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Whole-genome sequencing elucidates the species-wide diversity and evolution of fungicide resistance in the early blight pathogen Alternaria solani - PubMed

  • ️Sat Jan 01 2022

. 2022 Feb 22;15(10):1605-1620.

doi: 10.1111/eva.13350. eCollection 2022 Oct.

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Whole-genome sequencing elucidates the species-wide diversity and evolution of fungicide resistance in the early blight pathogen Alternaria solani

Severin Einspanier et al. Evol Appl. 2022.

Abstract

Early blight of potato is caused by the fungal pathogen Alternaria solani and is an increasing problem worldwide. The primary strategy to control the disease is applying fungicides such as succinate dehydrogenase inhibitors (SDHI). SDHI-resistant strains, showing reduced sensitivity to treatments, appeared in Germany in 2013, shortly after the introduction of SDHIs. Two primary mutations in the SDH complex (SdhB-H278Y and SdhC-H134R) have been frequently found throughout Europe. How these resistances arose and spread, and whether they are linked to other genomic features, remains unknown. For this project, we performed whole-genome sequencing for 48 A. solani isolates from potato fields across Europe to better characterize the pathogen's genetic diversity in general and understand the development and spread of the genetic mutations that lead to SDHI resistance. The isolates can be grouped into seven genotypes. These genotypes do not show a geographical pattern but appear spread throughout Europe. We found clear evidence for recombination on the genome, and the observed admixtures might indicate a higher adaptive potential of the fungus than previously thought. Yet, we cannot link the observed recombination events to different Sdh mutations. The same Sdh mutations appear in different, non-admixed genetic backgrounds; therefore, we conclude they arose independently. Our research gives insights into the genetic diversity of A. solani on a genome level. The mixed occurrence of different genotypes, apparent admixture in the populations, and evidence for recombination indicate higher genomic complexity than anticipated. The conclusion that SDHI tolerance arose multiple times independently has important implications for future fungicide resistance management strategies. These should not solely focus on preventing the spread of isolates between locations but also on limiting population size and the selective pressure posed by fungicides in a given field to avoid the rise of new mutations in other genetic backgrounds.

Keywords: agriculture; alternaria solani; fungicide resistance; plant pathology; population genetics – empirical; potato.

© 2022 The Authors. Evolutionary Applications published by John Wiley & Sons Ltd.

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Conflict of interest statement

The authors have no conflict of interest.

Figures

FIGURE 1
FIGURE 1

Overview of the sampling locations used in this study

FIGURE 2
FIGURE 2

Principal component analysis (PCA) and phylogenetic tree constructed of the 48 Alternaria solani isolates. (a) Scatter plots of the first two principal components made using SNPRelate and ggplot2 packages in R. The x‐ and y‐axis represents the PC1 (with variance explained 21%) and PC2 (with variance explain 16%). The isolates are colour‐coded according to their region of origin. Highlighted clusters in yellow, green, and purple are based on the clustering on the phylogenetic tree. (b) Phylogeny of reconstructed whole‐genome sequences for each of the 48 isolates, made using RAxML (GTRGAMMA) with 100 bootstraps. The phylogenetic tree is constructed using treeio and ggtree packages in R. The colour coding of the isolates corresponds to the region of origin. The x‐axis and scale bar indicate the branch length

FIGURE 3
FIGURE 3

Ancestry analysis on A. solani samples. Ancestry analysis was performed on A. solani isolates (n=47, BE_SL002 excluded) using the R‐package LEA [snmf(K=1:15, rep=10, ploidy=1)] for 6 (a), 7 (b), and 8 (c) ancestral populations. Colours represent individual genotypes assigned by sparse nonnegative matrix factorization. Bar plots show the admixture of each genotype in every isolate. Diamonds represent mutations against SDHIs found in the data set. The numbers in panel B denominate the assigned genotype (GT) as used in Table 1 and other parts of this manuscript

FIGURE 4
FIGURE 4

Minimum spanning network analyses (MSN) for our A. solani samples. MSN showing the relatedness of the samples as produced by the R package poppR. Both panels show the same network, with identical scaling (x axis). Each circle represents an individual isolate. Colours in (a) correspond to previously assigned genotypes, colours in (b) highlight the isolate's SDHI mutations

FIGURE 5
FIGURE 5

Splitstree analyses for the A solani isolates. Splitstree analysis reveals the same genetic clusters as our ancestry and MSN analysis. Several isolates show clear admixture or signals of recombination, as shown by the lines connecting the individual branches. The circles represent the dominant genotype as assigned with LEA, isolates that have no coloured background are admixed. The text colour for our each isolate indicates the respective SDHI mutation of the isolate

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