Abstract
Shikonin derivatives are specialized lipophilic metabolites, secreted in abundant amounts from the root epidermal cells of Lithospermum erythrorhizon. Because they have anti-microbial activities, these compounds, which are derivatives of red naphthoquinone, are thought to serve as a chemical barrier for plant roots. The mechanism by which they are secreted from cells is, however, largely unknown. The shikonin production system in L. erythrorhizon is an excellent model for studying the mechanism by which lipophilic compounds are secreted from plant cells, because of the abundant amounts of these compounds produced by L. erythrorhizon, the 0 to 100% inducibility of their production, the light-specific inhibition of production, and the visibility of these products as red pigments. To date, many factors regulating shikonin biosynthesis have been identified, but no mechanism that regulates shikonin secretion without inhibiting biosynthesis has been detected. This study showed that inhibitors of membrane traffic strongly inhibit shikonin secretion without inhibiting shikonin production, suggesting that the secretion of shikonin derivatives into the apoplast utilizes pathways common to the ADP-ribosylation factor/guanine nucleotide exchange factor (ARF/GEF) system and actin filament polymerization, at least in part. These findings provide clues about the machinery involved in secreting lipid-soluble metabolites from cells.
Highlights
Higher plants produce a large number of secondary metabolites, which play various roles in responding to environmental stresses
Hairy roots in liquid cultures of L. erythrhorizon were found to have a reddish appearance in M9 medium, due to the excretion of shikonin derivatives into the apoplast (Figure 1Ba)
Comparing the accumulation rate between root tissues and the cultured medium, shikonin derivatives produced by hairy root cultures were found to root tissues, higher amounts were recovered from the culture medium (Figures 2A,B)
Summary
Higher plants produce a large number of secondary metabolites, which play various roles in responding to environmental stresses. These natural compounds function as chemical barriers against herbivores, bacteria, and fungi and in protecting plants from harmful UV irradiation (Croteau et al, 2000; Yazaki, 2004; Muranaka and Saito, 2013). Hydrophobic metabolites cannot freely move within the cytosol Many of these compounds exhibit strong biological toxicity, making it unlikely that they are slowly transported across membranes. Rather, following their biosynthesis, they are likely efficiently excreted from the cytosol into the apoplast. In citrus species, hydrophobic monoterpenes and furanocoumarins are biosynthesized in epithelial cells of oil glands, with the final products accumulating inside the oil glands, which are apoplastic spaces (Voo et al, 2012)
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