Effect of temperature on the pathogenesis, accumulation of viral and satellite RNAs and on plant proteome in peanut stunt virus and satellite RNA-infected plants

Abstract

Temperature is an important environmental factor influencing plant development in natural and diseased conditions. The growth rate of plants grown at C27°C is more rapid than for plants grown at 21°C. Thus, temperature affects the rate of pathogenesis progression in individual plants. We have analyzed the effect of temperature conditions (either 21°C or 27°C during the day) on the accumulation rate of the virus and satellite RNA (satRNA) in Nicotiana benthamiana plants infected by peanut stunt virus (PSV) with and without its satRNA, at four time points. In addition, we extracted proteins from PSV and PSV plus satRNA-infected plants harvested at 21 dpi, when disease symptoms began to appear on plants grown at 21°C and were well developed on those grown at 27°C, to assess the proteome profile in infected plants compared to mock-inoculated plants grown at these two temperatures, using 2D-gel electrophoresis and mass spectrometry approaches. The accumulation rate of the viral RNAs and satRNA was more rapid at 27°C at the beginning of the infection and then rapidly decreased in PSV-infected plants. At 21 dpi, PSV and satRNA accumulation was higher at 21°C and had a tendency to increase further. In all studied plants grown at 27°C, we observed a significant drop in the identified proteins participating in photosynthesis and carbohydrate metabolism at the proteome level, in comparison to plants maintained at 21°C. On the other hand, the proteins involved in protein metabolic processes were all more abundant in plants grown at 27°C. This was especially evident when PSV-infected plants were analyzed, where increase in abundance of proteins involved in protein synthesis, degradation, and folding was revealed. In mock-inoculated and PSV-infected plants we found an increase in abundance of the majority of stress-related differently-regulated proteins and those associated with protein metabolism. In contrast, in PSV plus satRNA-infected plants the shift in the temperature barely increased the level of stress-related proteins.

The Defense Response of Nicotiana benthamiana to Peanut Stunt Virus Infection in the Presence of Symptom Exacerbating Satellite RNA

“…Genes involved in photosynthesis were down-regulated in both PSV-G and PSV-G + satRNA infected plants, but in the latter case the number of DEGs and their fold-change were much bigger. Similar observations have been reported in numerous plant–virus pathosystems [ 19 , 24 , 47 , 48 , 49 ], which suggests that this is a relatively common phenomenon and that cellular photosynthetic components participate in plant immunity signaling [ 50 ]. This finding is directly associated with another observation; that is, the cellular component severely affected during PSV infection was chloroplast, involving DEGs that encode proteins that are components of the chloroplast thylakoid membrane, chloroplast envelope, stroma, and photosystem.…”

“…The latter case was found to occur in PSV-induced pathogenesis in N. benthamiana plants. It was shown that plants infected with PSV-P, which was naturally associated with satRNA, react differently to the satRNA presence under various temperature conditions, delaying or exacerbating and accelerating symptoms of disease [ 24 ]. On the other hand, addition of the same satRNA to PSV-G strain under all temperature conditions accelerated and enhanced symptoms on N. benthamiana plants.…”

Effects of Grapevine leafroll‐associated virus 3 on the physiology in asymptomatic plants of Vitis vinifera

“…Surprisingly, the results obtained in 2012 showed a completely opposite trend with an increase in virus population during these 2 months. This different trend between both years could be attributed to differences in mean daily temperatures during these growing seasons, because temperature during plant growth could affect the rate of pathogenesis progression in individual plants (Obrępalska‐Stęplowska et al ., ). During summer of 2012, the highest mean daily temperature value was registered in August, while in 2013 it was slightly lower and registered in July (Fig.…”

Impact of Abiotic Stresses on Plant Virus Transmission by Aphids

“…The authors assumed that the higher temperature prohibited virus replication and movement due to the activation of plant defence mechanisms [85,99]. Similarly, viral accumulation of the cucumovirus Peanut stunt virus showed a rapid increase at the beginning of the infection at a higher temperature (27 • C vs. 21 • C), followed by a dramatic decrease in N. benthamiana plants due to the induction of plant defences [100].…”