Abstract
Homospermidine synthase (HSS) is the first specific enzyme in pyrrolizidine alkaloid (PA) biosynthesis, a pathway involved in the plant's chemical defense. HSS has been shown to be recruited repeatedly by duplication of a gene involved in primary metabolism. Within the lineage of the Boraginales, only one gene duplication event gave rise to HSS. Here, we demonstrate that the tissue-specific expression of HSS in three boraginaceous species, Heliotropium indicum, Symphytum officinale, and Cynoglossum officinale, is unique with respect to plant organ, tissue, and cell type. Within H. indicum, HSS is expressed exclusively in nonspecialized cells of the lower epidermis of young leaves and shoots. In S. officinale, HSS expression has been detected in the cells of the root endodermis and in leaves directly underneath developing inflorescences. In young roots of C. officinale, HSS is detected only in cells of the endodermis, but in a later developmental stage, additionally in the pericycle. The individual expression patterns are compared with those within the Senecioneae lineage (Asteraceae), where HSS expression is reproducibly found in specific cells of the endodermis and the adjacent cortex parenchyma of the roots. The individual expression patterns within the Boraginales species are discussed as being a requirement for the successful recruitment of HSS after gene duplication. The diversity of HSS expression within this lineage adds a further facet to the already diverse patterns of expression that have been observed for HSS in other PA-producing plant lineages, making this PA-specific enzyme one of the most diverse expressed proteins described in the literature.
Highlights
Homospermidine synthase (HSS) is the first specific enzyme in pyrrolizidine alkaloid (PA) biosynthesis, a pathway involved in the plant’s chemical defense
reverse transcription (RT)-PCR was performed with primers highly specific for the complementary DNA (cDNA) of HSS and deoxyhypusine synthase (DHS) to test for the presence or absence of the respective transcripts in the various plant tissues and to allow, at best, a rough estimate of transcript levels
Young and older stems, leaves, and flower from the bud to fruit stage (Fig. 1A). This result confirmed previous tracer-feeding studies that identified the shoot of H. indicum as the site of PA biosynthesis
Summary
Homospermidine synthase (HSS) is the first specific enzyme in pyrrolizidine alkaloid (PA) biosynthesis, a pathway involved in the plant’s chemical defense. Tracer feeding experiments have shown that, first, the core pathway for PAs from putrescine and spermidine via homospermidine is the same as the pathway in Senecio species, and second, despite the common origin of HSS within the Boraginales lineage, different species differ with respect to their site of PA biosynthesis: PAs are produced exclusively in the shoots of H. indicum (Heliotropiaceae), exclusively in the roots of S. officinale (Boraginaceae), and in shoots and roots of C. officinale (Boraginaceae; Van Dam et al, 1995; Frölich et al, 2007) To analyze these variations at the cellular level, we have studied the expression patterns of HSS and DHS, which share a common ancestor. A comparative analysis of a further member of the Senecioneae lineage (Asteraceae) supports the view that this variability of expression patterns is a unique characteristic of the Boraginales lineage and not a general concept valid for all PA-producing lineages
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