Repeated Evolution of the Pyrrolizidine Alkaloid–Mediated Defense System in Separate Angiosperm Lineages w⃞

Reimann, Andreas; Nurhayati, Niknik; Backenköhler, Anita; Ober, Dietrich

doi:10.1105/tpc.104.023176

Cited by 103 publications

(124 citation statements)

References 55 publications

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“…For example, the pyrrolizidine alkaloids are found in such diverse families as the Orchidaceae, Fabaceae, Boraginaceae, and Asteraceae. Analysis of the first biosynthetic step, homospermidine synthase, indicated that this enzyme has been recruited from a primary metabolic enzyme, deoxyhypusine synthase, at least four times over the course of evolution (32). Besides alkaloids, groups such as the cardenolides, a type of glycosylated steroid found in the Liliaceae, Ranunculaceae, Brassicaceae, and Apocynaceae, among other families, have also been proposed to have originated polyphyletically (33).…”

Section: Discussionmentioning

confidence: 99%

Plant tropane alkaloid biosynthesis evolved independently in the Solanaceae and Erythroxylaceae

Jirschitzka

Schmidt

Reichelt

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

101

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The pharmacologically important tropane alkaloids have a scattered distribution among angiosperm families, like many other groups of secondary metabolites. To determine whether tropane alkaloids have evolved repeatedly in different lineages or arise from an ancestral pathway that has been lost in most lines, we investigated the tropinone-reduction step of their biosynthesis. In species of the Solanaceae, which produce compounds such as atropine and scopolamine, this reaction is known to be catalyzed by enzymes of the short-chain dehydrogenase/reductase family. However, in Erythroxylum coca (Erythroxylaceae), which accumulates cocaine and other tropane alkaloids, no proteins of the shortchain dehydrogenase/reductase family were found that could catalyze this reaction. Instead, purification of E. coca tropinonereduction activity and cloning of the corresponding gene revealed that a protein of the aldo-keto reductase family carries out this reaction in E. coca. This protein, designated methylecgonone reductase, converts methylecgonone to methylecgonine, the penultimate step in cocaine biosynthesis. The protein has highest sequence similarity to other aldo-keto reductases, such as chalcone reductase, an enzyme of flavonoid biosynthesis, and codeinone reductase, an enzyme of morphine alkaloid biosynthesis. Methylecgonone reductase reduces methylecgonone (2-carbomethoxy-3-tropinone) stereospecifically to 2-carbomethoxy-3β-tropine (methylecgonine), and has its highest activity, protein level, and gene transcript level in young, expanding leaves of E. coca. This enzyme is not found at all in root tissues, which are the site of tropane alkaloid biosynthesis in the Solanaceae. This evidence supports the theory that the ability to produce tropane alkaloids has arisen more than once during the evolution of the angiosperms.

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Section: Discussionmentioning

confidence: 99%

Plant tropane alkaloid biosynthesis evolved independently in the Solanaceae and Erythroxylaceae

Jirschitzka

Schmidt

Reichelt

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

101

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“…The emergence of a complex benzylisoquinoline alkaloid pathway in an ancestor common to the basal angiosperms is in contrast with the proposed independent recruitment of pyrrolizidine alkaloid biosynthetic enzymes in at least four different angiosperm lineages (Reimann et al, 2004). Two scenarios have emerged concerning the relationship between the cell type-specific localization and evolutionary origin of plant alkaloids.…”

Section: Discussionmentioning

confidence: 99%

Cell Type–Specific Localization of Transcripts Encoding Nine Consecutive Enzymes Involved in Protoberberine Alkaloid Biosynthesis

2005

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Molecular clones encoding nine consecutive biosynthetic enzymes that catalyze the conversion of L-dopa to the protoberberine alkaloid (S)-canadine were isolated from meadow rue (Thalictrum flavum ssp glaucum). The predicted proteins showed extensive sequence identity with corresponding enzymes involved in the biosynthesis of related benzylisoquinoline alkaloids in other species, such as opium poppy (Papaver somniferum). RNA gel blot hybridization analysis showed that gene transcripts for each enzyme were most abundant in rhizomes but were also detected at lower levels in roots and other organs. In situ RNA hybridization analysis revealed the cell type-specific expression of protoberberine alkaloid biosynthetic genes in roots and rhizomes. In roots, gene transcripts for all nine enzymes were localized to immature endodermis, pericycle, and, in some cases, adjacent cortical cells. In rhizomes, gene transcripts encoding all nine enzymes were restricted to the protoderm of leaf primordia. The localization of biosynthetic gene transcripts was in contrast with the tissue-specific accumulation of protoberberine alkaloids. In roots, protoberberine alkaloids were restricted to mature endodermal cells upon the initiation of secondary growth and were distributed throughout the pith and cortex in rhizomes. Thus, the cell type-specific localization of protoberberine alkaloid biosynthesis and accumulation are temporally and spatially separated in T. flavum roots and rhizomes, respectively. Despite the close phylogeny between corresponding biosynthetic enzymes, distinct and different cell types are involved in the biosynthesis and accumulation of benzylisoquinoline alkaloids in T. flavum and P. somniferum. Our results suggest that the evolution of alkaloid metabolism involves not only the recruitment of new biosynthetic enzymes, but also the migration of established pathways between cell types.

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“…During the last 10 years, scientists have had fascinating insights into the evolutionary creation of genetic diversity of secondary metabolism. The evolution of new genes by duplicating the genes of primary metabolism, followed by the functional diversification or new functionalization of the duplicates under the selection pressure of the environment (41,42), has been demonstrated for key biosynthetic enzymes of a number of classes of secondary metabolites, such as terpenoids (43), polyketides (44), phenolic esters (45), benzoxazinone alkaloids (46), and pyrrolizidine alkaloids (47). In conclusion, we see that the evolutionary ideas of Stahl and his contemporaries are confirmed by recent concepts of molecular evolution of plant secondary metabolism.…”

Section: Early Chemical Ecology: Why Neglected and Forgotten For Decamentioning

confidence: 99%

The lost origin of chemical ecology in the late 19th century

Hartmann

2008

Proc. Natl. Acad. Sci. U.S.A.

115

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The origin of plant chemical ecology generally dates to the late 1950s, when evolutionary entomologists recognized the essential role of plant secondary metabolites in plant-insect interactions and suggested that plant chemical diversity evolved under the selection pressure of herbivory. However, similar ideas had already flourished for a short period during the second half of the 19th century but were largely forgotten by the turn of the century. This article presents the observations and studies of three protagonists of chemical ecology: Anton Kerner von Marilaun (1831-1898, Innsbruck, Austria, and Vienna, Austria), who mainly studied the impact of geological, climatic, and biotic factors on plant distribution and survival; Lé o Errera (1858 -1906, Brussels, Belgium), a plant physiologist who analyzed the localization of alkaloids in plant cells and tissues histochemically; and Ernst Stahl (1848 -1919, Jena, Germany), likely the first experimental ecologist and who performed feeding studies with snails and slugs that demonstrated the essential role of secondary metabolites in plant protection against herbivores. All three, particularly Stahl, suggested that these ''chemical defensive means'' evolved in response to the relentless selection pressure of the heterotrophic community that surrounds plants. Although convincingly supported by observations and experiments, these ideas were forgotten until recently. Now, more than 100 years later, molecular analysis of the genes that control secondary metabolite production underscores just how correct Kerner von Marilaun, Errera, and, particularly, Stahl were in their view. Why their ideas were lost is likely a result of the adamant rejection of all things ''teleological'' by the physiologists who dominated biological research at the time.herbivore ͉ historical basis ͉ plant protection ͉ secondary metabolism C hemical ecology refers to chemically mediated interactions between organisms and their biotic and abiotic environment. It covers a broad range of chemical interactions and signaling processes; major facets are (i) the chemical communication (chemical language, e.g., pheromones) of animals, particularly expressed in arthropods; (ii) the mutualistic interactions of organisms, e.g., plants and animals (pollination), plants and fungi (mycorrhiza), and plants and bacteria (symbiotic nitrogen fixation); (iii) the chemical defenses of organisms, e.g., plant defenses against herbivores and pathogens, animal defenses against predators and parasitoids, and microorganism defenses against food competitors; and (iv) protection against abiotic stress, e.g., plant defenses against damage by UV light, drought, or cold.A major area of chemical ecology concerns the constant competition between the worlds of autotrophs and heterotrophs or simply plants and animals. During their evolution, plants have evolved sophisticated adaptations to cope with herbivores and pathogens while the latter developed similarly elaborated counteradaptations to overcome plants' defenses. Plants produce a...

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Repeated Evolution of the Pyrrolizidine Alkaloid–Mediated Defense System in Separate Angiosperm Lineages w⃞

Cited by 103 publications

References 55 publications

Plant tropane alkaloid biosynthesis evolved independently in the Solanaceae and Erythroxylaceae

Plant tropane alkaloid biosynthesis evolved independently in the Solanaceae and Erythroxylaceae

Cell Type–Specific Localization of Transcripts Encoding Nine Consecutive Enzymes Involved in Protoberberine Alkaloid Biosynthesis

The lost origin of chemical ecology in the late 19th century

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