Genomic analysis of branched chain fatty acid and acyl sugar production in Solanum pennellii and Nicotiana benthamiana

Authors: SLOCOMBE, STEPHEN - UNIVERSITY OF YORK, UK; SCHAUVINHOLD, INES - UNIVERSITY OF YORK, UK; AZZIZ, NAVID - UNIVERSITY OF YORK, UK; LARSON, TONY - UNIVERSITY OF YORK, UK; Giovannoni, James; DIXON, RICHARD - NOBLE FOUNDATION; BROUN, PIERRE - UNIVERSITY OF YORK, UK

Submitted to: Plant Physiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/9/2009
Publication Date: 7/15/2009
Citation: Slocombe, S., Schauvinhold, I., Azziz, N., Larson, T., Giovannoni, J.J., Dixon, R., Broun, P. 2009. Genomic analysis of branched chain fatty acid and acyl sugar production in Solanum pennellii and Nicotiana benthamiana. Plant Physiology. 148:1830-1846.

Interpretive Summary: Glandular trichomes are epidermal secretory structures that play a central defensive role in many plant species. Due to their unique and versatile metabolism, they contribute significantly to the wide diversity of phytochemicals derived from plants. Some trichome types produce acyl sugars, which are non-volatile metabolites that the trichomes exude onto the surface of aerial organs. These highly viscous lipids can constitute a significant proportion of leaf biomass and are produced in particularly large amounts in the wild tomato species Solanum pennellii. They are also produced, albeit in lesser quantities in tobacco species, such as Nicotiana benthamiana. Because of their potent insecticidal properties, increasing acyl sugar production has long been a target of tomato and potato breeding programs Here we summarize both conserved and divergent genetic and molecular mechanisms in the production of important defence compounds in the Solanaceae, aplant family that includes many important vegetable species such as tomato, potato, eggplant and pepper.

Technical Abstract: Acyl sugars are extracellular epidermal lipids that are exuded from glandular trichomes and coat the aerial organs of many species in the Solanaceae. These highly viscous surfactants, which often contain branched-chain fatty acids (BCFA), play an important defensive role against pest and insects. On the basis of isotope feeding studies, BCFA elongation has been proposed to proceed in two-carbon steps in the high acyl sugar-producing tomato species Solanum pennellii and in one-carbon increments in its tobacco relative Nicotiana benthamiana. To shed light on the molecular mechanisms underlying BCFA production in trichomes, we have taken a comparative genomic approach, with the aim of identifying critical enzymatic steps and probing metabolic regulation in S. pennellii and N. benthamiana. Using EST and microarray analysis, we found that acyl sugar production is associated with the strong expression in trichomes of genes associated with both branched-chain amino acid production and catabolism. Genes encoding enzymes of the branched-chain keto acid dehydrogenase complex (BCKD) are expressed at particularly high levels in trichomes and we show using virus-induced gene silencing that they are essential for BCFA and acyl sugar synthesis in both species. The results of our functional analysis also support the involvement of the Fatty Acid Synthase complex in BCFA production in S. pennellii and indicate the requirement for specific fatty acid elongases of the KAS I type.