Dynamic changes to the plant cuticle include the production of volatile cuticular wax-derived compounds.

Abstract

The cuticle is a hydrophobic structure that seals plant aerial surfaces from the surrounding environment. To better understand how cuticular wax composition changes over development, we conducted an untargeted screen of leaf surface lipids from black cottonwood (<i>Populus trichocarpa</i>). We observed major shifts to the lipid profile across development, from a phenolic and terpene-dominated profile in young leaves to an aliphatic wax-dominated profile in mature leaves. Contrary to the general pattern, levels of aliphatic <i>cis</i>-9-alkenes decreased in older leaves following their accumulation. A thorough examination revealed that the decrease in <i>cis</i>-9-alkenes was accompanied by a concomitant increase in aldehydes, one of them being the volatile compound nonanal. By applying exogenous alkenes to <i>P. trichocarpa</i> leaves, we show that unsaturated waxes in the cuticle undergo spontaneous oxidative cleavage to generate aldehydes and that this process occurs similarly in other alkene-accumulating systems such as balsam poplar (<i>Populus balsamifera</i>) leaves and corn (<i>Zea mays</i>) silk. Moreover, we show that the production of cuticular wax-derived compounds can be extended to other wax components. In bread wheat (<i>Triticum aestivum</i>), 9-hydroxy-14,16-hentriacontanedione likely decomposes to generate 2-heptadecanone and 7-octyloxepan-2-one (a caprolactone). These findings highlight an unusual route to the production of plant volatiles that are structurally encoded within cuticular wax precursors. These processes could play a role in modulating ecological interactions and open the possibility for engineering bioactive volatile compounds into plant waxes.