Elsevier

Journal of Plant Physiology

Volume 163, Issue 3, 10 February 2006, Pages 348-357
Journal of Plant Physiology

Lipoxygenases: Occurrence, functions and catalysis

https://doi.org/10.1016/j.jplph.2005.11.006Get rights and content

Summary

Lipid peroxidation is common to all biological systems, both appearing in developmentally and environmentally regulated processes. Products are hydroperoxy polyunsaturated fatty acids and metabolites derived there from collectively named oxylipins. They may either originate from chemical oxidation or are synthesized by the action of various enzymes, such as lipoxygenases (LOXes). Signalling compounds such as jasmonates, antimicrobial and antifungal compounds such as leaf aldehydes or divinyl ethers, and a plant-specific blend of volatiles including leaf alcohols are among the numerous products. Cloning of many LOXes and other key enzymes metabolizing oxylipins, as well as analyses by reverse genetic approaches and metabolic profiling revealed new insights on oxylipin functions, new reactions and the first hints on enzyme mechanisms. These aspects are reviewed with respect to function of specific LOX forms and on the development of new models on their substrate and product specificity.

Introduction

Composition of intracellular lipids is frequently altered during plant development. This turnover is among the first targets of environmental cues (Somerville et al., 2000). Apart from the turnover of fatty acids within lipids, formation of oxidized polyunsaturated fatty acids (PUFAs), collectively called oxylipins, is one of the main reactions in lipid alteration (Müller, 2004). The initial formation of hydroperoxides may occur either by chemical oxidation (Müller, 2004) or by the action of enzymes such as lipoxygenases (LOXes) (Brash, 1999) or α-dioxygenase (Hamberg et al., 2002). The metabolism of PUFAs via the LOX-catalyzed step and the subsequent reactions are collectively named LOX pathway (Blée, 2002). Recent cloning, expression, and functional analysis of genes coding for LOXes and other members of the LOX pathway, as well as metabolite profiling and enzyme-mechanistic studies, shed new light on the function of specific LOXes. Occurrence, functions and properties of some specialized LOXes, are the main focus of this review.

LOXes (linoleate:oxygen oxidoreductase, EC 1.13.11.12) constitute a large gene family of non-heme iron containing fatty acid dioxygenases, which are ubiquitous in plants and animals (Brash, 1999; Feussner and Wasternack, 2002). LOXes catalyze the regio- and stereo-specific dioxygenation of PUFAs containing a (1Z,4Z)-pentadiene system, e.g., linoleic acid (LA), α-linolenic acid (LeA), or arachidonic acid (AA; Fig. 1). Plant LOXes are classified with respect to their positional specificity of LA oxygenation. LA is oxygenated either at carbon atom 9 (9-LOX) or at C-13 (13-LOX) of the hydrocarbon backbone of the fatty acid leading to two groups of compounds, the (9S)-hydroperoxy- and the (13S)-hydroperoxy derivatives of LA. An alternative and more comprehensive classification of plant LOXes, based on comparison of their primary structure, has been proposed (Shibata et al., 1994). According to their overall sequence similarity, plant LOXes can be grouped into two gene subfamilies. Those enzymes harboring no plastidic transit peptide have a high sequence similarity (>75%) to one another and are designated type 1-LOXes. However, another subset of LOXes carry a plastidic transit peptide sequence. Based on this N-terminal extension and the fact that these enzymes show only a moderate overall sequence similarity (∼35%) to one another, they have been classified as type 2-LOXes. To date, these LOXes all belong to the subfamily of linoleate 13-LOXes.

Section snippets

Occurrence

As LOXes form gene families in all plants analyzed so far ranging from six genes in Arabidopsis to at least 14 genes in potato, the intracellular localization of a LOX provides a clue as to the physiological function of the different LOXes (Feussner and Wasternack, 2002). This has been analyzed in more detail in cotyledons, fruits, and leaves and a parallel occurrence of particulate, cytosolic, and vacuolar LOXes was observed. In cucumber cotyledons, besides soluble LOXes, particulate LOXes

Functions

In case of storage-lipid mobilization a new pathway has been suggested that is associated with the expression of a specific type 1-LOX and may occur in parallel to classical lipase-dependent pathway in certain oilseeds such as cucumber, sunflower and linseed (Fig. 2) (Feussner et al., 2001). As a first step disruption of the integrity of the lipid body membrane is required. This might be facilitated by two sequential or simultaneous reactions: (i) proteolytic digestion of the membrane-shielding

Catalysis of LOXes

Oxygenation of naturally occurring PUFAs may proceed enzymatically and/or chemically. Both reactions lead to the formation of hydroperoxy PUFAs but there are important differences between the two processes (Kühn and Thiele, 1999). The most important difference is the specificity of the product pattern. Non-enzymatic lipid peroxidation leads to an unspecific product mixture consisting of various positional and optical isomers. In contrast, during LOX reaction PUFAs are usually oxygenated to one

Concluding remarks

PUFA oxidation is implicated in plant development and in responding to diverse and variable environmental conditions. The past decade has seen a remarkable increase in our understanding in the involvement of the LOX reactions and their physiological significance. The number and structural as well as functional diversity of LOXes enables the plant to appropriately respond to environmental challenges and not only to metabolize its lipids, but to introduce new functionalities in these important

Acknowledgements

The research of our lab was supported by a grant (project B23 of the SFB 363) of the Deutsche Forschungsgemeinschaft.

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