Coilin, the signature protein of Cajal bodies, differentially modulates the interactions of plants with viruses in widely different taxa

Abstract

Cajal bodies (CBs) are distinct nuclear bodies physically and functionally associated with the nucleolus. In addition to their traditional function in coordinating maturation of certain nuclear RNAs, CBs participate in cell cycle regulation, development, and regulation of stress responses. A key "signature" component of CBs is coilin, the scaffolding protein essential for CB formation and function. Using an RNA silencing (loss-of-function) approach, we describe here new phenomena whereby coilin also affects, directly or indirectly, a variety of interactions between host plants and viruses that have RNA or DNA genomes. Moreover, the effects of coilin on these interactions are manifested differently: coilin contributes to plant defense against tobacco rattle virus (tobravirus), tomato black ring virus (nepovirus), barley stripe mosaic virus (hordeivirus), and tomato golden mosaic virus (begomovirus). In contrast, with potato virus Y (potyvirus) and turnip vein clearing virus (tobamovirus), coilin serves to increase virus pathogenicity. These findings show that interactions with coilin (or CBs) may involve diverse mechanisms with different viruses and that these mechanisms act at different phases of virus infection. Thus, coilin (CBs) has novel, unexpected natural functions that may be recruited or subverted by plant viruses for their own needs or, in contrast, are involved in plant defense mechanisms that suppress host susceptibility to the viruses.

Cajal bodies and their role in plant stress and disease responses

“…18 In addition to being responsive to such cues, it has been suggested that CBs could perhaps participate in the transduction of these signals and also those of other biological processes such as cell cycle, development and abiotic stress mitigation, 18 gene silencing and non-sense mediated decay (reviewed in 19 ); suggesting new and unexpected functions for these sub-nuclear compartments. Moreover, in just the past decade CBs have been discovered to play a critical role in modulating some virus infections, 20,21 either by providing viruses with some functions required for their replication, or by enhancing host defense mechanisms against viruses. Thus, these enigmatic sub-nuclear bodies are emerging as highly complex and multifunctional regulatory compartments, and model systems including plants, have implicated CBs in a surprisingly diverse range of biological mechanisms which we are only just beginning to understand.…”

The Nucleolar Fibrillarin Protein Is Required for Helper Virus-Independent Long-Distance Trafficking of a Subviral Satellite RNA in Plants

“…(B) Accumulation of satBaMV RNA, coilin, and fibrillarin mRNA and fibrillarin protein in N. benthamiana leaves from satBaMV transgenic stock and grafted wild-type, fibrillarin, and coilin RNAi (Shaw et al, 2014) transgenic scions. RNA and protein analysis were performed at 9 DAG as described in (A).…”

“…To further confirm that satBaMV systemic movement without HV depends on fibrillarin, we grafted the N. benthamiana fibrillarin knockdown line (Shaw et al, 2014) onto satBaMV transgenic plants. RNAi knockdown of coilin, encoding one of the main components of Cajal bodies (Ogg and Lamond, 2002), served as a control.…”

“…Coilin RNAi transgenic N. benthamiana plants were previously characterized (Shaw et al, 2014). Transformation and regeneration of fibrillarin and coilin RNAi transgenic plants were as previously described (Taliansky et al, 2004).…”

“…The transgenic N. tabacum line expressing satCMV driven by the 35S promoter was a gift from Yau-Heiu Hsu (National Chung Hsing University, Taichung, Taiwan). The Plant Cell Fibrillarin RNAi transgenic N. benthamiana plants were generated by transformation with Agrobacterium tumefaciens LBA4404 carrying the plasmid pFGC5941.Fibrillarin39, as described for coilin RNAi plants (Shaw et al, 2014). The plasmid consisted of a 321-bp fragment (region 501 to 821) of the N. benthamiana fibrillarin gene (AM269909) cloned in opposite orientations flanking the CHALCONE SYNTHASE intron.…”