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 = À0.98, P = 2E-21) and 2 (r = À0.52, 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.

Vitis labrusca genome assembly reveals diversification between wild and cultivated grapevine genomes

“…(2019) were enriched in defense response functions, and hemizygosity also affected berry color in Chardonnay, an important crop trait, which suggests hemizygous genes can contribute to desirable agronomic traits. On the other hand, in apple, another clonally propagated crop, a hemizygous somatic deletion, resulting in the loss of the MdACT7 functional allele in Autumn Gala, contributed to a delay of fruit maturation ( Ban et al., 2022 ). Fruit maturation time is an important trait and early maturing cultivars may be more desirable for some orchards.…”

Somatic Mutations in Fruit Trees: Causes, Detection Methods, and Molecular Mechanisms

“…Examples of internal factors include DNA replication errors [ 18 ], DNA repair errors [ 19 ], transposable elements [ 20 , 21 ], and deletion [ 22 ]. Environmental factors can also affect the frequency and type of somatic mutations [ 23 ].…”

“…Additionally, fruit color has a significant impact on consumer preference [ 73 , 74 , 75 ], which likely explains why researchers have shown particular interest in elucidating the underlying mechanisms of these anthocyanin variants. Research on somatic mutations related to fruit maturation and ripening has been actively conducted in apples [ 22 , 44 , 47 ], citrus [ 56 ], grapes [ 61 ], peaches [ 66 ], and plums [ 72 ]. This is because the selling time of a crop variety is determined by its maturation date, and distinct storage techniques and durations are necessary based on the maturation date and ripening characteristics.…”

“…The candidate genes were then screened using RNA-Seq, and transgenic lines were created using the candidate gene to verify phenotypic differences. In a second example, a 2.8 Mb hemizygous deletion, which is considered the cause of late maturation in somatic mutations, was identified [ 22 ]. Candidate genes were narrowed down using RNA-Seq data from fruit development stages, and transgenic lines were created using the candidate gene MdACT7 for phenotype verification in Arabidopsis .…”