Dynamic product-precursor relationships underlie cuticular lipid accumulation on maize silks

Abstract

The hydrophobic cuticle is the first line of defense between aerial portions of a plant and the external environment. On maize silks, the cuticular cutin matrix is infused with cuticular lipids, consisting of a homologous series of very-long-chain fatty acids (VLCFAs), aldehydes, and hydrocarbons that serve as precursors, intermediates, and end-products of the elongation, reduction, and decarbonylation reactions of the hydrocarbon-producing pathway. To deconvolute the potentially confounding impacts of the silk microenvironment and silk development on the hydrocarbon-producing pathway, spatio-temporal cuticular lipid profiling was conducted on the agronomically important inbreds B73 and Mo17, and their reciprocal hybrids. Statistical interrogation via multivariate analyses of the metabolite abundances of the hydrocarbon-producing pathway demonstrate that the cellular VLCFA pool is positively correlated with the cuticular lipid metabolome, and this metabolome is primarily affected by the silk microenvironment and the plant genotype. Moreover, genotype has a major effect on the pathway, with increased cuticular hydrocarbon and concomitant reduction of cuticular VLCFA accumulation on B73 silks, suggesting that conversion of VLCFAs to hydrocarbons is more effective in B73 than Mo17. Statistical modeling of the ratios between cuticular hydrocarbons and cuticular VLCFAs reveals the complexity of the product-precursor ratio relationship, demonstrating a significant role of precursor chain length. Longer-chain VLCFAs are preferentially utilized as precursors for hydrocarbon biosynthesis. Collectively, these findings demonstrate maize silks as an effective and novel system for dissection of the complex dynamics of cuticular lipid accumulation in plants.

Characterization of the metabolic networks and gene-metabolite associations underlying cuticle production in maize via systems’ biology approaches

“…Indeed, our earlier study of silk wax metabolomes has noted progressive accumulation (1.4-fold increase) of all wax constituents from the silk base to the point of emergence from the encasing husk leaves, and a much more dramatic accumulation (2.5-fold increase) during transition of silk microenvironment (Chen et al, 2021). In addition, further dissection of the dynamic relationship between VLCFA precursors and the corresponding hydrocarbon products reveals a profound influence of genetic background, in that VLC-fatty acyl CoAs are presumably preferentially recruited for hydrocarbon production in inbred line B73 as opposed to conversion to VLCFAs and deposition in the cuticle in inbred Mo17 (Chen et al, 2021). Likewise, both development and change in microenvironment impact the silk transcriptome by causing strong differential expression of ~1,500 genes that are involved in stress responses, hormone signaling, and cell-cell communication .…”

“…For an individual maize leaf, a a transition of cuticular wax composition occurs acropetally (i.e., from leaf base to tip): hydrocarbons comprise the entire cuticular wax metabolome within 2 -4 cm from the leaf base but decrease by 70% in regions that are >10 cm away from the base and meanwhile alkyl esters accumulate from nearly undetectable levels to 60% of the total wax abundance . In the case of maize silks, hydrocarbons comprise >90% of the cuticular wax metabolome, and VLCFAs, aldehydes and alcohols constitute the remainder of the metabolome 3 Chen et al, 2021).…”

“…The cuticle is comprised of an aliphatic cutin polyester matrix of epoxy-and hydroxy-fatty acids that provides the structural framework for the deposition of cuticular waxes within (intracuticular) and atop (epicuticular) the cutin matrix. These cuticular waxes can include very-long-chain fatty acids (VLCFAs) and VLCFA-derivatives such as aldehydes, hydrocarbons, alcohols, ketones, and wax esters, and the cuticular wax composition differs considerably among organisms, organs, and the developmental ages of organs Chen et al, 2021) . The cuticular wax fraction of the cuticle has specifically been shown to be protective against environmental stress, including drought tolerance by controlling non-stomatal transpirational water loss (Xue et al, 2017), and in being a deterrent to pathogens and insects by regulating plant-pathogen/insect interactions (Wang et al, 2020).…”

“…In addition, alky esters accumulate from nearly undetectable levels to 60% of the total wax abundance . In the case of maize silks, hydrocarbons comprise >90% of the cuticular wax metabolome, demonstrating that the decarbonylation pathway is strongly favored in this organ Chen et al, 2021).…”

“…Such a systems biology approach is adopted in this study utilizing the previously characterized silk metabolome (Chen et al, 2021) and transcriptome datasets. Using a suite of joint-statistical analysis approaches, approximately 309 genes are identified as significantly associated with the spatio-temporal changes of silk cuticular wax composition between the two agronomically important maize inbreds, B73 and Mo17.…”