Biosynthesis of nitric oxide in plants: An oxidative pathway orchestrated by the interplay of CYP79s, N-OX FMOs, and peroxidases

Abstract

Nitric oxide (NO) is in the Pantheon of plant signal molecules and hormones controlling plant growth, development, and adaptation to environmental challenges. The route of NO biosynthesis in plants has remained enigmatic. Previous studies have shown the ability of peroxidases to utilize oximes for production of NO. Peroxidases are widely spread and highly expressed in plant tissues. What then is the identity of the pathway signature enzyme(s) offering tight, spatio-temporal regulation of NO production to effectuate its specific signal functions? And what are the key selection criteria to be fulfilled for genes and enzymes operating at the global level in an oxidative pathway for NO production in plants? Convergently evolved CYP79s and N-OX FMOs catalyze conversion of different amino acids into oximes. In this Perspective, we delineate how these oxygenases fine-tune spatio-temporal formation of the oximes as committed substrates for peroxidase catalyzed NO production. Based on the spatio-temporal location of the CYP79s and N-OX FMOs present in a specific plant species, NO formation in its different meristematic tissues is catalyzed by CYP79s, N-OX FMOs, or by their operation in conjunction. The oxime-based NO production is accompanied by formation of stoichiometric amounts of a diagnostic specific aldehyde detectable by GLC/LC-MS. When oximes derived from tryptophan, tyrosine, or phenylalanine are substrates for NO production, the different aldehydes formed may be oxidized to auxins. The outlined oxidative route for NO production in plants explains observations difficult to interpret in previous plant signal and hormone studies. FMOs may also contribute to NO-formation in animals.