Three distinct mutational mechanisms acting on a single gene underpin the origin of yellow flesh in peach

Abstract

Peach flesh color (white or yellow) is among the most popular commercial criteria for peach classification, and has implications for consumer acceptance and fruit nutritional quality. Despite the increasing interest in improving cultivars of both flesh types, little is known about the genetic basis for the carotenoid content diversity in peach. Here we describe the association between genotypes at a locus encoding the carotenoid cleavage dioxygenase 4 (PpCCD4), localized in pseudomolecule 1 of the Prunus persica reference genome sequence, and the flesh color for 37 peach varieties, including two somatic revertants, and three ancestral relatives of peach, providing definitive evidence that this locus is responsible for flesh color phenotype. We show that yellow peach alleles have arisen from various ancestral haplotypes by at least three independent mutational events involving nucleotide substitutions, small insertions and transposable element insertions, and that these mutations, despite being located within the transcribed portion of the gene, also result in marked differences in transcript levels, presumably as a consequence of differential transcript stability involving nonsense-mediated mRNA decay. The PpCCD4 gene provides a unique example of a gene for which humans, in their quest to diversify phenotypic appearance and qualitative characteristics of a fruit, have been able to select and exploit multiple mutations resulting from a variety of mechanisms.

CAROTENOID CLEAVAGE DIOXYGENASE4Is a Negative Regulator of β-Carotene Content inArabidopsisSeeds

“…These data suggest that allele-specific differences in CCD4 expression in developing seeds significantly contribute to natural variation in seed b-carotene levels ( Figure 4B), a finding consistent with studies of carotenoid natural variation in maize kernels, where altered gene expression at loci for pathway biosynthetic enzymes also make large contributions to traits (Harjes et al, 2008;Yan et al, 2010). Regulation of tissue carotenoid levels by alteration of CCD4 expression appears to be an evolutionarily conserved mechanism, as it also underlies the selection through breeding of elevated carotenoid levels in nonseed tissues, including Chrysanthemum morifolium petals, potato (Solanum tuberosum) tubers, and peach (Prunus persica) fruit flesh (Ohmiya et al, 2006;Campbell et al, 2010;Brandi et al, 2011;Falchi et al, 2013).…”

Molecular genetics of blood‐fleshed peach reveals activation of anthocyanin biosynthesis by NAC transcription factors

“…Error bars show the SE of the mean. being controlled by a single locus (Y), with white flesh dominant over yellow flesh (Falchi et al, 2013). Cultivars DHP and SG have YY and yy genotypes at the Y locus, respectively.…”

“…In Europe, blood-fleshed peach cultivars were grown as early as 1659 (Hedrick, 1917). More recently, several studies have revealed that the yellow-flesh trait results from the accumulation of carotenoids, which are controlled by a single gene encoding carotenoid cleavage dioxygenase in peach (Falchi et al, 2013;Ma et al, 2014). However, the molecular mechanism underlying the blood-flesh trait remains unclear.…”

Application of sequence specific amplified polymorphism (SSAP) and simple sequence repeat (SSR) markers for variability and molecular assisted selection (MAS) studies of the Mexican guava

“…The association of retroelements with QTL related to fruit color has been described in economically important fruit crops such as peach (Falchi et al, 2013), grapevine (Kobayashi et al, 2004;Pelsy, 2010), and blood orange (Butelli et al, 2012). It has been suggested that high levels of activity of mobile elements (retroelements) can contribute to increment allelic diversity related to fruit color (Tao et al, 2005;Rico-Cabañas andMartinezIzquierdo, 2007, De Felice et al, 2009;Butelli et al, 2012).…”