Comparative genomic analyses reveal different genetic basis of two types of fruit in Maloideae

Fleshy fruits are classified as ethylene-dependent or ethylene-independent according to the ethylene climacteric at the onset of ripening. However, the mechanism forming these two types of fruits is unclear. Pears (Pyrus spp.) contain the both types, thus can serve as a model system to answer this question. Here, we assemble haplotype-resolved and chromosome-level genomes for ethylene-dependent and ethylene-independent accessions, and re-sequence 118 pear accessions. Two long noncoding RNAs named Ethylene Inhibiting Factor 1 (EIF1) and EIF2 are identified, which suppress the transcription of ethylene biosynthesis gene ACS1 and ethylene biosynthesis, generating ethylene-independent fruit. Comparative genomic analyses reveal that allele-specific structural variations result in the loss of EIF1 and/or EIF2, removing the suppression on ACS1 transcription and generating ethylene-dependent fruit. Further study reveals that, in most common fleshy fruits of Maloideae, EIF homologue exits in ethylene-independent pear and loquat and is transcribed; while in ethylene-dependent apple and hawthorn, EIF homologue does not exist in their genomes. Based on the ethylene climacteric at the onset of ripening, fleshy fruits can be classified as ethylene-dependent and ethylene-independent. Here, the authors assemble the genomes of both types of pears and reveal genetic basis for their formation.