Cuticle development and underlying transcriptome-metabolome associations during early seedling establishment

The plant cuticle is a complex extracellular lipid barrier that provides protection from numerous environmental stressors and is critical for normal organ development. In this study, we investigated cuticle deposition by integrating metabolomics and transcriptomics data gathered from six different maize seedling organs of four genotypes, the inbred lines B73 and Mo17, and their reciprocal hybrids. These datasets captured the developmental transition of the seedling from heterotrophic skotomorphogenic growth to autotrophic photomorphogenic growth, which is a transition that is highly vulnerable to environmental stresses. Statistical interrogation of these data reveals that the predominant determinant of cuticle composition is seedling organ type, whereas the seedling genotype has a smaller effect on this phenotype. Gene-to-metabolite associations assessed by joint statistical analyses of transcriptome and metabolome datasets identified three gene networks connected with the deposition of different fractions of the cuticle: a) cuticular waxes; b) cutin of aerial organs and suberin of roots; and c) both of these fractions. These networks consist of genes that encode known components of the machinery that supports cuticle deposition, demonstrating the utility of this integrated omics approach. Moreover, these gene networks reveal three additional metabolic programs that appear to support cuticle deposition, including processes of a) chloroplast biogenesis, b) lipid metabolism, and c) molecular regulation (e.g., transcription factors, post-translational regulators and phytohormones). This study demonstrates the wider physiological metabolic context that can determine cuticle deposition and lays the groundwork for new targets for modulating properties of this protective barrier.