Plant Poly(ADP-Ribose) Polymerase 1 Is a Potential Mediator of Cross-Talk between the Cajal Body Protein Coilin and Salicylic Acid-Mediated Antiviral Defence

Abstract

The nucleolus and Cajal bodies (CBs) are sub-nuclear domains with well-known roles in RNA metabolism and RNA-protein assembly. However, they also participate in other important aspects of cell functioning. This study uncovers a previously unrecognised mechanism by which these bodies and their components regulate host defences against pathogen attack. We show that the CB protein coilin interacts with poly(ADP-ribose) polymerase 1 (PARP1), redistributes it to the nucleolus and modifies its function, and that these events are accompanied by substantial increases in endogenous concentrations of salicylic acid (SA), activation of SA-responsive gene expression and callose deposition leading to the restriction of tobacco rattle virus (TRV) systemic infection. Consistent with this, we also find that treatment with SA subverts the negative effect of the pharmacological PARP inhibitor 3-aminobenzamide (3AB) on plant recovery from TRV infection. Our results suggest that PARP1 could act as a key molecular actuator in the regulatory network which integrates coilin activities as a stress sensor for virus infection and SA-mediated antivirus defence.

Cell Fractionation and the Identification of Host Proteins Involved in Plant–Virus Interactions

“…Nucleolar localization of the ORF3 protein is essential for the formation of viral ribonucleoprotein particles capable of intercellular movement leading to systemic infection [35]. Tobacco rattle virus (TRV) infection induces nucleolar re-distribution of coilin via a mechanism that is dependent on TRV protein 16K interacting with Poly(ADP-ribose) polymerase 1 (PAR1), a key regulator of salicylic acid mediated defense [71]. This is critical for viruses causing important diseases that have not been extensively studied such as Maize chlorotic mottle virus, a causal agent of maize lethal necrosis disease [72].…”

Coilin and Cajal bodies

“…Upon activation, PARP and other PARylated proteins accumulate in CBs [ 119 ]. PARP localization to CB correlates with increased production of salicylic acid, which has also been linked to the antiviral function of coilin [ 120 , 121 ]. In animals, PML bodies are involved in innate antiviral immunity (reviewed in [ 40 ].…”

Viruses and Cajal Bodies: A Critical Cellular Target in Virus Infection?

“…A stable interaction of 16K and coilin has been demonstrated in vitro, as well as the nucleolar localisation of coilin via interaction with 16K in WT plants [141]. A molecule, poly(ADP-ribose) polymerase 1 (PARP-1), that links the processes of SA-activated gene expression and plant resistance to TRV infection has recently been identified and can also participate in the coilin/16K complex [154].…”