Xiaohan Li ^1,2,3* Bing He ⁴ Anis Djari ⁵ Pierre Frasse ^5* Elie Maza ⁵ Farid REGAD ⁵ Julien Pirrello ^5* GUOJIAN HU ^1,2,3,5* Mondher Bouzayen ^5*

• ¹ College of Agriculture and Biotechnology, Zhejiang University, Hangzhou, Zhejiang Province, China
• ² Zhejiang Provincial Key Laboratory of Horticultural Plant Integrative Biology, Zhejiang University, Zijingang Campus,, Hangzhou, China
• ³ Key Laboratory of Horticultural Plant Growth, Development and Quality Improvement, Ministry of Agriculture, College of Agriculture and Biotechnology, Zhejiang University, Hangzhou, Zhejiang Province, China
• ⁴ College of Horticulture, China Agricultural University, Haidian, Beijing Municipality, China
• ⁵ Laboratoire de Recherche en Sciences Végétales—Génomique et Biotechnologie des Fruits—UMR5546, Université de Toulouse, CNRS, UPS, Toulouse-INP, Toulouse, France

The transition from flower to fruit, naturally triggered by flower pollination and known as fruit set, is instrumental to plant reproduction, seed formation and crop yield. It is noteworthy that this developmental process can also proceed in the absence of flower fertilization, although it remains unclear whether pollination-dependent and independent fruit set undergo similar transcriptomic reprogramming. Genome-wide transcriptomic profiling of the flower-to-fruit transition either pollination-induced or triggered by auxin treatment show that the two types of triggers modulate the expression of a common large set of genes that are primarily expressed in maternal tissues. These include genes related to auxin, gibberellin, brassinosteroid and ethylene signaling.Furthermore, inspection of changes in histone marking during this transition phase indicated that gene reprogramming underlying both types of fruit set mainly correlated with dynamic changes of H3K9ac and H3K4me3 histone marks. Notably, MADS-box and NAC genes were extensively down-regulated from flower to fruit, suggesting their negative roles in fruit initiation. In contrast, TCP, SBP, SNF2, GRF and SET family genes were significantly up-regulated in both pollinated and auxin-treated young developing fruits, suggesting their active role in promoting fruit set. Despite these similarities, the comparative analysis of the impact of natural pollination and auxin treatment revealed several differences mainly related to seed development and hormone signaling.Taken together, the data support the idea that auxin is the central hormone to hub the extensive gene reprogramming associated with the process of fruit initiation in tomato.