Haplotype-resolved genome assembly of Ficus carica L. reveals allele-specific expression in the fruit

Abstract

In this study, we produced a haplotype-phased genome sequence of the fig tree (Ficus carica L.), a non-Rosaceae fruit tree model species, providing a systematic overview of the organization of a heterozygous diploid genome and, for the first time in a fruit tree, evidence of allelic expression direction-shifting among haplotypes. The genome was used for whole genome analysis of heterozygosis, allelic cytosine methylation, and expression profiles in peel and pulp fruit tissues. The two pseudo-haplotypes spanned approximately 355 and 346 Mbp, respectively, and 97% of the sequences were associated with 13 chromosome pairs of the fig tree. Overall, the methylation profile in peel and pulp tissues showed no variations between the homologous chromosomes. However, we detected differential DNA methylation within defined heterozygous allelic gene regions, particularly in upstream regions. Among 6768 heterozygous coding sequences identified, 4024 exhibited allele-specific expression, with approximately 18% specific to the peel and 14% to the pulp. Specifically, 2715 genes were consistent, with one allele always more expressed than the other in both peel and pulp. On the contrary, 22 allele-specific expressed genes switched allele expression among the fig fruit peel and pulp tissues, indicating evidence of overdominance and suggesting that the genome can express one of the two alleles higher or lower depending on developmental or environmental triggers. Notably, these genes were associated with key biological processes, including fruit maturation regulation, seed maturation, and stress response, highlighting their potential role in the plant's developmental and adaptive functions in view of gene editing-based breeding.