ABSTRACT
The molecular mechanisms associated with secondary cell wall (SCW) deposition in sorghum remain largely uncharacterized. Here, we employed untargeted metabolomics and large-scale transcriptomics to correlate changes in SCW deposition with variation in global gene expression profiles and metabolite abundance along an elongating internode of sorghum, with a major focus on lignin and phenolic metabolism. To gain deeper insight into the metabolic and transcriptional changes associated with pathway perturbations, a bmr6 mutant [with reduced cinnamyl alcohol dehydrogenase (CAD) activity] was analyzed. In the wild type, internode development was accompanied by an increase in the content of oligolignols, p-hydroxybenzaldehyde, hydroxycinnamate esters, and flavonoid glucosides, including tricin derivatives. We further identified modules of genes whose expression pattern correlated with SCW deposition and the accumulation of these target metabolites. Reduced CAD activity resulted in the accumulation of hexosylated forms of hydroxycinnamates (and their derivatives), hydroxycinnamaldehydes, and benzenoids. The expression of genes belonging to one specific module in our co-expression analysis correlated with the differential accumulation of these compounds and contributed to explaining this metabolic phenotype. Metabolomics and transcriptomics data further suggested that CAD perturbation activates distinct detoxification routes in sorghum internodes. Our systems biology approach provides a landscape of the metabolic and transcriptional changes associated with internode development and with reduced CAD activity in sorghum.
Subject(s)
Sorghum , Sorghum/genetics , Sorghum/metabolism , Lignin/metabolism , Gene Expression Regulation, Plant , Edible Grain/metabolism , Flavonoids/metabolism , Glucosides/metabolism , Esters/metabolismABSTRACT
Although several aspects of lignin metabolism have been extensively characterized, the mechanism(s) by which lignin monomers are transported across the plasma membrane remains largely unknown. Biochemical, proteomic, expression and co-expression analyses from several plant species support the involvement of active transporters, mainly those belonging to the ABC superfamily. Here, we report on the genome-wide characterization of the ABCG gene subfamily in the model C4 grass Setaria viridis and further identification of the members potentially involved in monolignol transport. A total of 48 genes encoding SvABCGs were found in the S. viridis genome, from which 21 SvABCGs were classified as full-size transporters and 27 as half-size transporters. Comprehensive analysis of the ABCG subfamily in S. viridis based on expression and co-expression analyses support a role for SvABCG17 in monolignol transport: (i) SvABCG17 is orthologous to AtABCG29, a monolignol transporter in Arabidopsis thaliana; (ii) SvABCG17 displays a similar expression profile to that of lignin biosynthetic genes in a set of different S. viridis tissues and along the elongating internode; (iii) SvABCG17 is highly co-expressed with lignin-related genes in a public transcriptomic database; (iv) SvABCG17displays particularly high expression in the top of the S. viridis elongating internode, a tissue undergoing active lignification; (v) SvABCG17 mRNA localization coincides with the histochemical pattern of lignin deposition; and (vi) the promoter of SvABCG17 is activated by secondary cell wall-associated transcription factors, especially by lignin-specific activators of the MYB family. Further studies might reveal further aspects of this potential monolignol transporter, including its real substrate specificity and whether it works redundantly with other ABC members during S. viridis lignification.