Dissecting the transcriptional response to elicitors in Vitis vinifera cells.

Lorena Almagro,Sarai Belchí-Navarro,María A Pedreño,Pablo Carbonell-Bejerano,Diego Lijavetzky,José M Martínez-Zapater,Roque Bru,Guangxiao Yang

doi:10.1371/journal.pone.0109777

Abstract

The high effectiveness of cyclic oligosaccharides like cyclodextrins in the production of trans-resveratrol in Vitis vinifera cell cultures is enhanced in the presence of methyl jasmonate. In order to dissect the basis of the interactions among the elicitation responses triggered by these two compounds, a transcriptional analysis of grapevine cell cultures treated with cyclodextrins and methyl jasmonate separately or in combination was carried out. The results showed that the activation of genes encoding enzymes from phenylpropanoid and stilbene biosynthesis induced by cyclodextrins alone was partially enhanced in the presence of methyl jasmonate, which correlated with their effects on trans-resveratrol production. In addition, protein translation and cell cycle regulation were more highly repressed in cells treated with cyclodextrins than in those treated with methyl jasmonate, and this response was enhanced in the combined treatment. Ethylene signalling was activated by all treatments, while jasmonate signalling and salicylic acid conjugation were activated only in the presence of methyl jasmonate and cyclodextrins, respectively. Moreover, the combined treatment resulted in a crosstalk between the signalling cascades activated by cyclodextrins and methyl jasmonate, which, in turn, provoked the activation of additional regulatory pathways involving the up-regulation of MYB15, NAC and WRKY transcription factors, protein kinases and calcium signal transducers. All these results suggest that both elicitors cause an activation of the secondary metabolism in detriment of basic cell processes like the primary metabolism or cell division. Crosstalk between cyclodextrins and methyl jasmonate-induced signalling provokes an intensification of these responses resulting in a greater trans-resveratrol production.

Highlights

Vitis vinifera produces stilbenes, which are a small group of compounds characterized by a 1,2-diphenylethylene backbone
RNA samples obtained from the four treatments (C, methyl jasmonate (MJ), CD and CDMJ) at 0 and 24 h were used for the gene expression analyses
Cyclodextrins and/or methyl jasmonate induced the biosynthesis of defense-related proteins

Summary

Introduction

Vitis vinifera produces stilbenes, which are a small group of compounds characterized by a 1,2-diphenylethylene backbone. The activation of stilbene biosynthesis by particular elicitors is well-documented in grapevine, where the expression of STS genes and the production of stilbenes are induced upon elicitation with different fungal pathogens [18,19]. Cyclodextrins (CD) are cyclic oligosaccharides that chemically resemble to the pectic oligosaccharides naturally released from the cell walls during a fungal attack [2] They act as true elicitors since they provoke stilbene accumulation and induce the accumulation of new gene products like peroxidases, b-1,3-glucanases and chitinases [23,24]. MartınezEsteso et al [25] observed that enzymes from the trans-R biosynthesis pathway like STS were up-regulated by CD in grapevine (V. vinifera cv Gamay) cell cultures. We identified regulators which are activated in each treatment and discussed their possible involvement in the control of different physiological processes as well as the putative interaction of physiological and cellular responses giving rise to the synergistic accumulation of trans-R in the combined treatment

Results

Discussion

Experimental Procedures