Transcriptional analyses of differential cultivars during resistant and susceptible interactions with Peronospora effusa, the causal agent of spinach downy mildew

Authors: Kandel, Shyam; Hulse-Kemp, Amanda; STOFFEL, KEVIN - University Of California; KOIKE, STEVEN - Trical Inc; SHI, AINONG - University Of Arkansas; Mou, Beiquan; VAN DEYNZE, ALLEN - University Of California; Klosterman, Steven

Submitted to: Scientific Reports
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/3/2020
Publication Date: 4/21/2020
Citation: Kandel, S.L., Hulse-Kemp, A.M., Stoffel, K., Koike, S.T., Shi, A., Mou, B., Van Deynze, A., Klosterman, S.J. 2020. Transcriptional analyses of differential cultivars during resistant and susceptible interactions with Peronospora effusa, the causal agent of spinach downy mildew. Scientific Reports. 10. Article 6719. https://doi.org/10.1038/s41598-020-63668-3.
DOI: https://doi.org/10.1038/s41598-020-63668-3

Interpretive Summary: Downy mildew, caused by Peronospora effusa, remains a devastating disease of spinach in California and worldwide where spinach is cultivated. While the disease can be controlled in conventional production with fungicides, an increasing amount of acreage is devoted to organic production. Furthermore, new virulent strains of P. effusa can infect previously resistant spinach cultivars, which represent a serious threat to the organic sector. This article describes and illustrates the changes in gene expression in resistant and susceptible spinach cultivars in response to P. effusa. The study also describes major proteins of P. effusa expressed in the susceptible cultivar which are thought to be important for this pathogen to infect the plant based upon what is known of related organisms. This article provides the information about candidate genes with the potential to confer host resistance to downy mildew in spinach cultivars. This study and future studies that provide candidate genes whose products underlie the molecular basis of the spinach-P. effusa interaction may enable development of effective management strategies for spinach downy mildew.

Technical Abstract: Downy mildew of spinach is caused by the obligate oomycete pathogen, Peronospora effusa. the disease causes significant economic losses, especially in the organic sector of the industry where the use of synthetic fungicides is not permitted for disease control. New pathotypes of this pathogen are increasingly reported which are capable of breaking resistance. In this study, we took advantage of new spinach genome resources to conduct RNA-seq analyses of transcriptomic changes in leaf tissue of resistant and susceptible spinach cultivars Solomon and Viroflay, respectively, at an early stage of pathogen establishment (48 hours post inoculation, hpi) to a late stage of symptom expression and pathogen sporulation (168 hpi). Fold change differences in gene expression were recorded between the two cultivars to identify candidate genes for resistance. In Solomon, the hypersensitive inducible genes such as pathogenesis-related gene PR-1, glutathione-S-transferase, phospholipid hydroperoxide glutathione peroxidase and peroxidase were significantly up-regulated uniquely at 48 hpi and genes involved in zinc finger CCCH protein, glycosyltransferase, 1-aminocyclopropane-1-carboxylate oxidase homologs, receptor-like protein kinases were expressed at 48 hpi through 168 hpi. The types of genes significantly up-regulated in Solomon in response to the pathogen suggests that salicylic acid and ethylene signaling pathways mediate resistance. Furthermore, many genes involved in the flavonoid and phenylpropanoid pathways were highly expressed in Viroflay compared to Solomon at 168 hpi. As anticipated, an abundance of significantly down-regulated genes was apparent at 168 hpi, reflecting symptom development and sporulation in cultivar Viroflay, but not at 48 hpi. In the pathogen, genes encoding RxLR-type effectors were expressed during early colonization of cultivar Viroflay while crinkler-type effector genes were expressed at the late stage of the colonization. Our results provide insights on gene expression in resistant and susceptible spinach-P. effusa interactions, which can guide future studies to assess candidate genes necessary for downy mildew resistance in spinach.