An apple somatic mutation of delayed fruit maturation date is primarily caused by a retrotransposon insertion-associated large deletion

Abstract

Somatic mutations may alter important traits in tree fruits, such as fruit color, size and maturation date. Autumn Gala (AGala), a somatic mutation from apple cultivar Gala, matures 4 weeks later than Gala. To understand the mechanisms underlying the delayed maturation, RNA-seq analyses were conducted with fruit sampled at 13 (Gala) and 16 (AGala) time-points during their growth and development. Weighted gene co-expression network analysis (WGCNA) of 23 372 differentially expressed genes resulted in 25 WGCNA modules. Of these, modules 1 (r = -0.98, P = 2E-21) and 2 (r = -0.52, P = 0.004), which were suppressed in AGala, were correlated with fruit maturation date. Surprisingly, 77 of the 152 member genes in module 1 were harbored in a 2.8-Mb genomic region on chromosome 6 that was deleted and replaced by a 10.7-kb gypsy-like retrotransposon (Gy-36) from chromosome 7 in AGala. Among the 77 member genes, MdACT7 was the most suppressed (by 10.5-fold) in AGala due to a disruptive 2.5-kb insertion in coding sequence. Moreover, MdACT7 is the exclusive apple counterpart of Arabidopsis ACT7 known of essential roles in plant development, and the functional allele MdACT7, which was lost to the deletion in AGala, was associated with early fruit maturation in 268 apple accessions. Overexpressing alleles MdACT7 and Mdact7 in an Arabidopsis act7 line showed that MdACT7 largely rescued its stunted growth and delayed initial flowering while Mdact7 did not. Therefore, the 2.8-Mb hemizygous deletion is largely genetically causal for fruit maturation delay in AGala, and the total loss of MdACT7 might have contributed to the phenotype.

Keywords: ACT7; apple; fruit maturation; large deletion; somatic mutation; transposition.