Genetic mechanisms associated with floral initiation and the repressive effect of fruit on flowering in apple (Malus x domestica Borkh)

Many apple cultivars are subject to biennial fluctuations in flowering and
fruiting. It is believed that this phenomenon is caused by a repressive
effect of developing fruit on the initiation of flowers in the apex of
proximal bourse shoots. However, the genetic pathways of floral initiation
are incompletely described in apple, and the biological nature of floral
repession by fruit is currently unknown. In this study, we characterize
the transcriptional landscape of bourse shoot apices in the biennial
cultivar, 'Honeycrisp', during the period of floral initiation,
in trees bearing a high fruit load and in trees without fruit. Trees with
high fruit load produced almost exclusively vegetative growth in the
subsequent year, whereas the trees without fruit produced flowers on the
majority of the potential flowering nodes. Using RNA-based sequence data,
we documented gene expression at high resolution, identifying
>11,000 transcripts that had not been previously annotated, and
characterized expression profiles associated with vegetative growth and
flowering. We also conducted a census of genes related to known flowering
genes, organized the phylogenetic and syntenic relationships of these
genes, and compared expression among homologs. Several genes closely
related to AP1, FT, FUL,
LFY, and SPLS were more strongly expressed in
apices from non-bearing, floral-determined trees, consistent with their
presumed floral-promotive roles. In contast, a homolog
of TFL1 exhibited strong and persistent up-regulation
only in apices from bearing, vegetative-determined trees, suggesting a
roles in floral repression. Additionally, we identified
four GIBBERELLIC ACID (GA) 2 OXIDASE genes that were
expressed to relatively high levels in apices from bearing trees. These
results define the flowering-related transcriptional landscape in apple,
and strongly support previous studies implicating both gibberellins
and TFL1 as key components in repression of flowering by
fruit.