Abstract
Impatiens balsamina L. is a tropical ornamental and traditional medicinal herb rich in natural compounds, especially 2-methoxy-1,4-naphthoquinone (MNQ) which is a bioactive compound with tested anticancer activities. Characterization of key genes involved in the shikimate and 1,4-dihydroxy-2-naphthoate (DHNA) pathways responsible for MNQ biosynthesis and their expression profiles in I. balsamina will facilitate adoption of genetic/metabolic engineering or synthetic biology approaches to further increase production for pre-commercialization. In this study, HPLC analysis showed that MNQ was present in significantly higher quantities in the capsule pericarps throughout three developmental stages (early-, mature- and postbreaker stages) whilst its immediate precursor, 2-hydroxy-1,4-naphthoquinone (lawsone) was mainly detected in mature leaves. Transcriptomes of I. balsamina derived from leaf, flower, and three capsule developmental stages were generated, totalling 59.643 Gb of raw reads that were assembled into 94,659 unigenes (595,828 transcripts). A total of 73.96% of unigenes were functionally annotated against seven public databases and 50,786 differentially expressed genes (DEGs) were identified. Expression profiles of 20 selected genes from four major secondary metabolism pathways were studied and validated using qRT-PCR method. Majority of the DHNA pathway genes were found to be significantly upregulated in early stage capsule compared to flower and leaf, suggesting tissue-specific synthesis of MNQ. Correlation analysis identified 11 candidate unigenes related to three enzymes (NADH-quinone oxidoreductase, UDP-glycosyltransferases and S-adenosylmethionine-dependent O-methyltransferase) important in the final steps of MNQ biosynthesis based on genes expression profiles consistent with MNQ content. This study provides the first molecular insight into the dynamics of MNQ biosynthesis and accumulation across different tissues of I. balsamina and serves as a valuable resource to facilitate further manipulation to increase production of MNQ.
Highlights
Increased focus on bio-based economy has meant a renewed drive in the plant biotechnology sector to produce high-value bio-ingredients for various downstream applications
differentially expressed genes (DEGs) which were assigned with Kyoto Encyclopedia of Genes and Genomes (KEGG) ID but not mapped to any pathway accounted for 1086 unigenes (2.14%)
With regards to the relevant pathway terms involved in secondary metabolisms, ‘Biosynthesis of other secondary metabolites’ contained 1.86% DEGs, whereby 0.78%- and 0.30% DEGs were classified under the subcategories of ‘Phenylpropanoid biosynthesis’ and ‘Flavonoid biosynthesis’ respectively
Summary
Increased focus on bio-based economy (or bioeconomy) has meant a renewed drive in the plant biotechnology sector to produce high-value bio-ingredients for various downstream applications. Comparison of results from these studies generally indicated that MNQ (and lawsone) accumulated at differing degrees in parts of I. balsamina. Naphthoquinones such as MNQ and lawsone comprise a subclass of quinones, structurally related to naphthalene and characterized by the substitution of the naphthalene skeleton at position C1 and C4 (1,4-naphthoquinones) or C1 and C2 (1,2-naphthoquinones)[29]. DHNA is a key precursor used in the biosynthesis of phylloquinone (2-methyl-3-phytyl-1,4-naphtho-quinone or vitamin K1) in plants, in addition to other specialized 1,4-naphthoquinones such as lawsone39,42, juglone36, anthraquinones[43], and lapachol[34]. None of the genes involved in MNQ biosynthesis pathways has been characterized for I. balsamina, many studies exist on its bioactivities, total content, and different extraction and purification methods
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