Altering potato isoprenoid metabolism increases biomass and induces early flowering

Authors: SI, M. - Washington State University; LANGE, IRIS - Washington State University; LANGE, B.M. - Washington State University; Navarre, Duroy - Roy

Submitted to: Journal of Experimental Botany
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/14/2020
Publication Date: 4/16/2020
Citation: Si, M., Lange, I., Lange, B., Navarre, D.A. 2020. Altering potato isoprenoid metabolism increases biomass and induces early flowering. Journal of Experimental Botany. 71(14):4109-4124. https://doi.org/10.1093/jxb/eraa185.
DOI: https://doi.org/10.1093/jxb/eraa185

Interpretive Summary: Isoprenoids constitute the largest class of plant natural products and have diverse biological functions including in plant growth and development. In potato (Solanum tuberosum), the regulatory mechanism underlying the biosynthesis of isoprenoids through the mevalonate pathway is unclear. We assessed the role of 3-hydroxy-3-methylglutaryl-CoA reductase (HMGR) homologs in potato development and in the metabolic regulation of isoprenoid biosynthesis by generating transgenic lines with down-regulated expression (RNAi-hmgr) or overexpression (OE) of one (StHMGR1 or StHMGR3) or two genes, HMGR and farnesyl diphosphate synthase (FPS; StHMGR1/StFPS1 or StHMGR3/StFPS1). Levels of sterols, steroidal glycoalkaloids (SGAs), and plastidial isoprenoids were elevated in the OE-HMGR1, OE-HMGR1/FPS1, and OE-HMGR3/FPS1 lines, and these plants exhibited early flowering, increased stem height, increased biomass, and increased total tuber weight. However, OE-HMGR3 lines showed dwarfism and had the highest sterol amounts, but without an increase in SGA levels, supporting a rate-limiting role for HMGR3 in the accumulation of sterols. Potato RNAi-hmgr lines showed inhibited growth and reduced cytosolic isoprenoid levels. We also determined the relative importance of transcriptional control at regulatory points of isoprenoid precursor biosynthesis by assessing gene–metabolite correlations. These findings provide novel insights into specific end-products of the sterol pathway and could be important for crop yield and bioenergy crops.

Technical Abstract: Isoprenoids make up the largest class of natural products and play diverse biological functions in plants as essential components in plant growth and development. In potato (Solanum tuberosum), the regulatory mechanism underlying the biosynthesis of isoprenoids through the mevalonate pathway is unclear. We assessed the role of 3-hydroxy-3-methylglutaryl coenzyme A reductase (HMGR) in plant development and the metabolic regulation of isoprenoid biosynthesis by generating transgenic potato lines with downregulated expression (RNAi-hmgr) or overexpression (OE) of one (StHMGR1 or StHMGR3), or two genes, (StHMGR1/StFPS1 or StHMGR3/StFPS1). Levels of sterols, steroidal glycoalkaloids (SGAs) and plastidial isoprenoids were elevated in the OE-HMGR1, OE-HMGR1/FPS1 and OE-HMGR3/FPS1 lines, and plants exhibited early flowering, increased stem height, increased biomass and increased total tuber weight. However, OE-HMGR3 lines showed dwarfism and had the highest sterol amounts, but without an increase in SGA levels, supporting a rate-limiting role of HMGR3 in the accumulation of sterols. Like hmgr1 functional knockdown mutants in other plants, potato RNAi-hmgr lines showed inhibited growth and reduced cytosolic isoprenoid levels. By assessing the correlation of transgene expression levels with isoprenoid marker metabolites (gene-to-metabolite correlation), we determined the relative importance of transcriptional control at regulatory points of isoprenoid precursor biosynthesis, which could be used to enhance flux toward specific end-products of the sterol pathway or enhance plant growth.