SlKNUCKLES regulates floral meristem activity and controls fruit size in Solanum lycopersicum

Dongbao Li , Wen Yang , Zhiyue Wu , Yonghua Yang , Zhongling Wen , Bo Sun

Horticulture Research ›› 2025, Vol. 12 ›› Issue (3) : 331

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Horticulture Research ›› 2025, Vol. 12 ›› Issue (3) :331 DOI: 10.1093/hr/uhae331
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SlKNUCKLES regulates floral meristem activity and controls fruit size in Solanum lycopersicum
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Abstract

Timed termination of floral meristem (FM) is crucial for proper development of floral organs and fruits. In Solanum lycopersicum, CLAVATA3 (CLV3)-WUSCHEL (WUS) feedback regulation maintains FM homeostasis in early stage of floral buds. It is known that the zinc finger protein SlKNUCKLES (SlKNU) functions to promote FM determinacy by directly repressing the stem cell identity gene SlWUS. However, how the robust FM activity is suppressed to secure fruit development is not fully understood in tomato. Here, we demonstrate that SlKNU also directly represses the stem cell marker gene SlCLV3 and the receptor gene SlCLV1 for FM determinacy control. Besides, loss-of-function mutants of SlKNU generated by CRISPR-Cas9 show increased fruit size of tomato. Moreover, overexpression of SlKNU attenuates the activities of the shoot apical meristem (SAM) and FM in Arabidopsis, but normal carpel development is still maintained. Hence, although the function of KNU in tomato and Arabidopsis may diverge during evolution, the role of KNU for FM determinacy and fruit size control is conserved and may potentially be useful for enhancing fruit yield of tomato.

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Dongbao Li, Wen Yang, Zhiyue Wu, Yonghua Yang, Zhongling Wen, Bo Sun. SlKNUCKLES regulates floral meristem activity and controls fruit size in Solanum lycopersicum. Horticulture Research, 2025, 12(3): 331 DOI:10.1093/hr/uhae331

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Acknowledgements

This work was supported by the Youth Fund of the National Natural Science Foundation of China (32101383 to Zl.W.) and the Fundamental Research Funds for the Central Universities (020814380180 to B.S.).

Author contributions

B.S. conceived and designed the research. D.L., W.Y., Zy.W., and Zl.W. participated in and completed the experiments. D.L., Zl.W., and B.S. wrote the manuscript. Y.Y. and B.S. revised the manuscript. All authors have read and approved the final version of the manuscript.

Data availability

Data supporting the findings of this work are available within the article/supplementary files. The plant materials and datasets generated and analyzed during the study are available from the corresponding authors upon reasonable request.

Conflict of interest statement

The authors declare no conflicts of interest.

References

[1]

Han H, Liu X, Zhou Y. Transcriptional circuits in control of shoot stem cell homeostasis. Curr Opin Plant Biol. 2020;53: 50-6

[2]

Pfeiffer A, Wenzl C, Lohmann JU. Beyond flexibility: controlling stem cells in an ever changing environment. Curr Opin Plant Biol. 2017;35: 117-23

[3]

Sun S, Wang X, Liu Z. et al. Tomato APETALA 2 family member SlTOE1 regulates inflorescence branching by repressing SISTER of TM3. Plant Physiol. 2023;192: 293-306

[4]

Park SJ, Jiang K, Schatz MC. et al. Rate of meristem maturation determines inflorescence architecture in tomato. Proc Natl Acad Sci USA. 2012;109: 639-44

[5]

Wang X, Liu Z, Sun S. et al. SISTER OF TM3 activates FRUIT-FULL1 to regulate inflorescence branching in tomato. Hortic Res. 2021;8:251

[6]

Périlleux C, Huerga-Fernández S. Reflections on the triptych of meristems that build flowering branches in tomato. Front Plant Sci. 2022;13:798502

[7]

Zhang C, Wang J, Wang X. et al. UF, a WOX gene, regulates a novel phenotype of un-fused flower in tomato. Plant Sci. 2020a;297:110523

[8]

Zúñiga-Mayo VM, Gómez-Felipe A, Herrera-Ubaldo H. et al. Gynoecium development: networks in Arabidopsis and beyond. JExpBot. 2019;70: 1447-60

[9]

Quinet M, Angosto T, Yuste-Lisbona FJ. et al. Tomato fruit devel-opment and metabolism. Front Plant Sci. 2019;10: 1-23

[10]

Zhao X, Muhammad N, Zhao Z. et al. Molecular regulation of fruit size in horticultural plants: a review. Sci Hortic (Amsterdam). 2021;288:110353

[11]

Jha P, Ochatt SJ, Kumar V. WUSCHEL: a master regulator in plant growth signaling. Plant Cell Rep. 2020;39: 431-44

[12]

Lopes FL, Galvan-Ampudia C, Landrein B. WUSCHEL in the shoot apical meristem: old player, new tricks. JExp Bot. 2021;72: 1527-35

[13]

Hu C, Zhu Y, Cui Y. et al. A group of receptor kinases are essential for CLAVATA signalling to maintain stem cell homeostasis. Nat Plants. 2018;4: 205-11

[14]

Shang E, Wang X, Li T. et al. Robust control of floral meristem determinacy by position-specific multifunctions of KNUCKLES. Proc Natl Acad Sci USA. 2021;118: 1-11

[15]

Song XF, Hou XL, Liu CM. CLE peptides: critical regulators for stem cell maintenance in plants. Planta. 2022;255: 1-17

[16]

Rodriguez-Leal D, Xu C, Kwon CT. et al. Evolution of buffering in a genetic circuit controlling plant stem cell proliferation. Nat Genet. 2019;51: 786-92

[17]

Galli M, Gallavotti A. Expanding the regulatory network for meristem size in plants. Trends Genet. 2016;32: 372-83

[18]

Han L, Huang Y, Li C. et al. Heterotrimeric Gα-subunit regulates flower and fruit development in CLAVATA signaling pathway in cucumber. Hortic Res. 2024;11:uhae110

[19]

Rodríguez-Leal D, Lemmon ZH, Man J. et al. Engineering quanti-tative trait variation for crop improvement by genome editing. Cell. 2017;171: 470-480.e8

[20]

Chu YH, Jang JC, Huang Z. et al. Tomato locule number and fruit size controlled by natural alleles of lc and fas. Plant Direct. 2019;3:e00142

[21]

Li H, Qi M, Sun M. et al. Tomato transcription factor SLWUS plays an important role in tomato flower and locule development. Front Plant Sci. 2017;8: 1-8

[22]

Du Y, Lunde C, Li Y. et al. Gene duplication at the fascicled ear1 locus controls the fate of inflorescence meristem cells in maize. Proc Natl Acad Sci USA. 2021;118:e2019218118

[23]

Sun B, Zhou Y, Cai J. et al. Integration of transcriptional repres-sion and Polycomb-mediated silencing of WUSCHEL in floral meristems. Plant Cell. 2019;31: 1488-505

[24]

Bollier N, Sicard A, Leblond J. et al. At-MINI ZINC FINGER2 and Sl-INHIBITOR OF MERISTEM ACTIVITY, a conserved missing link in the regulation of floral meristem termination in Arabidopsis and tomato. Plant Cell. 2018;30: 83-100

[25]

Müller R, Bleckmann A, Simon R. The receptor kinase CORYNE of Arabidopsis transmits the stem cell-limiting signal CLAVATA3 independently of CLAVATA1. Plant Cell. 2008;20: 934-46

[26]

Yuste-Lisbona FJ, Fernández-Lozano A, Pineda B. et al. ENO regu-lates tomato fruit size through the floral meristem development network. Proc Natl Acad Sci USA. 2020;117: 8187-95

[27]

Castañeda L, Giménez E, Pineda B. et al. Tomato CRABS CLAW paralogues interact with chromatin remodelling factors to mediate carpel development and floral determinacy. New Phytol. 2022;234: 1059-74

[28]

Baile F, Merini W, Hidalgo I. et al. EAR domain-containing tran-scription factors trigger PRC2-mediated chromatin marking in Arabidopsis. Plant Cell. 2021;33: 2701-15

[29]

SunB XuY,NgKH. et al. A timing mechanism for stem cell main-tenance and differentiation in the Arabidopsis floral meristem. Genes Dev. 2009;23: 1791-804

[30]

Somssich M, Je B Il, Simon R. et al. CLAVATA-WUSCHEL signaling in the shoot meristem. Development. 2016;143: 3238-48

[31]

Tanksley SD. The genetic, developmental, and molecular bases of fruit size and shape variation in tomato. Plant Cell. 2004;16: S181-9

[32]

Aguirre L, Hendelman A, Hutton SF. et al. Idiosyncratic and dose-dependent epistasis drives variation in tomato fruit size. Science. 2023;382: 315-20

[33]

Wu J, Li P, Li M. et al. Heat stress impairs floral meristem termination and fruit development by affecting the BR-SlCRCa cascade in tomato. Plant Commun. 2024;5:100790

[34]

Hawar A, Xiong S, Yang Z. et al. Histone acetyltransferase SlGCN5 regulates shoot meristem and flower development in Solanum lycopersicum. Front Plant Sci. 2022;12: 1-10

[35]

Muniz L, Nicolas E, Trouche D. RNA polymerase II speed: a key player in controlling and adapting transcriptome composition. EMBO J. 2021;40: 1-21

[36]

Sun B, Looi LS, Guo S. et al. Timing mechanism dependent on cell division is invoked by Polycomb eviction in plant stem cells. Science. 2014;343:1248559

[37]

Yamaguchi N, Huang J, Xu Y. et al. Fine-tuning of auxin home-ostasis governs the transition from floral stem cell maintenance to gynoecium formation. Nat Commun. 2017;8:1125

[38]

Xu C, Liberatore KL, Macalister CA. et al. A cascade of arabinosyl-transferases controls shoot meristem size in tomato. Nat Genet. 2015;47: 784-92

[39]

Kwa´sniewska K, Breathnach C, Fitzsimons C. et al. Expression of KNUCKLES in the stem cell domain is required for its function in the control of floral meristem activity in Arabidopsis. Front Plant Sci. 2021;12: 1-14

[40]

Zhang X, Henriques R, Lin SS. et al. Agrobacterium-mediated transformation of Arabidopsis thaliana using the floral dip method. Nat Protoc. 2006;1: 641-6

[41]

Cortina C, Culiáñez-Macià FA. Tomato transformation and transgenic plant production. Plant Cell Tissue Organ Cult. 2004;76: 269-75

[42]

Xing HL, Dong L, Wang ZP. et al. A CRISPR/Cas 9 toolkit for multiplex genome editing in plants. BMC Plant Biol. 2014;14: 1-12

[43]

Zhang Y, Chen M, Siemiatkowska B. et al. A highly efficient agrobacterium-mediated method for transient gene expression and functional studies in multiple plant species. Plant Commun. 2020;1:100028

[44]

Chen W, Zheng Y, Wang J. et al. Ethylene-responsive SbWRKY 50 suppresses leaf senescence by inhibition of chlorophyll degra-dation in sorghum. New Phytol. 2023;238: 1129-45

[45]

Alexander MP. Differential staining of aborted and nonaborted pollen. Biotech Histochem. 1969;44: 117-22

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