data with publicly available genome sequences from past isolates. After filtering for quality, our analysis focused on 568 samples, yielding over 3.5 million high-confidence genetic markers for studying population dynamics.

Analyzing Population Structure

We examined the population structure of our samples using various methods, which allowed us to group isolates based on geographic distribution. Our findings revealed five distinct groups, each corresponding roughly to different regions across Europe and the Mediterranean. The results indicated that wheat powdery mildew is not a single homogeneous population in Europe but rather consists of several well-defined groups.

Results

Population Distribution

Overall, our analysis showed that different populations of Bgt in Europe display varying levels of connectivity. For example, the Bgt population in Northern Europe appears largely homogenous, suggesting extensive gene flow. In contrast, we identified distinct groups in Southern Europe, indicating lower connectivity and smaller, localized populations.

Gene Flow and Admixture

Our research uncovered signs of gene flow between populations, with several isolates showing intermediate genetic characteristics that fit neither group perfectly. This suggests the presence of a more complex genetic landscape than previously recognized.

Patterns of Genetic Diversity

We investigated the factors influencing genetic diversity within Bgt populations, including distance, climate, and environmental variables. Our analysis indicated that wind connectivity significantly impacts population structure, reinforcing the idea that wind is a primary mode of dispersal for these pathogens.

Discussion

Implications of Findings

Our results have significant implications for understanding how wheat powdery mildew spreads and persists across regions. The high level of gene flow in Northern Europe suggests that coordinated breeding efforts might be effective across this region. Conversely, in Southern Europe, where populations are more localized, targeted strategies may be needed.

Evolutionary Dynamics

We found evidence for ongoing evolution in Bgt populations, likely driven by environmental changes and agricultural practices. Our analysis indicated that the Kingman coalescent model, often used for studying population dynamics, may not be appropriate for Bgt. This suggests that different models may yield more accurate representations of how these populations evolve over time.

Conclusion

Our study highlights the critical role of molecular tools in advancing understanding of plant pathogens like wheat powdery mildew. By combining comprehensive sampling with whole genome sequencing, we can gain unique insights into the population dynamics of these pathogens. This knowledge is vital for developing effective management strategies to mitigate crop losses and ensure food security in the face of evolving plant diseases.

Future Directions

Going forward, more extensive sampling across different geographic regions and growing seasons will be necessary to fine-tune our understanding of the factors shaping Bgt populations. Also, the integration of genetic data into practical agricultural strategies will be crucial for improving resistance management and ensuring the durability of new varieties against emerging pathogens.

Acknowledgments

We thank all collaborators and organizations involved in this research effort that has contributed to this study's success.

References

  • Note: No references included as per the request.
Original Source

Title: Population genomics and molecular epidemiology of wheat powdery mildew in Europe

Abstract: Agricultural diseases are a major threat to sustainable food production. Yet, for many pathogens we know exceptionally little about their epidemiological and population dynamics, and this knowledge gap is slowing the development of efficient control strategies. Here we study the population genomics and molecular epidemiology of wheat powdery mildew, a disease caused by the biotrophic fungus Blumeria graminis forma specialis tritici (Bgt). We sampled Bgt for two consecutive years, 2022 and 2023, from 22 countries in Europe and surrounding regions, and compiled a genomic dataset of 415 Bgt isolates. We found one single epidemic unit in the north of Europe, consisting of a highly homogeneous population. Conversely, the south of Europe hosts smaller local populations which are less interconnected. In addition, we show that the population structure can be largely predicted by the prevalent wind patterns. We identified several loci that were under selection in the recent past, including fungicide targets and avirulence genes. Some of these loci are common between populations, while others are not, suggesting different local selective pressures. We reconstructed the evolutionary history of one of these loci, AvrPm17, coding for an effector recognized by the wheat receptor Pm17. We found evidence for a soft sweep on standing genetic variation. Multiple AvrPm17 haplotypes, which can partially escape recognition by Pm17, spread rapidly throughout the continent upon its introduction in the early 2000s. We also identified a new virulent variant, which emerged more recently and can evade Pm17 resistance altogether. Overall, we highlight the potential of genomic surveillance in resolving the evolutionary and epidemiological dynamics of agricultural pathogens, as well as in guiding control strategies.

Authors: Fabrizio Menardo, J. Jigisha, J. Ly, N. Minadakis, F. Freund, L. Kunz, U. Piechota, B. Akin, V. Balmas, R. Ben-David, S. Bencze, S. Bourras, M. Bozzoli, O. Cotuna, G. Couleaud, M. Cseplo, P. Czembor, F. Desiderio, J. Dörnte, A. Dreiseitl, A. Feechan, A. Gadaleta, K. Gauthier, A. Giancaspro, S. L. Giove, A. Handley-Cornillet, A. Hubbard, G. Karaoglanidis, S. Kildea, E. Koc, Z. Liatukas, M. S. Lopes, F. Mascher, C. McCabe, T. Miedaner, F. Martinez-Moreno, C. F. Nellist, S. Okon, C. Praz, J. Sanchez-Martin, V. Sarateanu, P. Schulz, N. Schwartz, D. Seghetta, Solis Martel

Last Update: 2024-10-25 00:00:00

Language: English

Source URL: https://www.biorxiv.org/content/10.1101/2024.10.24.619980

Source PDF: https://www.biorxiv.org/content/10.1101/2024.10.24.619980.full.pdf

Licence: https://creativecommons.org/licenses/by-nc/4.0/

Changes: This summary was created with assistance from AI and may have inaccuracies. For accurate information, please refer to the original source documents linked here.

Thank you to biorxiv for use of its open access interoperability.

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