Progressive Regulation of Sesquiterpene Biosynthesis in Arabidopsis and Patchouli (Pogostemon cablin) by the miR156-Targeted SPL Transcription Factors

Abstract

Plant metabolites vary at different stages of their life cycle. Although it is well documented that environmental factors stimulate biosynthesis of secondary metabolites, the regulation by endogenous developmental cues remains poorly understood. The microRNA156 (miR156)-targeted squamosa promoter binding protein-like (SPL) factors function as a major age cue in regulating developmental phase transition and flowering. We show here that the miR156-targeted SPL transcription factor plays an important role in the spatiotemporal regulation of sesquiterpene biosynthesis. In Arabidopsis thaliana, the miR156-SPL module regulates the formation of (E)-β-caryophyllene in the flowering stage through modulating expression of the sesquiterpene synthase gene TPS21. We demonstrated that SPL9 directly binds to TPS21 promoter and activates its expression. In the perennial fragrant herb Pogostemon cablin, the accumulation of patchouli oil, largely composed of sesquiterpenes dominated by (-)-patchoulol, is also age-regulated, and the SPL promotes biosynthesis of sesquiterpenes in elder plants by upregulating patchoulol synthase (PatPTS) gene expression. As miR156-SPLs are highly conserved in plants, our finding not only uncovers a molecular link between developmental timing and sesquiterpene production but also suggests a new strategy to engineer plants for accelerated growth with enhanced production of terpenoids.

An Insight into microRNA156 Role in Salinity Stress Responses of Alfalfa

“…We observed downregulation of SPL genes in leaves and roots under stress conditions indicating that miR156 expedites the cleavage of SPLs to modulate stress responses in alfalfa. SPL genes respond to abiotic stress and stimulate the synthesis of secondary metabolites (Wang M. et al, 2013; Yu et al, 2015) showing that they may directly or indirectly be involved in stress tolerance.…”

Genome-Wide Identification of MicroRNAs and Their Targets in the Leaves and Fruits of Eucommia ulmoides Using High-Throughput Sequencing

“…bHLH3 transcription factor, a target gene of miR828, regulates the accumulation of anthocyanins in apple after debagging (Qu et al, 2016). miR156 is highly conserved in plants and predicted to target the SPL transcription factor, which plays an important part in the spatiotemporal regulation of sesquiterpene biosynthesis in A. thaliana and Pogostemon cablin (Yu et al, 2015). miR171 targets mRNAs coding for the scarecrow-like proteins, which is a transcription factor that has been implicated in gibberellins synthesis in Arabidopsis (Llave et al, 2002b).…”

Jasmonate response decay and defense metabolite accumulation contributes to age-regulated dynamics of plant insect resistance

“…For overexpression of miR156 and SPL9 in coi1-2 , the constructs of 35S:MIR156 and SPL9:rSPL9 (ref. 23) were used. For JAZ3:JAZ3-FLA G, JAZ3 promoter and the coding region linked to FLAG were cloned into pCAMBIA1300.…”

“…The level of miR156 is high during the juvenile stage and steadily decreases during later plant growth and development, leading to a progressive increase in the level of SPLs, which regulate a broad range of processes including flowering2021, secondary metabolite production2223, trichome initiation242526, vernalization2728 and shoot regeneration29. The phytohormone gibberellin (GA) plays an important role in regulating diverse aspects of plant growth and development3031.…”