Interaction of a plant virus protein with the signature Cajal body protein coilin facilitates salicylic acid‐mediated plant defence responses

Abstract

Summary In addition to well‐known roles in RNA metabolism, the nucleolus and Cajal bodies (CBs), both located within the nucleus, are involved in plant responses to biotic and abiotic stress. Previously we showed that plants in which expression of the CB protein coilin is downregulated are more susceptible to certain viruses including tobacco rattle virus (TRV), suggesting a role of coilin in antiviral defence. Experiments with coilin‐deficient plants and the deletion mutant of the TRV 16K protein showed that both 16K and coilin are required for restriction of systemic TRV infection. The potential mechanisms of coilin‐mediated antiviral defence were elucidated via experiments involving co‐immunoprecipitation, use of NahG transgenic plants deficient in salicylic acid (SA) accumulation, measurement of endogenous SA concentrations and assessment of SA‐responsive gene expression. Here we show that TRV 16K interacts with and relocalizes coilin to the nucleolus. In wild‐type plants these events are accompanied by activation of SA‐responsive gene expression and restriction of TRV systemic infection. By contrast, viral systemic spread was enhanced in NahG plants, implicating SA in these processes. Our findings suggest that coilin is involved in plant defence, responding to TRV infection by recognition of the TRV‐encoded 16K protein and activating SA‐dependent defence pathways.

The Cajal Body in Plant-Virus Interactions

“…Nevertheless, whether these functional effects are directly linked to RNA metabolism and/or snRNP formation or, on the contrary, rely on other functions of CBs remains to be clarified. Particularly intriguing is the interplay between CBs and the infection by viruses, which is emerging as a relevant aspect in multiple plant-virus interactions [5,[21][22][23][24][25][26][27][28] (Table 1); the nature of this relationship, however, might vary depending on viral properties as discussed below. In recent years, multiple works have drawn a connection between plant CBs and responses to abiotic and biotic stresses (reviewed in [2]).…”

“…Phenuiviridae, genus Tenuivirus; (−)ssRNA genome), the nuclear inclusion protein A (NIa) from Potato virus A (PVA) (Potyviridae, Potyvirus; (+)ssRNA genome), and the protein encoded by open reading frame 3 (ORF3) from Groundnut rosette virus (GRV) (Tombusviridae, Umbravirus; (+)ssRNA genome) interact with the CB and nucleolar component fibrillarin [21][22][23]25]. The movement protein (TGBp1) from Poa semilatent virus (Virgaviridae, Hordeovirus; (+)ssRNA genome) and the 16K protein from Tobacco rattle virus (Virgaviridae, Tobravirus), on the other hand, interact with the signature CB protein coilin [24,26]. The V2 protein from Tomato yellow leaf curl virus (TYLCV) (Geminiviridae, Begomovirus) interacts with AGO4 mostly in CBs, where it accumulates [27].…”

“…Hordeovirus; (+)ssRNA genome) and the 16K protein from Tobacco rattle virus (Virgaviridae, Tobravirus), on the other hand, interact with the signature CB protein coilin [24,26]. The V2 protein from Tomato yellow leaf curl virus (TYLCV) (Geminiviridae, Begomovirus) interacts with AGO4 mostly in CBs, where it accumulates [27].…”

“…The functional relevance of the CB (or, more specifically, of its signature component coilin) has been assessed in an unbiased manner using transgenic N. benthamiana and tobacco plants in which coilin has been silenced [5,24]. In these plants, CBs cannot be detected, and are therefore a perfect model system to investigate the role of this subnuclear compartment.…”

“…Subsequent investigations shed light on the effect of coilin on the infection by TRV [24]: the TRV-encoded silencing suppressor 16K physically associates with coilin and triggers its re-localization from CBs to the nucleolus, a change that is potentially perceived by the plant, since it correlates with the activation of salicylic acid (SA) accumulation and signaling. In turn, SA responses restrict TRV invasion, allowing for the recovery of the infected plant.…”