Evolution of the biochemistry underpinning purine alkaloid metabolism in plants

Abstract

Purine alkaloids are naturally occurring nitrogenous methylated derivatives of purine nucleotide degradation products, having essential roles in medicine, food and various other aspects of our daily lives. They are generated through convergent evolution in different plant species. The pivotal reaction steps within the purine alkaloid metabolic pathways have been largely elucidated, and the convergent evolution of purine alkaloids has been substantiated through bioinformatic, biochemical and other research perspectives within S-adenosyl-ʟ-methionine-dependent N-methyltransferases. Currently, the biological and ecological roles of purine alkaloids, further refinement of the purine alkaloid metabolic pathways and the investigation of purine alkaloid adaptive evolutionary mechanisms continue to attract widespread research interest. The exploration of the purine alkaloid metabolic pathways also enhances our comprehension of the biochemical mechanism, providing insights into inter-species interactions and adaptive evolution and offering potential value in drug development and agricultural applications. Here, we review the progress of research in the distribution, metabolic pathway elucidation and regulation, evolutionary mechanism and ecological roles of purine alkaloids in plants. The opportunities and challenges involved in elucidating the biochemical basis and evolutionary mechanisms of the purine alkaloid metabolic pathways, as well as other research aspects, are also discussed. This article is part of the theme issue 'The evolution of plant meta-bolism'.

Keywords: convergent evolution; genomic and biochemical investigation; metabolic pathway elucidation; purine alkaloids.

Figure 1.

Chemical structure of purine alkaloids and related metabolites in plants.

Figure 2.

Simplified purine skeleton donor pathways of purine alkaloids in plants. The main metabolites, enzymes and reactions involved in this metabolic pathway are shown. Enzymes are represented by abbreviated names in black text and metabolites are highlighted in different colours. Arrows indicate the direction of chemical reactions: the solid black arrows represent enzymes participating in this reaction that have been clearly identified in plants, while dashed black arrows represent enzymes that have not yet been explicitly validated. PRPP: 5-phosphoribosyl-1-pyrophosphate; Gln: glutamine; IMP: inosine 5’-monophosphate; IMPDH: IMP dehydrogenase; AMP: adenosine monophosphate; AMPD: AMP deaminase; XMP: xanthosine monophosphate; XMPP: XMP phosphatase; GMP: guanosine monophosphate; GMPS: GMP synthetase; GMPP: GMP phosphatase; SAM: S-adenosyl-l-methionine; SAMS: SAM synthase; NMT: SAM-dependent N-methyltransferase; SAH: S-adenosyl-l-homocysteine; SAHH: SAH hydrolase; Hcy: l-homocysteine; HMT: homocysteine methyltransferase; ADK: ATP-dependent adenosine kinase; APRT: adenine phosphoribosyltransferase; PNP: purine nucleoside phosphorylase; ANase: adenosine nucleosidase; ADSS: adenylosuccinate synthase; ADSL: adenylosuccinate phosphoribosyltransferase; GSDA: guanosine deaminase; GDA: guanine deaminase; XDH: xanthine dehydrogenase; IGK: inosine/guanosine kinase; NSH: nucleoside hydrolase.

Figure 3.

Core purine alkaloid metabolic pathways in plants. Solid arrows represent characterized reactions in plants; enzymes catalysing the corresponding reaction in caffeinated species are labelled next to itthe species name; unvalidated reactions are highlighted with dashed arrows.