Fruit initiation following fertilization in angiosperms is strictly regulated by phytohormones. In tomato (Solanum lycopersicum), auxin and gibberellin (GA) play central roles in promoting fruit initiation. Without fertilization, elevated GA or auxin signaling can induce parthenocarpy (seedless fruit production). The GA-signaling repressor SlDELLA and auxin-signaling components SlIAA9 and SlARF7 repress parthenocarpy, but the underlying mechanism is unknown. Here, we show that SlDELLA and the SlARF7/SlIAA9 complex mediate crosstalk between GA and auxin pathways to regulate fruit initiation. Yeast-two-hybrid and coimmunoprecipitation assays showed that SlARF7 and additional activator SlARFs interact with SlDELLA and SlIAA9 through distinct domains. SlARF7/SlIAA9 and SlDELLA antagonistically modulate the expression of feedback-regulated genes involved in GA and auxin metabolism, whereas SlARF7/SlIAA9 and SlDELLA coregulate the expression of fruit growth-related genes. Analysis of procera (della), SlARF7 RNAi (with downregulated expression of multiple activator SlARFs), and entire (iaa9) single and double mutants indicated that these genes additively affect parthenocarpy, supporting the notion that the SlARFs/SlIAA9 and SlDELLA interaction plays an important role in regulating fruit initiation. Analysis of the GA-deficient mutant gib1 showed that active GA biosynthesis and signaling are required for auxin-induced fruit initiation. Our study reveals how direct crosstalk between auxin-and GA-signaling components is critical for tomato fruit initiation.
Bibliographical noteFunding Information:
We thank Maarten Koornneef for providing pro and procera gib1 mutants, Wim Vriezen and Ivo Rieu for the SlARF7 RNAi line, Miltos Tsian-tis and Klaus Theres for providing pGPTV-Kan-PROCERA, Zachary B. Lippman for identifying the slmp-1 mutation, and Yossi Capua and Yuval Eshed for providing the SlARF7 construct. We also thank Gregory Martin for help with tomato transient expression, Neelima Sinha and Siobhan Brady for sharing protocols and tomato sequence information, George Allen and Sergei Krasnyanski at the Plant Transformation Laboratory at NC State University for tomato transformation, Rodolfo Zentella, Ning Sui, and Jonathan Dayan for generating the modified Y2H vectors, and Jiayu Chen for technical assistance. This work was supported by grants to T.-p.S. from the USDA (2010-65116-20460, 2014-67013-21548, and 2018-67013-27395), the National Institutes of Health (R01 GM100051), and the National Science Foundation (MCB-0923723).
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