HCPro suppression of callose deposition contributes to strain-specific resistance against potato virus Y

Authors: CHOWDHURY, R - University Of Wisconsin; LASKY, DANNY - University Of Wisconsin; Karki, Hari; ZHANG, ZONGYING - University Of Wisconsin; GOYER, AYMERIC - Oregon State University; Halterman, Dennis; RAKOTONDRAFARA, AURELIE - University Of Wisconsin

Submitted to: Phytopathology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/13/2019
Publication Date: 11/29/2019
Citation: Chowdhury, R.N., Lasky, D., Karki, H.S., Zhang, Z., Goyer, A., Halterman, D.A., Rakotondrafara, A.M. 2019. HCPro suppression of callose deposition contributes to strain-specific resistance against potato virus Y. Phytopathology. 110:164-173. https://doi.org/10.1094/PHYTO-07-19-0229-FI.
DOI: https://doi.org/10.1094/PHYTO-07-19-0229-FI

Interpretive Summary: Potato virus Y (PVY) is a global challenge for potato production. New strains of the virus, derived from the recombination of two different strains, is one important contributor as the new strains can overcome resistance in existing potato cultivars. Recently, popular potato cultivars have been released that can harbor the virus, but show no symptoms, leading to viral propagation in both production and seed potato fields. Nytbr is a commonly found PVY-associated resistance gene in potato. It induces hypersensitive resistance (HR) against the ordinary PVYO strain but fails to restrain necrotic strains such as PVYN. Here we show that callose deposition plays a key role in restricting virus movement within the plant in Nytbr-mediated resistance. Callose accumulation was actively induced by PVYO but not by the necrotic strain PVYN:O, which is a recombinant PVY strain. We have identified one gene, called HCPro, within the PVY genome that is capable of inducing callose production in potato plants with Nytbr. We have evidence that the inhibition of callose is sufficient to allow PVYO to spread. Moreover, we uncovered that PVYN:O does not induce callose accumulation (in line with its ability to spread systemically), and is also capable of suppressing callose accumulation when different elicitors are used. Our data suggest that callose suppression is due to increased expression of genes involved in active callose degradation. Our findings will impact future investigations into the mechanisms that allow PVY to elude or suppress resistance responses in potato. The results will also impact the development of effective disease management strategies for PVY in potato.

Technical Abstract: Potato virus Y (PVY) is a global challenge for potato production. One important contributor is the emergence of new viral recombinants and the popularity of potato cultivars that are resistant to specific virus strains, hence changing the PVY population in the fields. Nytbr is a commonly found PVY-associated resistance gene in potato. It induces hypersensitive resistance (HR) against the ordinary PVYO strain but fails to restrain necrotic strains such as PVYN. Here we showed that callose deposition plays a key function in restricting virus movement in Nytbr-mediated resistance. Its deposition was actively induced by PVYO but not by the necrotic strain PVYN:O, which is a recombinant isolate with a genome essentially of O type except for the P1 and HCPro, which resemble PVYN. A similar phenotype was observed with the infiltration with HCPro from PVYO alone, suggesting that HCPro-O may be the determinant for callose induction. We have evidence that the inhibition of callose synthase activity is sufficient to allow PVYO to spread. Moreover, we uncovered that not only does PVYN:O not induce callose accumulation (in line with its ability to spread systemically), but it is also capable of suppressing flagellin-22 induced callose, which correlates with a specific upregulation of b-1-3 glucanase enzyme expression, which is involved in callose degradation.