Recent advances in oomycete genomics

McGowan, Jamie; Fitzpatrick, David A.

doi:10.1016/bs.adgen.2020.03.001

Cited by 51 publications

(52 citation statements)

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“…By using the historical specimens of both pathogens, we gained some evidence for an ongoing speciation within P. cubensis. Recent evidence from -omics research has added several important genomic and metabolic insights to the accumulated molecular and host-pathogen interactions and specificity evidence of oomycetes speciation (Burkhardt and Day, 2013;McGowan and Fitzpatrick, 2020;Rodenburg et al, 2020). These include alternative splicing in the effector genes (Savory et al, 2012;Summers et al, 2015b), recombination and partial reshuffling of the genetic material (Cohen and Rubin, 2012;Thomas et al, 2017b), and functionally, host jumps and geographic separation from the preferred host species, which necessitated the evolution of parasitic behavior by genetic adjustments (Dussert et al, 2019;Rahman et al, 2019;Thines, 2019;Rodenburg et al, 2020;Wallace et al, 2020).…”

Section: Discussionmentioning

confidence: 99%

“…It needs to be stressed that the presently available draft assemblies cover only about 73% (P. cubensis) or about 54% (P. humuli) of their genome sizes estimated by the Feulgen method (Voglmayr and Greilhuber, 1998). This method proved reliable in assessing the genome sizes when compared with other oomycete genomes assembled and regarded as complete, such as Albugo candida, B. lactucae, or P. viticola (McGowan and Fitzpatrick, 2020;Rodenburg et al, 2020). We did observe a small amount of "noise" (misaligned contigs), which, as noted above, underlines the need for improved genomic resources of downy mildew pathogens.…”

Section: Discussionmentioning

confidence: 99%

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“Jumping Jack”: Genomic Microsatellites Underscore the Distinctiveness of Closely Related Pseudoperonospora cubensis and Pseudoperonospora humuli and Provide New Insights Into Their Evolutionary Past

et al. 2021

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Downy mildews caused by obligate biotrophic oomycetes result in severe crop losses worldwide. Among these pathogens, Pseudoperonospora cubensis and P. humuli, two closely related oomycetes, adversely affect cucurbits and hop, respectively. Discordant hypotheses concerning their taxonomic relationships have been proposed based on host–pathogen interactions and specificity evidence and gene sequences of a few individuals, but population genetics evidence supporting these scenarios is missing. Furthermore, nuclear and mitochondrial regions of both pathogens have been analyzed using microsatellites and phylogenetically informative molecular markers, but extensive comparative population genetics research has not been done. Here, we genotyped 138 current and historical herbarium specimens of those two taxa using microsatellites (SSRs). Our goals were to assess genetic diversity and spatial distribution, to infer the evolutionary history of P. cubensis and P. humuli, and to visualize genome-scale organizational relationship between both pathogens. High genetic diversity, modest gene flow, and presence of population structure, particularly in P. cubensis, were observed. When tested for cross-amplification, 20 out of 27 P. cubensis-derived gSSRs cross-amplified DNA of P. humuli individuals, but few amplified DNA of downy mildew pathogens from related genera. Collectively, our analyses provided a definite argument for the hypothesis that both pathogens are distinct species, and suggested further speciation in the P. cubensis complex.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

“Jumping Jack”: Genomic Microsatellites Underscore the Distinctiveness of Closely Related Pseudoperonospora cubensis and Pseudoperonospora humuli and Provide New Insights Into Their Evolutionary Past

et al. 2021

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“…Oomycetes are filamentous eukaryotes that resemble fungi in terms of morphology but evolved independently from fungi (McGowan and Fitzpatrick, 2020). In the tree of life, oomycetes group together with the brown algae and diatoms in the Stramenopile lineage (Beakes et al, 2012).…”

Section: Oomycete-host Interactionsmentioning

confidence: 99%

“…time, developmental stage or tissue) of an organism (Rodenburg et al, 2018b). In the last decade, there has been a continuous flow of published genome sequences for oomycetes, accompanied by numerous studies publishing comparative genomics, transcriptomics, proteomics, and metabolomics research (McGowan and Fitzpatrick, 2020). These large-scale omics datasets are analyzed to understand how oomycetes evolve, reproduce and interact with their hosts.…”

Section: From Genome Sequence To Genome-scale Metabolic Modelmentioning

confidence: 99%

Uncovering oomycete metabolism using systems biology

Rodenburg

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Metabolism is essential for life. The metabolism of an organism defines its capabilities to take up nutrients from the environment and to convert these into its essential building blocks, such as nucleic acids and amino acids (Lazar and Birnbaum, 2012). Cellular metabolism can be described as a system of biochemical conversions (reactions), most of which are catalyzed by metabolic enzymes. Typically, a genome encodes a few thousand metabolic enzymes (Yilmaz and Walhout, 2017). Each enzyme acts on a selection of substrates and converts these into products, typically by adding or removing reactive groups. Reactions that share substrates or products can be considered functionally connected. Consequently, the collection of biochemical reactions within a cell forms a large interconnected network, representing the routes by which the organism converts simple nutrients into complex metabolites and vice-versa. This network is distributed over different subcellular compartments (organelles). Transporter proteins and channels facilitate the transport of metabolites across the lipid bilayers that surround the cell and the organelles (Sahoo et al., 2014). The overall system is subject to many parameters, such as variability in substrates, temperature, or the pH, not only between cells and the extracellular space but also within cells. Cells regulate this system to maintain homeostasis, i.e. the ability to perform important cellular functions despite variations (perturbations), and this provides robustness (Eberl, 2018; Nijhout et al., 2019). The ability to sense environmental variations and metabolic cues and to adapt metabolism accordingly, depends on a tightly interlinked regulatory system (Watson et al., 2015). This involves regulatory feedback loops embedded in interaction networks crossing metabolic, protein, transcript, and (epi)genetic levels (Figure 1). Pathogen G e n o m e T ra n s c ri p to m e P ro te o m e M e ta b o lo m e Host FIGURE 1 | The molecular layers of a cell are all interconnected, and form a complex and integrated system. In the symbiosis of a pathogen and a host, their systems are connected, and interactions occur between all molecular layers. As such, the phenotype of the cell is an emergent property of the system's complexity (Aderem, 2005). The rates of individual metabolic reactions are a direct consequence of the overall state General introduction

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“…This resemblance is the result of convergent evolution rather than evolutionary kinship because oomycetes and fungi species are very distantly related within the eukaryotes [2,3]. As opposed to fungi, oomycetes have aseptate hyphae, cell walls composed mainly of cellulose rather than chitin and typically motile biflagellate zoospores (that have been lost in many species) [4]. Oomycetes belong to the Straminipila phylum that includes diatoms and brown algae and hosts species that occupy diverse habitats and have an extraordinary array of lifestyles [5].…”

Section: Biology and Taxonomy Of Phytopathogenic Oomycetesmentioning

confidence: 99%

RxLR and CRN effectors of the spinach downy mildew Peronospora effusa and their interacting plant proteins

Neilen¹

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Cellular programming: Immune signaling P. infestans effector Pi02860 was found to repress immune signaling through indirect manipulation of SWAP70, a positive regulator of infestin 1 (INF1)-triggered cell death [84, 108]. The effector was found to interact with StNRL1 (NPH3/RPT2-like), a predicted substrate adaptor of a CULLIN3-associated ubiquitin E3 ligase [109]. Silencing of the N. benthamiana ortholog of NLR1 abolished the ability of Pi02860 to suppress cell death and led to reduced plant colonization by P. infestans. These observations suggest that NRL1 is a susceptibility factor that negatively regulates immunity. NLR1 homodimers were found to bind SWAP70, a guanine exchange factor that positively regulates cell death, and target it for proteasome-mediated degradation. By interacting with NRL1 P. infestans effector Pi02860 enhances the turnover of SWAP70, thereby suppressing the cell death response [84]. Cellular programming: Hormone signaling The tight and accurate regulation of plant immune responses is regulated by defense hormones. Generally, salicylic acid is induced upon infection with biotrophic pathogens while jasmonic acid and ethylene are upregulated when a plant is attacked by a necrotrophic pathogen or herbivore. These opposite hormonal signaling networks are known to antagonize each other to optimally arm the plant to fight off the current attacker. The crosstalk between the hormone pathways is exploited by a RxLR effector of H. arabidopsidis. Effector HaRxL10 was shown to interact with JAZ3, a transcriptional repressor involved in jasmonic acid signaling, and to target it for proteasome-mediated degradation. Degradation of JAZ3 led to enhanced jasmonic acid signaling and eventually reduced SA-signaling mediated by the release of the JAZ3-guarded MYC2 transcription factor. Arabidopsis plants expressing HaRxL10 also showed enhanced susceptibility to the biotrophic bacterium Pseudomonas syringae pv. DC3000 compared to Col-0 [93]. General introduction 1 25 Cellular programming: transcriptional and posttranscriptional manipulation Cellular reprogramming by oomycete effectors can occurs through gene regulation [86] and post transcriptionally through alternative splicing [100] and interference with RNA silencing [110]. P. sojae RxLR effector PsAvh23 was found to reduce histone acetylation levels thereby suppressing the activation of defense genes [98]. DNA in cells is organized around nucleosomes, that consist of an octamer of basic proteins called histones. Acetylation of the tails of these proteins by histone acetyltransferases (HATs) is associated with enhanced gene transcription whereas histone deacetylases (HDACs) reverse the modification and repress gene transcription [111] In plants, the HAT General Control Non-depressive 5 (GCN5) is part of the prototypical nucleosome-acetylating modification complex. GCN5 is modulated by Alteration/Deficiency IN Activation 2 (ADA2) that directs the complex to the histone H3-tail. PsAvh23 competitively binds to ADA2 leading to reduced HAT activity of GCN5 hen...

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Recent advances in oomycete genomics

Cited by 51 publications

References 144 publications

“Jumping Jack”: Genomic Microsatellites Underscore the Distinctiveness of Closely Related Pseudoperonospora cubensis and Pseudoperonospora humuli and Provide New Insights Into Their Evolutionary Past

“Jumping Jack”: Genomic Microsatellites Underscore the Distinctiveness of Closely Related Pseudoperonospora cubensis and Pseudoperonospora humuli and Provide New Insights Into Their Evolutionary Past

Uncovering oomycete metabolism using systems biology

RxLR and CRN effectors of the spinach downy mildew Peronospora effusa and their interacting plant proteins

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