Although flowering in mature fruit trees is recurrent, floral induction can be strongly inhibited by concurrent fruiting, leading to a pattern of irregular fruiting across consecutive years referred to as biennial bearing. The genetic determinants of biennial bearing in apple were investigated using the 114 flowering individuals from an F1 population of 122 genotypes, from a ‘Starkrimson’ (strong biennial bearer)בGranny Smith’ (regular bearer) cross. The number of inflorescences, and the number and the mass of harvested fruit were recorded over 6 years and used to calculate 26 variables and indices quantifying yield, precocity of production, and biennial bearing. Inflorescence traits exhibited the highest genotypic effect, and three quantitative trait loci (QTLs) on linkage group (LG) 4, LG8, and LG10 explained 50% of the phenotypic variability for biennial bearing. Apple orthologues of flowering and hormone-related genes were retrieved from the whole-genome assembly of ‘Golden Delicious’ and their position was compared with QTLs. Four main genomic regions that contain floral integrator genes, meristem identity genes, and gibberellin oxidase genes co-located with QTLs. The results indicated that flowering genes are less likely to be responsible for biennial bearing than hormone-related genes. New hypotheses for the control of biennial bearing emerged from QTL and candidate gene co-locations and suggest the involvement of different physiological processes such as the regulation of flowering genes by hormones. The correlation between tree architecture and biennial bearing is also discussed.
HighlightQTLs and candidate genes for the regulation of budbreak and flowering time reveal new hypotheses on temperature perception in growth resumption at spring time in apple.
SUMMARYIn many perennial fruit trees, flowering in the year following a year with heavy fruit load can be quite limited. This biennial cycle of fruiting, termed alternate bearing, was described 170 years ago in apple (Malus domestica). Apple inflorescences are mainly found on short branches (spurs). Bourse shoots (BS) develop from the leaf axils of the spur. BS apices may terminate~100 days after flowering, with formation of next year's inflorescences. We sought to determine how developing fruit on the spur prevents the adjacent BS apex from forming an inflorescence. The presence of adjacent fruit correlated with reaccumulation of transcript encoding a potential flowering inhibitor, MdTFL1-2, in BS apices prior to inflorescence initiation. BS apices without adjacent fruit that did not flower due to late fruitlet removal, neighbouring fruit on the tree, or leaf removal, also reaccumulated the MdTFL1-2 transcript. Fruit load and gibberellin (GA) application had similar effects on the expression of MdTFL1-2 and genes involved in GA biosynthesis and metabolism. Some apple cultivars are less prone to alternate bearing. We show that the response of a BS apex to different numbers of adjacent fruit differs among cultivars in both MdTFL1-2 accumulation and return flowering. These results provide a working model for the further study of alternate bearing, and help clarify the need for cultivar-specific approaches to reach stable fruit production.
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