Genome-wide analysis of the grapevine stilbene synthase multigenic family: genomic organization and expression profiles upon biotic and abiotic stresses

Abstract

BackgroundPlant stilbenes are a small group of phenylpropanoids, which have been detected in at least 72 unrelated plant species and accumulate in response to biotic and abiotic stresses such as infection, wounding, UV-C exposure and treatment with chemicals. Stilbenes are formed via the phenylalanine/polymalonate-route, the last step of which is catalyzed by the enzyme stilbene synthase (STS), a type III polyketide synthase (PKS). Stilbene synthases are closely related to chalcone synthases (CHS), the key enzymes of the flavonoid pathway, as illustrated by the fact that both enzymes share the same substrates. To date, STSs have been cloned from peanut, pine, sorghum and grapevine, the only stilbene-producing fruiting-plant for which the entire genome has been sequenced. Apart from sorghum, STS genes appear to exist as a family of closely related genes in these other plant species.ResultsIn this study a complete characterization of the STS multigenic family in grapevine has been performed, commencing with the identification, annotation and phylogenetic analysis of all members and integration of this information with a comprehensive set of gene expression analyses including healthy tissues at differential developmental stages and in leaves exposed to both biotic (downy mildew infection) and abiotic (wounding and UV-C exposure) stresses. At least thirty-three full length sequences encoding VvSTS genes were identified, which, based on predicted amino acid sequences, cluster in 3 principal groups designated A, B and C. The majority of VvSTS genes cluster in groups B and C and are located on chr16 whereas the few gene family members in group A are found on chr10. Microarray and mRNA-seq expression analyses revealed different patterns of transcript accumulation between the different groups of VvSTS family members and between VvSTSs and VvCHSs. Indeed, under certain conditions the transcriptional response of VvSTS and VvCHS genes appears to be diametrically opposed suggesting that flow of carbon between these two competing metabolic pathways is tightly regulated at the transcriptional level.ConclusionsThis study represents an overview of the expression pattern of each member of the STS gene family in grapevine under both constitutive and stress-induced conditions. The results strongly indicate the existence of a transcriptional subfunctionalization amongst VvSTSs and provide the foundation for further functional investigations about the role and evolution of this large gene family. Moreover, it represents the first study to clearly show the differential regulation of VvCHS and VvSTS genes, suggesting the involvement of transcription factors (TFs) in both the activation and repression of these genes.

Regulation of stilbene biosynthesis in plants

“…The available literature data demonstrate that STS genes in sorghum, spruce, pine, peanut, and mulberry form small gene families composed of 1-10 members (Preisig-Müller et al 1999;Yu et al 2005;Paterson et al 2009;Zhu et al 2014;Warren et al 2015;Li et al 2016), while STS gene family in grapevine consists of 48 STS genes with at least 32 potentially functional ones as revealed by the genomewide analysis of the grapevine genome (Vannozzi et al 2012;Parage et al 2012). Functional analysis of nine STS genes representing most diversity of the STS gene family in grapevine performed by Parage et al (2012) revealed that the genes encode proteins possessing STS activity.…”

“…However, there are currently no clear experimental data whether grapevine and other plant STS proteins in each multigene family differ in their enzyme activities and specificity for stilbene biosynthesis. The expressional analyses of the STS gene family members in grapevine and mulberry revealed that some STS genes exhibit differences in transcriptional responses during development and in response to environmental stresses (Vannozzi et al 2012;Shi et al 2014;Dai et al 2012). There were also differences in tissue-specific expression of some grapevine and mulberry STS gene family members (Vannozzi et al 2012;Shi et al 2014;Li et al 2016).…”

“…The expressional analyses of the STS gene family members in grapevine and mulberry revealed that some STS genes exhibit differences in transcriptional responses during development and in response to environmental stresses (Vannozzi et al 2012;Shi et al 2014;Dai et al 2012). There were also differences in tissue-specific expression of some grapevine and mulberry STS gene family members (Vannozzi et al 2012;Shi et al 2014;Li et al 2016). Therefore, it is possible that distinct STS genes can be activated under various developmental or environmental cues or in different plant tissues leading to accumulation of stilbenes.…”

“…and -UV-B treatments was statistically significant. Vannozzi et al (2012) recently performed a genome-wide analysis of the STS multigenic family expression profiles in V. vinifera after UV-C exposure, wounding, post-harvest berry withering, and infection with P. viticola by a whole transcriptome (mRNA-seq) and quantitative RT-PCR approaches. According to the results obtained, all treatments resulted in a considerable up-regulation of expression of at least several members of the multigenic VvSTS gene family.…”

Research Article Coupled transcript and metabolite identification: insights on induction and synthesis of resveratrol in peanut, wild relatives and synthetic allotetraploid.

“…Resveratrol is synthesized by a one-step reaction (Hanhineva et al, 2009) of resveratrol synthase gene (RS) that is differentially regulated under different stimuli and in different tissues (Chung et al, 2003) and belongs to a large multigene family (Vannozzi et al, 2012). Arachis hypogaea RS genes were already cloned (Schröder et al, 1988;Huang et al, 2012).…”