Citrus tristeza virus p23: a unique protein mediating key virus–host interactions

Ricardo Flores,Pedro Moreno,Jesús Sánchez-Navarro,Susana Ruiz-Ruiz,Carmelo López,Leandro Peña,Carmen Fagoaga,Luis Navarro,Nuria Soler

doi:10.3389/fmicb.2013.00098

Abstract

The large RNA genome of Citrus tristeza virus (CTV; ca. 20 kb) contains 12 open reading frames, with the 3′-terminal one corresponding to a protein of 209 amino acids (p23) that is expressed from an abundant subgenomic RNA. p23, an RNA-binding protein with a putative zinc-finger domain and some basic motifs, is unique to CTV because no homologs have been found in other closteroviruses, including the type species of the genus Beet yellows virus (despite both viruses having many homologous genes). Consequently, p23 might have evolved for the specific interaction of CTV with its citrus hosts. From a functional perspective p23 has been involved in many roles: (i) regulation of the asymmetrical accumulation of CTV RNA strands, (ii) induction of the seedling yellows syndrome in sour orange and grapefruit, (iii) intracellular suppression of RNA silencing, (iv) elicitation of CTV-like symptoms when expressed ectopically as a transgene in several Citrus spp., and (v) enhancement of systemic infection (and virus accumulation) in sour orange and CTV release from the phloem in p23-expressing transgenic sweet and sour orange. Moreover, transformation of Mexican lime with intron-hairpin constructs designed for the co-inactivation of p23 and the two other CTV silencing suppressors results in complete resistance against the homologous virus. From a cellular point of view, recent data indicate that p23 accumulates preferentially in the nucleolus, being the first closterovirus protein with such a subcellular localization, as well as in plasmodesmata. These major accumulation sites most likely determine some of the functional roles of p23.

Highlights

Citrus tristeza virus (CTV) – a member of the genus Closterovirus, family Closteroviridae – features singular biological and physical properties
CTV is peculiar from a physical standpoint because its monopartite, single-stranded RNA (+) genome (19.3 kb), the largest reported for a plant virus, is organized in 12 open reading frames (ORFs) potentially encoding at least 17 proteins, confined between 5 and 3 untranslated regions (UTRs; Figure 2; Karasev et al, 1995; Mawassi et al, 1996; Vives et al, 1999; Yang et al, 1999)
No significant similarity was observed between p23 and other amino acid sequences deposited in databases (Pappu et al, 1994), a basic motif and some conserved cysteines, found in proteins with RNA-binding properties encoded at the 3 -proximal region of the genomic RNA (gRNA) of some filamentous viruses, suggested that p23 might have RNA-binding properties and be engaged in regulating viral gene expression (Dolja et al, 1994)