Repression of Floral Meristem Fate Is Crucial in Shaping Tomato Inflorescence

Johanna Thouet,Jean-Marie Kinet,Claire Périlleux,Stanley Lutts,Muriel Quinet,Miguel A Blazquez

doi:10.1371/journal.pone.0031096

Johanna Thouet, Jean-Marie Kinet + Show 4 more

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https://doi.org/10.1371/journal.pone.0031096

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Abstract

Tomato is an important crop and hence there is a great interest in understanding the genetic basis of its flowering. Several genes have been identified by mutations and we constructed a set of novel double mutants to understand how these genes interact to shape the inflorescence. It was previously suggested that the branching of the tomato inflorescence depends on the gradual transition from inflorescence meristem (IM) to flower meristem (FM): the extension of this time window allows IM to branch, as seen in the compound inflorescence (s) and falsiflora (fa) mutants that are impaired in FM maturation. We report here that JOINTLESS (J), which encodes a MADS-box protein of the same clade than SHORT VEGETATIVE PHASE (SVP) and AGAMOUS LIKE 24 (AGL24) in Arabidopsis, interferes with this timing and delays FM maturation, therefore promoting IM fate. This was inferred from the fact that j mutation suppresses the high branching inflorescence phenotype of s and fa mutants and was further supported by the expression pattern of J, which is expressed more strongly in IM than in FM. Most interestingly, FA - the orthologue of the Arabidopsis LEAFY (LFY) gene - shows the complementary expression pattern and is more active in FM than in IM. Loss of J function causes premature termination of flower formation in the inflorescence and its reversion to a vegetative program. This phenotype is enhanced in the absence of systemic florigenic protein, encoded by the SINGLE FLOWER TRUSS (SFT) gene, the tomato orthologue of FLOWERING LOCUS T (FT). These results suggest that the formation of an inflorescence in tomato requires the interaction of J and a target of SFT in the meristem, for repressing FA activity and FM fate in the IM.

Highlights

Flowering is an important process that determines fruit and seed production in Angiosperms
Several environmental and developmental signalling pathways which trigger the floral transition of the shoot apical meristem (SAM) have been disclosed; they converge on the transcriptional regulation of two major ‘‘integrator genes’’, FLOWERING LOCUS T (FT) and SUPPRESSOR OF OVEREXPRESSION OF CONSTANS 1 (SOC1), which in turn activate the flower meristems (FM) identity genes LEAFY (LFY) and APETALA1 (AP1)
FT was identified as a major output of the photoperiodic pathway that promotes flowering in Arabidopsis by the extension of daylength; the FT protein is synthesized in the leaves, travels through the phloem towards the SAM where it interacts with the bZIP transcription factor FD to activate AP1

Summary

Introduction

Flowering is an important process that determines fruit and seed production in Angiosperms. The shoot apical meristem (SAM) switches from leaf production to inflorescence meristem (IM) fate and initiates flower meristems (FM) on its flanks. Several environmental and developmental signalling pathways which trigger the floral transition of the SAM have been disclosed; they converge on the transcriptional regulation of two major ‘‘integrator genes’’, FLOWERING LOCUS T (FT) and SUPPRESSOR OF OVEREXPRESSION OF CONSTANS 1 (SOC1), which in turn activate the FM identity genes LEAFY (LFY) and APETALA1 (AP1). FT was identified as a major output of the photoperiodic pathway that promotes flowering in Arabidopsis by the extension of daylength; the FT protein is synthesized in the leaves, travels through the phloem towards the SAM where it interacts with the bZIP transcription factor FD to activate AP1 (reviewed in [4]). FT activates SOC1, which together with AGAMOUS LIKE 24 (AGL24) in the SAM, up-regulates LFY [5,6]

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