Effect of cultivars and temperature on synergistic interaction between panicum mosaic virus and satellite panicum mosaic virus in switchgrass

Authors: Muhle, Anthony; Palmer, Nathan - Nate; Edme, Serge; Sarath, Gautam; YUEN, GARY - University Of Nebraska; Mitchell, Robert - Rob; Tatineni, Satyanarayana - Ts

Submitted to: Phytopathology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/29/2022
Publication Date: 3/28/2022
Citation: Muhle, A.A., Palmer, N.A., Edme, S.J., Sarath, G., Yuen, G., Mitchell, R., Tatineni, S. 2022. Effect of cultivars and temperature on synergistic interaction between panicum mosaic virus and satellite panicum mosaic virus in switchgrass. Phytopathology. https://doi.org/10.1007/s00705-022-05412-y.
DOI: https://doi.org/10.1007/s00705-022-05412-y

Interpretive Summary: A productive and successful switchgrass cultivar needs to have good levels of resistance or tolerance to known diseases affecting its performance in forage and bioenergy production systems. To understand the interplay between virus and plants, a greenhouse study was carried out with two switchgrass cultivars, ‘Kanlow’ as a lowland ecotype and ‘Summer’ as an upland ecotype. Both cultivars were challenged with the Panicum mosaic virus (PMV alone) and in combination with its parasite satellite SPMV (i.e. PMV + SPMV). In field studies, Kanlow is known to be resistant and Summer susceptible to these viruses. The plants were observed for visual symptoms and for the number of RNA copies of the virus in their cells at different times after inoculation under two different temperatures (24 C and 32 C). Summer was susceptible to PMV and PMV+SPMV at both temperatures. For Kanlow, the resistance persists at 24 C (no symptoms, localized infections, low number of RNA copies) but not at 32 C, indicating that higher temperatures may overcome it with time. At 24 C, the long-distance movement of the virus in the upper leaves of Kanlow was prevented whereas, at 32 C, the number of RNA copies increased with the PMV+SPMV combination with no corresponding visible symptoms on the plants. These data indicated that resistance in Kanlow switchgrass is expressed in the long-distance and not in the cell-to-cell movement of the virus, as also reported for other viruses. The results also explained that complete resistance does not exist in Kanlow which can be overcome by the synergistic PMV+SPMV interactions under temperatures as high as 32 C and that concurs with field observations.

Technical Abstract: Panicum mosaic virus (PMV), the type member of the genus Panicovirus in the family Tombusviridae, naturally infects switchgrass (Panicum virgatum L.). PMV and its molecular parasite, satellite panicum mosaic virus (SPMV), interact synergistically in co-infected proso millet (Panicum miliaceum L.) and pearl millet [Cenchrus americanus (L.) Morrone] plants with exacerbated disease phenotype and increased accumulation of PMV, compared to plants infected only by PMV. In this study, we examined the reaction of switchgrass cvs. Summer and Kanlow to PMV and PMV+SPMV infections at 24°C and 32°C. Switchgrass cv. Summer was susceptible to PMV and SPMV at both temperatures. In contrast, cv. Kanlow was resistant to PMV and SPMV at 24°C but not at 32°C, suggesting that Kanlow harbors temperature-sensitive resistance against PMV and SPMV. At 24°C, both viruses were readily detected in inoculated leaves but not in upper non-inoculated leaves of Kanlow plants, suggesting that resistance to PMV and SPMV was likely mediated by abrogation of long-distance virus transport but did not impact cell-to-cell movement. Co-infection of cv. Summer with PMV and SPMV caused a mild disease synergism with a slightly increased accumulation of PMV genomic RNA compared to those infected only by PMV. In contrast, no detectable disease synergism was observed in cv. Kanlow plants co-infected with PMV and SPMV. However, co-inoculation of cv. Kanlow by PMV+SPMV caused an enhanced symptomless infection, suggesting a role for SPMV in enhancing symptomless infection in a resistant cultivar. These data suggest that interaction between PMV and SPMV enhanced symptomless infections in virus-resistant switchgrass cultivar that could serve as a source for virus spread and play an important role in panicum mosaic disease epidemiology under field conditions.