Synchronization of the flowering transition by the tomato TERMINATING FLOWER gene

MacAlister, Cora A.; Park, Soon Ju; Jiang, Ke; Marcel, Fabien; Bendahmane, Abdelhafid; Izkovich, Yinon; Eshed, Yuval; Lippman, Zachary B.

doi:10.1038/ng.2465

Cited by 127 publications

(157 citation statements)

References 52 publications

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“…The recessive pro ΔGRAS allele was isolated from an activation-tagging population of Micro-Tom, mutagenized with an Ac/Ds system carrying a 4335S enhancer element in the Ds transposon (MacAlister et al, 2012). The pro ΔGRAS line used in this study was backcrossed with M82 (SP + ) plants four times.…”

Section: Plant Materials and Growth Conditionsmentioning

confidence: 99%

Uncovering DELLA-Independent Gibberellin Responses by Characterizing New TomatoproceraMutants

et al. 2015

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Gibberellin (GA) regulates plant development primarily by triggering the degradation/deactivation of the DELLA proteins. However, it remains unclear whether all GA responses are regulated by DELLAs. Tomato (Solanum lycopersicum) has a single DELLA gene named PROCERA (PRO), and its recessive pro allele exhibits constitutive GA activity but retains responsiveness to external GA. In the loss-of-function mutant pro DGRAS , all examined GA developmental responses were considerably enhanced relative to pro and a defect in seed desiccation tolerance was uncovered. As pro, but not pro DGRAS , elongation was promoted by GA treatment, pro may retain residual DELLA activity. In agreement with homeostatic feedback regulation of the GA biosynthetic pathway, we found that GA20oxidase1 expression was suppressed in pro DGRAS and was not affected by exogenous GA 3 . In contrast, expression of GA2oxidase4 was not affected by the elevated GA signaling in pro DGRAS but was strongly induced by exogenous GA 3 . Since a similar response was found in Arabidopsis thaliana plants with impaired activity of all five DELLA genes, we suggest that homeostatic GA responses are regulated by both DELLA-dependent and -independent pathways. Transcriptome analysis of GA-treated pro DGRAS leaves suggests that 5% of all GA-regulated genes in tomato are DELLA independent. INTRODUCTIONThe phytohormone gibberellin (GA) regulates numerous developmental processes throughout the plant life cycle, including seed germination, stem elongation, flowering, and fruit set (Yamaguchi, 2008). The signaling pathway from GA perception to transcriptional activation has been intensively studied over the past two decades and its major components have been identified. The nuclear DELLA proteins, a subgroup of the GRAS transcription factors family, suppress GA signaling (Locascio et al., 2013). GA binding to the soluble GIBBERELLIN INSENSITIVE DWARF1 (GID1) receptor triggers GID1 interaction with the DELLA proteins (Ueguchi-Tanaka et al., 2005;Nakajima et al., 2006;Griffiths et al., 2006), which then stimulates assembly of the DELLA proteins into an SCF E3 ubiquitin ligase complex via the GID2/SLEEPY1 F-box proteins. The SCF complex polyubiquitinates the DELLA proteins, targeting them for destruction by the 26S proteosome (Sasaki et al., 2003;Dill et al., 2004;Griffiths et al., 2006;Harberd et al., 2009;Hauvermale et al., 2012). GA, via GID1, can also reduce DELLA activity through a degradation-independent mechanism (Ariizumi et al., , 2013Ueguchi-Tanaka et al., 2008).Despite the central role of DELLAs in GA signaling, the mechanism underlying this regulation is not fully understood. Several studies have shown that protein-protein interactions play a major role in DELLA function. DELLAs bind to various transcription factors and proteins affecting transcription, including PHYTOCHROME-INTERACTING FACTORs (PIFs), ALCATRAZ, MYC2, JASMONATE-ZIM-DOMAIN PROTEIN9, SCARECROW LIKE3 (SCL3), and TCP transcription factors (de Lucas et al., 2008;Feng et al., 2008;Arnaud et al., 2010;Ga...

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Section: Plant Materials and Growth Conditionsmentioning

confidence: 99%

Uncovering DELLA-Independent Gibberellin Responses by Characterizing New TomatoproceraMutants

et al. 2015

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“…Reference images of meristem stages for all species except S. prinohyllum and C. annuum were adapted from MacAlister et al (2012) and Park et al (2012). , we extracted mRNA from pooled meristems of the same stage for the other three species and performed Illumina sequencing.…”

Section: A Continuum Of Inflorescence Complexity In the Solanaceae Famentioning

confidence: 99%

“…For example, in maize, the zinc finger transcription factor gene INDETERMINATE1 (ID1) promotes flowering, and the RAMOSA (RA) genes are major regulators of ear and tassel inflorescence development (Colasanti et al 1998;Gallavotti et al 2010). In contrast, critical players in tomato are the unrelated transcriptional regulators TERMINATING FLOWER (TMF), COMPOUND INFLORESCENCE (S), and the floral identity gene ANANTHA (AN) (Lippman et al 2008;MacAlister et al 2012). In rice, the functions of ID1 and TMF are conserved (Park et al 2008;Yoshida et al 2013), but the RAs have no known role in panicle development (Vollbrecht et al 2005), and the homolog of S primarily controls tillering (Wang et al 2014).…”

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The evolution of inflorescence diversity in the nightshades and heterochrony during meristem maturation

et al. 2016

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One of the most remarkable manifestations of plant evolution is the diversity for floral branching systems. These "inflorescences" arise from stem cell populations in shoot meristems that mature gradually to reproductive states in response to environmental and endogenous signals. The morphology of the shoot meristem maturation process is conserved across distantly related plants, raising the question of how diverse inflorescence architectures arise from seemingly common maturation programs. In tomato and related nightshades (Solanaceae), inflorescences range from solitary flowers to highly branched structures bearing hundreds of flowers. Since reproductive barriers between even closely related Solanaceae have precluded a genetic dissection, we captured and compared meristem maturation transcriptomes from five domesticated and wild species reflecting the evolutionary continuum of inflorescence complexity. We find these divergent species share hundreds of dynamically expressed genes, enriched for transcription factors. Meristem stages are defined by distinct molecular states and point to modified maturation schedules underlying architectural variation. These modified schedules are marked by a peak of transcriptome expression divergence during the reproductive transition, driven by heterochronic shifts of dynamic genes, including transcriptional regulators with known roles in flowering. Thus, evolutionary diversity in Solanaceae inflorescence complexity is determined by subtle modifications of transcriptional programs during a critical transitional window of meristem maturation, which we propose underlies similar cases of plant architectural variation. More broadly, our findings parallel the recently described transcriptome "inverse hourglass" model for animal embryogenesis, suggesting both plant and animal morphological variation is guided by a mid-development period of transcriptome divergence.

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“…As an example, stable over-expression in tomato and in strawberry of the newly discovered GDP-l-galactose phosphorylase (VTC2/VTC5) with the GDP-mannose epimerase (GME) led to two to six-fold increases in ascorbate levels (Bulley et al 2012). Recently published results also highlighted how the functional analysis of various target genes in tomato can benefit from the availability of allelic series of mutations identified in tomato EMS mutant collections by TILLING (Di Matteo et al 2013;Gady et al 2012;MacAlister et al 2012). Indeed, EMS mutagenesis is well adapted to tomato, in contrast to other gene inactivation approaches such as the T-DNA insertional mutagenesis commonly used in Arabidopsis that involves tedious and lengthy steps of plant transformation and requires large mutant populations to reach saturation mutagenesis in tomato (Emmanuel and Levy 2002).…”

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Investigating the role of vitamin C in tomato through TILLING identification of ascorbate-deficient tomato mutants

Baldet

Brès

Okabe

et al. 2013

Plant Biotechnology

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Besides being a model for fleshy fruits and Solanaceae species, tomato represents one of the main sources of ascorbate (vitamin C) in human diet in many parts of the world. Ascorbate fulfills various roles in plants due to its antioxidant potential and to its connection with other metabolic pathways e.g. cell wall biosynthesis. Among the functional genomic tools recently developed in tomato, EMS (ethyl methanesulfonate) mutant collections provide an opportunity for identifying allelic series of mutations in target genes by TILLING (Targeting Induced Local Lesions IN Genomes). We describe here the use of tomato EMS mutant collections in the miniature cv. Micro-Tom for the discovery of allelic variants in three ascorbate biosynthetic genes encoding the GDP-d-mannose pyrophosphorylase (GMP), the GDP-dmannose epimerase (GME) and the GDP-l-galactose phosphorylase (GGP) respectively. We report on the discovery of several missense, truncation and splice junction mutations in these genes affecting plant ascorbate content to various levels, and show that several tomato mutant lines with strongly reduced ascorbate content undergo severe bleaching upon exposure to high light intensity.

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Synchronization of the flowering transition by the tomato TERMINATING FLOWER gene

Cited by 127 publications

References 52 publications

Uncovering DELLA-Independent Gibberellin Responses by Characterizing New TomatoproceraMutants

Uncovering DELLA-Independent Gibberellin Responses by Characterizing New TomatoproceraMutants

The evolution of inflorescence diversity in the nightshades and heterochrony during meristem maturation

Investigating the role of vitamin C in tomato through TILLING identification of ascorbate-deficient tomato mutants

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