Comparative Analysis of Transcripts Differentially Expressed in Regular and Alternative Fruit-bearing Apple (Malus × domestica Borkh.) Cultivars with Various Bioactive Gibberellic Acid Levels

Abstract

Many horticultural trees, including apple (Malus × domestica Borkh.), exhibit alternative fruit bearing. Despite many observations suggesting that bearing tendency is a genetic trait, genetic factors related to bearing tendency have rarely been investigated, as most previous studies have focused on comparing phytohormone and gene expression levels between ON- and OFF-years within a cultivar. Therefore, to gain insights into the genetic factors related to the strength of biennial bearing, we compared gene expression levels between the regular bearing cultivar ‘McIntosh’ and the alternative bearing cultivar ‘Wijcik’ (the bud mutant of ‘McIntosh’). Over a three-year period, the flowering rate of ‘McIntosh’ remained relatively stable, ranging from 89% to 95%, whereas that of ‘Wijcik’ showed significant variation from 83% to 24% before returning to 89%. Comparative transcriptome analysis of terminal buds during the floral induction period revealed 7,200 genes that were differentially expressed between the two cultivars, with 1,423 genes showing annual variation only in ‘Wijcik’. Gene Ontology enrichment analysis revealed upregulation of many genes related to photosynthesis and response to high light intensity in the OFF-year in ‘Wijcik’. Moreover, the relative expression levels of flowering repressors, such as MdTFL1-1, MdTFL1-2, MdRAP2.7, and MdJMJ13, at 75 days after full bloom were significantly higher in the ON-year than in the OFF-year for ‘Wijcik’. Our findings suggest that the high biennial bearing tendency of columnar apples may be attributed, in part, to greater annual variation in the expression of MdTFL1 and light-related genes.