Malformed fruits depreciate a plant's market value. In tomato (Solanum lycopersicum), fruit malformation is associated with the multi-locule trait, which involves genes regulating shoot apical meristem (SAM) development. The expression pattern of TOPLESS3 (SlTPL3) throughout SAM development prompted us to investigate its func-tional significance via RNA interference (RNAi) and clustered regularly interspaced short palindromic repeats/CRISPR-associated nuclease 9 (Cas9)-mediated gene editing. Lower SlTPL3 transcript levels resulted in larger fruits with more locules and larger SAMs at the 5 d after germination (DAG5) stage. Differentially expressed genes in the SAM of wild-type (WT) and SlTPL3-RNAi plants, identified by transcriptome deep se-quencing (RNA-seq), were enriched in the gibber-ellin (GA) biosynthesis and plant hormone sig-naling pathways. Moreover, exogenous auxin and paclobutrazol treatments rescued the multi-locule phenotype, indicating that SlTPL3 affects SAM size by mediating auxin and GA levels in the SAM. Furthermore, SlTPL3 interacted with WUSCHEL (SlWUS), which plays an important role in SAM size maintenance. We conducted RNA-seq and DNA affinity purification followed by sequencing (DAP-seq) analyses to identify the genes regulated by SlTPL3 and SlWUS in the SAM and to de-termine how they regulate SAM size. We detected 24 overlapping genes regulated by SlTPL3 and SlWUS and harboring an SlWUS-binding motif in their promoters. Furthermore, functional annota-tion revealed a notable enrichment for functions in auxin transport, auxin signal transduction, and GA biosynthesis. Dual-luciferase assays also revealed that SlTPL3 enhances SlWUS-mediated regulation (repression and activation) of SlPIN3 and SlGA2ox4 transcription, indicating that the SlTPL3–SlWUS module regulates SAM size by mediating auxin distribution and GA levels, and perturbations of this module result in enlarged SAM. These results provide novel insights into the molecular mechanism of SAM maintenance and locule formation in tomato and highlight the SlTPL3–SlWUS module as a key regulator.

Shiwei Song;Binbin Huang;Zanlin Pan;Qiuxiang Zhong;Yinghua Yang;Da Chen;Lisha Zhu;Guojian Hu;Mi He;Caiyu Wu;Mohammed Zouine;Riyuan Chen;Mondher Bouzayen;Yanwei Hao

Key Laboratory of Horticultural Crop Biology and Germplasm Innovation in South China,Ministry of Agriculture,College of Horticulture,South China Agricultural University,Guangzhou 510642,China;Laboratory of Genomics and Biotechnology of Fruits,INRA,Toulouse INP,University of Toulouse,Castanet Tolosan F-31326,France

植物学报（英文版）

[1]Shiwei Song;Binbin Huang;Zanlin Pan;Qiuxiang Zhong;Yinghua Yang;Da Chen;Lisha Zhu;Guojian Hu;Mi He;Caiyu Wu;Mohammed Zouine;Riyuan Chen;Mondher Bouzayen;Yanwei Hao-.The SlTPL3–SlWUS module regulates multi-locule formation in tomato by modulating auxin and gibberellin levels in the shoot apical meristem OO)[J].植物学报（英文版）,2022(11):2150-2167

SlTPL3,SlWUS,locule,Malformed,depreciate,TOPLESS3,locules,DAG5,gibber,ellin,annota,SlPIN3,SlGA2ox4

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