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Identification of lipoxygenase (LOX) genes putatively involved in fruit flavour formation in apple (Malus × domestica)

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Abstract

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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Acknowledgments

This research was financially supported by the Deutsche Forschungsgemeinschaft in frame of the project numbers AOBJ 575560 and AOBJ 575561. The authors wish to thank Ines Kasten and Kirsten Weiß for excellent technical assistance on volatile analysis.

Data archiving statement

The annotated nucleotide sequences of the cloned Malus LOX genes are deposited in the NCBI GenBank database under the following accession numbers: KC489087, KC489088, KC489089, KC489090, KC489091, KC489092, KC494371, KC494372, KC494373, KC494374, KC494375, KC494376, KC494377, KC494378, KC494379, KC494380, KC494381, KC494382, KC494383, KC494384, KC494385, KC494386, KC494387, KC494388, KC494389, KC494390, KC494391, KC747489, KC747490 and KC747491. Details of the sequences are listed in Table 2. Additional figures and tables are provided in the electronic supplementary section.

Author information

Authors and Affiliations

  1. Institute for Breeding Research on Horticultural and Fruit Crops, Julius Kühn Institute (JKI), Pillnitzer Platz 3a, 01326, Dresden, Germany

    Jörg Vogt

  2. Biotechnology of Natural Products, Technische Universität München, Liesel-Beckmann-Str. 1, 85354, Freising, Germany

    Doreen Schiller & Wilfried Schwab

  3. Institute for Ecological Chemistry, Plant Analysis and Stored Product Protection, Julius Kühn Institute (JKI), Erwin-Baur-Str. 27, 06484, Quedlinburg, Germany

    Detlef Ulrich

  4. Institute for Breeding Research on Horticultural and Fruit Crops, Julius Kühn Institute (JKI), Erwin-Baur-Str. 27, 06484, Quedlinburg, Germany

    Frank Dunemann

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  1. Jörg Vogt
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  2. Doreen Schiller
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  3. Detlef Ulrich
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  4. Wilfried Schwab
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  5. Frank Dunemann
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Corresponding author

Correspondence to Frank Dunemann.

Additional information

Communicated by D. Neale

Electronic supplementary material

Below is the link to the electronic supplementary material.

Suppl. Figure 1

Annotation of selected genes in close proximity to the two MdLOX1/MdLOX7 clusters on chromosomes 4 and 12 and the two MdLOX5 clusters on chromosomes 2 and 7. Genes with the same functional annotation are connected by lines. A high overall collinearity is visible for the respective parts of the putatively homologous chromosome parts originating by a genome-wide duplication event (Velasco et al. 2010). (PDF 30 kb)

Suppl. Figure 2

Sub-cellular localization of all putatively complete deduced apple LOX proteins calculated bioinformatically by multiple sequence alignment. The deduced proteins of underlined genes were expected to be localized in chloroplasts while the others are either cytosolic or might be located either in the cytosol or the chloroplast, respectively. The deduced proteins were ordered in columns as predicted by the software tools used for prediction of sub-cellular localization. (PDF 97 kb)

Suppl. Table 1

List of used PCR primers with their respective sequence and annealing temperature (PDF 36 kb)

Suppl. Table 2

List of biochemically characterized LOX proteins used for construction of the phylogenetic tree shown in Figure 4. The positional specificity of linoleic acid oxygenation and amino acid constitutions at the putative product specificity site are shown. Plant LOX protein designation follows proposals of Feussner and Wasternack (2002), Bannenberg et al. (2009), and Podolyan et al. (2010). (PDF 32 kb)

Suppl. Table 3

Sequence characteristics and allelic diversity for apple LOX genes MdLOX1a and MdLOX7a determined from six cloned full-length sequences of different cultivars. (PDF 22.8 kb)

Suppl. Table 4

QTLs associated with volatile compounds measured in the C3 apple population derived from the cross 'Discovery' x 'Prima' (PDF 21.6 kb)

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Vogt, J., Schiller, D., Ulrich, D. et al. Identification of lipoxygenase (LOX) genes putatively involved in fruit flavour formation in apple (Malus × domestica). Tree Genetics & Genomes 9, 1493–1511 (2013). https://doi.org/10.1007/s11295-013-0653-5

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