Enzyme That Makes You Cry–Crystal Structure of Lachrymatory Factor Synthase from Allium cepa

Abstract

The biochemical pathway that gives onions their savor is part of the chemical warfare against microbes and animals. This defense mechanism involves formation of a volatile lachrymatory factor (LF) ((Z)-propanethial S-oxide) that causes familiar eye irritation associated with onion chopping. LF is produced in a reaction catalyzed by lachrymatory factor synthase (LFS). The principles by which LFS facilitates conversion of a sulfenic acid substrate into LF have been difficult to experimentally examine owing to the inherent substrate reactivity and lability of LF. To shed light on the mechanism of LF production in the onion, we solved crystal structures of LFS in an apo-form and in complex with a substrate analogue, crotyl alcohol. The enzyme closely resembles the helix-grip fold characteristic for plant representatives of the START (star-related lipid transfer) domain-containing protein superfamily. By comparing the structures of LFS to that of the abscisic acid receptor, PYL10, a representative of the START protein superfamily, we elucidated structural adaptations underlying the catalytic activity of LFS. We also delineated the architecture of the active site, and based on the orientation of the ligand, we propose a mechanism of catalysis that involves sequential proton transfer accompanied by formation of a carbanion intermediate. These findings reconcile chemical and biochemical information regarding thioaldehyde S-oxide formation and close a long-lasting gap in understanding of the mechanism responsible for LF production in the onion.

Thiosulfinate Tolerance Is a Virulence Strategy of an Atypical Bacterial Pathogen of Onion

“…In onion, the combined action of alliinase and a second enzyme, lachrymatory factor synthase (LFS) converts the majority of isoalliin (S-1-propenyl-L-cysteine sulfoxide, Figure 1, structure 1c) into syn-propanethial-S-oxide (a.k.a. lachrymatory factor, Figure 1, structure 4), the chemical irritant of onion associated with inducing tears [22]. Conversely, garlic, which lacks LFS-like activity, accumulates nearly 100-fold higher total thiosulfinate per gram fresh weight than onion [21].…”

Pantoea ananatis defeats Allium chemical defenses with a plasmid-borne virulence gene cluster

“…In onion, the combined action of alliinase and a second enzyme, lachrymatory factor synthase (LFS) converts the majority of isoalliin ( S -1-propenyl-L-cysteine sulfoxide, structure 1c) into syn-propanethial-S-oxide (a.k.a. lachrymatory factor, structure 4), the chemical irritant of onion associated with inducing tears (11). Conversely, garlic, which lacks LFS, accumulates nearly 100-fold higher total thiosulfinate per gram fresh weight than onion (10).…”

Allithiolanes: Nine Groups of a Newly Discovered Family of Sulfur Compounds Responsible for the Bitter Off-Taste of Processed Onion

“…Since then, understanding of the chemistry taking place during onion processing has extended enormously. The correct structure of the lachrymatory factor of onion, propanethial S -oxide, has been established, , and the exact mechanism of its formation has been clarified. , Furthermore, a great number of other sulfur compounds formed upon the disruption of onion tissue have been discovered, such as zwiebelanes, cepaenes, , bis­(sulfine), cepathiolanes, , and onionins A − (Figure ). Organoleptic characteristics of some of these compounds were evaluated, but none were reported to exhibit a bitter taste…”