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Biological and Ecological Roles of Club Mosses (Lycopodiaceae) Alkaloids

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Plant Specialized Metabolites

Part of the book series: Reference Series in Phytochemistry ((RSP))

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Abstract

This paper is a critical overview of studies concerning the Lycopodium alkaloids and presentation of hypotheses that address the biological purpose of alkaloid presence in club mosses. Alkaloids are the largest class of nitrogen-containing secondary metabolites. It is estimated that over 20% of seed-bearing plants produce alkaloids and in the club moss species of the order Lycopodiales, alkaloids are the main secondary metabolites. The very high alkaloid content in club mosses and their chemical structure and biological properties are unparalleled among all cryptogams. To date, about 400 alkaloids have been identified in 12–15% of the investigated club moss species of the Lycopodiaceae, which means that the Lycopodiaceae are the most abundant source of alkaloids among vascular plants. The Lycopodium alkaloids are piperidine derivatives, biogenetically derived from lysine. To date, a number of genes and their products have been identified, which are involved in the biosynthesis of alkaloids. These are a type III polyketide synthase, which catalyzes a crucial imine-polyketide condensation, and Fe (II)/2-oxoglutarane-dependent dioxygenase (2OGD) enzymes that catalyze pyridine ring-forming desaturation, pyridine ring cleavage, and redox-neutral isomerization. Also of key importance is the bifunctional lysine/ornithine decarboxylase (L/ODC) that catalyzes decarboxylation of the alkaloid biosynthesis precursor lysine to cadaverine. There is no scientific explanation for the abundance of specific alkaloids in the Lycopodiaceae and their putative diverse biological properties. The polyamine (PA) cadaverine and its derivatives are likely to be involved in the processes of plant growth and development as growth regulators.

Investigations have demonstrated that PAs are ubiquitous in plants, frequently species-, organ-, and tissue-specific, and their cellular content depends on the equilibrium between their biosynthesis, transmembrane transport, and apoplastic catabolism. In plants, polyamine oxidases and diamine oxidases oxidize PAs and generate reactive oxygen species (ROS) directly involved in the processes of plant growth and development. In club mosses, the products of lysine decarboxylation and alkaloids may serve as nitrogen donors, possibly included in the biosynthetic pathways of PAs or nitric oxide (NO). Nitric oxide may regulate the expression of genes associated with the processes of plant maturation, senescence, and the response to pathogens. The evident structural resemblance of huperzine A (HupA) and some other structurally similar alkaloids to acetylcholine (ACh) and to the active center of acetylcholine esterase (AChE) indirectly indicates a likely role of alkaloids in the signal transduction involving the plant cholinergic system. As reported in the literature, alkaloids with the AChE inhibitory activity enhanced tissue sensitivity to the effects of red light and ACh in experimental models. In club mosses variations in the levels of alkaloid biosynthesis and alterations in their qualitative composition potentially may act to initiate morphogenetic processes. It has been demonstrated that in L. annotinum reverting to the generative growth and formation of strobili is associated with altered activities of two genes LAMB1 and LAMB2. It is possible that alkaloids that are AChE inhibitors acting on the phytochrome controlling signaling cascades are involved in the regulation of these genes.

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Abbreviations

2OGD:

Fe (II)/2-oxoglutarane-dependent dioxygenase

4PAA:

4-(2-Piperidyl) acetoacetate

4PAACoA:

4-(2-Piperidyl)acetyl-CoA

ABA:

Abscisic acid

ACh:

Acetylocholine

AChE:

Acetylcholinesterase

BuChE:

Pseudocholinesterase

ChE:

Pseudocholinesterase

CuAO:

Copper amine oxidase

DAO:

Diamine oxidase

DW:

Dry weight

GUS:

The GUS (β-glucuronidase) reporter gene system

HPLC-DAD:

Liquid chromatography with diode-array detection

HupA:

Huperzine A (selagine)

HupB:

Huperzine B

IAA:

3-Acetic acid

L/ODC:

Bifunctional lysine/ornithine decarboxylase

LA/LAs:

Lycopodium alkaloids

LC-TOF-MS:

Liquid chromatography/time-of-flight/mass spectrometry

Lys:

Lysine

NADPH:

Reduced nicotinamide adenine dinucleotide phosphate

NOX:

NADPH oxidase

NO:

Nitric oxide

PA/PAs:

Polyamine/polyamines

PAO:

Polyamine oxidase

PCA:

Principal component analysis

PKS:

III polyketide synthase

POWO:

Plants of the World Online https://powo.science.kew.org/

PPG I:

Pteridophyte Phylogeny Group

subsp:

Subspecies

TLC:

Thin layer chromatography

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Authors and Affiliations

  1. Department of Pharmaceutical Biology, Faculty of Pharmacy, The Medical University of Warsaw, Warsaw, Poland

    Wojciech J. Szypuła & Agnieszka Pietrosiuk

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  1. Wojciech J. Szypuła
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  2. Agnieszka Pietrosiuk
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Correspondence to Wojciech J. Szypuła .

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  1. Faculty of Pharmaceutical Sciences, Institute of Vine and Wine Sciences, University of Bordeaux, Villenave d'Ornon, France

    Jean-Michel Mérillon

  2. Department of Botany, M. L. Sukhadia University, Udaipur, Rajasthan, India

    Kishan Gopal Ramawat

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Szypuła, W.J., Pietrosiuk, A. (2023). Biological and Ecological Roles of Club Mosses (Lycopodiaceae) Alkaloids. In: Mérillon, JM., Ramawat, K.G. (eds) Plant Specialized Metabolites. Reference Series in Phytochemistry. Springer, Cham. https://doi.org/10.1007/978-3-031-30037-0_23-1

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