Genome Sequences of Three Races of <i>Peronospora effusa</i>: A Resource for Studying the Evolution of the Spinach Downy Mildew Pathogen

Feng, Chunda; Lamour, Kurt; Bluhm, Burt H.; Sharma, Sandeep; Shrestha, Sandesh; Dhillon, Braham; Correll, James C.

doi:10.1094/mpmi-04-18-0085-a

Cited by 14 publications

(14 citation statements)

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“…The genomes of Pfs race 13 and 14 have recently been published [82, 83], with a similar genome size (32.1 Mb, and 30.8 Mb respectively) and gene content (∼ 8000 gene models) compared to the assembly of Pfs1 . Contrary to our assembly method, the input data for those genome assemblies were filtered by alignment to an oomycete and bacterial database to discard reads that do not belong to the oomycete genus.…”

Section: Discussionmentioning

confidence: 99%

Genome reconstruction of the non-culturable spinach downy mildew Peronospora effusa by metagenome filtering

Klein

Neilen

Verk

et al. 2019

Preprint

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Peronospora effusa (previously known as P. farinosa f. sp. spinaciae, and here referred to as Pfs) is an obligate biotrophic oomycete that causes downy mildew on spinach (Spinacia oleracea). To combat this destructive disease resistant cultivars are continually bred. However, new Pfs races rapidly break the employed resistance genes. To get insight into the gene repertoire of Pfs and identify infection-related genes, the genome of the first reference race, Pfs1, was sequenced, assembled, and annotated. Due to the obligate biotrophic nature of this pathogen, material for DNA isolation can only be collected from infected spinach leaves that, however, also contain many other microorganisms. The obtained sequences are, therefore, considered a metagenome. To filter and obtain Pfs sequences we utilized the CAT tool to taxonomically annotate ORFs residing on long sequences of a genome pre-assembly. This study is the first to show that CAT filtering performs well on eukaryotic contigs. Based on the taxonomy, determined on multiple ORFs, contaminating long sequences and corresponding reads were removed. Filtered reads were re-assembled to provide a clean and improved Pfs genome sequence of 32.40 Mbp consisting of 8,635 scaffolds. Transcript sequencing of a range of infection time points aided the prediction of a total of 13,277 gene models, including 99 RXLR(-like) effector, and 14 putative Crinkler genes. Comparative analysis identified common features in the secretomes of different obligate biotrophic oomycetes, regardless of their phylogenetic distance. Their secretomes are generally smaller, compared to hemibiotrophic and necrotrophic oomycete species. We observe a reduction in proteins involved cell wall degradation, in Nep1-like proteins (NLPs), proteins with PAN/apple domains, and host translocated effectors. The genome of Pfs1 will be instrumental in studying downy mildew virulence and for understanding the molecular adaptations by which new isolates break spinach resistance.

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Section: Discussionmentioning

confidence: 99%

Genome reconstruction of the non-culturable spinach downy mildew Peronospora effusa by metagenome filtering

Klein

Neilen

Verk

et al. 2019

Preprint

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“…Oospores of P. effusa have been observed from spinach seed [12][13][14] and spinach plants in one downy mildew sample of 2008 [5], two samples in 2016, and 28 samples in 2018 collected from CA (Correll et al, unpublished). Difference was found in the mating proteins in the genome sequences of isolates of P. effusa [42], oospores can be produced by co-inoculation of two isolates selected accordingly to different mating features [47], indicating heterothallic sexual reproduction occurs in P. effusa, which was also found in several other oomycetes, such as Phytophthora, Bremia, and Plasmopara [21]. Among those isolates that rejected sexual reproduction hypotheses, nine isolates contained multiple lesions, but only one genotype was observed, suggesting clonal production among these isolates of P. effusa.…”

Section: Discussionmentioning

confidence: 97%

“…Some genome resources of P. effusa are now available and a large number of SNPs have been identified [18,42]. It may be possible to get additional insight of the population structure and evolution of P. effusa by using genome-wide SNPs.…”

Section: Discussionmentioning

confidence: 99%

Genetic diversity of the spinach downy mildew pathogen based on hierarchical sampling

Feng

Lamour

Dhillon

et al. 2020

Preprint

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Downy mildew, caused by the obligate oomycete pathogen Peronospora effusa, is the most economically important disease of spinach. In the past 30 years, 14 new races and 13 strains with novel virulence have been identified. However, the mechanism(s) driving the rapid evolution of virulence remains unknown. To understand reproductive strategies potentially driving the emergence of new races in P. effusa, 67 composite isolates (a collection of symptomatic leaves from a single cultivar grown in a defined area) of P. effusa obtained from 13 states between 2010 and 2018 were used to analyze the population genetic diversity hierarchically. Genotypes at 33 SNP loci of 719 lesions from these 67 isolates were determined by targeted sequencing. Diversity was then evaluated among individual lesions within the composite isolates, between isolates, host cultivars, geographic locations, and years of isolates collected. A total of 380 genotypes were identified from 719 individual lesions. Of the 380 genotypes, 350 (92%) were unique while the most common genotype was identified in 110 lesions of 16 isolates collected from 13 cultivars from CA and AZ in 2016. Variation within composite isolates ranged from none (a single genotype among lesions from a composite isolate) to 38 unique genotypes recovered from 39 lesions of a composite isolate. An index of association analysis suggested asexual (clonal) and sexual reproduction play important roles in population structure. Based on discriminant analysis of principal components, four distinct subpopulations were identified. Host cultivar, origin, and time of collection had an effect on population differentiation, and genotypes specific to a certain location or collection period were identified. Some subpopulations were unique to certain areas, and were only detected after 2014-2016. The co-existence of sexual and asexual reproduction strategies may partially explain the rapid emergence and spread of new races and novel strains of P. effusa.

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“…The availability of next-generation sequencing enables economical and facile analysis of genomes, leading to many important insights into the biology of many oomycetes (Baxter et al 2010; Ali et al 2017; McCarthy and Fitzpatrick 2017; Lamour et al 2012; Raffaele and Kamoun 2012; Tyler et al 2006; Lévesque et al 2010; Tian et al 2011; Soanes et al 2007; Sharma et al 2015; Judelson 2012; Grünwald 2012; Jiang et al 2013; Links et al 2011; Haas et al 2009; Schena et al 2008; Gaulin et al 2018). Because of their economic importance, some downy mildews have had their genomes sequenced, including: Bremia lactucae, Hyaloperonospora arabidopsidis, Peronospora effusa, Peronospora tabacina, Plasmopara viticola, Plasmopara halstedii, Plasmopara muralis, Plasmopara obducβns, Pseuoperonospora cubensis, Pseudoperonospora humuli, and Sclerospora graminicola (Fletcher et al 2019; Baxter et al 2010; Feng et al 2018; Fletcher et al 2018; Derevnina et al 2015; Sharma et al 2015; Kobayashi et al 2017; Tian et al 2011; Ye et al 2016; Nayaka et al 2017, respectively). Here we augment this repertoire with the annotated genome sequence of Pe.…”

Section: Introductionmentioning

confidence: 99%

The genome ofPeronospora belbahriireveals high heterozygosity, a low number of canonical effectors and CT-rich promoters

Thines

Sharma

Rodenburg

et al. 2019

Preprint

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Along withPlasmopara destructor, Peronosopora belbahriihas arguably been the economically most important newly emerging downy mildew pathogen of the past two decades. Originating from Africa, it has started devastating basil production throughout the world, most likely due to the distribution of infested seed material. Here we present the genome of this pathogen and results from comparisons of its genomic features to other oomycetes. The assembly of the nuclear genome was ca. 35.4 Mbp in length, with an N50 scaffold length of ca. 248 kbp and an L50 scaffold count of 46. The circular mitochondrial genome consisted of ca. 40.1 kbp. From the repeat-masked genome 9049 protein-coding genes were predicted, out of which 335 were predicted to have extracellular functions, representing the smallest secretome so far found in peronosporalean oomycetes. About 16 % of the genome consists of repetitive sequences, and based on simple sequence repeat regions, we provide a set of microsatellites that could be used for population genetic studies ofPe. belbahrii. Peronospora belbahriihas undergone a high degree of convergent evolution, reflecting its obligate biotrophic lifestyle. Features of its secretome, signalling networks, and promoters are presented, and some patterns are hypothesised to reflect the high degree of host specificity inPeronosporaspecies. In addition, we suggest the presence of additional virulence factors apart from classical effector classes that are promising candidates for future functional studies.

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Genome Sequences of Three Races of Peronospora effusa: A Resource for Studying the Evolution of the Spinach Downy Mildew Pathogen

Cited by 14 publications

References 10 publications

Genome reconstruction of the non-culturable spinach downy mildew Peronospora effusa by metagenome filtering

Genome reconstruction of the non-culturable spinach downy mildew Peronospora effusa by metagenome filtering

Genetic diversity of the spinach downy mildew pathogen based on hierarchical sampling

The genome ofPeronospora belbahriireveals high heterozygosity, a low number of canonical effectors and CT-rich promoters

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