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A peroxisomal β-oxidative pathway contributes to the formation of C6-C1 aromatic volatiles in poplar.

ABSTRACT: Benzenoids (C6-C1 aromatic compounds) play important roles in plant defense and are often produced upon herbivory. Black cottonwood (Populus trichocarpa) produces a variety of volatile and nonvolatile benzenoids involved in various defense responses. However, their biosynthesis in poplar is mainly unresolved. We showed feeding of the poplar leaf beetle (Chrysomela populi) on P. trichocarpa leaves led to increased emission of the benzenoid volatiles benzaldehyde, benzylalcohol, and benzyl benzoate. The accumulation of salicinoids, a group of nonvolatile phenolic defense glycosides composed in part of benzenoid units, was hardly affected by beetle herbivory. In planta labeling experiments revealed that volatile and nonvolatile poplar benzenoids are produced from cinnamic acid (C6-C3). The biosynthesis of C6-C1 aromatic compounds from cinnamic acid has been described in petunia (Petunia hybrida) flowers where the pathway includes a peroxisomal-localized chain shortening sequence, involving cinnamate-CoA ligase (CNL), cinnamoyl-CoA hydratase/dehydrogenase (CHD), and 3-ketoacyl-CoA thiolase (KAT). Sequence and phylogenetic analysis enabled the identification of small CNL, CHD, and KAT gene families in P. trichocarpa. Heterologous expression of the candidate genes in Escherichia coli and characterization of purified proteins in vitro revealed enzymatic activities similar to those described in petunia flowers. RNA interference-mediated knockdown of the CNL subfamily in gray poplar (Populus x canescens) resulted in decreased emission of C6-C1 aromatic volatiles upon herbivory, while constitutively accumulating salicinoids were not affected. This indicates the peroxisomal β-oxidative pathway participates in the formation of volatile benzenoids. The chain shortening steps for salicinoids, however, likely employ an alternative pathway.

SUBMITTER: Lackus ND

PROVIDER: S-EPMC8195509 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundCinnamomum cassia Presl, classified in the Lauraceae family, is widely used as a spice, but also in medicine, cosmetics, and food. Aroma is an important factor affecting the medicinal and flavoring properties of C. cassia, and is mainly determined by volatile organic compounds (VOCs); however, little is known about the composition of aromatic VOCs in C. cassia and their potential molecular regulatory mechanisms. Here, integrated transcriptomic and volatile metabolomic analyses were employed to provide insights into the formation regularity of aromatic VOCs in C. cassia bark at five different harvesting times.ResultsThe bark thickness and volatile oil content were significantly increased along with the development of the bark. A total of 724 differentially accumulated volatiles (DAVs) were identified in the bark samples, most of which were terpenoids. Venn analysis of the top 100 VOCs in each period showed that twenty-eight aromatic VOCs were significantly accumulated in different harvesting times. The most abundant VOC, cinnamaldehyde, peaked at 120 months after planting (MAP) and dominated the aroma qualities. Five terpenoids, α-copaene, β-bourbonene, α-cubebene, α-funebrene, and δ-cadinene, that peaked at 240 MAP could also be important in creating C. cassia's characteristic aroma. A list of 43,412 differentially expressed genes (DEGs) involved in the biosynthetic pathways of aromatic VOCs were identified, including phenylpropanoids, mevalonic acid (MVA) and methylerythritol phosphate (MEP). A gene-metabolite regulatory network for terpenoid and phenylpropanoid metabolism was constructed to show the key candidate structural genes and transcription factors involved in the biosynthesis of terpenoids and phenylpropanoids.ConclusionsThe results of our research revealed the composition and changes of aromatic VOCs in C. cassia bark at different harvesting stages, differentiated the characteristic aroma components of cinnamon, and illuminated the molecular mechanism of aroma formation. These foundational results will provide technical guidance for the quality breeding of C. cassia.

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A peroxisomal β-oxidative pathway contributes to the formation of C6-C1 aromatic volatiles in poplar.

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