A tomato B-box protein regulates plant development and fruit quality through the interaction with PIF4, HY5 and RIN transcription factors.

During the last decade, the knowledge about BBX proteins has abruptly increased. Genome-wide studies identified BBX gene family in several ornamental, industry and food crops; however, the reports regarding the role of these genes as regulators of agronomically important traits are scarce. Here, by phenotyping a knockout mutant, we performed a comprehensive functional characterization of the tomato locus Solyc12g089240, hereafter called SlBBX20. The data revealed the encoded protein as a positive regulator of light signaling affecting several physiological processes during plant lifespan. By the inhibition of PHYTOCHROME INTERACTING FACTOR 4 (SlPIF4)-auxin crosstalk, SlBBX20 regulates photomorphogenesis. Later, it controls the balance between cell division and expansion to guarantee the correct vegetative and reproductive development. In fruits, SlBBX20 is transcriptionally induced by the master transcription factor RIPENING INHIBITOR (SlRIN) and, together with ELONGATED HYPOCOTYL 5 (SlHY5), upregulates flavonoids biosynthetic genes. Finally, SlBBX20 promotes the accumulation of steroidal glycoalkaloids and attenuates Botrytis cinerea infection. This work clearly demonstrates that BBX proteins are multilayer regulators of plant physiology, not only because they affect multiple processes along plant development but also regulate other genes at the transcriptional and post-translational levels.

• Publication year

  2024

• Venue

  Journal of Experimental Botany

• Publication date

  2024-03-16

• Fields of study

  Biology, Agricultural and Food Sciences, Medicine, Environmental Science

• Identifiers
  DOI 10.1093/jxb/erae119PMID 38492237
• External record

  Open on Semantic Scholar

• Source metadata

  Semantic Scholar, PubMed

• No claims are published for this paper.

• No concepts are published for this paper.

• SlMPK1- and SlMPK2-mediated SlBBX17 phosphorylation positively regulates CBF-dependent cold tolerance in tomato.

  2023cited by this paper
• Multi-layered roles of BBX proteins in plant growth and development

  2023cited by this paper
• Characterization and expression profiles of the B-box gene family during plant growth and under low-nitrogen stress in Saccharum

  2023cited by this paper
• A natural promoter variation of SlBBX31 confers enhanced cold tolerance during tomato domestication

  2023cited by this paper
• Identification of BBX gene family and its function in the regulation of microtuber formation in yam

  2023cited by this paper
• OsBBX19-OsBTB97/OsBBX11 module regulates spikelet development and yield production in rice.

  2023cited by this paper
• The Function of BBX Gene Family under Multiple Stresses in Nicotiana tabacum

  2022cited by this paper
• The tomato CONSTANS-LIKE protein SlCOL1 regulates fruit yield by repressing SFT gene expression

  2022cited by this paper
• SlBBX28 positively regulates plant growth and flower number in an auxin-mediated manner in tomato

  2022cited by this paper
• DeepLoc 2.0: multi-label subcellular localization prediction using protein language models

  2022cited by this paper
• Phytochrome-Mediated Light Perception Affects Fruit Development and Ripening Through Epigenetic Mechanisms

  2022cited by this paper
• Genome-Wide Identification of the B-Box Gene Family and Expression Analysis Suggests Their Potential Role in Photoperiod-Mediated β-Carotene Accumulation in the Endocarp of Cucumber (Cucumis sativus L.) Fruit

  2022cited by this paper
• Overexpression of SlBBX17 affects plant growth and enhances heat tolerance in tomato.

  2022cited by this paper
• Pivotal roles of ELONGATED HYPOCOTYL5 in regulation of plant development and fruit metabolism in tomato.

  2022cited by this paper
• Genome-Wide Characterization and Anthocyanin-Related Expression Analysis of the B-BOX Gene Family in Capsicum annuum L.

  2022cited by this paper
• Activation and negative feedback regulation of SlHY5 transcription by the SlBBX20/21-SlHY5 transcription factor module in UV-B signaling.

  2022cited by this paper
• SlBBX20 attenuates JA signalling and regulates resistance to Botrytis cinerea by inhibiting SlMED25 in tomato

  2022cited by this paper
• Genome-wide identification of BBX gene family and their expression patterns under salt stress in soybean

  2022cited by this paper
• Genome-wide identification and expression pattern analysis of quinoa BBX family

  2022cited by this paper
• The transcription factor SlHY5 regulates the ripening of tomato fruit at both the transcriptional and translational levels

  2021cited by this paper
• An autoregulatory negative feedback loop controls thermomorphogenesis in Arabidopsis

  2021cited by this paper
• Shade Avoidance: Expanding the Color and Hormone Palette.

  2021cited by this paper
• Genome-Wide Identification of the B-BOX Genes that Respond to Multiple Ripening Related Signals in Sweet Cherry Fruit

  2021cited by this paper
• Genome-Wide Identification and Expression Analysis of BBX Transcription Factors in Iris germanica L.

  2021cited by this paper
• Auxin and its role in plant development: structure, signalling, regulation and response mechanisms.

  2021cited by this paper
• SlBBX20 interacts with the COP9 signalosome subunit SlCSN5-2 to regulate anthocyanin biosynthesis by activating SlDFR expression in tomato

  2021cited by this paper
• BBX11 promotes red light-mediated photomorphogenic development by modulating phyB-PIF4 signaling

  2021cited by this paper
• Comprehensive identification and expression analysis of B-Box genes in cotton

  2021cited by this paper
• Beyond Arabidopsis: BBX Regulators in Crop Plants

  2021cited by this paper
• A light-dependent molecular link between competition cues and defence responses in plants

  2020cited by this paper
• Identification of BBX proteins as rate-limiting cofactors of HY5

  2020cited by this paper
• BBX28/BBX29-HY5-BBX30/31 form a feedback loop to fine-tune photomorphogenic development.

  2020cited by this paper
• Genome-wide identification and analysis of B-BOX gene family in grapevine reveal its potential functions in berry development

  2020cited by this paper
• Control of Plant Growth and Defense by Photoreceptors: From Mechanisms to Opportunities in Agriculture.

  2020cited by this paper
• Light and ripening-regulated BBX protein-encoding genes in Solanum lycopersicum

  2020cited by this paper
• Characterization of B-BOX gene family and their expression profiles under hormonal, abiotic and metal stresses in Poaceae plants

  2019cited by this paper
• BBX16, a B‐box protein, positively regulates light‐induced anthocyanin accumulation by activating MYB10 in red pear

  2019cited by this paper
• Comparative analysis of B-BOX genes and their expression pattern analysis under various treatments in Dendrobium officinale

  2019cited by this paper
• A tomato B-box protein SlBBX20 modulates carotenoid biosynthesis by directly activating PHYTOENE SYNTHASE 1, and is targeted for 26S proteasome-mediated degradation.

  2018cited by this paper
• Genome-wide identification and expression analysis of the B-box gene family in the Apple (Malus domestica Borkh.) genome

  2018cited by this paper
• Manipulation of Light Signal Transduction Factors as a Means of Modifying Steroidal Glycoalkaloids Accumulation in Tomato Leaves

  2018cited by this paper
• Rewiring of auxin signaling under persistent shade

  2018cited by this paper
• Light, Ethylene and Auxin Signaling Interaction Regulates Carotenoid Biosynthesis During Tomato Fruit Ripening

  2018cited by this paper
• PlantPAN3.0: a new and updated resource for reconstructing transcriptional regulatory networks from ChIP-seq experiments in plants

  2018cited by this paper
• Modulation of steroidal glycoalkaloid biosynthesis in tomato (Solanum lycopersicum) by jasmonic acid.

  2018cited by this paper
• Genome-wide survey of B-box proteins in potato (Solanum tuberosum)—Identification, characterization and expression patterns during diurnal cycle, etiolation and de-etiolation

  2017cited by this paper
• A Multipurpose Toolkit to Enable Advanced Genome Engineering in Plants[OPEN]

  2017cited by this paper
• Shade Inhibits Leaf Size by Controlling Cell Proliferation and Enlargement in Soybean

  2017cited by this paper
• TomExpress, a unified tomato RNA‐Seq platform for visualization of expression data, clustering and correlation networks

  2017cited by this paper
• B-BOX genes: genome-wide identification, evolution and their contribution to pollen growth in pear (Pyrus bretschneideri Rehd.)

  2017cited by this paper
• Manipulation of a Senescence-Associated Gene Improves Fleshy Fruit Yield1[OPEN]

  2017cited by this paper
• Converging Light, Energy and Hormonal Signaling Control Meristem Activity, Leaf Initiation, and Growth1[CC-BY]

  2017cited by this paper
• CONSTANS Imparts DNA Sequence Specificity to the Histone Fold NF-YB/NF-YC Dimer[OPEN]

  2017cited by this paper
• The Impact of Steroidal Glycoalkaloids on the Physiology of Phytophthora infestans, the Causative Agent of Potato Late Blight.

  2017cited by this paper
• Arabidopsis B-BOX32 interacts with CONSTANS-LIKE3 to regulate flowering

  2016cited by this paper
• BBX21, an Arabidopsis B-box protein, directly activates HY5 and is targeted by COP1 for 26S proteasome-mediated degradation

  2016cited by this paper
• Genomic Organization, Phylogenetic and Expression Analysis of the B-BOX Gene Family in Tomato

  2016cited by this paper
• Contrasting growth responses in lamina and petiole during neighbor detection depend on differential auxin responsiveness rather than different auxin levels.

  2015cited by this paper
• Development of fruit color in Solanaceae: a story of two biosynthetic pathways.

  2015cited by this paper
• Tomato GOLDEN2-LIKE Transcription Factors Reveal Molecular Gradients That Function during Fruit Development and Ripening[W][OPEN]

  2014cited by this paper
• The HY5-PIF Regulatory Module Coordinates Light and Temperature Control of Photosynthetic Gene Transcription

  2014cited by this paper
• The BBX family of plant transcription factors.

  2014cited by this paper
• Transient expression assays in tobacco protoplasts.

  2013cited by this paper
• Shade tolerance: when growing tall is not an option.

  2013cited by this paper
• Yeast two-hybrid analysis of jasmonate signaling proteins.

  2013cited by this paper
• A Large-Scale Identification of Direct Targets of the Tomato MADS Box Transcription Factor RIPENING INHIBITOR Reveals the Regulation of Fruit Ripening[W]

  2013cited by this paper
• A Quartet of PIF bHLH Factors Provides a Transcriptionally Centered Signaling Hub That Regulates Seedling Morphogenesis through Differential Expression-Patterning of Shared Target Genes in Arabidopsis

  2013cited by this paper
• Transcriptional regulation of tocopherol biosynthesis in tomato

  2013cited by this paper
• The Rice B-Box Zinc Finger Gene Family: Genomic Identification, Characterization, Expression Profiling and Diurnal Analysis

  2012cited by this paper
• NIH Image to ImageJ: 25 years of image analysis

  2012cited by this paper
• The Tomato FRUITFULL Homologs TDR4/FUL1 and MBP7/FUL2 Regulate Ethylene-Independent Aspects of Fruit Ripening[W]

  2012cited by this paper
• The Rg1 allele as a valuable tool for genetic transformation of the tomato 'Micro-Tom' model system

  2010cited by this paper
• The flowering time regulator CONSTANS is recruited to the FLOWERING LOCUS T promoter via a unique cis-element.

  2010cited by this paper
• Cellular responses to auxin: division versus expansion.

  2010cited by this paper
• Ripening-Regulated Susceptibility of Tomato Fruit to Botrytis cinerea Requires NOR But Not RIN or Ethylene1[W][OA]

  2009cited by this paper
• New GATEWAY vectors for high throughput analyses of protein-protein interactions by bimolecular fluorescence complementation.

  2009cited by this paper
• Six Classes of Nuclear Localization Signals Specific to Different Binding Grooves of Importin α*

  2009cited by this paper
• HPLC assay of tomato carotenoids: validation of a rapid microextraction technique.

  2009cited by this paper
• Amplification efficiency: linking baseline and bias in the analysis of quantitative PCR data

  2009cited by this paper
• Tomatinase from Fusarium oxysporum f. sp. lycopersici is required for full virulence on tomato plants.

  2008cited by this paper
• α‐Tomatine, the major saponin in tomato, induces programmed cell death mediated by reactive oxygen species in the fungal pathogen Fusarium oxysporum

  2007cited by this paper
• A dynamic analysis of the shade-induced plasticity in Arabidopsis thaliana rosette leaf development reveals new components of the shade-adaptative response.

  2006cited by this paper
• The CCAAT binding factor can mediate interactions between CONSTANS-like proteins and DNA.

  2006cited by this paper
• BaCelLo: a balanced subcellular localization predictor

  2006cited by this paper
• CONSTANS acts in the phloem to regulate a systemic signal that induces photoperiodic flowering of Arabidopsis

  2004cited by this paper
• GATEWAY vectors for Agrobacterium-mediated plant transformation.

  2002cited by this paper
• A MADS-Box Gene Necessary for Fruit Ripening at the Tomato Ripening-Inhibitor (Rin) Locus

  2002cited by this paper
• Fungal Sensitivity to and Enzymatic Degradation of the Phytoanticipin alpha-Tomatine.

  1998cited by this paper
• Genomic libraries and a host strain designed for highly efficient two-hybrid selection in yeast.

  1996cited by this paper
• The CONSTANS gene of Arabidopsis promotes flowering and encodes a protein showing similarities to zinc finger transcription factors.

  1995cited by this paper

• Multiomics Analysis Revealed the Role of LsBBX22-LsHY5a/b Module in Promoting UV-B-Mediated Anthocyanin Accumulation in Lettuce.

  2026cites this paper
• SlBBX20 is a regulator of plant development in response to shade in tomato.

  2026cites this paper
• Multifaceted roles of BBX transcription factors: impacts on key agronomical traits and environmental resilience.

  2026cites this paper
• Identification of the IDA peptide family in tomato and function of SlIDA8 in salt stress

  2026cites this paper
• Decoding the Multifunctionality of B‐Box Proteins: Bridging Light, Stress and Developmental Networks in Diverse Plant Species

  2025cites this paper
• Efficient mutagenesis and genotyping of maize inbreds using biolistics, multiplex CRISPR/Cas9 editing, and Indel-Selective PCR

  2025cites this paper
• SlBBX26 regulates vegetative growth, flowering and fruit development through the modulation of SlPIF4.

  2025cites this paper
• VvBBX32 responds to high temperatures and mediates anthocyanin biosynthesis in 'Merlot' grape (Vitis vinifera L.) berries.

  2025cites this paper
• B-BOX PROTEINS (BBXs) Transcription Factors in Plant: A Comprehensive Review of Their Growth, Development, Abiotic Stress Responses and Phytohormone Signals

  2025cites this paper
• The BBX Gene Family in Papaya (Carica papaya L.): Genome-Wide Identification and Expression Profiling During Fruit Ripening

  2025cites this paper
• Highly Efficient Agrobacterium-Mediated Transformation of Tomato cv Micro-Tom From Cotyledon Explants

  2025cites this paper
• Pan-Genomic Identification and Analysis of the Maize BBX Family

  2025cites this paper
• Potato steroidal glycoalkaloids: properties, biosynthesis, regulation and genetic manipulation

  2024cites this paper
• MsMYB206-MsMYB450-MsHY5 complex regulates alfalfa tolerance to salt stress via regulating flavonoid biosynthesis during the day and night cycles.

  2024cites this paper
• ChBBX6 and ChBBX18 are positive regulators of anthocyanins biosynthesis and carotenoids degradation in Cerasus humilis.

  2024cites this paper
• Efficient mutagenesis of maize inbreds using biolistics, multiplex CRISPR/Cas9 editing, and Indel-Selective PCR

  2024cites this paper
• B-BOX proteins:Multi-layered roles of molecular cogs in light-mediated growth and development in plants.

  2024cites this paper
• Multiplex Approach of Metabolomic and Transcriptomic Reveals the Biosynthetic Mechanism of Light-induced Flavonoids and CGA in Chrysanthemum

  2024cites this paper
• TmCOP1‐TmHY5 module‐mediated blue light signal promotes chicoric acid biosynthesis in Taraxacum mongolicum

  2024cites this paper