Tomato floral induction and flower development are orchestrated by the interplay between gibberellin and two unrelated microRNA‐controlled modules

Abstract

Age-regulated microRNA156 (miR156) and targets similarly control the competence to flower in diverse species. By contrast, the diterpene hormone gibberellin (GA) and the microRNA319-regulated TEOSINTE BRANCHED/CYCLOIDEA/PCF (TCP) transcription factors promote flowering in the facultative long-day Arabidopsis thaliana, but suppress it in the day-neutral tomato (Solanum lycopersicum).We combined genetic and molecular studies and described a new interplay between GA and two unrelated miRNA-associated pathways that modulates tomato transition to flowering.Tomato PROCERA/DELLA activity is required to promote flowering along with the miR156-targeted SQUAMOSA PROMOTER BINDING-LIKE (SPL/SBP) transcription factors by activating SINGLE FLOWER TRUSS (SFT) in the leaves and the MADS-Box gene APETALA1(AP1)/MC at the shoot apex. Conversely, miR319-targeted LANCEOLATE represses floral transition by increasing GA concentrations and inactivating SFT in the leaves and AP1/MC at the shoot apex. Importantly, the combination of high GA concentrations/responses with the loss of SPL/SPB function impaired canonical meristem maturation and flower initiation in tomato.Our results reveal a cooperative regulation of tomato floral induction and flower development, integrating age cues (miR156 module) with GA responses and miR319-controlled pathways. Importantly, this study contributes to elucidate the mechanisms underlying the effects of GA in controlling flowering time in a day-neutral species.

Tomato gynoecium patterning and fruit development are orchestrated by the interplay between microRNAs and gibberellin

“…It is unlikely that this mechanism involving the homologs of TCP4 (LANCEOLATE -LA), CUC2 (GOB) and SBP9 (SBP15) is conserved in tomato. We showed in a previous study that LA proteins do not interact with SBP15 by Yeast Two Hybrid (Y2H) and Bimolecular fluorescence complementation (BiFC) assays (Silva et al, 2019). However, a similar post translational mechanism may operate in boundary establishment also in tomato Besides regulating GOB transcriptional levels, PRO proteins interact with GOB.…”

“…In Arabidopsis and tomato, 11 out of 17 SBP/SPLs harbor the miR156 recognition site (Salinas et al, 2012;Preston and Hileman, 2013). The miR156 module (miR156-targeted SBP/SPLs) defines the evolutionary conserved age-dependent floral pathway in several plants, including tomato (Silva et al, 2018). Interestingly, the miR156 module has been proposed as a main target for crop improvement, aiming to enhance agronomic traits such as the timing of vegetative and reproductive phase change, leaf development, tillering/branching, panicle/tassel architecture, fruit development and fertility .…”

“…For Yeast Two Hybrid assays (Y2H), GOB (Solyc07g062840) ORF was cloned from cDNA into pENTR D-TOPO and recombined into pDEST22 and pDEST32 (ThermoFischer Scientific). PRO, SBP3 and SBP15 Y2H constructs were described by Silva et al (2019).…”

“…The mechanistic relationship between GA and miR156 still remains to be dissected in plants that negatively respond to GA in terms of flowering time. Nevertheless, we recently showed that the SPL9 ortholog in tomato SBP15 does not form dimer with PRO (Silva et al, 2019).…”

“…Interestingly, increased GA levels delays flowering in tomato(G. F. F. Silva et al, 2019). Loss of function of the tomato DELLA PROCERA (PRO) increases time to flowering.…”