Abstract
Plant viruses cause a range of plant diseases symptoms that are often responsible for significant crop production losses and the severity and spread of the symptoms may be affected by climate change. While the increase in anthropogenic activities has caused a critical problem of increased CO2 levels in the atmosphere, these elevated CO2 levels have been reported to reduce virus disease severity in some plant species. In such instances, it is not clear if the plant defense mechanisms are being enhanced or virus-mediated mechanisms to overcome plant resistance are being defeated. Additionally, a few studies have been attempted in this area to determine if reduced disease is the norm or the exception under enhanced CO2 levels. In the present study, the effects of elevated CO2 levels (750 ppm vs. 390 ppm) on RNAi-mediated resistance of Nicotiana tabacum against the cucumber mosaic virus (CMV), and the activity of viral suppressor of RNAi (VSR) 2b protein of CMV were evaluated. On the one hand, our results showed that elevated CO2 decreased the transcription of dicer-like protein 2 (DCL2), DCL4, and argonaut 1 (AGO1) genes with functions related to RNAi-mediated resistance when infected by CMV, which is contradictory with the decreased CMV copy numbers under elevated CO2. On the other hand, we found that elevated CO2 increased the calcium concentration and expression of the calcium-binding protein rgs-CaM in tobacco plants when infected by CMV, which directly weakened the function of 2b protein, the VSR of CMV, and therefore decreased the infection efficiency of the virus and suppressed the severity of CMV in tobacco plants under elevated CO2. This study provides molecular insights into the ecological implications underlying the development of prevention strategies against plant virus infection in the context of climate change.
Highlights
The atmospheric CO2 concentration has risen from 280 ppm to 400 ppm since the industrial revolution, and is predicted to reach 540–900 ppm by the end of this century [1]
We propose two hypotheses underlying the positive effects of elevated CO2 on plant RNA-silencing processes against viruses: (1) elevated CO2 enhances the key genes involved in plant RNA-silencing processes against viruses and (2) elevated CO2 activates the host factor calmodulin to suppress the viral suppressor of RNA interference (RNAi) (VSR) activity and subsequently relieve the RNA-silencing ability of host plants
Our specific goals were to determine: (1) how elevated CO2 affected cucumber mosaic virus (CMV) severity associated with tobacco plants; (2) whether elevated CO2 directly affected the RNA-silencing related key gene expression of wild-type plants when infected by CMV; and (3) whether elevated CO2 affected the 2b protein expression of CMV by altering the calcium signal and downstream calmodulin expression and whether the changes in 2b protein would, in turn, affect the RNA-silencing ability of plants
Summary
The atmospheric CO2 concentration has risen from 280 ppm to 400 ppm since the industrial revolution, and is predicted to reach 540–900 ppm by the end of this century [1]. Cellular RNA-dependent RNA polymerases (RDRs) that use single-stranded RNA (ssRNA) to amplify long, perfect dsRNA [19], which serve as a substrate for the DCL-dependent formation of secondary vsiRNAs [17] These vsiRNAs are degraded by the core components of the RNA-induced silencing complex (RISC) argonaut (AGO) protein [18]. Once 2b protein is mutated, Nicotiana benthamiana and Arabidopsis do not exhibit the disease symptoms It seems that the activity of 2b protein in CMV is a determinant for the infection efficiency of the virus. It was speculated that the effects of elevated CO2 on host calcium concentration and calmodulin gene expression may affect the VSR activity and the interaction between plants and viruses. Our specific goals were to determine: (1) how elevated CO2 affected CMV severity associated with tobacco plants; (2) whether elevated CO2 directly affected the RNA-silencing related key gene expression of wild-type plants when infected by CMV; and (3) whether elevated CO2 affected the 2b protein expression of CMV by altering the calcium signal and downstream calmodulin expression and whether the changes in 2b protein would, in turn, affect the RNA-silencing ability of plants
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