Identification of lipoxygenase (LOX) genes putatively involved in fruit flavour formation in apple (Malus × domestica)
Lipoxygenases (LOXs) are non-heme iron-containing enzymes that catalyse the dioxygenation of polyunsaturated fatty acids. The resulting hydroperoxides are further metabolized into biologically active oxylipins including jasmonic acid and green leaf volatiles (GLV) such as C6-aldehydes and C6-alcohols. LOXs are also known to play a decisive role in the production of volatiles that influence the flavour and aroma of fruits and vegetables. To obtain an overview of the inventory of the apple LOX gene family, the published Golden Delicious genome was mined for LOX coding sequences. In total, 23 putative functional LOX genes were identified and used for the construction of a phylogenetic tree. Two sub-trees were found which differentiate the LOX sequences into type 1- and type 2-LOXs. Their chromosomal locations were assigned to the predicted chromosomes of the assembled Golden Delicious genome sequence. Single LOX genes as well as clusters consisting of up to four genes were detected on apple chromosomes 2, 4, 5, 6, 7, 9, 11, 12, 13 and 16. LOX gene clusters on chromosomes 2 and 7, and on 4 and 12, respectively, indicated duplicated genome regions with high homology, which supports previous hypotheses of an ancient genome-wide duplication event in Malus. By using a PCR-based strategy, eight genes belonging to both type 1- and type 2-LOXs with altogether 30 full-length sequences were cloned. Several putative LOX alleles were detected within the same and among different apple cultivars. Two parental genetic maps available for ‘Discovery’ and ‘Prima’ were used for a quantitative trait locus (QTL) mapping experiment of apple volatile compounds known to be produced by the LOX biosynthetic pathway. The QTL detection resulted in a total number of 15 QTLs for eight volatiles (esters and the aldehyde hexanal) which were located on chromosomes 2, 7, 9 and 12 determined in silico as carriers of at least one LOX gene. To examine the putative roles of apple LOX genes in fruit volatile production, the spatial and temporal expression patterns were analysed by RT-PCR-based transcription analyses of apple leaf and fruit tissues. Two genes, MdLOX1a and MdLOX5e, were identified as candidate genes to be involved in fruit aroma volatile production in apple. The genetic association of QTLs found for the GLV hexanal at the top of chromosome 7, three clustered MdLOX5 genes with a putative 13-LOX function and published apple aphid resistance factors located all in the same region of chromosome 7 indicate that a lipoxygenase action might be involved in Malus aphid resistance reactions.
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