Genome structure variation analyses of peach reveal population dynamics and a 1.67 Mb causal inversion for fruit shape

Abstract

Background Structural variations (SVs), a major resource of genomic variation, can have profound consequences on phenotypic variation, yet the impacts of SVs remain largely unexplored in crops. Results Here, we generate a high-quality de novo genome assembly for a flat-fruit peach cultivar and produce a comprehensive SV map for peach, as a high proportion of genomic sequence is occupied by heterozygous SVs in the peach genome. We conduct population-level analyses that indicate SVs have undergone strong purifying selection during peach domestication, and find evidence of positive selection, with a significant preference for upstream and intronic regions during later peach improvement. We perform a SV-based GWAS that identifies a large 1.67-Mb heterozygous inversion that segregates perfectly with flat-fruit shape. Mechanistically, this derived allele alters the expression of the PpOFP2 gene positioned near the proximal breakpoint of the inversion, and we confirm in transgenic tomatoes that PpOFP2 is causal for flat-fruit shape. Conclusions Thus, beyond introducing new genomics resources for peach research, our study illustrates how focusing on SV data can drive basic functional discoveries in plant science.

Many candidates for a single chair: a critical review of the genetic determinant of flat fruit shape trait in peach (Prunus persica L. Batsch)

“…1) and consists of a large chromosomal inversion of about 1.67 Mb (hereafter 1.7-INV) in flat cultivars (compared to the reference genome of the round fruit accession 'Lovell'). This rearrangement was reported by three closely published studies (Zhou et al 2021;Guo et al 2020;Guan et al 2021) perfectly co-segregate in a wide panel of more than 700 accessions from peach and other related species, being H1H2 flat, H1H1 round and H2H2 flat aborting. Haplotypes were obtained by analysing available Illumina re-sequencing data (although several libraries are characterized by a low sequencing depth).…”

“…Following the release of the peach genome sequence (Verde et al 2013), building upon the chromosomal position of the S locus (spanning about 3 Mb) and the strong association of the flat trait with some SSR markers, different research groups moved from classical genetics to genome-wide approaches in search of the causal gene(s) and/or causal variant(s) (Micheletti et al 2015). This approach led to a series of publications identifying at least four different candidate genes for the S trait: Prupe.6G292200, having homology with a constitutively activated cell death 1 protein (hereafter PpCAD1) (Cao et al 2016); Prupe.6G281100, similar to a leucine-rich repeat receptor-like kinase orthologous to the Brassinosteroid insensitive 1-associated receptor kinase 1 group (PpLRR-RLK) (López-Girona et al 2017); Prupe.6G290900 encoding a putative OVATE Family Protein (PpOFP1) (Zhou et al 2021;Guo et al 2020;Guan et al 2021); and Prupe.6G323700, homologous of sucrose non-fermenting 1-related kinase, (PpSnRK1βγ/PpSNF4) (Guo et al 2021). Before discussing the rationale behind each candidate gene claim in the abovementioned studies, we first attempt to improve the resolution of the mapped interval at the S locus.…”

“…At the PB border, 'Pan Tao Weihai' sequence reads span the round H1 allele (violet) but not the flat H2 allele (split reads in blue), clearly indicating the absence of a breakpoint. In contrast, the alignment at the DB border is unclear in either H1 or H2 alleles reported the identification (and validation in their respective germplasm collections) of the 1.7-INV through Pac-Bio sequencing of 'Xinjiang Pan Tao #2', an aborting-type P. ferganensis accession (Guo et al 2020), and 'Rui You Pan 1', a flat peach cultivar (Guan et al 2021). Of particular importance, Guan et al (2021) apparently reported a unique large chromosomal rearrangement at the end of chromosome 6 (i.e.…”

“…In contrast, the alignment at the DB border is unclear in either H1 or H2 alleles reported the identification (and validation in their respective germplasm collections) of the 1.7-INV through Pac-Bio sequencing of 'Xinjiang Pan Tao #2', an aborting-type P. ferganensis accession (Guo et al 2020), and 'Rui You Pan 1', a flat peach cultivar (Guan et al 2021). Of particular importance, Guan et al (2021) apparently reported a unique large chromosomal rearrangement at the end of chromosome 6 (i.e. the 1.7-INV) in comparison to Zhou et al (2021), probably due to the adoption of a more stringent cut-off for structural variant identification.…”

“…Authors also speculated about the hypothesis of recombination suppression induced by 1.7-INV as supported by high linkage disequilibrium (LD) levels between SNPs positioned within or adjacent to the inversion in the flat-fruit accessions as compared to the round-fruit ones. Zhou et al (2021), Guo et al (2020) and Guan et al (2021) concentrated their efforts on the proximal breakpoint downstream of Prupe.6G290900 (curiously renamed PpOFP2 by Guan et al (2021) and hereafter indicated only as PpOFP1). This gene is by far the most promising candidate, considering the well-established role of OFP family members in tomato, where they synergistically regulate fruit shape during early organ development by primarily modulating cell division patterns through the OFP-TRM module (Liu et al 2002).…”