BrRRG通过调控大白菜细胞周期基因表达影响叶片大小

doi:10.1016/j.jia.2025.12.067

Journal of Integrative Agriculture ›› 2026, Vol. 25 ›› Issue (5): 1961-1970.DOI: 10.1016/j.jia.2025.12.067

BrRRG通过调控大白菜细胞周期基因表达影响叶片大小

收稿日期:2025-02-10 修回日期:2025-12-31 接受日期:2025-08-29 出版日期:2026-05-20 发布日期:2026-04-09

BrRRG regulates leaf size by controlling cell cycle gene expression in Chinese cabbage

Qianyun Wang¹, Rui Yang¹, Daling Feng¹, Yongcheng Li¹, Rui Li¹, Mengyang Liu¹, Yiguo Hong¹, Na Li^2#, Wei Ma^1#, Jianjun Zhao^1#

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
²School of Breeding and Multiplication (Sanya Institute of Breeding and Multiplication), Hainan University, Sanya 572025, China

Received:2025-02-10 Revised:2025-12-31 Accepted:2025-08-29 Online:2026-05-20 Published:2026-04-09
About author:#Correspondence Jianjun Zhao, E-mail: yyzjj@hebau.edu.cn; Wei Ma, E-mail: mawei0720@163.com; Na Li, E-mail: 13521251421@163.com
Supported by:
This work was supported by the National Natural Science Foundation of China (32172594, 32330096, and 32222076), and the Innovative Research Group Project of Hebei Natural Science Foundation, China (C2024204246).

摘要/Abstract

摘要： 大白菜（Brassica rapa subsp. pekinensis）是十字花科芸苔属的一种叶菜类蔬菜。可食用叶片的大小决定其经济价值和营养价值。然而，目前对大白菜叶片发育的认识有限。本研究通过对大白菜叶片发育缺陷突变体mini24的正向遗传分析，我们确定了调控大白菜叶片细胞分裂的BrRRG基因。进一步证明了BrRRG通过调控E2Fa转录因子和细胞周期相关基因的表达来影响白菜的叶片大小。此外，我们还发现BrRRG影响大白菜的生长素和细胞分裂素信号的响应。本研究揭示了BrRRG对地下部（根）和地上部（叶）发育调节的不同机制，BrRRG对大白菜叶片的生长至关重要。

Abstract:

Chinese cabbage (Brassica rapa subsp. pekinensis) is an important leafy vegetable in the Brassica genus of the Brassicaceae family. The size of its edible leaves is an essential trait that determines its economic and nutritional values. However, the current understanding of leaf development in Chinese cabbage remains limited. Here, through forward genetic analysis of the mutant mini24 with defective leaf and root development, we identified the BrRRG gene, which regulates cell division in Chinese cabbage by map-based cloning. We demonstrated that BrRRG impacts leaf size by regulating the expression of E2Fa transcription factors and cell cycle-related genes in Chinese cabbage. Furthermore, BrRRG was found to modulate Chinese cabbage’s response to auxin (indole-3-acetic acid, IAA) and cytokinins hormones, revealing a distinct regulatory mechanism by which BrRRG coordinates the development of underground roots and aboveground leaves. Thus, these results indicate that mutation in BrRRG impairs the growth and development of Chinese cabbage.

Key words: Chinese cabbage , BrRRG , cell division , cell cycle gene

Qianyun Wang, Rui Yang, Daling Feng, Yongcheng Li, Rui Li, Mengyang Liu, Yiguo Hong, Na Li, Wei Ma, Jianjun Zhao. BrRRG通过调控大白菜细胞周期基因表达影响叶片大小[J]. Journal of Integrative Agriculture, 2026, 25(5): 1961-1970.

Qianyun Wang, Rui Yang, Daling Feng, Yongcheng Li, Rui Li, Mengyang Liu, Yiguo Hong, Na Li, Wei Ma, Jianjun Zhao. BrRRG regulates leaf size by controlling cell cycle gene expression in Chinese cabbage[J]. Journal of Integrative Agriculture, 2026, 25(5): 1961-1970.

参考文献

Aboul-Maaty N A F, Oraby H A S. 2019. Extraction of high-quality genomic DNA from different plant orders applying a modified CTAB-based method. Bulletin of the National Research Centre , 43, 25.

Andriankaja M, Dhondt S, De Bodt S, Vanhaeren H, Coppens F, De Milde L, Mühlenbock P, Skirycz A, Gonzalez N, Beemster G T, Inzé D. 2012. Exit from proliferation during leaf development in Arabidopsis thaliana: a not-so-gradual process. Developmental Cell, 22, 64–78.

Bogre L, Magyar Z, Lopez-Juez E. 2008. New clues to organ size control in plants. Genome Biology, 9, 226.

Breuer C, Ishida T, Sugimoto K. 2010. Developmental control of endocycles and cell growth in plants. Current Opinion in Plant Biology, 13, 654–660.

De Veylder L, Larkin J C, Schnittger A. 2011. Molecular control and function of endoreplication in development and physiology. Trends in Plant Science, 16, 624–634.

Dewitte W, Scofield S, Alcasabas A A, Maughan S C, Menges M, Braun N, Collins C, Nieuwland J, Prinsen E, Sundaresan V, Murray J A. 2007. Arabidopsis CYCD3 D-type cyclins link cell proliferation and endocycles and are rate-limiting for cytokinin responses. Proceedings of the National Academy of Sciences of the United States of America, 104, 14537–14542.

Ding Q, Cui B, Li J, Li H, Zhang Y, Lv X, Qiu N, Liu L, Wang F, Gao J. 2018. Ectopic expression of a Brassica rapa AINTEGUMENTA gene (BrANT-1) increases organ size and stomatal density in Arabidopsis. Scientific Reports, 8, 10528.

Elliott R C, Betzner A S, Huttner E, Oakes M P, Tucker W Q, Gerentes D, Perez P, Smyth D R. 1996. AINTEGUMENTA, an APETALA2-like gene of Arabidopsis with pleiotropic roles in ovule development and floral organ growth. The Plant Cell, 8, 155–168.

Fang W, Wang Z, Cui R, Li J, Li Y. 2012. Maternal control of seed size by EOD3/CYP78A6 in Arabidopsis thaliana. Plant Journal, 70, 929–939.

Gonzalez N, Vanhaeren H, Inze D. 2012. Leaf size control: complex coordination of cell division and expansion. Trends in Plant Science, 17, 332–340.

Gu A X, Zhao J J, Li L M, Wang Y H, Zhao Y J, Hua F, Xu Y C, Shen S X. 2016. Analyses of phenotype and ARGOS and ASY1 expression in a ploidy Chinese cabbage series derived from one haploid. Breeding Science, 66, 161–168.

Guo X, Liang J, Lin R, Zhang L, Wu J, Wang X. 2021. Series-spatial transcriptome profiling of leafy head reveals the key transition leaves for head formation in Chinese cabbage. Frontiers in Plant Science, 12, 787826.

Gutierrez C, Ramirez-Parra E, Castellano M M, del Pozo J C. 2002. G(1) to S transition: more than a cell cycle engine switch. Current Opinion in Plant Biology, 5, 480–486.

He S S, Liu J, Xie Z, O’Neill D, Dotson S. 2004. Arabidopsis E2Fa plays a bimodal role in regulating cell division and cell growth. Plant Molecular Biology, 56, 171–184.

Herridge R P, Day R C, Macknight R C. 2014. The role of the MCM2-7 helicase complex during Arabidopsis seed development. Plant Molecular Biology, 86, 69–84.

Hong J K, Oh S W, Kim J H, Lee S B, Lee Y H. 2017. Overexpression of Brassica rapa GROWTH-REGULATING FACTOR genes in Arabidopsis thaliana increases organ growth by enhancing cell proliferation. Journal of Plant Biotechnology, 44, 271–286.

Hong S Y, Kim O K, Kim S G, Yang M S, Park C M. 2011. Nuclear import and DNA binding of the ZHD5 transcription factor is modulated by a competitive peptide inhibitor in Arabidopsis. Journal of Biological Chemistry, 286, 1659–1668.

Hur Y S, Um J H, Kim S, Kim K, Park H J, Lim J S, Kim W Y, Jun S E, Yoon E K, Lim J, Ohme-Takagi M, Kim D, Park J, Kim G T, Cheon C I. 2015. Arabidopsis thaliana homeobox 12 (ATHB12), a homeodomain-leucine zipper protein, regulates leaf growth by promoting cell expansion and endoreduplication. New Phytologist, 205, 316–328.

Jeleńska J, Deckert J, Kondorosi E, Legocki A B. 2000. Mitotic B-type cyclins are differentially regulated by phytohormones and during yellow lupine nodule development. Plant Science, 150, 29–39.

John P C, Mews M, Moore R. 2001. Cyclin/Cdk complexes: their involvement in cell cycle progression and mitotic division. Protoplasma, 216, 119–142.

Johnson K, Lenhard M. 2011. Genetic control of plant organ growth. New Phytologist, 191, 319–333.

Kosugi S, Ohashi Y. 2003. Constitutive E2F expression in tobacco plants exhibits altered cell cycle control and morphological change in a cell type-specific manner. Plant Physiology, 132, 2012–2022.

Kwon S H, Lee B H, Kim E Y, Seo Y S, Lee S, Kim W T, Song J T, Kim J H. 2009. Overexpression of a Brassica rapa NGATHA gene in Arabidopsis thaliana negatively affects cell proliferation during lateral organ and root growth. Plant and Cell Physiology, 50, 2162–2173.

Lee B H, Ko J H, Lee S, Lee Y, Pak J H, Kim J H. 2009. The Arabidopsis GRF-INTERACTING FACTOR gene family performs an overlapping function in determining organ size as well as multiple developmental properties. Plant Physiology, 151, 655–668.

Limas J C, Cook J G. 2019. Preparation for DNA replication: the key to a successful S phase. FEBS Letters, 593, 2853–2867.

Lu D, Wang T, Persson S, Mueller-Roeber B, Schippers J H. 2014. Transcriptional control of ROS homeostasis by KUODA1 regulates cell expansion during leaf development. Nature Communications, 5, 3767.

Mironov V V, De Veylder L, Van Montagu M, Inze D. 1999. Cyclin-dependent kinases and cell division in plants the nexus. The Plant Cell, 11, 509–522.

Naouar N, Vandepoele K, Lammens T, Casneuf T, Zeller G, van Hummelen P, Weigel D, Rätsch G, Inzé D, Kuiper M, De Veylder L, Vuylsteke M. 2009. Quantitative RNA expression analysis with Affymetrix Tiling 1.0R arrays identifies new E2F target genes. Plant Journal, 57, 184–194.

Neelam K, Brown-Guedira G, Huang L. 2013. Development and validation of a breeder-friendly KASPar marker for wheat leaf rust resistance locus Lr21. Molecular Breeding, 31, 233–237.

Ni D A, Sozzani R, Blanchet S, Domenichini S, Reuzeau C, Cella R, Bergounioux C, Raynaud C. 2009. The Arabidopsis MCM2 gene is essential to embryo development and its over-expression alters root meristem function. New Phytologist, 184, 311–322.

Nisa M, Eekhout T, Bergis C, Pedroza-Garcia J A, He X, Mazubert C, Vercauteren I, Cools T, Brik-Chaouche R, Drouin-Wahbi J, Chmaiss L, Latrasse D, Bergounioux C, Vandepoele K, Benhamed M, De Veylder L, Raynaud C. 2023. Distinctive and complementary roles of E2F transcription factors during plant replication stress responses. Molecular Plant, 16, 1269–1282.

Omidbakhshfard M A, Fujikura U, Olas J J, Xue G P, Balazadeh S, Mueller-Roeber B. 2018. GROWTH-REGULATING FACTOR 9 negatively regulates Arabidopsis leaf growth by controlling ORG3 and restricting cell proliferation in leaf primordia. PLoS Genetics, 14, e1007484.

Omidbakhshfard M A, Proost S, Fujikura U, Mueller-Roeber B. 2015. Growth-regulating factors (GRFs): A small transcription factor family with important functions in plant biology. Molecular Plant, 8, 998–1010.

Ramirez-Parra E, Fründt C, Gutierrez C. 2003. A genome-wide identification of E2F-regulated genes in Arabidopsis. Plant Journal, 33, 801–811.

Ratnayeke N, Baris Y, Chung M, Yeeles J T P, Meyer T. 2023. CDT1 inhibits CMG helicase in early S phase to separate origin licensing from DNA synthesis. Molecular Cell, 83, 26–42.e13.

Reddy G V, Heisler M G, Ehrhardt D W, Meyerowitz E M. 2004. Real-time lineage analysis reveals oriented cell divisions associated with morphogenesis at the shoot apex of Arabidopsis thaliana. Development, 131, 4225–4237.

Shi J, Zhang Q, Yan X, Zhang D, Zhou Q, Shen Y, Anupol N, Wang X, Bao M, Larkin R M, Luo H, Ning G. 2021. A conservative pathway for coordination of cell wall biosynthesis and cell cycle progression in plants. Plant Journal, 106, 630–648.

Springer P S, Holding D R, Groover A, Yordan C, Martienssen R A. 2000. The essential Mcm7 protein PROLIFERA is localized to the nucleus of dividing cells during the G(1) phase and is required maternally for early Arabidopsis development. Development, 127, 1815–1822.

Stortenbeker N, Bemer M. 2019. The SAUR gene family: the plant’s toolbox for adaptation of growth and development. Journal of Experimental Botany, 1, 17–27.

Sun X, Li X, Lu Y, Wang S, Zhang X, Zhang K, Su X, Liu M, Feng D, Luo S, Gu A, Fu Y, Chen X, Xuan S, Wang Y, Xu D, Chen S, Ma W, Shen S, Cheng F, Zhao J. 2022. Construction of a high-density mutant population of Chinese cabbage facilitates the genetic dissection of agronomic traits. Molecular Plant, 15, 913–924.

Trimarchi J M, Lees J A. 2002. Sibling rivalry in the E2F family. Nature Reviews Molecular Cell Biology, 3, 11–20.

Tsukaya H. 2015. Yield increase: GRFs provide the key. Nature Plants, 2, 15210.

Vandepoele K, Vlieghe K, Florquin K, Hennig L, Beemster G T, Gruissem W, Van de Peer Y, Inze D, De Veylder L. 2005. Genome-wide identification of potential plant E2F target genes. Plant Physiology, 139, 316–328.

Vlieghe K, Boudolf V, Beemster G T, Maes S, Magyar Z, Atanassova A, de Almeida Engler J, De Groodt R, Inze D, De Veylder L. 2005. The DP-E2F-like gene DEL1 controls the endocycle in Arabidopsis thaliana. Current Biology, 15, 59–63.

Vlieghe K, Vuylsteke M, Florqu in K, Rombauts S, Maes S, Ormenese S, Van Hummelen P, Van de Peer Y, Inze D, De Veylder L. 2003. Microarray analysis of E2Fa-DPa-overexpressing plants uncovers a cross-talking genetic network between DNA replication and nitrogen assimilation. Journal of Cell Science, 116, 4249–4259.

Wang B, Zhou X, Xu F, Gao J. 2010. Ectopic expression of a Chinese cabbage BrARGOS gene in Arabidopsis increases organ size. Transgenic Research, 19, 461–472.

Wang F, Zheng T, Wu G, Lang C, Hu Z, Shi J, Jin W, Chen J, Liu R. 2015. Overexpression of miR319a affects the balance between mitosis and endoreduplication in Arabidopsis leaves. Plant Molecular Biology Reporter, 33, 2006–2013.

Wang G, Kong H, Sun Y, Zhang X, Zhang W, Altman N, DePamphilis C W, Ma H. 2004. Genome-wide analysis of the cyclin family in Arabidopsis and comparative phylogenetic analysis of plant cyclin-like proteins. Plant Physiology, 135, 1084–1099.

Wang J, Jin D, Deng Z, Zheng L, Guo P, Ji Y, Song Z, Zeng H Y, Kinoshita T, Liao Z, Chen H, Deng X W, Wei N. 2025. The apoplastic pH is a key determinant in the hypocotyl growth response to auxin dosage and light. Nature Plants, 11, 279–294.

Wang Y, Huang S, Liu Z, Tang X, Feng H. 2018. Changes in endogenous phytohormones regulated by microRNA-target mRNAs contribute to the development of dwarf autotetraploid Chinese cabbage (Brassica rapa L. ssp. pekinensis). Molecular Genetics and Genomics, 293, 1535–1546.

Xu H, Lantzouni O, Bruggink T, Benjamins R, Lanfermeijer F, Denby K, Schwechheimer C, Bassel G W. 2020. A molecular signal integration network underpinning Arabidopsis seed germination. Current Biology, 30, 3703–3712.e3704.

Zhang G, Zhai N, Zhu M, Zheng K, Sang Y, Li X, Xu L. 2025. Cell wall remodeling during plant regeneration. Journal of Integrative Plant Biology, 67, 1060–1076.

Zhou X, Li Q, Chen X, Liu J, Zhang Q, Liu Y, Liu K, Xu J. 2011. The Arabidopsis RETARDED ROOT GROWTH gene encodes a mitochondria-localized protein that is required for cell division in the root meristem. Plant Physiology, 157, 1793–1804.

BrRRG通过调控大白菜细胞周期基因表达影响叶片大小

BrRRG regulates leaf size by controlling cell cycle gene expression in Chinese cabbage

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