Physiological implications of arginine metabolism in plants

Abstract

Nitrogen is a limiting resource for plant growth in most terrestrial habitats since large amounts of nitrogen are needed to synthesize nucleic acids and proteins. Among the 21 proteinogenic amino acids, arginine has the highest nitrogen to carbon ratio, which makes it especially suitable as a storage form of organic nitrogen. Synthesis in chloroplasts via ornithine is apparently the only operational pathway to provide arginine in plants, and the rate of arginine synthesis is tightly regulated by various feedback mechanisms in accordance with the overall nutritional status. While several steps of arginine biosynthesis still remain poorly characterized in plants, much wider attention has been paid to inter- and intracellular arginine transport as well as arginine-derived metabolites. A role of arginine as alternative source besides glutamate for proline biosynthesis is still discussed controversially and may be prevented by differential subcellular localization of enzymes. Apparently, arginine is a precursor for nitric oxide (NO), although the molecular mechanism of NO production from arginine remains unclear in higher plants. In contrast, conversion of arginine to polyamines is well documented, and in several plant species also ornithine can serve as a precursor for polyamines. Both NO and polyamines play crucial roles in regulating developmental processes as well as responses to biotic and abiotic stress. It is thus conceivable that arginine catabolism serves on the one hand to mobilize nitrogen storages, while on the other hand it may be used to fine-tune development and defense mechanisms against stress. This review summarizes the recent advances in our knowledge about arginine metabolism, with a special focus on the model plant Arabidopsis thaliana, and pinpoints still unresolved critical questions.

Keywords: arginase; arginine; arginine biosynthesis; nitric oxide; ornithine aminotransferase; polyamines; urease.

FIGURE 1

Arginine biosynthesis in plastids and its connection to ammonium assimilation by the GS2/GOGAT-system; GS2: Glutamine synthetase 2; GOGAT: Glutamate synthase; NAGS: N-acetylglutamate synthase; NAGK: N-acetylglutamate kinase; NAGPR: N-acetylglutamatyl-5-P reductase; NAOAT: N-acetylornithine aminotransferase; NAOGAcT: N-acetylornithine-glutamate acetyltransferase; NAOD: N-acetylornithine deacetylase; OTC: Ornithine transcarbamylase; ASSY: Argininosuccinate synthase; ASL: Argininosuccinate lyase; CoA: Coenzyme A; CPS: Carbamoyl phosphate synthetase; NAGK/PII double headed arrow: Regulatory interaction of NAGK and PII protein.

FIGURE 2

Catabolism of arginine in Arabidopsis; BAC1/BAC2: Basic amino acid transporter 1/2; δOAT: Ornithine-δ-aminotransferase; ProDH: Proline dehydrogenase; P5CDH: P5C dehydrogenase; P5C: Pyrroline-5-carboxylate; Q/QH₂: oxidized/reduced ubiquinone.

FIGURE 3

Metabolism of arginine and its utilization for polyamine synthesis and NO generation in Arabidopsis; ODC: Ornithine decarboxylase; OTC: Ornithine transcarbamylase; ASSY: Argininosuccinate synthase; ASL: Argininosuccinate lyase; ADC: Arginine decarboxylase; AIH: Agmatine iminohydrolase; NLP: N-carbamoylputrescine amidase; SPDS: Spermidine synthase; SPMS: Spermine synthase; dSAM: decarboxylated S-Adenosyl-L-methionine; NOS-like: Nitric oxide synthase like; NO: Nitric oxide.