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

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Abstract

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Overexpression of a tomato TCTP impacts plant biomass production and performance under stress. These phenotypic alterations were associated with the up-regulation of genes mainly related to photosynthesis, fatty acid metabolism and water transport.

Abstract

The translationally controlled tumor protein (TCTP) is a multifaceted and highly conserved eukaryotic protein. In plants, despite the existence of functional data implicating this protein in cell proliferation and growth, the detailed physiological roles of many plant TCTPs remain poorly understood. Here we focused on a yet uncharacterized TCTP from tomato (SlTCTP). We show that, when overexpressed in tobacco, SlTCTP may promote plant biomass production and affect performance under salt and osmotic stress. Transcriptomic analysis of the transgenic plants revealed the up-regulation of genes mainly related to photosynthesis, fatty acid metabolism and water transport. This induced photosynthetic gene expression was paralleled by an increase in the photosynthetic rate and stomatal conductance of the transgenic plants. Moreover, the transcriptional modulation of genes involved in ABA-mediated regulation of stomatal movement was detected. On the other hand, genes playing a pivotal role in ethylene biosynthesis were found to be down-regulated in the transgenic lines, thus suggesting deregulated ethylene accumulation in these plants. Overall, these results point to a role of TCTP in photosynthesis and hormone signaling.

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Acknowledgements

We are grateful to Poliane Alfenas-Zerbini (Universidade Federal de Viçosa - UFV) for providing the polyclonal antibody against SlTCTP. M. de Carvalho was recipient of a Ph.D. fellowship from FAPESP (2011/10309-3). L. M. de Araújo and M. L. C. Arcuri were recipients of undergraduate FAPESP fellowships (2011/17462-1 and 2014/03241-1). M. L. Acencio was a recipient of a PNPD/CAPES postdoctoral fellowship. I. G. Maia is recipient of a research fellowship from CNPq.

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Correspondence to Ivan G. Maia.

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Communicated by Marcelo Menossi.

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299_2017_2117_MOESM1_ESM.tif

Fig. S1. Photographs showing increased lateral root formation of representative seedlings from the SlTCTP-OE lines grown under control and mannitol-stressed conditions. WT – wild-type nontransgenic seedlings (TIF 641 KB)

299_2017_2117_MOESM2_ESM.jpg

Fig. S2. R2 linear regression of the RNA-Seq data from both SlTCTP-OE lines (TCTP7 and TCTP8). The R2 values were calculated using the Sigma Stat package based on the RPKM values derived from RNA-Seq data and after eliminating genes with zero count (JPG 16 KB)

299_2017_2117_MOESM3_ESM.jpg

Fig. S3. Gene Ontology (GO) analysis of the up-regulated differentially expressed genes. The distribution within the three main GO categories (CC- cellular component; MF - molecular function; BP - biological process) is shown. Only DEGs that were in common between the two SlTCTP-OE lines (TCTP7 and TCTP8) were included in the analysis (JPG 101 KB)

299_2017_2117_MOESM4_ESM.jpg

Fig. S4. Gene Ontology (GO) analysis of the down-regulated differentially expressed genes. The distribution within the three main GO categories (CC- cellular component; MF - molecular function; BP - biological process) is shown. Only DEGs that were in common between the two SlTCTP-OE lines (TCTP7 and TCTP8) were included in the analysis (JPG 44 KB)

299_2017_2117_MOESM5_ESM.jpg

Fig. S5. Non-parametric Spearman correlation analysis of RNA-Seq and RT-qPCR expression data. Nine up-regulated (panels A and C) and eight down-regulated (panels B and D) genes were selected for validation and a Spearman’s correlation was calculated based on the expression values generated for each transgenic OE line (TCTP7 and TCTP8). Correlation coefficients (r) are indicated for each comparison. Asterisks denote statistically significant correlations (*p value between 0.01 and 0.05; **p value between 0.0001 and 0.01) (JPG 89 KB)

299_2017_2117_MOESM6_ESM.jpg

Fig. S6. RT-qPCR validation of a chosen set of differentially expressed genes. (A) Validation of the selected up-regulated genes. (B) Validation of the selected down-regulated genes. WT expression was used as calibrator and arbitrarily set to 1. Bars indicate standard errors of triplicate reactions. Asterisks denote significant differences between WT and OE lines (*p<0.05; **p<0.01; ***p<0.0001) (JPG 139 KB)

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de Carvalho, M., Acencio, M.L., Laitz, A.V.N. et al. Impacts of the overexpression of a tomato translationally controlled tumor protein (TCTP) in tobacco revealed by phenotypic and transcriptomic analysis. Plant Cell Rep 36, 887–900 (2017). https://doi.org/10.1007/s00299-017-2117-0

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