Review
Pathways of straight and branched chain fatty acid catabolism in higher plants

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Abstract

Significant advances in our knowledge of fatty acid breakdown in plants have been made since the subject was last comprehensively reviewed in the early 1990s. Many of the genes encoding the enzymes of peroxisomal β-oxidation of straight chain fatty acids have now been identified. Biochemical genetic approaches in the model plant, Arabidopsis thaliana, have been particularly useful not only in the identification and functional characterisation of genes involved in fatty acid β-oxidation but also in establishing the role of β-oxidation at different stages in plant development. Advances in our understanding of branched chain amino acid catabolism have provided convincing evidence that mitochondria play an important role in this process. This work is discussed in the context of the long running debate on the sub-cellular localisation of fatty acid β-oxidation in plants. A significant aspect of this review is that it provides the opportunity to present a comprehensive analysis of the complete Arabidopsis genome sequence for each of the different gene families that are known to be involved in β-, α-, and ω-oxidation of fatty acids in plants. Inevitably, this increase in information, as well as providing many answers also raises many new intriguing questions, particularly as regards the regulation and physiological role of fatty acid catabolism throughout the higher plant life cycle.

Introduction

Fatty acids play an essential role in membrane lipid structure in all living cells. In addition, these hydrophobic compounds can also play specific roles in metabolic processes and signalling events. For example, lipid in the form of triacylglycerol is a common form of high energy storage compound in a variety of organisms including plants where it is present in the seeds of many species. The capacity to synthesise and break down fatty acids evolved early in living cells and consequently there is a considerable degree of homology in the associated enzymatic steps and proteins across genera. However, there are also some important differences in terms of the types of fatty acids that are synthesised and broken down, the specific enzymatic steps involved and the subcellular localisation of both the synthesis and breakdown processes.

The biochemistry of fatty acid catabolism has been extensively studied in various organisms since its discovery in 1904 by Franz Knoop. In a landmark study, that involved feeding synthetic even and odd numbered fatty acids to dogs and monitoring the breakdown products in their urine, Knoop deduced that fatty acids are degraded by oxidation at the β-carbon and the removal of C-2 units. A substantial body of literature now exists on the enzymatic processes involved and in recent years this has extended to information on the associated genes. The last major review of fatty acid breakdown in plants in the current journal was almost 10 years ago [1] and that article still serves as an excellent account of the underlying enzymology associated with this process. The current review will focus on progress since then, most of which relates to the identification and functional characterisation of genes encoding the enzymes of peroxisomal β-oxidation, which is the predominant route for straight chain fatty acid breakdown in higher plants. Recent advances, through gene identification, in our understanding of the breakdown of branched chain amino acids that shed new light on the long-running debate of the involvement of mitochondria in β-oxidation in higher plants are also addressed.

The identification of a gene for a particular enzymatic step or biochemical process in one organism often leads to the rapid identification of homologues of that gene in others. The increase in the number and size of Expressed Sequence Tag (EST) and genomic sequence databases over the last few years has allowed simple pairwise sequence alignment algorithms to be used for the identification of plant homologs of genes identified in other organisms. This is particularly true for genes encoding enzymes of many of the pathways of primary metabolism. The recent completion of the Arabidopsis thaliana genome sequence [2] enables exhaustive searches for homologues of previously identified genes to be performed. We can therefore now aim to have a complete knowledge of all the genes and enzymes that are involved in a specific biochemical process in the various cell types throughout the life cycle of this model plant. Towards this, in the current review we will focus on Arabidopsis providing a comprehensive analysis of the genome sequence with respect to genes that are known or expected to be associated with the fatty acid breakdown process (Table 1).

Section snippets

Germination and post-germinative growth of oilseeds

Fatty acid catabolism is a major metabolic process in germinating oilseeds such as castor bean, cucumber and Arabidopsis. Fatty acids are β-oxidised to C-2 units that are converted to sucrose by way of the glyoxylate cycle and gluconeogenesis. Studies performed primarily in castor bean endosperm in the 1960s demonstrated that both β-oxidation and the glyoxylate cycle occur within specialised peroxisomes termed glyoxysomes [3], [4]. Recent work on the identification and characterisation of an

Fate of acetyl-CoA derived from peroxisomal β-oxidation

Acetyl-CoA derived from the breakdown of storage lipid during oilseed germination is used to support growth during early seedling development. The glyoxylate cycle plays a key role during this period since it enables the acetyl-CoA to be used for the synthesis of carbohydrate [8]. The extent to which acetyl-CoA derived from breakdown of seed storage lipid contributes to gluconeogenesis versus respiration appears to relate to the physiology of the oilseed [11], [12]. Some oilseeds such as castor

Maintenance of reducing equivalents for peroxisomal β-oxidation

Both fatty acid β-oxidation and glyoxylate cycle operation require a supply of NAD+. Mettler and Beevers [39] proposed a malate/aspartate shuttle transferring reducing equivalents across the peroxisomal membrane to account for the reoxidation of NADH. Work carried out in S. cereviseae has shown that a mutation in the peroxisomal malate dehydrogenase impairs fatty acid β-oxidation and growth of cells on oleate, suggesting that the enzyme is involved in the regeneration of NAD+ for this pathway

Subcellular localisation of fatty acid β-oxidation—the peroxisome versus mitochondrion debate

The dramatic breakdown of storage triacylglycerol derived fatty acids that occurs during germination and post-germinative growth of oilseeds was originally shown to occur predominantly in specialised peroxisomes termed glyoxysomes which house enzymes of the glyoxylate cycle and β-oxidation [40], [41]. More recently Hoppe and Theimer have demonstrated that during post-germinative growth of oilseed rape β-oxidation of straight chain fatty acids occurs exclusively in these organelles [42]. Kunce

Degradation of common straight-chain fatty acids

In this section the present state of knowledge concerning the degradation of straight-chain saturated and unsaturated fatty acids (lacking additional groups) is reviewed. In brief, fatty acids are first activated to acyl-CoAs by acyl-CoA synthetase, making them available for oxidative attack at the C-3 position (or β-carbon). The acyl-CoAs are imported into the peroxisome and in the β-oxidation spiral C-2 units are repeatedly cleaved from the thiol end of the fatty acid yielding acetyl-CoA (

Degradation of branched-chain 2-oxo acids

2-Oxo acids are intermediates in the catabolism of the branched chain amino acids (BCAAs) leucine, isoleucine and valine. Transamination of BCAAs produces α-keto acids and these then undergo oxidative decarboxylation and esterification to form acyl-CoA esters. The breakdown of these esters requires β-oxidation (Fig. 3). The cellular location of branched chain amino acid breakdown remains a topic of debate. Work performed on peroxisomes and mitochondria from mung bean hypocotyls demonstrated

Germination and post-germinative growth

Changes in enzyme activities closely reflect those of mRNA levels for β-oxidation genes during germination and post-germinative growth. For example the Arabidopsis AtACX1, AtACX2, AtACX3, AtACX4 genes that encode the family of acyl-CoA oxidase enzymes [14], [16], [18], [110], the MFP2 gene encoding the multifunctional protein [15], [33] and the thiolase encoding PED1 gene [6] all show an increase in mRNA levels during germination that correspond with an increase in enzyme activity. In

α-Oxidation of fatty acids in higher plants

The metabolic pathway for the oxidation of straight chain fatty acids at the α-position was first proposed by Stumpf [152] when he showed that a preparation from peanut cotyledons catalysed the oxidation of palmitic acid into a long chain fatty aldehyde and CO2. A reaction mechanism for α-oxidation of C14:0 to C18:x fatty acids was proposed by Shine and Stumpf [153] that involved the production of the intermediate D-2-hydroperoxyl fatty acid which is decarboxylated to fatty aldehyde and/or

Omega oxidation of fatty acids in higher plants

The recent description of three long-chain fatty acid alcohol oxidase genes from Candida species has led to the identification of a family of genes involved in lipid ω-oxidation in yeast with homologues in plants and bacteria [158]. Candida cloacae and Candida tropicalis metabolise both alkanes and long-chain fatty acids sequentially through a membrane bound ω-oxidation pathway and the peroxisomal β-oxidation pathway. During ω-oxidation the omega (last) carbon with respect to the carboxylate

Conclusions

Research over the last 10 years on the pathways of straight and branched chain fatty acid catabolism in higher plants has resulted in the identification of many of the genes encoding enzymes of the different pathways, provided information on their regulation and in some cases given an insight into their physiological role. The power of the genetic approach using Arabidopsis, coupled with rigorous biochemical analysis of mutant phenotypes will continue to make a major contribution to this field.

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