Long‐term and rapid evolution in powdery mildew fungi

Abstract

The powdery mildew fungi (Erysiphaceae) are globally distributed plant pathogens with a range of more than 10,000 plant hosts. In this review, we discuss the long‐ and short‐term evolution of these obligate biotrophic fungi and outline their diversity with respect to morphology, lifestyle, and host range. We highlight their remarkable ability to rapidly overcome plant immunity, evolve fungicide resistance, and broaden their host range, for example, through adaptation and hybridization. Recent advances in genomics and proteomics, particularly in cereal powdery mildews (genus Blumeria), provided first insights into mechanisms of genomic adaptation in these fungi. Transposable elements play key roles in shaping their genomes, where even close relatives exhibit diversified patterns of recent and ongoing transposon activity. These transposons are ubiquitously distributed in the powdery mildew genomes, resulting in a highly adaptive genome architecture lacking obvious regions of conserved gene space. Transposons can also be neofunctionalized to encode novel virulence factors, particularly candidate secreted effector proteins, which may undermine the plant immune system. In cereals like barley and wheat, some of these effectors are recognized by plant immune receptors encoded by resistance genes with numerous allelic variants. These effectors determine incompatibility (“avirulence”) and evolve rapidly through sequence diversification and copy number variation. Altogether, powdery mildew fungi possess plastic genomes that enable their fast evolutionary adaptation towards overcoming plant immunity, host barriers, and chemical stress such as fungicides, foreshadowing future outbreaks, host range shifts and expansions as well as potential pandemics by these pathogens.

Rapid evolutionary adaptation: Potential and constraints

“…In their contribution, Kusch et al. (2023) review evidence and recent studies of the long‐ and short‐term evolution of powdery mildew fungi ( Erysiphaceae ) pathogens of plants. The powdery mildew fungi are globally distributed plant pathogens with a range of more than 10,000 plant hosts.…”

“…The dynamics of TEs and the resulting mutational changes play an important role in the fungal mildew pathogen Blumeria of cereal crops to evade crop resistance and promote resistance to fungicides (Kusch et al, 2023).…”

“…Finally, a review summarises findings from genomic studies on the role of transposable elements (TEs) in determining the evolutionary potential of crop pathogens. The dynamics of TEs and the resulting mutational changes play an important role in the fungal mildew pathogen Blumeria of cereal crops to evade crop resistance and promote resistance to fungicides (Kusch et al., 2023).…”

Structure-Based Discovery of New Succinate Dehydrogenase Inhibitors via Scaffold Hopping Strategy

“…4 Most importantly, PM not only spreads rapidly, but also evolves resistance to fungicides quickly, making it a formidable challenge to manage. 5,6 For example, some classical fungicides, such as demethylase inhibitors (DMIs) and strobilurin-based (QoI) fungicides, have nearly lost sensitivity to PM diseases. 7,8 Thus, there is a high demand to develop novel fungicides to combat PM infections effectively.…”

“…Powdery mildew (PM), caused by erysiphales , is one of the most serious fungal diseases that poses a significant threat to crop production in both field and greenhouse, resulting in substantial yield losses. − According to the statistics of global authoritative institutions, the annual loss caused by PM in the world amounts to 5.8–6.3 billion US dollars . Most importantly, PM not only spreads rapidly, but also evolves resistance to fungicides quickly, making it a formidable challenge to manage. , For example, some classical fungicides, such as demethylase inhibitors (DMIs) and strobilurin-based (QoI) fungicides, have nearly lost sensitivity to PM diseases. , Thus, there is a high demand to develop novel fungicides to combat PM infections effectively.…”