Translationally controlled tumour protein (TCTP) from tomato and Nicotiana benthamiana is necessary for successful infection by a potyvirus

Abstract

Translationally controlled tumour protein (TCTP) is a ubiquitously distributed protein in eukaryotes, involved in the regulation of several processes, including cell cycle progression, cell growth, stress protection, apoptosis and maintenance of genomic integrity. Its expression is induced during the early stages of tomato (Solanum lycopersicum) infection by the potyvirus Pepper yellow mosaic virus (PepYMV, a close relative of Potato virus Y). Tomato TCTP is a protein of 168 amino acids, which contains all the conserved domains of the TCTP family. To study the effects of TCTP silencing in PepYMV infection, Nicotiana benthamiana plants were silenced by virus-induced gene silencing (VIGS) and transgenic tomato plants silenced for TCTP were obtained. In the early stages of infection, both tomato and N. benthamiana silenced plants accumulated less virus than control plants. Transgenic tomato plants showed a drastic reduction in symptoms and no viral accumulation at 14 days post-inoculation. Subcellular localization of TCTP was determined in healthy and systemically infected N. benthamiana leaves. TCTP was observed in both the nuclei and cytoplasm of non-infected cells, but only in the cytoplasm of infected cells. Our results indicate that TCTP is a growth regulator necessary for successful PepYMV infection and that its localization is altered by the virus, probably to favour the establishment of virus infection. A network with putative interactions that may occur between TCTP and Arabidopsis thaliana proteins was built. This network brings together experimental data of interactions that occur in other eukaryotes and helps us to discuss the possibilities of TCTP involvement in viral infection.

Impacts of the overexpression of a tomato translationally controlled tumor protein (TCTP) in tobacco revealed by phenotypic and transcriptomic analysis

“…Of note, since TCTP is highly regulated at the translational level, its accumulation in these transgenic lines may vary significantly as already evidenced for AtTCTP1 in Arabidopsis (only 50% increase at the protein level despite a 13-fold increase in gene expression; Berkowitz et al 2008). Consistent with this, the severity of the phenotypic alterations associated with the silencing of SlTCTP in tomato was directly correlated with the efficiency of gene knockdown (Bruckner et al 2016). Alternatively, the additive effect of the endogenous NtTCTP on the growth of the SlTCTP-OE plants could be envisaged.…”

“…It should be emphasized that SlTCTP shows 80% amino acid identity with NtTCTP. Also noteworthy, some of the described phenotypic alterations caused by the silencing of SlTCTP in tomato, such as stunting, modified inflorescence habit and abnormal fruit morphology (Bruckner et al 2016), resemble ethylene-associated pleiotropic effects reported in tomato (Lin et al 2008). In addition, the fact that the SlTCTP-OE lines exhibited enhanced lateral root…”

“…3a, b). Interestingly, an opposite behavior was detected in transgenic tomato lines with strong knockdown of SlTCTP expression (about 94-97% of the WT level), which exhibited stunted growth and delayed development compared to WT plants (Bruckner et al 2016).…”

“…In the present study we focused on a tomato (Solanum lycopersicum L.) TCTP coding gene (SlTCTP; Gene ID 543941) previously reported to be induced by virus infection (Alfenas-Zerbini et al 2009). Interestingly, effective knockdown of SlTCTP in tomato resulted in reduced plant stature, abnormal fruit morphology and decreased seed size (Bruckner et al 2016). Here, the functional relevance of SlTCTP in plants was assessed by its overexpression in transgenic tobacco plants and evaluation of the resultant phenotypic alterations.…”

The Two Translationally Controlled Tumor Protein Genes, CsTCTP1 and CsTCTP2, Are Negative Modulators in the Cucumis sativus Defense Response to Sphaerotheca fuliginea

“…Emerging evidence suggests a role of plant TCTP in growth regulation and programmed cell death control ( Berkowitz et al, 2008 ; Toscano-morales et al, 2015 ; Chou et al, 2016 ). Plant TCTP was also recently found to respond to pathogen stress ( Li et al, 2010 ; Hinojosamoya et al, 2013 ; Bruckner et al, 2017 ). In our previous work, we found that TCTP (XP-004134215) was significantly differentially expressed between two sister cucumber lines (genotypes that were either highly resistant or highly susceptible to S. fuliginea ) by 2-D gel electrophoresis ( Fan et al, 2014 ).…”