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Journal of Integrative Agriculture  2026, Vol. 25 Issue (7): 2836-2846    DOI: 10.1016/j.jia.2025.12.029
Horticulture Advanced Online Publication | Current Issue | Archive | Adv Search |
A mutation in BrPRPL1 causes leaf yellowing by influencing chloroplast protein translation in Chinese cabbage

Xiaowei Ren1, 2*, Xing Li1*, Jie Li1*, Jindi Fan1, Mengyao Yuan1, Yan Li1, Daling Feng1, Yin Lu1, Hao Liang1, Xiaofei Fan1, Lei Sun1, Kehui Ren1, Mengyang Liu1#, Wei Ma1#, Jianjun Zhao1#

 1 State Key Laboratory of North China Crop Improvement and Regulation/Key Laboratory of Vegetable Germplasm Innovation and Utilization of Hebei/Collaborative Innovation Center of Vegetable Industry in Hebei, College of Horticulture, Hebei Agricultural University, Baoding 071000, China

2 Department of Agriculture and Food Science, Shijiazhuang University, Shijiazhuang 050035, China

 Highlights 

The large subunit ribosomal protein L1 of the chloroplast (BrPRPL1) is the candidate gene of Mut298.
The silencing of BrPRPL1 results in leaf yellowing of Chinese cabbage.
A single nucleotide change from C to T in BrPRPL1 significantly reduces the accumulation of chloroplast genome-encoded proteins RbcL, PsaA, and PsaB.


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摘要  

叶色直接影响叶菜的外观质量和营养品质,决定其经济价值。我们从甲基磺酸乙酯(EMS)诱导的大白菜突变体库中鉴定出一种金黄叶色的突变体Mut298。通过正向遗传学的方法,已经证明Mut298的叶黄表型是由于编码叶绿体核糖体大亚基蛋白L1的BrPRPL1基因的保守结构域中发生了一个从C到T的突变引起的。PRPL1突变导致拟南芥胚胎致死,这使PRPL1在植物叶片发育中的作用知之甚少。在这项研究中,BrPRPL1的突变导致关键叶绿体核糖体编码蛋白(RbcL、PsaA和PsaB)的表达显著降低,并导致叶绿体发育异常。此外,Mut298植株的叶绿素含量和光合参数显著低于野生型植株,导致大白菜叶片呈金黄色。本研究详细介绍了PRPL1突变对叶绿体核糖体翻译的影响,为未来研究PRPL1在植物生长发育中的调节作用奠定了基础。



Abstract  

Leaf color directly affects the appearance quality and nutritional quality of leafy vegetables, thereby determining their economic value.  Here, we identified a golden leaf mutant, Mut298, from an ethyl methanesulfonate (EMS)-induced mutant library of Chinese cabbage.  Through the approach of forward genetics, it has been demonstrated that the phenotype of Mut298 is due to a single nucleotide substitution from C to T that changes glycine to arginine in the conserved domain of BrPRPL1, which encodes the large subunit ribosomal protein L1 of the chloroplast.  Because the PRPL1 mutation causes embryonic lethality in Arabidopsis, the function of PRPL1 in leaf development remains elusive.  In this study, the mutation of BrPRPL1 causes a substantial reduction in the expression of key chloroplast-encoded proteins (RbcL, PsaA, and PsaB) and disrupts chloroplast development.  Moreover, the chlorophyll content and photosynthetic parameters are significantly lower in Mut298 plants than in wild-type plants, resulting in golden yellow leaves in Chinese cabbage.  This study reveals the impact of PRPL1 mutation on ribosome translation within chloroplasts and provides a theoretical a foundation for future research into the regulatory roles of PRPL1 in plant growth and development.

Keywords:  Chinese cabbage       mutant       chloroplast       gene function       ribosome translation  
Received: 13 March 2025   Accepted: 17 November 2025 Online: 18 December 2025  
Fund: 

This study was supported by the grants from the National Natural Science Foundation of China (32222076, 32330096, 32472736, and 32272712), the Hebei Natural Science Foundation (C2023204308 and C2024204246), the Central Guiding Local Technology Development Fund (246Z6312G and 246Z6311G), the Earmarked Fund for CARS (CARS-23), and the State Key Laboratory of North China Crop Improvement and Regulation (NCCIR2023ZZ-19).

About author:  #Correspondence Mengyang Liu, E-mail: liumengyang_7@163.com; Wei Ma, E-mail: mawei0720@163.com; Jianjun Zhao, E-mail: yyzjj@hebau.edu.cn * These authors contributed equally to this study.

Cite this article: 

Xiaowei Ren, Xing Li, Jie Li, Jindi Fan, Mengyao Yuan, Yan Li, Daling Feng, Yin Lu, Hao Liang, Xiaofei Fan, Lei Sun, Kehui Ren, Mengyang Liu, Wei Ma, Jianjun Zhao. 2026. A mutation in BrPRPL1 causes leaf yellowing by influencing chloroplast protein translation in Chinese cabbage. Journal of Integrative Agriculture, 25(7): 2836-2846.

Asakura Y, Barkan A. 2006. Arabidopsis orthologs of maize chloroplast splicing factors promote splicing of orthologous and species-specific group II introns. Plant Physiology142, 1656–1663.

Bryant N, Lloyd J, Sweeney C, Myouga F, Meinke D. 2011. Identification of nuclear genes encoding chloroplast-localized proteins required for embryo development in ArabidopsisPlant Physiology155, 1678–1689.

Cazzonelli C I, Pogson B J. 2010. Source to sink: Regulation of carotenoid biosynthesis in plants. Trends in Plant Science15, 266–274.

Chalupska D, Lee H Y, Faris J D, Evrard A, Chalhoub B, Haselkorn R, Gornicki P. 2008. Acc homoeoloci and the evolution of wheat genomes. Proceedings of the National Academy of Sciences of the United States of America105, 9691–9696.

Chen L, Li C, Zhang J, Li Z, Zeng Q, Sun Q, Wang X, Zhao L, Zhang L, Li B. 2024. Physiological and transcriptome analyses of Chinese cabbage in response to drought stress. Journal of Integrative Agriculture23, 2255–2269.

Cheng M Z, Meng F Y, Mo F L, Chen X L, Zhang H, Wang A X. 2022. Insights into the molecular basis of a yellow leaf color mutant (ym) in tomato (Solanum lycopersicum). Scientia Horticulturae293, 110743.

Cocon K D, Luis P. 2024. The potential of rubisco in CO2 capture and utilization. Progress in Energy and Combustion Science105, 101184.

Fu Y T, Li X F, Fan B F, Zhu C, Chen Z X. 2022. Chloroplasts protein quality control and turnover: A multitude of mechanisms. International Journal of Molecular Sciences23, 14.

Hou X, Zhang C, Gao L. 2018. A TYMV virus induced endogenous gene silencing method in Brassicaceae and its application. China, CN107557383A. (in Chinese)

Kusumi K, Sakata C, Nakamura T, Kawasaki S, Yoshimura A, Iba K. 2011. A plastid protein NUS1 is essential for build-up of the genetic system for early chloroplast development under cold stress conditions. Plant Journal68, 1039–1050.

Lee J W, Jang S, Ryu S, Lee S, Park J, Lee S, An G. 2019. Mutation of plastid ribosomal protein L13 results in an albino seedling-lethal phenotype in rice. Plant Breeding and Biotechnology7, 395–404.

Li X, Ilarslan H, Brachova L, Qian H R, Li L, Che P, Wurtele E S, Nikolau B J. 2011. Reverse-genetic analysis of the two biotin-containing subunit genes of the heteromeric acetyl-coenzyme a carboxylase in Arabidopsis indicates a unidirectional functional redundancy. Plant Physiology155, 293–314.

Lin D, Jiang Q, Zheng K, Chen S, Zhou H, Gong X, Xu J, Teng S, Dong Y. 2015. Mutation of the rice ASL2 gene encoding plastid ribosomal protein L21 causes chloroplast developmental defects and seedling death. Plant Biology17, 599–607.

Linley P J, Landsberger M, Kohchi T. 2006. The molecular basis of heme oxygenase deficiency in the pcd1 mutant of pea. FEBS Journal273, 2594–2606.

Liu M Y, Ma W, Su X J, Zhang X M, Lu Y, Zhang S W, Yan J H, Feng D L, Ma L S, Taylor A, Ge Y J, Cheng Q, Xu K D, Wang Y H, Li N, Gu A X, Zhang J, Luo S X, Xuan S X, Chen X P, et al. 2022. Mutation in a chlorophyll-binding motif of ferrochelatase enhances both heme and chlorophyll biosynthesis. Cell Reports41, 10.

Liu W K, Chen G L, He M M, Wu J Q, Wen W X, Gu Q S, Guo S R, Wang Y, Sun J. 2023. ABI5 promotes heat stress-induced chlorophyll degradation by modulating the stability of MYB44 in cucumber. Horticulture Research10, uhad089.

Liu X Y, Zheng M D, Wang R, Wang R J, An L J, Rodermel S R, Yu F. 2013. Genetic interactions reveal that specific defects of chloroplast translation are associated with the suppression of mediated leaf variegation. Journal of Integrative Plant Biology55, 979–993.

Liu Z B, Mao L Z, Yang B Z, Cui Q Z, Dai Y H, Li X Q, Chen Y S, Dai X Z, Zou X X, Ou L J, Yang S. 2023. A multi-omics approach identifies bHLH71-like as a positive regulator of yellowing leaf pepper mutants exposed to high-intensity light. Horticulture Research10, uhad098.

Lu Y, Dai S, Gu A, Liu M, Wang Y, Luo S, Zhao Y, Wang S, Xuan S, Chen X. 2016. Microspore induced doubled haploids production from ethyl methanesulfonate (EMS) soaked flower buds is an efficient strategy for mutagenesis in Chinese cabbage. Frontiers in Plant Science7, 1780.

Luo T, Luo S, Wagner L. 2013. Virus-induced gene silencing of pea CHLI and CHLD affects tetrapyrrole biosynthesis, chloroplast development and the primary metabolic network. Plant Physiology and Biochemistry, 65, 17–26.

Masuda T. 2008. Recent overview of the Mg branch of the tetrapyrrole biosynthesis leading to chlorophylls. Photosynthesis Research96, 121–143.

Naing A H, Kyu S Y, Pe P P W. 2019. Silencing of the phytoene desaturase (PDS) gene affects the expression of fruit-ripening genes in tomatoes. Plant Methods15, 110.

Ostheimer G J, Williams-Carrier R, Belcher S, Osborne E, Gierke J, Barkan A. 2003. Group II intron splicing factors derived by diversification of an ancient RNA-binding domain. EMBO Journal22, 3919–3929.

Papenbrock J, Mock H P, Tanaka R, Kruse E, Grimm B. 2000. Role of magnesium chelatase activity in the early steps of the tetrapyrrole biosynthetic pathway. Plant Physiology122, 1161–1169.

Pesaresi P, Varotto C, Meurer J, Jahns P, Salamini F, Leister D. 2001. Knock-out of the plastid ribosomal protein L11 in Arabidopsis, effects on mRNA translation and photosynthesis. Plant Journal27, 179–189.

Polivka T, Frank H A. 2010. Molecular factors controlling photosynthetic light harvesting by carotenoids. Accounts of Chemical Research43, 1125–1134.

Robles P, Quesada V. 2022. Unveiling the functions of plastid ribosomal proteins in plant development and abiotic stress tolerance. Plant Physiology and Biochemistry189, 35–45.

Romani I, Tadini L, Rossi F, Masiero S, Pribil M, Jahns P, Kater M, Leister D, Pesaresi P. 2012. Versatile roles of Arabidopsis plastid ribosomal proteins in plant growth and development. Plant Journal72, 922–934.

Schultes N P, Sawers R J H, Brutnell T P, Krueger R W. 2000. Maize high chlorophyll fluorescent 60 mutation is caused by an Ac disruption of the gene encoding the chloroplast ribosomal small subunit protein 17. Plant Journal21, 317–327.

Shimoda Y, Ito H, Tanaka A. 2012. Conversion of chlorophyll b to chlorophyll a precedes magnesium dechelation for protection against necrosis in Arabidopsis. Plant Journal72, 501–511.

Sun X, Li X, Lu Y, Wang S, Zhang X, Zhang K, Su X, Liu M, Feng D, Luo S. 2022. Construction of a high-density mutant population of Chinese cabbage facilitates the genetic dissection of agronomic traits. Molecular Plant15, 913–924.

Sun Y, Zerges W. 2015. Translational regulation in chloroplasts for development and homeostasis. Biochimica et Biophysica Acta1847, 809–820.

Tanaka R, Tanaka A. 2011. Chlorophyll cycle regulates the construction and destruction of the light-harvesting complexes. Biochimica et Biophysica Acta-Bioenergetics1807, 968–976.

Tiller N, Bock R. 2014. The translational apparatus of plastids and its role in plant development. Molecular Plant7, 1105–1120.

Wang R, Song H, Zhang W J, Wang N, Zhang S J, Shao R Q, Liu C M. 2023. Structural insights into the functions of Raf1 and Bsd2 in hexadecameric Rubisco assembly. Molecular Plant16, 1927–1936.

Wang S, Shi K, Xiao Y, Ma W, Hong Y, Feng D, Zhao J. 2025. The circadian clock shapes diurnal gene expression patterns linked to glucose metabolic processes in Chinese cabbage. Journal of Integrative Agriculture24, 2155–2170.

Wang Z, Zhang L, Dong C. 2021. Characterization and functional analysis of phytoene synthase gene family in tobacco. BMC Plant Biology21, 32.

Wicke S, Schneeweiss G M, dePamphilis C W, Müller K F, Quandt D. 2011. The evolution of the plastid chromosome in land plants: Gene content, gene order, gene function. Plant Molecular Biology76, 273–297.

Woodson J D, Joens M S, Sinson A B, Gilkerson J, Salom P A, Weigel D. 2015. Ubiquitin facilitates a quality-control pathway that removes damaged chloroplasts. Science350, 450–454.

Wu Y, Liao W, Dawuda M M, Hu L, Yu J. 2019. 5-Aminolevulinic acid (ALA) biosynthetic and metabolic pathways and its role in higher plants: a review. Plant Growth Regulation87, 357–374.

Yang Y Y, An X H, Rui L, Liu G D, Tian Y, You C X, Wang X F. 2024. MdSnRK1.1 interacts with MdGLK1 to regulate abscisic acid-mediated chlorophyll accumulation in apple. Horticulture Research11, uhad288.

Yu X, Yu J, Lu Y, Li W, Huo G, Zhang J, Li J. 2024. An efficient and universal protoplast-based transient gene expression system for genome editing in Brassica crops. Horticultural Plant Journal10, 983–994.

Zhang J X, Yuan H, Yang Y, Fish T, Zhang L G, Li L. 2016. Plastid ribosomal protein S5 is involved in photosynthesis, plant development, and cold stress tolerance in ArabidopsisJournal of Experimental Botany67, 2731–2744.

Zhao C, Liu L, Safdar L B. 2020. Characterization and fine mapping of a yellow-virescent gene regulating chlorophyll biosynthesis and early stage chloroplast development in Brassica napusG3 Genes|Genomes|Genetics10, 3201–3211.

Zhao M H, Li X, Zhang X X, Zhang H, Zhao X Y. 2020. Mutation mechanism of leaf color in plants: A review. Forests11, 8.

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