Cultivated strawberry is a globally important fruit crop with high economic value. Fruit shape is an important aspect of fruit quality and diversity, and a key target in breeding programs; however, few regulatory genes governing fruit shape are known in strawberry. Here, we identified an ethyl methanesulfonate (EMS) ‘round fruit’ (rf) mutant that produces round or flat fruits in woodland strawberry. The causal point mutation is located in the second exon of FvH4_2g22810, resulting in a premature termination at amino acid 266. The encoded protein shares a high sequence similarity with TON1 RECRUITING MOTIF 5 (TRM5) in different plant species and was therefore named FveTRM5. Consistently, transforming the rf mutant with FveTRM5pro:FveTRM5 restored the wild-type fruit phenotype. FveTRM5 is ubiquitously expressed in various organs, and the protein localized to microtubules. Overexpression of FveTRM5 produced elongated organs in both Arabidopsis and woodland strawberry, suggesting a conserved role in different species. Observation of cell shape showed that FveTRM5 promotes cell elongation and inhibits cell division in the medial-lateral direction in the receptacle. Transcriptome analysis revealed 183 differentially expressed genes (DEGs) in the young receptacles of rf and 2976 DEGs in those of FveTRM5-OE, including several involved in the auxin and gibberellic acid pathways. In conclusion, our results suggest that FveTRM5 plays an essential role in regulating strawberry fruit shape by influencing cell elongation and cell division, providing an excellent target gene for breeding new fruit shape cultivars.

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