SlBEL11 regulates flavonoid biosynthesis, thus fine-tuning auxin efflux to prevent premature fruit drop in tomato

Authors: DONG, XIUFEN - Shenyang Agricultural University; LIU, XIANFENG - Shenyang Agricultural University; CHENG, LINA - Shenyang Agricultural University; LI, RUIZHEN - Shenyang Agricultural University; GE, SIQI - Shenyang Agricultural University; WANG, SAI - Shenyang Agricultural University; CAI, YUE - Shenyang Agricultural University; LIU, YANG - Shenyang Agricultural University; MENG, SIDA - Shenyang Agricultural University; Jiang, Cai-Zhong; SHI, CHUN-LIN - Angenovo; LI, TIANLAI - Shenyang Agricultural University; FU, DAQI - China Agriculture University; QI, MINGFANG - Shenyang Agricultural University; XU, TAO - Shenyang Agricultural University

Submitted to: Journal of Integrative Plant Biology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/2/2024
Publication Date: 2/29/2024
Citation: Dong, X., Liu, X., Cheng, L., Li, R., Ge, S., Wang, S., Cai, Y., Liu, Y., Meng, S., Jiang, C., Shi, C., Li, T., Fu, D., Qi, M., Xu, T. 2024. SlBEL11 regulates flavonoid biosynthesis, thus fine-tuning auxin efflux to prevent premature fruit drop in tomato. Journal of Integrative Plant Biology. 66(4):749-770. https://doi.org/10.1111/jipb.13627.
DOI: https://doi.org/10.1111/jipb.13627

Interpretive Summary: Abscission, a common phenomenon in plants, is an important development process involving the natural separation of organ from the main body. During their life cycle, plants can shed entire organs and tissues such as leaves, flowers and fruits in response to developmental and environmental cues. Several regulatory networks that function during environment-induced abscission have been revealed. However, the molecular mechanisms underlying development-dependent abscission remain obscure. The process of organ abscission typically takes place at a histologically identifiable cellular boundary between the organ and the plant body, known as the abscission zone (AZ). The anatomical structure known as the AZ consists of multiple layers of cells that exhibit functional specialization and distinct morphological characteristics. These characteristics include the presence of tiny, square-shaped cells that are joined by branched plasmodesmata and possess a thick cytoplasm. Citrus plants contain two AZs, AZ-A (between the twig and peduncle) and AZ-C (between the ovary wall and nectary), which are responsible for the first post-anthesis flower and fruitlet abscission and the second fruit abscission, respectively. The primary cause of first post-anthesis abscission can be attributed to inadequate pollination resulting from adverse weather conditions or a scarcity of pollinating agents, while an insufficient supply of carbohydrates to young fruits promotes second fruit abscission. Similarly, in tomato (Solanum lycopersicum), the detachment of flowers and fruitlets usually occurs in the pedicel AZ (PAZ), while the fruit abscission zone (FAZ) plays a role in fruit abscission after the PAZ has lost its function. Although different environmental stresses and an insufficient supply of carbohydrates might cause abscission to occur in different AZs, the detailed mechanism is still unclear. Free auxin content in AZ plays an important role for preventing abscission. Local auxin distribution in this region is mediated by auxin transport. A continuous auxin polar flux across the AZ may prevent the abscission, as application of polar auxin transport inhibitor could stimulate abscission, whereas treatment with auxin transport inhibitor could induce parthenocarpy. It is proposed that a threshold of polar auxin transport depends on AZ local free auxin content for preventing abscission. Auxin is transported from fruits, but auxin content varies among fruits. In detail, levels of first IAA peaks drop throughout tomato fruit expansion to very low levels at breaker. Similarly, the low levels of auxin in Arabidopsis (Arabidopsis thaliana) fruit are attributed to “flux-passage” during development. It is important to elucidate how auxin transport is fine-tuned in fruit to balance fruit ripening and the prevention of abscission. Flavonoid synthesis is tissue specifically and developmentally regulated. Quercetin, kaempferol, and naringenin chalcone synthesized in the first steps of the flavonoid biosynthetic pathway, are one class of the natural inhibitors of polar auxin transport. Moreover, flavonols affect polar auxin transport in apical tissues by modulating the amount of auxin loaded into the long-distance polar auxin transport stream. However, little is known about the roles of flavonols in mediating fruit auxin transport in fruits and in fruit abscission. The BEL1-like homeodomian is a class of transcription factor which belongs to the three-amio-acid-loop-extention (TALE) family, its function has been shown to control abscission, auxin distribution and secondary metabolites. However, the role of BEL1-like homeodomain in modulating auxin function during fruit abscission requires further exploration. Here, we investigated how SlBEL11 regulates pedicel abscission during tomato fruit ripening. We show that SlBEL11 regulates flavonoid contents in the FAZ to fine tu

Technical Abstract: The phytohormone auxin regulates flower and fruit abscission, but how developmental signals mediate auxin transport to regulate abscission remains incompletely comprehended. Here, we reveal the role of the tomato (Solanum lycopersicum) transcription factor BEL1-LIKE HOMEODOMAIN11 (SlBEL11) in this regulation. SlBEL11 is highly expressed in the fruit abscission zone, and its expression increases during fruit development. Knockdown of SlBEL11 expression by RNA interference (RNAi) caused premature fruit drop at the breaker (Br) and Br+3 stages of fruit development. We propose that SlBEL11 prevents premature fruit abscission by modulating auxin efflux from fruits, which is crucial for the formation of an auxin response gradient. The levels of most flavonoids decreased in SlBEL11-RNAi plants, especially quercetin, an auxin transport inhibitor. Quercetin treatment suppressed premature fruit drop in SlBEL11-RNAi plants. DAP-seq analysis indicated that SlBEL11 induces SlMYB111 expression by directly binding to its promoter. ChIP-qPCR and EMSA indicated that SlMYB111 induces the expression of the core flavonoid biosynthesis genes SlCHS1, SlCHI, SlF3H and SlFLS by directly binding to their promoters. Our findings suggest that the SlBEL11–SlMYB111 module mediates flavonoid biosynthesis to fine-tune auxin efflux from fruits to maintain an auxin response gradient in the pedicel, thereby preventing premature fruit drop.