Different flowering response to various fruit loads in apple cultivars correlates with degree of transcript reaccumulation of a TFL1-encoding gene

In 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 170years 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 similar to 100days 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. Significance Statement Biennial fruiting, also called alternate bearing, can affect fruit quality in heavy-bearing years and reduce yield in the subsequent sparce-bearing year. Here we use apple as a model to dissect the molecular events underlying alternate bearing; we show that the presence of adjacent fruit leads to reaccumulation of a flowering repressor in buds developing for the subsequent year. We further show that cultivars vary for this response, suggesting that cultivar-specific manipulations can improve annual fruit production.