The evolutionary history of the current globalRamularia collo-cygniepidemic

Abstract

Ramularia Leaf Spot (RLS) has emerged as a threat for barley production in many regions of the world. Late appearance of unspecific symptoms caused that Ramularia collo-cygni could only by molecular diagnostics be detected as the causal agent of RLS. Although recent research has shed more light on the biology and genomics of the pathogen, the cause of the recent global spread remains unclear.To address urgent questions, especially on the emergence to a major disease, life-cycle, transmission, and quick adaptation to control measures, we de-novo sequenced the genome of R. collo-cygni (urug2 isolate). Additionally, we sequenced fungal RNA from 6 different conditions, which allowed for an improved genome annotation. This resulted in a high quality draft assembly of about 32 Mb, with only 78 scaffolds with an N50 of 2.1 Mb. The overall annotation enabled the prediction of 12.346 high confidence genes. Genomic comparison revealed that R. collo-cygni has significantly diverged from related Dothidiomycetes, including gain and loss of putative effectors, however without obtaining species-specific genome features. To evaluate the species-wide genetic diversity, we sequenced the genomes of 19 R. collo-cygni isolates from multiple geographic locations and diverse hosts and mapped sequences to our reference genome. Admixture analyses show that R. collo-cygni is world-wide genetically uniform and that samples do not show a strong clustering on either geographical location or host species. To date, the teleomorph of R. collo-cygni has not been observed. Analysis of linkage disequilibrium shows that in the world-wide sample set there are clear signals of recombination and thus sexual reproduction, however these signals largely disappear when excluding three outliers samples, suggesting that the main global expansion of R. collo-cygni comes from mixed or clonally propagating populations. We further analysed the historic population size (Ne) of R. collo-cygni using Bayesian simulations.We discuss how our genomic data and population genetics analysis can help understand the current R. collocygni epidemic and provide different hypothesis that are supported by our data. We specifically highlight how recombination, clonal spreading and lack of host-specificity could further support global epidemics of this increasingly recognized plant disease and suggest specific approaches to combat this pathogen.

Comparative analysis of Argentinian and European populations of Ramularia collo‐cygni on barley

“…Although it was first reported in 2001 (Khier et al., 2002), since 2012, RLS has become an important biotic limitation for barley production in Argentina (mainly southern Buenos Aires province) and Uruguay (Carmona et al., 2013; Pereyra, 2013), even though it is considered as a sporadically occurring disease in both countries. Many Rcc characteristics such as a high number of transposable elements (Stam et al., 2018), huge effective population size, alternative hosts (wheat, oat, triticale, rye, among others; Huss, 2004, 2008; Huss & Miethbauer, 2010; Kaczmarek et al., 2017; Sutton & Waller, 1988) and evidence of sexual recombination (although it is considered a haploid organism; Hjortshøj et al., 2013; Piotrowska et al., 2016; Stam et al., 2017) suggest a high evolutionary potential and fast adaptation to environmental challenges (McDonald & Linde, 2002). Although host quantitative resistance (Hoheneder et al., 2021; McGrann & Brown, 2018) has recently been communicated, no major resistance genes in barley varieties have been reported against RLS.…”

Jasmonates, gibberellins, and powdery mildew modify cell cycle progression and evoke differential spatiotemporal responses along the barley leaf

“…Barley is a host for numerous pathogens and insect pests that attack the plant at different growth stages. Blumeria hordei causes barley powdery mildew and results in considerable loss in productivity despite fungicide treatment ( Kusch and Panstruga, 2017 ; Stam et al ., 2017 , Preprint; Cowger et al ., 2018 ; Liu et al ., 2019 ). Powdery mildews belong to the Helotiales ( Johnston et al , 2019 ), an ascomycete family representing an ancient lineage that evolved over 100 million years ago and that has diversified to more than 400 species colonizing nearly 10 000 plant species ( Takamatsu, 2004 ; Johnson et al ., 2010 ; Kusch and Panstruga, 2017 ).…”