Activation of senescence-associated Dark-inducible (DIN) genes during infection contributes to enhanced susceptibility to plant viruses

Abstract

Virus infections in plants cause changes in host gene expression that are common to other environmental stresses. In this work, we found extensive overlap in the transcriptional responses between Arabidopsis thaliana plants infected with Tobacco rattle virus (TRV) and plants undergoing senescence. This is exemplified by the up-regulation during infection of several senescence-associated Dark-inducible (DIN) genes, including AtDIN1 (Senescence 1, SEN1), AtDIN6 (Asparagine synthetase 1, AtASN1) and AtDIN11. DIN1, DIN6 and DIN11 homologues were also activated in Nicotiana benthamiana in response to TRV and Potato virus X (PVX) infection. Reduced TRV levels in RNA interference (RNAi) lines targeting AtDIN11 indicate that DIN11 is an important modulator of susceptibility to TRV in Arabidopsis. Furthermore, low accumulation of TRV in Arabidopsis protoplasts from RNAi lines suggests that AtDIN11 supports virus multiplication in this species. The effect of DIN6 on virus accumulation was negligible in Arabidopsis, perhaps as a result of gene or functional redundancy. However, TRV-induced silencing of NbASN, the DIN6 homologue in N. benthamiana, compromises TRV and PVX accumulation in systemically infected leaves. Interestingly, NbASN inactivation correlates with the appearance of morphological defects in infected leaves. We found that DIN6 and DIN11 regulate virus multiplication in a step prior to the activation of plant defence responses. We hypothesize on the possible roles of DIN6 and DIN11 during virus infection.

Keywords: Arabidopsis thaliana; Dark-inducible (DIN) genes; Nicotiana benthamiana; Potato virus X; Tobacco rattle virus; plant viruses; senescence-associated genes.