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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.

ABSTRACT: 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.

SUBMITTER: Nowicki M

PROVIDER: S-EPMC8317435 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Cucumber downy mildew, caused by P. cubensis, is an important leaf disease that can severely affect cucumber production. In recent years, cucumber target spot, caused by C. cassiicola, has been reported in both Asia and Europe and is now considered as a major disease disrupting cucumber production. Single-disease-resistant cucumber varieties have been unable to satisfy production needs. To explore the molecular mechanisms of cucumber resistance to these two diseases, cucumber cultivars D9320 (resistant to downy mildew and target spot) and D0401 (susceptible to downy mildew and target spot) were used as experimental materials in this study. We used transcriptome sequencing technology to identify genes related to disease resistance and verified using transgenic technology.We screened out the cucumber resistance-related gene CsERF004 using transcriptome sequencing technology. Induction by pathogens, salicylic acid (SA), and ethylene (ET) resulted in the up-regulation of CsERF004. Three treatments, namely, inoculation with C. cassiicola alone, inoculation with P. cubensis alone, and simultaneous inoculation with both pathogens, all resulted in the significant and sustained up-regulation of CsERF004 in the resistant cultivar D9320, during the early stage of infection. In the susceptible cultivar D0401, CsERF004 expression was also significantly up-regulated at the later stage of infection but to a lesser extent and for a shorter duration than in the resistant cultivar D9320. The CsERF004 gene encodes a protein localizes to the nucleus. The over-expression of CsERF004 in the susceptible cultivar D0401 resulted in the significant up-regulation of the CsPR1 and CsPR4 genes and increased the levels of SA and ET, which enhanced the resistance of cucumber to downy mildew and target spot.Analyses of the CsERF004 expression pattern in disease-resistant and susceptible cucumber cultivars and transgenic validation indicate that CsERF004 confers resistance to P. cubensis and C. cassiicola. The findings of this study can help to better understanding of mechanisms of response to pathogens and in establishment the genetic basis for the development of cucumber broad-spectrum resistant cultivars.

Dataset Information

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

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