The yellow‑green plant (Clygp) encodes a signal recognition particle 54 kDa protein regulating chloroplast development and photosynthesis in watermelon

doi:10.1016/j.jia.2025.11.013

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The yellow‑green plant (Clygp) encodes a signal recognition particle 54 kDa protein regulating chloroplast development and photosynthesis in watermelon

Shixiang Duan^{1, 2*}, Yaomiao Guo^{1, 2*}, Lin Deng^{1, 2}, Qishuai Kang^{1, 2}, Changbao Shen^{1, 2}, Xiaohang Xue^{1, 2}, Junling Dou^{1, 2}, Dongming Liu^{1, 2}, Sen Yang^{1, 2}, Xingping Zhang⁴, Yun Deng⁴, Huayu Zhu^{1, 2}^#, Yongdong Sun³^#, Luming Yang^{1, 2}^#

1 College of Horticulture, Henan Agricultural University, Zhengzhou 4500046, China；

2 Research Center of Cucurbit Germplasm Enhancement and Utilization of Henan Province, Zhengzhou 4500046, China；

3 School of Horticulture and Landscape Architecture, Henan Institute of Science and Technology, Xinxiang 453003, China

4 Peking University Institute of Advanced Agricultural Sciences, Weifang, 261325, China

Highlights

1. A novel chlorophyll-deficient yellow-green mutant PKH352 was identified from an EMS-induced watermelon mutant library.

2. Mutation in ClG42_04g0106300 gene, encoding a signal recognition particle 54 kDa protein, leads to the yellow-green phenotype and reduced photosynthetic efficiency in watermelon.

3. The ClG42_04g0106300 gene plays an essential regulatory role in chloroplast biogenesis and chlorophyll metabolism in watermelon.

Abstract
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摘要

光合作用作为高等植物营养物质合成的主要来源，提高光合效率有助于显著提高作物的产量和果实品质。叶色突变体作为研究高等植物叶绿体发育和光合作用机制的理想材料，在大田作物中被广泛研究，但其在西瓜中的研究与应用十分有限。本研究从西瓜EMS诱变突变体库中筛选获得一个黄绿表型突变体PKH352，其叶绿素含量和最大光化学效率显著降低。遗传分析表明该突变体的黄绿性状受隐性单基因调控，命名为Clygp（Citrullus lanatus yellow-green plant）。通过在440株的F₂群体中进行MutMap和连锁分析，我们鉴定出ClG42_04g0106300基因上的单核苷酸多态性（SNP）突变为PKH352黄绿表型变异的原因，该基因编码一个叶绿体信号识别颗粒54kD亚基蛋白。利用CRISPR/Cas9基因编辑体系验证，敲除ClG42_04g0106300基因导致西瓜出现黄绿表型，进一步验证了该基因的功能。此外，转录组分析显示，ClG42_04g0106300基因突变显著影响叶绿体发育和光合作用中相关基因的表达，充分表明其在这些生物学通路中起重要作用。综上所述，本研究为解析西瓜叶绿体发育和光合效率的分子机制提供了新的基因资源，为培育高光合效率西瓜品种奠定了理论基础。

Abstract

Photosynthesis serves as the primary source of nutrients synthesized in higher plants, and enhancing photosynthetic efficiency can significantly improve crop yield and fruit quality. Leaf color mutants, which are ideal materials for studying chloroplast development and photosynthesis mechanisms, have been extensively investigated in field crops. However, the study on their application in watermelon remains limited. In this study, we identified a yellow-green phenotype mutant, PKH352, from an EMS mutagenesis watermelon mutant library. The chlorophyll content and maximal photochemical efficiency in PKH352 was significantly reduced. Genetic analysis showed that the mutated trait was controlled by a single nuclear gene, which named as Clygp (Citrullus lanatus yellow-green plant). Through MutMap and linkage analysis in an F₂ population of 440 plants, we identified a single nucleotide polymorphism (SNP) mutation in ClG42_04g0106300, which encoded a signal recognition particle 54 kDa protein, as the causal variant for the yellow-green phenotype. Further validation using a CRISPR/Cas9-mediated system confirmed that knockout of ClG42_04g0106300 results in the yellow-green phenotype in watermelon. In addition, comparative transcriptomic analysis revealed that the ClG42_04g0106300 mutations greatly affected the expression of key genes associated with chloroplast development and photosynthesis, providing strong evidence that it plays a critical role in these biological pathways. Taken together, these findings provide insights into the molecular mechanisms underlying chloroplast development and photosynthetic efficiency, offering a theoretical basis for breeding watermelon varieties with high photosynthetic efficiency.

Keywords: watermelon yellow-green phenotype photosynthesis fine-mapping gene editing

Online: 13 November 2025

Fund:

This research was supported by the National Natural Science Foundation of China (Grant No.

32172602, 32472739), Excellent Youth Foundation of Henan Scientific Committee (Grant No. 242300421030), and Science and Technology Project of the Tibetan Plateau Seed Breeding Technology Innovation Center (No. LSQSCNYQ2025006).

About author: Shixiang Duan, E-mail: sxiangduan@163.com; Yaomiao Guo, E-mail: yaomiaoguo@163.com; #Correspondence Huayu Zhu, E-mail: hyzhu@henau.edu.cn; Yongdong Sun, E-mail: sunyd2001@163.com; Luming Yang, E-mail: lumingyang@henau.edu.cn *These authors contributed equally to this study

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Shixiang Duan, Yaomiao Guo, Lin Deng, Qishuai Kang, Changbao Shen, Xiaohang Xue, Junling Dou, Dongming Liu, Sen Yang, Xingping Zhang, Yun Deng, Huayu Zhu, Yongdong Sun, Luming Yang. 2025. The yellow‑green plant (Clygp) encodes a signal recognition particle 54 kDa protein regulating chloroplast development and photosynthesis in watermelon. Journal of Integrative Agriculture, Doi:10.1016/j.jia.2025.11.013

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