A wild origin of the loss‐of‐function lycopene beta cyclase (CYC‐b) allele in cultivated, red‐fleshed papaya (Carica papaya)

Abstract

PREMISE OF THE STUDY:The red fl esh of some papaya cultivars is caused by a recessive loss-of-function mutation in the coding region of the chromoplastspecifi c lycopene beta cyclase gene ( CYC-b ). We performed an evolutionary genetic analysis of the CYC-b locus in wild and cultivated papaya to uncover the origin of this loss-of-function allele in cultivated papaya. METHODS:We analyzed the levels and patterns of genetic diversity at the CYC-b locus and six loci in a 100-kb region fl anking CYC-b and compared these to genetic diversity levels at neutral autosomal loci. The evolutionary relationships of CYC-b haplotypes were assessed using haplotype network analysis of the CYC-b locus and the 100-kb CYC-b region.KEY RESULTS: Genetic diversity at the recessive CYC-b allele ( y ) was much lower relative to the dominant Y allele found in yellow-fl eshed wild and cultivated papaya due to a strong selective sweep. Haplotype network analyses suggest the y allele most likely arose in the wild and was introduced into domesticated varieties after the fi rst papaya domestication event. The shared haplotype structure between some wild, feral, and cultivated haplotypes around the y allele supports subsequent escape of this allele from red cultivars back into wild populations through feral intermediates. CONCLUSIONS:Our study supports a protracted domestication process of papaya through the introgression of wild-derived traits and gene fl ow from cultivars to wild populations. Evidence of gene fl ow from cultivars to wild populations through feral intermediates has implications for the introduction of transgenic papaya into Central American countries.

Domestication and Genetics of Papaya: A Review

“…By means of a haplotype network, the authors suggest that the y allele likely originated in the wild and was introduced into the domesticated varieties during the domestication of papaya. However, they found shared haplotype structure among some wild, feral, and cultivated haplotypes near the y allele, suggesting a successive escape of the y allele from red cultivars back into wild populations, probably through feral intermediates in Costa Rica (Wu et al, 2017). In other study, Porter et al (2009), using a genome-wide analysis, revealed that papaya has relatively few nucleotide-bindings sites (NBS) encoding genes, but structurally diverse showing a novel subgroup.…”

“…For instance, Wu et al (2017) found evidence of a recent emergence of the y allele and its selection in red fruited cultivation. Analysing the levels and patterns of genetic diversity at the CYC-b locus (y allele) and six loci in a 100-kb region flanking this locus, they found evidence of a strong selective sweep, as genetic diversity showed a reduction at the recessive y allele in comparison with the dominant Y allele present in the yellow-fleshed papayas (wild and cultivated).…”

Comprehensive metabolome and transcriptome analyses demonstrate divergent anthocyanin and carotenoid accumulation in fruits of wild and cultivated loquats

“…To date, dozens of enzymes have been identified with a function in carotenoid biosynthesis and metabolism (Nisar et al, 2015;Hermanns et al, 2020). For fruit production crops, natural variations in IPI (Isopentenyl diphosphate isomerase), PSY (phytoene synthase), CRTISO (carotenoid isomerase), LCYB (lycopene b-cyclase), ZEP (zeaxanthin epoxidase), OR (Orange), and NCED/CCD (9-cisepoxycarotenoid dioxygenase/carotenoid cleavage dioxygenase) genes resulted in diverse colored fruits ranging from white, yellow, pink, orange to red in tomato (Pankratov et al, 2016;Yoo et al, 2023), pepper (Lee et al, 2021), watermelon (Bang et al, 2007;Liu et al, 2021), melon (Tzuri et al, 2015), citrus (Zheng et al, 2019), peach (Falchi et al, 2013), papaya (Wu et al, 2017) and loquat (Fu et al, 2014). These genes encode enzymes that function in the carotenoid biosynthesis and metabolism pathway.…”