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ClZISO mutation leads to photosensitive flesh in watermelon

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Abstract

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The mutation of ClZISO identified in EMS-induced watermelon leads to photosensitive flesh in watermelon.

Abstract

Watermelon (Citrullus lanatus) has a colorful flesh that attracts consumers and benefits human health. We developed an ethyl-methanesulfonate mutation library in red-fleshed line ‘302’ to create new flesh color lines and found a yellow-fleshed mutant which accumulated ζ-carotene. The initial yellow color of this mutant can be photobleached within 10 min under intense sunlight. A long-term light-emitting diode (LED) light treatment turned flesh color from yellow to pink. We identified this unique variation as photosensitive flesh mutant (‘psf’). Using bulked segregant analysis, we fine-mapped an EMS-induced G-A transversion in ‘psf’ which leads to a premature stop codon in 15-cis-ζ-carotene isomerase (ClZISO) gene. We detected that wild-type ClZISO is expressed in chromoplasts to catalyze the conversion of 9,15,9’-tri-cis-ζ-carotene to 9,9’-di-cis-ζ-carotene. The truncated ClZISOmu protein in psf lost this catalytic function. Light treatment can partially compensate ClZISOmu isomerase activity via photoisomerization in vitro and in vivo. Transcriptome analysis showed that most carotenoid biosynthesis genes in psf were downregulated. The dramatic increase of ABA content in flesh with fruit development was blocked in psf. This study explores the molecular mechanism of carotenoid biosynthesis in watermelon and provides a theoretical and technical basis for breeding different flesh color lines in watermelon.

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Data availability

The transcriptome sequencing reads have been deposited into the NCBI sequence read archive (SRA) under accession no. PRJNA759595. The genome sequence of ‘97103’ (version 2) is also available at the Cucurbit Genomics Database (http://cucurbitgenomics.org/). SNPs between wild-type 302 and ‘psf’ mutant are available online in accordance with funder data retention policies (https://iibbc.com:51618/share/rfmrQD6Q). The other data used to support the findings of this study are available from the corresponding author upon request.

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Acknowledgements

We thank Dr. Li Li of Cornell University for providing the pAC-ZETA plasmid.

Funding

This research was supported financially by grants from the National Natural Science Foundation of China (31772329 and 31930096), the Ministry of Agriculture and Rural Affairs of China (Grant No. CARS-25), the Bei**g Scholar Program (Grant No. BSP026 and YBSP019), Innovation and Development Program of Bei**g Vegetable Research Center (KYCX202001-08), Key Project of Science and Technology of Ningbo (2019B10007) and Bei**g Agriculture Innovation Consortium (BAIC10-2021).

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Authors and Affiliations

  1. National Watermelon and Melon Improvement Center, Bei**g Academy of Agricultural and Forestry Sciences, Key Laboratory of Biology and Genetic Improvement of Horticultural Crops (North China), Bei**g Key Laboratory of Vegetable Germplasm Improvement, Bei**g, 100097, China

    Jie Zhang, Honghe Sun, Shaogui Guo, Yi Ren, Maoying Li, **fang Wang, Yongtao Yu, Haiying Zhang, Guoyi Gong, Hongju He, Chao Zhang & Yong Xu

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  1. Jie Zhang
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  2. Honghe Sun
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  3. Shaogui Guo
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  10. Hongju He
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  12. Yong Xu
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Contributions

JZ performed most of the experiments and contributed to the writing; HS and SG performed most of the bioinformatics analysis; YR, ML, JW and YY provided technical assistance to JZ; HZ and GG supervised the experiments; HH performed the HPLC analysis; CZ performed the light treat analysis; YX managed the study and agrees to serve as the author responsible for contact and ensures communication.

Corresponding author

Correspondence to Yong Xu.

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Communicated by Amnon Levi.

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Zhang, J., Sun, H., Guo, S. et al. ClZISO mutation leads to photosensitive flesh in watermelon. Theor Appl Genet 135, 1565–1578 (2022). https://doi.org/10.1007/s00122-022-04054-7

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