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Nucleotide variation in the phytoene synthase (ClPsy1) gene contributes to golden flesh in watermelon (Citrullus lanatus L.)

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Abstract

Key message

A gene controlling golden flesh trait in watermelon was discovered and fine mapped to a 39.08 Kb region on chromosome 1 through a forward genetic strategy, and Cla97C01G008760 (annotated as phytoene synthase protein, ClPsy1 ) was recognized as the most likely candidate gene.

Abstract

Vitamin A deficiency is a worldwide public nutrition problem, and β-carotene is the precursor for vitamin A synthesis. Watermelon with golden flesh (gf, which occurs due to an accumulated abundance of β-carotene) is an important germplasm resource. In this study, a genetic analysis of segregated gf gene populations indicated that gf was controlled by a single recessive gene. BSA-seq (Bulked segregation analysis) and an initial linkage analysis placed the gf locus in a 290-Kb region on watermelon chromosome 1. Further fine mapping in a large population including over 1000 F2 plants narrowed this region to 39.08 Kb harboring two genes, Cla97C01G008760 and Cla97C01G008770, which encode phytoene synthase (ClPsy1) and GATA zinc finger domain-containing protein, respectively. Gene sequence alignment and expression analysis between parental lines revealed Cla97C01G008760 as the best possible candidate gene for the gf trait. Nonsynonymous SNP mutations in the first exon of ClPsy1 between parental lines co-segregated with the gf trait only among individuals in the genetic population and were not related to flesh color in natural watermelon panels. Promoter sequence analysis of 26 watermelon accessions revealed two SNPs in the cis-acting element sequences corresponding to MYB and MYC2 transcription factors. RNA-seq data and qRT-PCR verification showed that two MYBs exhibited expression trends similar to that of ClPsy1 in the parental lines and may regulate the ClPsy1 expression. Further research findings indicate that the gf trait is determined not only by ClPsy1 but also by ClLCYB, ClCRTISO and ClNCED7, which play important roles in watermelon β-carotene accumulation.

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All data pertinent to the reported work are provided in the manuscript or supplemental online materials.

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Acknowledgements

This work was supported by funding from the University Nursing Program for Young Scholars with Creative Talents in Heilongjiang Province [Grant# UNPYSCT-201816]; the China Agriculture Research System [Grant No. CARS-25].

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Authors and Affiliations

  1. Key Laboratory of Biology and Genetic Improvement of Horticulture Crops (Northeast Region), Ministry of Agriculture and Rural Affairs, Northeast Agricultural University, Harbin, 150030, China

    Shi Liu, Zhongqi Gao, Xuezheng Wang & Feishi Luan

  2. Horticulture and Landscape Architecture College, Northeast Agricultural University, Harbin, 150030, China

    Shi Liu, Zhongqi Gao, Xuezheng Wang & Feishi Luan

  3. Anhui Jianghuai Horticulture Technology Co., Ltd., Hefei, 230031, China

    Zuyun Dai & Zhongzhou Yang

  4. Horticulture Institute, Anhui Academy of Agricultural Science, Hefei, 230031, China

    Qian Zhang

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  1. Shi Liu
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  4. Feishi Luan
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  5. Zuyun Dai
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Contributions

SL designed the experiment, analyzed the data and wrote the manuscript. ZG performed the major experiments, with the help of SL. XW and FL revised the manuscript. ZD, ZY, and QZ provided some of the materials used in this study and participated in phenotypic data collection. SL and ZG contributed equally to this work. XW and SL are the co-corresponding authors.

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Correspondence to Shi Liu or Xuezheng Wang.

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Liu, S., Gao, Z., Wang, X. et al. Nucleotide variation in the phytoene synthase (ClPsy1) gene contributes to golden flesh in watermelon (Citrullus lanatus L.). Theor Appl Genet 135, 185–200 (2022). https://doi.org/10.1007/s00122-021-03958-0

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