Innate resistance and phosphite treatment affect both the pathogen’s and host’s transcriptomes in the Tanoak-Phytophthora ramorum pathosystem

Authors: Kasuga, Takao; HAYDEN, KATHERINE - Institut National De La Recherche Agronomique (INRA); EYRE, CATHERINE - University Of California; CROUCHER, PETER - University Of California; SCHECHTER, SHANNON - University Of California; WRIGHT, JESSICA - Us Forest Service (FS); GARBELOTTO, MATTEO - University Of California

Submitted to: The Journal of Fungi
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/6/2021
Publication Date: 3/9/2021
Citation: Kasuga, T., Hayden, K., Eyre, C., Croucher, P., Schechter, S., Wright, J., Garbelotto, M. 2021. Innate resistance and phosphite treatment affect both the pathogen’s and host’s transcriptomes in the Tanoak-Phytophthora ramorum pathosystem. The Journal of Fungi. 7(3). Article 198. https://doi.org/10.3390/jof7030198.
DOI: https://doi.org/10.3390/jof7030198

Interpretive Summary: Tanoak is highly susceptible to the Sudden Oak Death Pathogen, Phytophthora ramorum, however, resistance lineages do exist. Phosphite compounds have been used in the control of the disease. Susceptible tanoak plants behave as resistance after phosphite treatment. In this research we first identified tanoak lineages that were tolerant to sudden oak death as well as those susceptible but responded effectively to phosphite treatment. We found that a set of genes were active among naturally resistant trees in comparison to susceptible trees. We also found that the same set of genes were activated in susceptible trees in response to phosphite treatment.

Technical Abstract: Phosphite compounds have been used in the control of sudden oak death; however, their precise mode of action is not fully understood. To study the action of phosphite in the context of naturally occurring host resistance, we first identified two open-pollinated family groups of tanoak that carried resistance. Stems at soil line were sprayed with phosphite, and 7 days later distal leaves were inoculated with the sudden oak death pathogen Phytophthora ramorum. Leaves were harvested before and seven days after inoculation for RNA extraction and transcriptomes of the host as well as the pathogen were analyzed. We found that tanoak families differed in the presence of innate resistance and in the effectiveness of phosphite treatment. Gene set enrichment analysis of GO terms and KEGG pathway was used to search for group of genes enriched in specific treatments or genetic makeup. There was little overlap between the sets of genes associated with innate immunity and also phosphite-induced immunity between tree families. However, within the same tree family, sets of genes for innate immunity and phosphite-induced immunity largely overlap, supporting the hypothesis that phosphite treatment increases the resistance of susceptible host plants to Phytophthora infection. In addition, our dual RNA-seq enabled to monitor gene regulation of the pathogen in planta. It was found that when P. ramorum was in tanoak foliage, genes for energy generation such as those in TCA cycle and genes for amino acid membrane transporters were upregulated whereas elicitin genes were downregulated relative to mycelium in the culture medium. We also found that genes involved in detoxification such as ATP-binding cassette (ABC) transporters and vitamin B6 biosynthesis genes were upregulated in the pathogen in phosphite-treated plants in relation to that in untreated plants. Upregulation of these genes have been observed for axenic culture of P. cinnamomi in the presence of phosphite, indicating these genes responded to the direct toxicity of phosphite. In summary, our dual RNA seq support the mode of action of phosphite compounds; direct toxic effect on P. ramorum and enhancing resistance of the tanoak host.