thesis transcription factor

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AP®︎/College Biology

Course: ap®︎/college biology > unit 6.

DNA and chromatin regulation
Regulation of transcription
Cellular specialization (differentiation)
Non-coding RNA (ncRNA)
Operons and gene regulation in bacteria
Overview: Gene regulation in bacteria
The lac operon
The trp operon
Overview: Eukaryotic gene regulation

Transcription factors

Regulation of gene expression and cell specialization

Key points:

Transcription factors are proteins that help turn specific genes "on" or "off" by binding to nearby DNA.
Transcription factors that are activators boost a gene's transcription. Repressors decrease transcription.
Groups of transcription factor binding sites called enhancers and silencers can turn a gene on/off in specific parts of the body.
Transcription factors allow cells to perform logic operations and combine different sources of information to "decide" whether to express a gene.

Introduction

Transcription: the key control point.

If a gene is not transcribed in a cell, it can't be used to make a protein in that cell.
If a gene does get transcribed, it is likely going to be used to make a protein (expressed). In general, the more a gene is transcribed, the more protein that will be made. Is that always the case? Not always. Sometimes, later stages of regulation can block even large quantities of mRNA from being used to make protein. For example, imagine that a gene is transcribed a lot, but the mRNA is "chopped up" (degraded) as soon as it leaves the nucleus. This would lead to very little protein getting made.

How do transcription factors work?

Binding sites, how is this different from e. coli , turning genes on in specific body parts, example: modular mouse, evolution of development, transcription factors and cellular "logic".

Activator A is present only in skin cells
Activator B is active only in cells receiving "divide now!" signals (growth factors) from neighbors
Repressor C is produced when a cell's DNA is damaged

Works cited:

Gilbert, S. F. (2000). Anatomy of the gene: Promoters and enhancers. In Developmental biology (6th ed.). Sunderland, MA: Sinauer Associates. Retrieved from https://www.ncbi.nlm.nih.gov/books/NBK10023/#_A751_ .
Gilbert, S. F. (2000). Silencers. In Developmental biology (6th ed.). Sunderland, MA: Sinauer Associates. Retrieved from http://www.ncbi.nlm.nih.gov/books/NBK10023/#_A777_ .
Menke, D. B., Guenther, C., and Kingsley, D. M. (2008). Dual hindlimb control elements in the Tbx4 gene and region-specific control of bone size in vertebrate limbs. Development , 135 , 2543-2553. http://dx.doi.org/10.1242/dev.017384 .
Wray, Gregory A. (2007). The evolutionary significance of cis -regulatory mutations. Nature Reviews Genetics , 8 , 206-216. http://dx.doi.org/10.1038/nrg2063 .
Reece, J. B., Urry, L. A., Cain, M. L., Wasserman, S. A., Minorsky, P. V., and Jackson, R. B. (2011). Combinatorial control of gene activation. In Campbell Biology (10th ed., pp. 37). San Francisco, CA: Pearson.
Reményi, Attila, Hans R. Schöler, and Matthias Wilmanns. (2004). Combinatorial control of gene expression. Nature Structural & Molecular Biology , 11 (9), 812. http://dx.doi.org/10.1038/nsmb820 . Retrieved from http://www.nature.com/scitable/content/Combinatorial-control-of-gene-expression-16976 .

Additional references:

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Transcription factor binding sites identification using machine learning techniques

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The AP2/ERF transcription factor SmERF1L1 regulates the biosynthesis of tanshinones and phenolic acids in Salvia miltiorrhiza

Affiliations.

1 Laboratory of Medicinal Plant Biotechnology, College of Pharmacy, Zhejiang Chinese Medical University, Hangzhou, Zhejiang 310053, PR China; Institute of Plant Biotechnology, College of Life and Environment Sciences, Shanghai Normal University, Shanghai 200234, PR China.
2 Institute of Plant Biotechnology, College of Life and Environment Sciences, Shanghai Normal University, Shanghai 200234, PR China.
3 Laboratory of Medicinal Plant Biotechnology, College of Pharmacy, Zhejiang Chinese Medical University, Hangzhou, Zhejiang 310053, PR China.
4 Jiangsu Provincial Key Laboratory of Coastal Wetland Biological Resources and Environmental Protection, School of Marine and Biological Engineering, Yancheng Teachers Uninversity, Yancheng, Jiangsu Province 224051, PR China.
5 Laboratory of Medicinal Plant Biotechnology, College of Pharmacy, Zhejiang Chinese Medical University, Hangzhou, Zhejiang 310053, PR China; Institute of Plant Biotechnology, College of Life and Environment Sciences, Shanghai Normal University, Shanghai 200234, PR China. Electronic address: [email protected].
PMID: 30372953
DOI: 10.1016/j.foodchem.2018.08.119

Tanshinones and phenolic acids are two important metabolites synthesized by the traditional Chinese medicinal plant Salvia miltiorrhiza. There is increasing market demand for these compounds. Here, we isolated and functionally characterized SmERF1L1, a novel JA (Jasmonic acid)-responsive gene encoding AP2/ERF transcription factor, from Salvia miltiorrhiza. SmERF1L1 was responsive to methyl jasmonate (MJ), yeast extraction (YE), salicylic acid (SA) and ethylene treatments. Subcellular localization assay indicated that SmERF1L1 located in the nucleus. Overexpression of SmERF1L1 significantly increased tanshinones production in transgenic S. miltiorrhiza hairy roots by comprehensively upregulating tanshinone biosynthetic pathway genes, especially SmDXR. Yeast one-hybrid (Y1H) and electrophoretic mobility shift assay (EMSA) showed that SmERF1L1 binds to the GCC-box of SmDXR promoter while dual luciferase (Dual-LUC) assay showed that SmERF1L1 positively regulated the expression of SmDXR. Our study suggested that the SmERF1L1 may be a good potential target for further metabolic engineering of bioactive component biosynthesis in S. miltiorrhiza.

Keywords: AP2/ERF transcription factor; Biosynthesis; Caffeic acid (PubChem CID: 689043); Cryptotanshinone (PubChem CID: 160254); Dihydrotanshinone (PubChem CID: 11425923); Phenolic acids; Rosmarinic acid (PubChem CID: 5315615); Salvia miltiorrhiza; Salvianolic acid A (PubChem CID: 5281793); Salvianolic acid B (PubChem CID: 11629084); Tanshinone I (PubChem CID: 114917); Tanshinone IIA (PubChem CID: 164676); Tanshinones.

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Open access
Published: 21 June 2024

Characterization of YABBY transcription factors in Osmanthus fragrans and functional analysis of OfYABBY12 in floral scent formation and leaf morphology

Tingting Shi 1 , 2 ,
Ling Zhou 1 , 2 ,
Yunfang Ye 1 , 2 ,
Xiulian Yang 1 , 2 ,
Lianggui Wang 1 , 2 &
Yuanzheng Yue 1 , 2

BMC Plant Biology volume 24 , Article number: 589 ( 2024 ) Cite this article

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The plant-specific YABBY transcription factor family plays important roles in plant growth and development, particularly leaf growth, floral organ formation, and secondary metabolite synthesis.

Here, we identified a total of 13 OfYABBY genes from the Osmanthus fragrans genome. These 13 OfYABBY genes were divided into five subfamilies through phylogenetic analysis, and genes in the same subfamily showed similar gene structures and conserved protein motifs. Gene duplication promoted the expansion of the OfYABBY family in O . fragrans . Tissue-specific expression analysis showed that the OfYABBY family was mainly expressed in O . fragrans leaves and floral organs. To better understand the role of OfYABBY genes in plant growth and development, OfYABBY12 was selected for heterologous stable overexpression in tobacco, and OfYABBY12 -overexpressing tobacco leaves released significantly fewer volatile organic compounds than wild-type tobacco leaves. Overexpression of OfYABBY12 led to the downregulation of NtCCD1/4 and decreased β-ionone biosynthesis. Correspondingly, a dual-luciferase assay showed that OfYABBY12 negatively regulated the expression of OfCCD4 , which promotes β-ionone synthesis. Furthermore, tobacco leaves overexpressing OfYABBY12 were curled and wrinkled and had significantly reduced leaf thickness and leaf inclusions and significantly extended flower pistils (styles).

Overall, the results suggest that the OfYABBY gene family may influence the biosynthesis of the floral scent (especially β-ionone) in O . fragrans and may regulate leaf morphogenesis and lateral organs.

Peer Review reports

Introduction

Osmanthus fragrans is an important ornamental evergreen tree or shrub that is widely cultivated for its pleasing floral scent. It is commonly used in the landscaping and fragrance industries, where it has significant ornamental and economic value [ 1 , 2 ]. Many O . fragrans cultivars have been cultivated in China for more than 2,500 years. These cultivars have significant differences in floral scent, floral color, leaf shape, and leaf color [ 3 , 4 , 5 ]. Previous studies have shown that the YABBY gene family not only participates in the formation and development of plant leaves and floral organs but also affects the biosynthesis of secondary metabolites, such as terpene floral metabolites [ 6 , 7 , 8 ]. In this study, it was hypothesized that the phenotypic difference in the leaves, flowers, and floral scents of different O . fragrans cultivars may be regulated by the O . fragrans YABBY family.

The YABBY family is a class of plant-specific transcription factors [ 9 ]. Due to the roles these transcription factors play in many of the biological processes of plants, the YABBY family has attracted great interest from researchers. The YABBY proteins contain two conserved domains, an N-terminal C 2 C 2 zinc finger domain and a C-terminal YABBY domain. In Arabidopsis thaliana , Solanum lycopersicum , and other dicotyledonous plants, the YABBY transcription factors are classified into five subfamilies, namely CRABS CLAW (CRC), FILAMENTOUS FLOWER (FIL)/YABBY3 (YAB3), INNER NO OUTER (INO), YABBY2 (YAB2), and YABBY5 (YAB5). However, in Oryza sativa , Zea mays , and other monocotyledons, contain only four subfamilies and lack the YAB5 subfamily [ 9 ]. It has been indicated that the YABBY transcription factors in monocotyledonous and dicotyledonous plants have undergone functional divergence, and four gene duplication events have occurred in the YABBY family, leading to genes with innovative or redundant functions [ 10 ].

Some studies have shown that YABBY transcription factors are related to abaxial axis cell differentiation in lateral organs, thereby affecting leaf growth [ 11 , 12 ] or the development of floral organs [ 13 , 14 ] and fruit (seeds) [ 15 , 16 ]. The YABBY family also participates in the biosynthesis of primary and secondary plant metabolites [ 8 , 17 , 18 ] and in response to biotic and abiotic stress [ 19 , 20 , 21 ]. In A. thaliana , AtYAB2 , AtFIL , AtYAB3 , and AtYAB5 are expressed in the cotyledons, leaves, petals, stamens, and carpels and participate in regulating bud and leaf development and the formation of leaf polarity and floral organs [ 6 , 7 ]. However, AtCRC is only expressed in nectaries and carpels, regulating the abaxial development of these structures [ 22 ]. Similarly, AtINO is only expressed in the abaxial axis of the outer integument and mainly regulates ovule development, thereby affecting seed growth and development [ 23 , 24 ]. In S. lycopersicum , SlYABBY1 regulates leaf and flower sizes [ 25 ], SlYABBY2 regulates pericarp development and fruit maturation [ 26 ], and SlCRCa regulates flower and fruit size [ 27 ]. In Chrysanthemum morifolium , CmDRP (FlL/YAB3 subfamily) can regulate gibberellin biosynthesis to affect chrysanthemum plant height [ 28 ]. In addition, one study has shown that YABBY genes have dual functions, as they can act as both an activator and a repressor of secondary metabolites [ 29 ]. For example, MsYABBY5 of Mentha spicata negatively regulates the synthesis of monoterpenes [ 8 ], whereas in Artemisia annua , AaYABBY5 positively regulates the biosynthesis of artemisinin [ 17 ] and flavonoids [ 18 ]. Hence, YABBY transcription factors show tissue specificity in plants and play a variety of roles in plant growth and development.

Here, a comprehensive analysis of the O . fragrans YABBY gene family was conducted based on whole genome data, and OfYABBY12 was stably overexpressed in tobacco to investigate whether OfYABBY12 affects the growth and development of leaves and floral organs, as well as the synthesis of volatile organic compounds (VOCs). These results help to understand the OfYABBY family in O . fragrans and provide insight into the function of the OfYABBY12 gene. The findings have important significance for further study of the functions of the OfYABBY family in O . fragrans.

Materials and methods

Plant materials.

The experimental material was three-year-old O. fragrans ‘Rixiang Gui’ cuttings obtained from our O . fragrans germplasm resource bank (Jiangsu, China). Various tissues, including roots, stems, young leaves (from current-year branchlets), and mature leaves (from non-current-year branchlets) were sampled on March 26, 2022, and flowers at the full blooming stage were sampled on October 9, 2022. Nicotiana benthamiana and Nicotiana tabacum ‘K326’ seeds were saved by our group and planted in the greenhouse of Nanjing Forestry University under the following growth conditions: a 16/8 h light/dark cycle, a light intensity of 110 µmol photons m − 2 s − 1 white light, a temperature of 25 ± 2 °C, and 60–70% relative humidity.

Identification of O. fragrans YABBY transcription factors and protein physicochemical analysis

The whole genome sequence of O . fragrans was obtained from the O . fragrans ‘Rixiang Gui’ genomic database [ 30 ]. HMMER software (v3.0) was then used to screen for family members in the Pfam YABBY (PF04690) domain [ 31 ]. Three online tools, Batch CD-search ( http://www.ncbi.nlm.nih.gov/Structure/cdd/wrpsb.cgi ), Pfam ( http://pfam.xfam.org/search#searchBatchBlock ), and SMART ( http://smart.embl.de/smart/batch.pl ), were used to validate the YABBY domains. In addition, ExPASy ( https://web.expasy.org/compute_pi/ ) was employed to predict the molecular weight and isoelectric point of the identified YABBY protein sequences.

Gene structure, conserved motif, and cis-acting element analysis

In this study, DNAMAN software (v6.0.40) was used for multi-sequence alignment and the analysis of the conserved protein domains of YABBY amino acid sequences in O . fragrans . In addition, MEME online software ( http://meme-suite.org/ ) was used to analyze the conserved motifs of the OfYABBY protein sequences. The gene sequences 2,000 bp upstream of the start codon were obtained from the O . fragrans genome sequences, and the plantCARE database ( http://bioinformatics.psb.ugent.be/webtools/plantcare/html/ ) was used to retrieve the obtained sequences to analyze the potential cis-acting elements in the promoter. Finally, TBtools software (v1.120) [ 32 ] was used to visualize the gene structure, conserved motifs, and cis-acting elements of OfYABBYs.

Phylogenetic, chromosome localization, and gene duplication analysis

Genomic data were obtained from different databases, including A . thaliana ( https://www.arabidopsis.org/ ), S . lycopersicum ( https://solgenomics.net/ ), O. sativa ( http://rice.uga.edu/ ), and Z. mays ( https://maize-pangenome.gramene.org/ ). Furthermore, the protein sequences of YABBYs from Vitis vinifera [ 15 ], Camellia sinensis [ 33 ], Mimulus lewisii [ 34 ], M . spicata [ 8 ], Chimonanthus praecox [ 35 ], and A . annua [ 17 ] were obtained from relevant references.

Clustal X2.1 was used for the sequence alignment of the YABBY protein sequences of O . fragrans and other plants. In addition, MEGA X software was utilized to construct phylogenetic trees using the maximum likelihood method (Bootstrap = 1000) [ 36 ], and Fig Tree software (v1.4.3) was employed for visualization.

The chromosome locations of the OfYABBY genes were obtained based on the O . fragrans genome GFF3 file, and TBtools was used for visualization. Multiple Collinearity Scan Toolkits (MCScanX) and Ka/Ks calculators (NG) were used to further analyze the gene duplication events of the OfYABBY genes.

RNA extraction and quantitative reverse-transcription polymerase chain reaction (qRT-PCR) analyses

The RNAprep Pure Plant Kit (Tiangen, Beijing, China) was used to obtain the total RNA of plant materials, and One-Step gDNA Removal and cDNA Synthesis Super Mix (Transgen, Beijing, China) were used for reverse transcription to obtain complementary DNA (cDNA).

Primer Premier 5.0 software was used to design the qRT-PCR primers (Table S1 ). The ABI StepOne Plus PCR system and SYBR® Premix Ex Taq™ II Kit (Takara, Dalian, China) were used to measure gene expression levels. In addition, 10-fold diluted cDNA was used as a template, and OfACTIN was used as an internal reference gene [ 37 ]. The 2 −ΔΔCT method [ 38 ] was employed to calculate the relative expression level. Biological triplicates were set up for each qRT-PCR reaction, and technical triplicates were set up for each biological triplicate.

Subcellular localization and transactivation assay

The cDNAs of OfYABBY3 , OfYABBY5 , OfYABBY7 , OfYABBY8 , OfYABBY12 , and OfYABBY13 were cloned (primers shown in Table S2 ) and inserted into pCAMBIA1300 vectors to build the pCAMBIA1300-GFP-OfYABBY constructs. These constructed plasmids were transformed into N . benthamiana leaves by Agrobacterium tumefaciens strain GV3101 (Weidi Biotechnology, Shanghai, China). After 48 h, a Zeiss LSM 710 confocal microscope (Zeiss, Oberkochen, Germany) was used to observe fluorescence signals.

The cDNAs of OfYABBY3 , OfYABBY5 , OfYABBY7 , OfYABBY8 , OfYABBY12 , and OfYABBY13 were cloned into the pGBKT7 vector (primers shown in Table S2 ). These recombination vectors and the pGBKT7 empty vector were transformed into Saccharomyces cerevisiae (AH109). The suspended yeast was then diluted to different concentrations, and 5 µL dilutions were plated on SD-Trp, SD-Trp/Ade, and SD-Trp/Ade (X-α-gal) culture media. These were cultured at 30 °C in the dark for 3 d, and the growth status was then observed.

Transformation of OfYABBY12 in N. tabacum

A. tumefaciens cells carrying the pCAMBIA1300-OfYABBY12 plasmid were cultured overnight, and the culture products were collected when the OD600 reached 0.4–0.5. A solution of 10 mM MgCl 2 , 10 mM MES, and 150 mM acetosyringone was used to resuspend the Agrobacterium cultures for transformation. In addition, tobacco ( N . tabacum ‘K326’) seeds were sterilized and sown on MS medium, and when grown to three to four leaves, sterile tobacco leaves were cut into 0.5 cm × 0.5 cm cubes (that is, explants) and infiltrated with Agrobacterium cultures for 10 min. Subsequently, after 3 d of co-cultivation in the dark on the co-culture medium (MS + 2.25 mg/L 6-BA + 0.3 mg/L NAA), the explants were transferred to selective medium (MS + 2.25 mg/L 6-BA + 0.3 mg/L NAA + 400 mg/L cefotaxime + 100 mg/L kanamycin). The culture was kept at 25 °C with a 16/8 h light/dark cycle with the medium changed every 15 d. When the callus and resistant shoots emerged, the explants were transferred to germination medium (MS + 0.1 mg/L 6-BA + 0.01 mg/L NAA + 400 mg/L cefotaxime + 100 mg/L kanamycin). When the shoots grew to around 2 cm in length, the explants were transferred to rooting medium (MS + 400 mg/L cefotaxime + 100 mg/L kanamycin). Finally, after the roots were developed and mature, the plantlets were removed from the medium and planted in sterile soil.

After one month of growth, a Plant Rapid Genome Extraction kit (Tsingke, Wuhan, China) was used for a positive test of pCAMBIA1300-OfYABBY12 transgenic and wild-type (WT) tobacco leaves. Positive plants and WT plants were used for semi-quantitative validation, and transgenic lines with high levels of expression were selected for phenotype observation, scanning electron microscopy, gas chromatography–mass spectrometry (GC–MS), and RNA sequencing (RNA-Seq).

GC–MS volatile analysis

Headspace solid-phase microextraction (HS-SPME) was used to collect VOCs released from tobacco leaves or flowers. The samples of fresh leaves or flowers were ground in liquid nitrogen, 1 g of leaf or flower powder was placed in a 10-mL SPME vial with 3 mL NaCl saturated solution, and 1 µL of 5000-fold diluted ethyl caprate was added as the internal standard. Each vial was placed at room temperature (25 ± 2 °C) for 30 min and then extracted at 55 °C for 30 min using an extraction head composed of 65 µM polydimethylsiloxane (PDMS)/divinylbenzene (DVB) fiber (Supelco Co., Bellefonte, PA, USA) for GC–MS detection. GC–MS sequencing was conducted according to a previously described protocol [ 30 ].

Scanning electron microscopy

Fresh tobacco leaf samples were fixed in formalin–acetic acid–ethyl alcohol (FAA) at 4 °C for 48 h. The samples were then dehydrated sequentially in a gradient ethanol series, and after dehydration, the samples were vacuum-dried and sprayed with a gold film layer. Finally, the samples were placed under an environmental scanning electron microscope (Quanta 200, FEI Inc, Netherlands) for observation and photographs.

RNA-Seq analysis

Total RNA was extracted from mature WT and OfYABBY12 -overexpressing ( OfYABBY12-OE ) tobacco leaves using an RNAprep Pure Plant Kit (Tiangen, Beijing, China). Each sample had three biological replicates. RNA-Seq was performed by the Guangzhou Gene Denovo Biotechnology Co. (Guangzhou, China) using the Illumina HiSeq2500 platform. All sequencing data were uploaded to the National Center for Biotechnology Information (NCBI) Sequence Read Archive (SRA) database ( https://www.ncbi.nlm.nih.gov/sra/ ) under the accession number SRP450701.

Dual-luciferase transient expression assay

The coding sequence (CDS) of OfYABBY12 was amplified via PCR using gene-specific primers (Table S2 ) and connected to the pGreenII 62-SK vector to generate an effector, which was transformed into the A . tumefaciens strain GV3101 (pSoup). Then, the A . tumefaciens cells carrying the effector and reporter (pGreenII 0800-LUC-OfCCD4, preserved by our group) plasmids were mixed in a 4:3 ratio (v/v) and injected into N. benthamiana leaves. After 48 h, the luciferase (LUC) signal was detected using BERTHOLD NightSHADE LB 985 (Berthold, Bad Wildbad, Germany), and LUC and renilla luciferase (REN) were detected using a Dual-Luciferase Reporter Assay System kit (Yeasen Biotechnology, Shanghai, China).

Statistical analysis

One-way analysis of variance (ANOVA), Duncan’s multiple range test, and Student’s t-test were performed using IBM SPSS Statistics (version 20.0). A p -value smaller than 0.05 was considered significant. A minimum of three biological replicates were utilized for all experiments. Bar graphs were created using Origin Pro 2018. Heat maps were generated using TBtools software (version 1.120). Principal component analysis (PCA) and orthogonal partial least squares discrimination analysis (OPLS-DA) of VOCs were performed using SIMCA-13.0 software (version 13.0.3).

Identification and classification of YABBY gene family members in O. fragrans

In this study, HMMER was used to identify 19 candidate YABBY genes in the O . fragrans whole genome database, and six sequences without intact structural domains were removed using NCBI-CDD, Pfam, and SMART. A total of 13 YABBY genes were identified in the O . fragrans genome. The OfYABBY genes were named based on their position on chromosomes as OfYABBY1–OfYABBY13 , and these 13 genes were located on O . fragrans chromosomes 6, 10, 11, 16, 21, and 23 (Fig. 1 A). The length of OfYABBY proteins ranged from 149 aa (OfYABBY13) to 247 aa (OfYABBY2), and the protein molecular weight ranged from 16.69 kDa (OfbYABBY13) to 27.39 kDa (OfbYABBY2). The theoretical isoelectric point (pI) was 6.18–9.3, and OfYABBY5, OfYABBY8, OfYABBY9, and OfYABBY10 were acidic proteins (pI < 7.00), while the remaining proteins were basic (Table S3 ).

The sequence alignment results of the 13 OfYABBY proteins revealed that all OfYABBY proteins contained two highly conserved protein domains, of which one was a C 2 C 2 zinc finger domain in the N terminal, and one was a YABBY domain in the C terminal (Fig. S1 A). In addition, the 13 OfYABBY genes contained four to seven introns, of which most OfYABBY genes contained six introns. OfYABBY5 and OfYABBY 8 contained the greatest number of introns at seven. Overall, OfYABBY genes that clustered together shared identical or similar exon/intron structures. The conserved motifs of the OfYABBY family were analyzed (Table S4 ). All members contained at least two motifs, motifs 1 and 2, and genes that clustered together had similar motifs (Fig. S1 B). These genes may have similar functions.

Interactions between cis- and trans-acting factors can regulate gene expression. The promoters and their upstream cis-acting elements were analyzed to predict their corresponding gene functions. In the O . fragrans YABBY gene family, every gene promoter contained four to 10 cis-acting elements (Fig. S2 ). Most were considered involved in light response, including GT1-motif, Box 4, TCT-motif, G-Box, AE-box, GA-motif, ATCT-motif, GATA-motif, chs-CMA1a, 3-AF1 binding, I-box, AE-box, TCCC-motif, MRE, and ACE. The responses to gibberellin, abscisic acid, salicylic acid, auxin, and methyl jasmonate included TATC-box, P-box, GARE-motif, ABRE, TCA-element, TGA-box, TGA-element, TGACG-motif, and CGTCA-motif. LTR, MBS, ARE, and TC-rich repeats might be involved in responding to drought, anaerobic, and low temperature stress. In addition, cis-acting elements such as CAT-box and HD-Zip 1 were involved in the developmental regulation of plant tissues and organs. This means that OfYABBY s may be involved in the responses to many plant hormones and environmental stress and play a role in plant growth and development.

Phylogenetic analysis and gene duplication

To understand the phylogenetic relationship between various YABBYs, 56 YABBY proteins from dicotyledonous plants ( O . fragrans , A . thaliana , S . lycopersicum , and V . vinifera [ 15 ]) and monocotyledonous plants ( O . sativa and Z . mays ) were used to construct a phylogenetic tree (Fig. 1 B). Based on the classification of A. thaliana YABBY proteins [ 39 ], the 13 OfYABBYs were divided into five subfamilies, namely FIL/YAB3, YAB5, YAB2, CRC, and INO. The FIL/YAB3 subfamily included five OfYABBY proteins, and the YAB2 subfamily included four OfYABBY proteins. In addition, the INO subfamily included two YABBY proteins, and the CRC and YAB5 subfamilies each included one OfYABBY (Table S3 ). As predicted, phylogenetic analysis showed that OfYABBYs had the closest phylogenetic relationship to YABBYs from dicotyledonous plants. The YABBYs of dicotyledonous plants were all clustered together. Moreover, the YABBYs of monocotyledonous plants, such as rice ( O . sativa ), formed a parallel branch, consistent with previous reports [ 9 ]. This shows that YABBY genes may function in the differentiation of monocotyledonous and dicotyledonous plants and that they are conserved in dicotyledonous plants.

In addition, phylogenetic analysis of O . fragrans YABBY protein sequences was conducted based on YABBYs in M . lewisii , C . sinensis , C . praecox , A . annua , and M . spicata . This is because their functions have been sufficiently discussed, such as MlYAB1 / 2 / 3 / 5 , CsFILa / b , and CsYAB2 , which are involved in leaf development regulation [ 33 , 34 ], and CpFIL , CpCRC , CpYABBY2 , CpYABBY5-1 / -2 , AaYABBY5 and MsYABBY5 , which are involved in secondary metabolite biosynthesis [ 8 , 17 , 18 , 35 ]. Based on the results (Fig. S3 ), it was deduced that the functions of OfYABBY1 / 2 / 3 / 4 / 5 / 6 / 7 / 8 / 12 / 13 genes of the FIL/YAB3, YAB2, and YAB5 subfamilies in O. fragrans may be related to leaf development or secondary metabolite synthesis. In addition, as shown in Fig. 1 B, the FIL/YAB3 and YAB2 subfamilies contained more OfYABBY genes than other subfamilies, exhibiting significant gene duplication. However, because the number of O . fragrans YABBY family members was low, gene collinearity analysis did not find tandem repeat OfYABBY genes, but three segmental duplication of OfYABBY genes ( OfYABBY1/OfYABBY12 , OfYABBY2/OfYABBY13 , and OfYABBY4/OfYABBY7 ) were detected (Fig. 1 C).

Chromosomal distribution, phylogenetic relationships, and collinearity analysis of Osmanthus fragrans YABBY genes. ( A ) Chromosome locations of the OfYABBY genes. ( B ) Phylogenetic analysis of YABBYs from O . fragrans , Arabidopsis thaliana , Vitis vinifera , Solanum lycopersicum , Oryza sativa and Zea mays . Numbers at the nodes indicate bootstrap values; values lower than 50% are not shown. The sequences of the YABBYs used for phylogenetic relationship analysis are listed in Table S5 . ( C ) Collinearity analysis for all OfYABBY genes

Expression patterns of OfYABBYs

Transcriptome data were obtained to analyze the expression patterns of OfYABBY s in different O . fragrans cultivars [ 40 ] and different flowering stages (bud-pedicel stage, bud-eye stage, primary blooming stage, full blooming stage, and flower fading stage) (unpublished, Table S6 ). The results showed that two OfYABBY genes in the INO subfamily ( OfYABBY9 and OfYABBY10 ) and OfYABBY11 in the CRC subfamily had limited expression or were not expressed in floral tissues. Previous studies have reported that INO and CRC subfamily genes are only expressed in reproductive organs, and it is hypothesized in this study that OfYABBY s in the CRC and INO subfamilies may not participate in the formation of floral organs. Unlike OfYABBY9 , OfYABBY10 , and OfYABBY11 , OfYABBY genes in the FIL/YAB3, YAB2, and YAB5 subfamilies, except from OfYABBY4 and OfYABBY8 , were highly expressed in floral tissues, especially OfYABBY12 and OfYABBY13 (Fig. 2 A).

Expression analysis of OfYABBY genes. ( A ) Differential expression profiles of OfYABBY genes in 13 cultivars at the full blooming stage, and five flowering stages including the bud-pedicel stage ( S1 ), bud-eye stage ( S2 ), primary blooming stage ( S3 ), full blooming stage ( S4 ), and flower fading stage ( S5 ) of Osmanthus fragrans ‘Rixiang Gui’ based on RNA sequencing data. ( B ) Expression patterns of OfYABBY genes were confirmed in roots, stems, leaves (young and mature leaves), and flowers (full blooming stage) using quantitative reverse-transcription polymerase chain reaction (qRT-PCR) analysis. Error bars indicate the standard deviations of three biological replicates. Different letters indicate a significant difference ( p < 0.05) as determined by analysis of variance (ANOVA), which is based on Duncan’s multiple range test

This study further conducted qRT-PCR analysis of the expression levels of 10 OfYABBY genes from the FIL/YAB3, YAB2, and YAB5 subfamilies in the roots, stems, leaves (young and mature leaves), and floral tissues. The expression patterns of various OfYABBY s in different tissues showed significant differences (Fig. 2 B). Overall, these 10 OfYABBY genes were slightly or not expressed in roots and stems. Among them, OfYABBY4/5/6/7/8 from the FIL/YAB3 subfamily exhibited preferential expression in young leaves, and OfYABBY3 from the YAB5 subfamily had low expression in roots, stems, and mature leaves, and highest expression in young leaves, followed by flowers. Notably, OfYABBY1 /2 /12/13 exhibited similar expression patterns, with significantly higher expression in flowers than in other tissues.

Subcellular localization and transcriptional activation activity of OfYABBYs

To examine the potential function of OfYABBY genes in transcriptional regulation, this study selected six OfYABBY genes from the FIL/YAB3, YAB2, and YAB5 subfamilies for subcellular localization analysis based on the bioinformatics analysis. Laser confocal microscopy revealed that the green fluorescent protein (GFP) fluorescence signals of 35 S::GFP-OfYABBY3/5/7/8/12/13 fusion proteins were detected mainly in the cell nuclei (Fig. 3 ). In addition, this work further cloned these six OfYABBY genes into the yeast expression vector pGBKT7 and found that yeast strains carrying the pGBKT7 empty vector (negative control) and the pGBKT7-OfYABBY vectors exhibited good growth on SD/-Trp culture medium. Only pGBKT7-OfYABBY5/8-transformed yeast could grow on SD/-Trp-Ade culture medium, and these strains showed normal growth and blue colonies on X-α-gal containing SD/-Trp-Ade culture medium (Fig. 4 ). This indicates that OfYABBY5/8 shows transcriptional activity in yeast, while OfYABBY3/7/12/13 does not show transcriptional activity.

Subcellular localization of selected OfYABBY proteins. The OfYABBY proteins fused with green fluorescent protein (GFP) were transiently expressed in tobacco leaf cells to observe subcellular localization through laser confocal microscopy. GFP fluorescence is shown in green and the nucleus is blue with 4’,6-diamidino-2-phenylindole (DAPI) staining

Transcriptional activation analysis of selected OfYABBY proteins. The transformed yeast cells containing pGBKT7 and pGBKT7-OfYABBYs were spread on SD/-Trp, SD/-Trp-Ade, and SD/-Trp-Ade + X-α-gal media

Phenotypes of transgenic N. tabacum overexpressing OfYABBY12

Plant YABBY transcription factors participate in the development of plant leaves and floral organs, as well as the biosynthesis of secondary metabolites, such as floral VOCs. Therefore, this study selected OfYABBY12 , significantly more highly expressed in O. fragrans flowers than in other organs, for heterologous overexpression in tobacco. This allowed the further examination of the potential function of OfYABBY s. Positive transgenic tobacco plants were selected using semi-quantitative RT-PCR, and 10 transgenic lines were obtained (Fig. S4 ). Three lines with higher expression levels (lines 2, 5, and 12) were selected for subsequent analysis.

The phenotypic observation of tobacco leaves showed that, compared with the WT, the most intuitive phenotypic difference was that wrinkles appeared at the early stages of development in OfYABBY12-OE tobacco leaves and became more severe (Fig. 5 A). Compared with WT tobacco, leaves in the overexpressing lines exhibited significant downward curvature and wrinkling (Fig. 5 B), indicating that OfYABBY12 participated in the establishment of abaxial polarity in tobacco leaves. Scanning electron microscopy images of tobacco leaves (Fig. 5 C) showed that the cross-sections of leaves from overexpression lines were significantly thinner, while the palisade and spongy mesophyll tissues were denser compared with WT tobacco (panels a–d). The leaf thickness of OfYABBY12-OE in lines 2, 5, and 12 decreased by 33, 33, and 57%, respectively, compared with the WT (Fig. S6 ). It was also observed that WT tobacco leaves were filled with granular inclusions, while there were significantly fewer inclusions in overexpressing lines (panels e–h). However, no significant difference was observed in leaf epidermal cells. Specifically, no significant differences were observed in epidermal hair (panels i–l) or stomata (panels m–p).

Phenotypic analysis of OfYABBY12 transgenic plants. ( A ) Leaf morphology of the wild-type (WT) and OfYABBY12-OE lines (overexpression of OfYABBY12 in tobacco (OE)) at different developmental stages. ( B ) OfYABBY12 transgenic plants produced curled leaves when compared with the WT. ( C ) Scanning electron microscopic images of tobacco leaves. (a–h) Transverse sections of tobacco leaves. (i–p) Epidermal structures of tobacco leaves. Red arrows show the inclusions in the tobacco leaves

Phenotypic observation of tobacco flowers showed that the pistil (style) of overexpressing tobacco lines was significantly extended compared with the WT, while the stamen length remained unchanged after OfYABBY12 gene expression was upregulated (Fig. S7 ).

Detection of VOCs in transgenic N. tabacum overexpressing OfYABBY12

To further determine the function of OfYABBY12 , this study assessed VOC levels in the leaves of OfYABBY12-OE tobacco plants. PCA revealed significant metabolic differences between WT and OfYABBY12-OE tobacco leaves (Fig. 6 A), and variable importance in projection (VIP) values from OPLS-DA showed that β-ionone was the key differential metabolite between WT and OfYABBY12-OE tobacco leaves (Table S7 ). In OfYABBY12-OE tobacco leaves, the β-ionone content and total VOC content were both significantly lower than in the WT leaves (Figs. 6 B and C). However, the GC–MS of the tobacco flowers showed no significant differences in VOCs released from WT and OfYABBY12-OE tobacco, and β-ionone was not detected in any of the tobacco flowers. PCA also showed that VOCs released by WT and overexpressing tobacco flowers could not be differentiated (Fig. S8 ).

Effects of OfYABBY12 overexpression on volatile organic compound (VOC) metabolism and the structure of tobacco leaves. ( A ) Principal component analysis (PCA) of VOCs in wild-type (WT) and OfYABBY12 -overexpressing ( OfYABBY12-OE ) leaves. ( B , C ) Relative content analysis of β-ionone and total compounds of tobacco leaves. Two replicates per strain are shown in ( B ), and the means calculated from three strains with error bars reflecting standard deviations are shown in ( C ). ( D ) The dual-luciferase assay verified the relationship between OfYABBY12 and Pro- OfCCD4 . Renilla (REN) luminescence was used to normalize the luciferase (LUC) activity. The mean ± standard deviation (SD) from three replicates is shown. Asterisks indicate significant differences (Student’s t-test: * P < 0.05; ** P < 0.01)

In O . fragrans , carotenoid cleavage dioxygenase gene 4 ( CCD4 ) positively regulates β-ionone biosynthesis [ 41 , 42 ]. Thus, this study verified the regulatory relationship between OfYABBY12 and the OfCCD4 promoter using a dual-luciferase assay. Tobacco leaf cells had strong LUC signals, but the LUC/REN ratio of the experimental group (35 S::OfYABBY12 + p OfCCD4 ::LUC) was significantly lower than that of the control group (empty vector + p OfCCD4 ::LUC), indicating that OfYABBY12 negatively regulated the expression of OfCCD4 (Fig. 6 D).

Subsequently, RNA-Seq analysis was conducted on tobacco leaves to study the effects of OfYABBY12 overexpression on the transcription levels in overexpressing tobacco. A total of 3721 differentially expressed genes (DEGs, expression change > 2-fold, p < 0.05) were identified (Fig. S9 ). The Kyoto Encyclopedia of Genes and Genomes (KEGG) analysis of DEGs showed that these DEGs mainly participate in signaling pathways and metabolism in plants. Most DEGs found in the present study were concentrated in secondary metabolite synthetic pathways, such as in the biosynthesis of terpenes, flavonoids, and phenylpropanoids (Fig. 7 A). In addition, Gene Ontology (GO) enrichment analysis of these DEGs found three GO entries in the top 20 enriched items related to terpene biosynthesis (Fig. 7 B). Analysis of the DEGs that participate in terpene biosynthesis found that most upstream genes in the metabolic pathway were upregulated in the overexpressing lines. Among downstream genes, some NtTPSs were downregulated, and some were upregulated. NtCCD1 and NtCCD4 were significantly downregulated (Fig. 7 C).

Transcriptome profiling of tobacco leaves. ( A ) Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway analysis of differentially expressed genes (DEGs) in transgenic leaves. ( B ) Gene Ontology (GO) classification of unigenes among the annotated DEGs of OfYABBY12 overexpression in transgenic leaves. The bubble chart shows the enrichment of DEGs in certain pathways. ( C ) Overview of transcript changes in terpene biosynthesis pathway genes in wild-type (WT) and OfYABBY12 -overexpressing ( OfYABBY12-OE ) leaves. DXS: 1-deoxy-D-xylulose-5-phosphate synthase; DXR: 1-deoxy-D-xylulose-5-phosphate reductoisomerase; MCT: 2-C-methyl-D-erythritol 4-phosphate cytidylyltransferase; CMK: 4-diphosphocytidyl-2-C-methyl-D-erythritol kinase; MDS: 2-C-methyl-D-erythritol 2,4-cyclodiphosphate synthase; HDS: (E)-4-hydroxy-3-methylbut-2-enyl-diphosphate synthase; HDR: 4-hydroxy-3-methylbut-2-enyl diphosphate reductase; AACT: acetyl-CoA C-acetyltransferase; HMGS: 3-hydroxy-3-methylglutaryl-CoA synthase; HMGR: 3-hydroxy-3-methylglutaryl CoA reductase; MVK: mevalonate kinase; PMK: phosphomevalonate kinase; MVD: diphosphomevalonate decarboxylase; TPS: terpene synthase; CCD: carotenoid cleavage dioxygenase

Overview of the YABBY gene family in O. fragrans

The YABBY gene family has relatively low membership in different species and is a small gene family. For example, six, nine, and seven YABBY gene members have been identified in A . thaliana [ 39 ], S . lycopersicum [ 43 ], and V . vinifera [ 15 ], respectively. In this study, 13 OfYABBY genes were identified in the O . fragrans genome. This relatively high number may be the result of gene duplication events. This study did not find tandem repeats of the YABBY genes in O . fragrans . However, three segmental duplication YABBY genes were identified (Fig. 1 C), indicating that the evolution of the O . fragrans YABBY gene family may have been driven by segmental duplication. In addition, genomic studies have shown that O . fragrans underwent two whole genome duplication events compared with A . thaliana and V . vinifera [ 30 ].

OfYABBY s in O . fragrans could be divided into five subfamilies based on phylogenetic and gene structural analysis. Genes in the same subfamily showed similar motifs and intron/exon structures, suggesting that they may have similar functions. In addition, an analysis of the promoter regions of O . fragrans YABBY genes showed that photo-responsive elements were present in all members and were the cis-acting elements with the highest quantity. These genes may play an important role in photo-response and photomorphogenesis, thereby affecting the growth and development of plant leaves. Moreover, some cis-acting elements involved in the developmental regulation of plant tissues and organs were identified. Previous studies have also reported that YABBY gene family members play extremely important roles in leaf development and synthesis [ 44 , 45 , 46 , 47 ]. In addition, the cis-acting elements include some plant hormone response elements, such as abscisic acid, auxin, and methyl jasmonate. One study reported that the interactions between A . thaliana FIL and JAZ proteins (an inhibitor of the jasmonic acid pathway) affected anthocyanidin accumulation [ 48 ]. O. fragrans OfYABBY1/2/4/6/7/8/9/10/11/12/13 all contain methyl jasmonate response elements. We speculate that these OfYABBY genes may be mediated by jasmonic acid signaling to regulate the synthesis of various secondary metabolites.

The function of O . fragrans YABBY genes can be predicted to some extent based phylogenetic relationships with previously studied YABBY genes. Consistent with previous studies, the O . fragrans YABBY genes were found to have closer phylogenetic relationships with YABBYs from dicotyledon plants than with those from monocotyledon plants ( A . thaliana , S . lycopersicum , and V . vinifera ) (Fig. 1 B). As important model plants, the functions of the A . thaliana and S . lycopersicum YABBY genes have been extensively examined. These genes mainly play important roles in plant growth and development, particularly in leaf growth, fruit development, floral organ formation, and the synthesis of plant secondary metabolites [ 14 , 27 , 49 , 50 ]. In addition, subcellular localization analysis showed that 35 S::GFP-OfYABBY3/5/7/8/12/13 fusion proteins were mainly located in the nucleus, suggesting that these proteins have diverse functions in the nucleus. Transcriptional activity analysis revealed that OfYABBY5/8 exhibited transcriptional activity in yeast cells and may directly regulate downstream target genes. However, OfYABBY3/7/12/13 did not exhibit transcriptional activity in yeast cells, and thus, these proteins may require interactions with other transcription factors or specific environmental conditions to perform their regulatory functions.

OfYABBY12 plays a negative role in VOC synthesis

YABBY transcription factors have been reported to have tissue specificity in plants and to play different roles in different plant tissues [ 44 ]. In the present study, OfYABBY9 , OfYABBY10 , and OfYABBY11 were not detected or exhibited extremely low transcriptional expression in different cultivars or different flowering stages in O . fragrans floral organs. In A . thaliana , AtINO and AtCRC are only expressed in reproductive organs [ 22 , 23 ]; OfYABBY9 , OfYABBY10 , and AtINO are in the same subfamily, and OfYABBY11 and AtCRC in the same subfamily (Fig. 1 B). This suggests that O. fragrans CRC and INO subfamily genes may not participate in regulating the development of floral organs. However, the FIL/YAB3, YAB2, and YAB5 subfamily genes, including OfYABBY1/2/3/6/7/12/13 , are highly expressed in O . fragrans leaves or flowers but lowly expressed or not expressed in roots and stems. This suggests that these genes may play important roles in O . fragrans leaves and floral organs. Furthermore, studies have reported that there is redundancy in the functions of genes in the FIL/YAB3, YAB2, and YAB5 subfamilies [ 22 , 51 ], and these genes often participate in regulating leaf morphogenesis, the development and differentiation of lateral organs, and the biosynthesis of secondary metabolites [ 8 , 11 , 13 , 17 , 28 ].

Notably, comparing the transcript levels of all OfYABBY s revealed that OfYABBY12 in the YAB2 subfamily had the highest transcript level (Fig. 2 A) and showed significant differences in expression levels among O . fragrans roots, stems, young leaves, mature leaves, and floral organs (Fig. 2 B). Therefore, this study selected OfYABBY12 for further functional validation. However, a stable genetic transformation system for O . fragrans has not yet been established. Thus, OfYABBY12 was stably overexpressed in tobacco to determine whether OfYABBY12 regulates the differentiation and formation of tobacco leaves and floral organs, as well as whether it affects their volatile metabolites. In the present study, RNA-Seq analysis of WT and OfYABBY12-OE tobacco leaves found that most DEGs were enriched in metabolic pathways related to the synthesis of terpenes, flavonoids, and phenylpropanoids (Figs. 7 A and B). GC–MS results showed that there were significant differences in the VOCs between WT and overexpressing tobacco leaves. The content of β-ionone and total VOCs were significantly decreased (Figs. 6 A and C), and critical genes that participate in β-ionone synthesis, such as NtCCD1 and NtCCD4 , were significantly downregulated in overexpressing tobacco leaves (Fig. 7 C). It has also been reported that MsYABBY5 negatively regulates the synthesis of volatile terpene compounds in M . spicata [ 8 ]. β-Ionone is a critical compound for floral scent synthesis in O . fragrans [ 52 ]. Our previous study also found that OfYABBY12 in the molecular regulatory network of β-ionone synthesis showed a significant negative correlation with critical enzyme genes in its metabolic pathway (Fig. S10 ) [ 40 ]. Correspondingly, the dual-luciferase assay in the present study showed that OfYABBY12 negatively regulated the expression of OfCCD4 , which has been reported to promote β-ionone synthesis [ 41 , 42 ]. The results suggest that OfYABBY12 negatively regulates β-ionone synthesis in O . fragrans .

In addition, it was observed that the inclusions of OfYABBY12-OE tobacco leaves were significantly decreased compared with the WT under scanning electron microscopy (Fig. 5 C), but whether this is related to the reduction of VOCs needs further study. However, OfYABBY12 overexpression did not significantly affect VOCs from tobacco flowers. This suggests that OfYABBY12 overexpression affects VOCs from tobacco leaves, but not from tobacco flowers. Further studies are also needed to determine the regulatory relationship.

OfYABBY12 is involved in the development of leaves and flowers

In the present study, the overexpression of OfYABBY12 in tobacco revealed that OfYABBY12 overexpression affected the formation of the adaxial–abaxial axis in tobacco leaves, causing leaves to curl and crenations to occur. In Saccharum spontaneum , SsYABBY2 overexpression causes the abaxial side of A . thaliana leaves to curl [ 53 ]. Overexpression of C . sinensis CsFIL and CsYAB2 in A . thaliana causes leaves to curl [ 33 ]. Furthermore, one study found that the overexpression of the V . vinifera VvYABBY4 gene in S . lycopersicum caused the pistils (stigma) of transgenic S . lycopersicum to become longer [ 15 ], while the downregulation of MlYAB1 , MlYAB2 , MlYAB3 , and MlYAB5 in M . lewisii inhibited style elongation [ 34 ]. In the present study, OfYABBY12 , VvYABBY4 , and MlYAB2 were in the same subfamily (Figs. 1 B and S3 ). Significant elongation was also observed in the pistils (stigma) of OfYABBY12-OE tobacco flowers, while anther length remained unchanged.

The present study identified 13 OfYABBY genes in the O . fragrans genome, which were classified into five subfamilies. Phylogenetic analysis and gene duplication events demonstrated that gene duplication aided in the expansion of the O . fragrans OfYABBY gene family and that the gene functions of the OfYABBY family may be conserved. The genes in the YAB2, FIL/YAB3, and YAB5 subfamilies may have overlapping functions. In addition, the OfYABBY gene expression pattern analysis indicated that OfYABBY genes in the YAB2, FIL/YAB3, and YAB5 subfamilies may play important roles in O . fragrans leaf and/or floral organs. Functional validation showed that OfYABBY12 significantly affected the VOCs from tobacco leaves, especially β-ionone, and the dual-luciferase assay revealed that OfYABBY12 negatively regulated the expression of OfCCD4 , which promoted β-ionone synthesis. OfYABBY12 also played an important role in the establishment of polarity in tobacco leaves and in the development of lateral organs (pistils). The above results suggest that the OfYABBY gene family may participate in the growth and development of O . fragrans leaves and lateral organs, as well as in the synthesis of O . fragrans floral scent. In conclusion, this study provides a foundation for further research on the YABBY gene family in O . fragrans as well as new findings regarding the biosynthesis of the floral scent substance β-ionone in O . fragrans .

Data availability

All data generated or analyzed during this study are included in this published article, its supplementary information files and publicly available repositories. RNA-Seq raw data were uploaded to the NCBI sequence read archive ( http://www.ncbi.nlm.nih.gov/sra/ ) under accession number SRP450701 and are accessible under Bioproject archive number PRJNA997126 ( http://www.ncbi.nlm.nih.gov/bioproject/ ).

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Acknowledgements

We would like to thank all of the colleagues in our laboratory for providing useful discussions and technical assistance.

This work was supported by the National Natural Science Foundation of China (32071828) and the Priority Academic Program Development of Jiangsu Higher Education Institutions (PAPD).

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T.T.S. and Y.Z.Y. conceived and designed the research; T.T.S. and Y.F.Y. performed all experiments; X.L.Y. and L.G.W. provided technical assistance; T.T.S. wrote the manuscript; and L. Z., Y.Z.Y., and L.G.W. revised the manuscript. All authors read and approved the final manuscript.

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Shi, T., Zhou, L., Ye, Y. et al. Characterization of YABBY transcription factors in Osmanthus fragrans and functional analysis of OfYABBY12 in floral scent formation and leaf morphology. BMC Plant Biol 24 , 589 (2024). https://doi.org/10.1186/s12870-024-05047-y

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Transcription factors in megakaryocytes and platelets

Hengjie yuan.

1 Tianjin Institute of Neurology, Department of Neurosurgery, Tianjin Medical University General Hospital, Tianjin, China

2 BloodWorks Research Institute, Seattle, WA, United States

Jianning Zhang

Jing-fei dong.

3 Division of Hematology, Department of Medicine, University of Washington, School of Medicine, Seattle, WA, United States

Zilong Zhao

Transcription factors bind promoter or regulatory sequences of a gene to regulate its rate of transcription. However, they are also detected in anucleated platelets. The transcription factors RUNX1, GATA1, STAT3, NFκB, and PPAR have been widely reported to play key roles in the pathophysiology of platelet hyper-reactivity, thrombosis, and atherosclerosis. These non-transcriptional activities are independent of gene transcription or protein synthesis but their underlying mechanisms of action remain poorly defined. Genetic and acquired defects in these transcription factors are associated with the production of platelet microvesicles that are known to initiate and propagate coagulation and to promote thrombosis. In this review, we summarize recent developments in the study of transcription factors in platelet generation, reactivity, and production of microvesicles, with a focus on non-transcriptional activities of selected transcription factors.

1. Introduction

Transcription factors (TFs) are a group of mediators that bind the promoter or regulatory sequence of a gene to control its rate of transcribing genetic information from DNA to messenger RNA ( 1 ). This transcription control is key to ensuring an adequate level of expression of a given protein in targeted cells at a particular developmental stage. It not only directs the processes of proliferation, growth, and death of a cell, but also controls the rate of cell migration and organizational development during embryonic development, as well as regulating cellular response to the extracellular matrices. Thus far, more than 1600 transcription factors have so far been identified ( 2 , 3 ), and they work in a coordinated fashion to down- as well as up-regulate target genes. The activation of a given gene can be regulated by multiple transcriptional factors and one transcription factor can regulate multiple genes. Such a multivalent activity is possible because of the modular structure of a transcriptional factor, which typically includes a DNA-binding domain, signal-sensing domain that contains binding sites for transcription co-regulators, and an optional transactivation domain, which senses external signals and transmits them to the rest of the transcription complex ( 4 , 5 ). Because of their roles in regulating gene transcription, the activation and suppression of transcription factors is extensively reported in cancer development ( 6 ).

Paradoxically, multiple transcription factors have been reported to express and be active in platelets ( Table 1 ), the anucleated offspring of megakaryocytes with a very limited capacity for protein synthesis ( 7 ). An obvious question is whether these transcription factors are merely leftover from parental megakaryocytes or have unique activities in platelets. Reports from studies on platelet transcription factors have been scarce in the literature, but increasing evidence suggests that transcription factors in platelets have unique activities of their own independent of their transcriptional activities ( 8 – 10 ). However, past research on transcription factors in platelets is often limited to reporting their presence and activation status, without further investigation of their activities in regulating platelet functions and, more importantly the underlying mechanism of their regulatory activities.

Table 1

Roles of transcription factors in platelets.

Transcription factor	Roles under activation or mutation	Associated hematologic abnormalities
RUNX1	Platelet granule development, platelet activation	MDS/AML
GATA1	Inhibit aggregation	Dyserythropoiesis
STAT3	Increase aggregation, P-selectin, thrombosis	Coronary artery diseases
NFkB	Increase aggregation, spreading, clot retraction, GPIBa shedding	Cardiovascular diseases
PPAR	Inhibition of platelet function	Cardiovascular diseases

AML, acute myeloid leukemia; MDS, myelodysplastic syndrome.

Platelets circulate along the vessel wall and act to stop bleeding at sites of vessel injury. This hemostatic process requires multiple ligand-receptor interactions to tether, activate, and aggregate platelets. The tightly controlled platelet activation and aggregation that occurs at the site of vascular injury during hemostasis can become dysregulated in pathological conditions, promoting thrombosis and inflammation. For example, platelets promote arterial thrombosis or thromboembolism when activated either on the surface of a ruptured atherosclerotic plaque or by pathological levels of high fluid shear stress in the area of arterial stenosis, leading to acute thrombotic events such as ischemic stroke and myocardial infarction ( 11 ). Emerging evidence further suggests that platelets also act as a cellular mediator in a variety of pathophysiological conditions such as cancer, rheumatoid arthritis, atherosclerosis, trauma, and immune response ( 12 – 14 ). How transcription factors regulate platelet production from megakaryocytes has been extensively reported, but their non-transcriptional activities (i.e., activity independent of gene regulations) have only begun to be recognized. Here, we discuss several transcription factors that have been reported to regulate platelet production and function.

2. Transcription factors in platelet production

2.1. runt-related transcription factor 1.

In 1969, Weiss, et al. identified a family with an autosomal dominant inherited thrombocytopenia, caused primarily by decreased dense granule contents ( 15 ). A heterozygous Y260X mutation in the RUNX1 gene was subsequently shown to be the genetic basis of this inherited platelet defect ( 15 , 16 ). To date, more than 200 families with RUNX1 variants have been reported ( 17 ). RUNX1/AML1 (also known as CBFA2 and PEBP2αB) is a member of the Runt family, which has three known transcription factors (RUNX1, RUNX2, and RUNX3), which share the Runt homology domain near the N-terminus. This domain interacts with CBFb to bind specific sequences of DNA to regulate its transcription ( 18 ).

RUNX1 regulates several genes that control platelet production, structure, function, and intracellular signaling. One report found that 22 patients in a family with autosomal dominant thrombocytopenia had mutations in the RUNX1 gene ( 19 ) and 6 of them developed hematologic malignancies ( 20 ). RUNX1-deficient mice die in uterus due to defective hematopoiesis and resultant severe bleeding ( 21 , 22 ). Mice with the conditional knockout survive but have an impaired megakaryocyte maturation with a significant reduction in megakaryocyte polyploidization ( 23 ). Variations in the RUNX1 gene often result in bleeding diathesis, primarily because of defective platelet granules ( 15 , 16 ), which reduce platelet activation and aggregation ( 24 ). For example, mice carrying the RUNX1 p.Leu43Ser variant (equivalent to human p.Leu56Ser) exhibit a prolonged bleeding time because of defective α-granule secretion and platelet spreading ( 25 ). RUNX1 deficiency can result in pallidin dysregulation and deficient dense granules in platelets ( 26 ) as well as the Ras-related protein RAB31-mediated early endosomal trafficking of von Willebrand factor (VWF) and epidermal growth factor receptor (EGFR) in megakaryocytes ( 27 ). RUNX1 regulates the development of platelet granules through interaction with genes involved in the biogenesis of platelet granules such as the nuclear factor erythroid 2 (NF-E2).

In addition, RUNX1 can also regulate genes related to platelet functions. For example, it regulates the transcription of the non-muscle myosin IIA (MYH9) and IIB (MYH10) genes, which encode non-muscle myosin II heavy chains; RUNX1 mutations are associated with dysregulated expression of MYH10 in platelets ( 28 ); and the expression level of non-muscle myosin is used as a marker for changes in transcriptional activity of RUNX1 as well as friend leukemia integration 1 transcription factor (FLI1) ( 29 ). RUNX1 also regulates the expression of the arachidonate 12-lipoxygenase gene (ALOX12) ( 30 ), which encodes the enzyme that acts on polyunsaturated fatty acid substrates to generate bioactive lipid mediators to regulate platelet function ( 30 ). PCTP (phosphatidylcholine transfer protein) regulates the intermembrane transfer of phosphatidylcholine and its upregulation by RUNX1 sensitizes platelet response to thrombin through protease-activated receptor 4 ( 31 ). RUNX1 also regulates the expression of platelet factor 4 through coordination with transcription factors in the ETS family that share a conserved winged helix-turn-helix DNA binding domain that recognizes unique DNA sequences containing GGAA/T ( 32 ). Platelet factor 4 belongs to the CXC chemokine family and is released from α-granules of activated platelets to promote coagulation and to participate in heparin-induced thrombocytopenia ( 33 , 34 ). A recent report shows that RUNX-1 haploinsufficiency inhibits the differentiation of hematopoietic progenitor cells (HPCs) into megakaryocytes ( 35 ).

2.2. GATA-binding protein 1

GATA-binding protein 1 (GATA1) is a transcription factor that contains two zinc finger domains: a C-terminal zinc finger that binds the (T/A) GATA(A/G) motif of DNA and an N-terminal zinc finger that is required for stabilizing the C-terminal structure and also interacts with a nuclear co-factor protein called friend for GATA1 (FOG1), which stabilizes GATA1 binding ( 36 , 37 ). GATA plays a pivotal role in hematopoietic development and is found in megakaryocytes ( 38 ). GATA1-deficient mice die before birth at approximately embryonic day 10, primarily because of severe anemia ( 39 ). However, mutations in the N-terminal zinc finger domain, which reduces the transcriptional activation of GATA1 ( 36 , 40 ), are found in patients with myeloproliferative disorders and acute megakaryoblastic leukemia ( 41 ), suggesting that GATA1-FOG1 interaction is essential for the development and maturation of megakaryocytes, the parental cells of platelets. Decreased GATA-1 expression has also been reported in patients with myelodysplastic syndrome ( 42 ).

Embryonic stem cells from GATA1-deficient mice are smaller and show low expression of megakaryocytic markers, but have a high rate of proliferation ( 43 ). Complementation of these cells with a wild-type GATA1 gene allows megakaryocytes and erythrocytes to develop in response to a variety of cytokines. Additionally, cell division is attenuated in the megakaryocytic progenitor G1ME cells that overexpress GATA1. A recent report further shows that impaired MYH10 silencing causes GATA1-related polyploidization defect during megakaryocyte differentiation ( 44 ).

Furthermore, platelet aggregation induced by collagen is inhibited in GATA1 - deficient mice ( 45 ), primarily due to reduced expression of the collagen receptor GPVI. Platelet adhesion and aggregation induced by shear stress are also reduced in GATA1 - deficient mice ( 45 ). How a GATA1 deficiency causes these changes in platelet reactivity remains unknown, but these phenotypic changes in the mice provide the first indication that transcription factors could perform non-transcriptional activities in anucleated platelets.

3. Non-transcriptional activity in platelets

3.1. signal transducer and activator of transcription 3.

STAT includes a family of transcription factors critical for inflammatory and acute-phase reactions ( 46 , 47 ). They also play vital roles in cancer development and hematopoiesis ( 48 ). The homologous STAT1, STAT3, and STAT5 are expressed in human platelets and are reported to regulate platelet reactivity through residual or mitochondrial transcriptional activity in platelets. For example, STAT3 affects mitochondrial transcription by binding to the regulatory D-loop region of mitochondrial DNA upon platelet activation ( 49 ).

However, STAT3 can also be activated (phosphorylated) and dimerized in platelets stimulated with thrombopoietin ( 49 , 50 ), suggesting that STAT3 can also regulate platelet reactivity through non-transcriptional means. We have shown that STAT3 is activated and dimerized in collagen-stimulated platelets to serve as a protein scaffold that facilitates the catalytic interaction between spleen tyrosine kinase (Syk) and its substrate, PLCγ to enhance collagen-induced calcium mobilization and platelet activation ( 8 ). More importantly, STAT3 is activated to form dimers by a complex of IL-6 with its soluble receptor IL-6Rα, which activates JAK2 ( 51 ). The pharmacological inhibition of platelet STAT3 reduces collagen-induced platelet aggregation and thrombus formation on the collagen matrix ( 8 , 52 ). Platelets from STAT3-deficient mice or mice infused with a STAT3 inhibitor have reduced collagen-induced aggregation. This non-transcriptional activity of STAT3 may be critical for the development of platelet hyper-reactivity, which has been widely associated with inflammation, especially that related to the activity of the proinflammatory cytokine IL-6 ( 8 ). We have also shown that the piper longum derivative piperlongumine (PL) blocks collagen-induced platelet reactivity in a dose-dependent manner by targeting STAT3 ( 53 ). Consistent with our observations, the small molecular STAT3 inhibitor SC99 has been shown to reduce platelet activation and aggregation induced by collagen and thrombin ( 54 ). These findings offer a new pathway for reducing platelet hyper-reactivity in conditions of inflammation and in prothrombotic states associated with trauma, cancer, autoimmune diseases, and severe infection.

3.2. Nuclear factor kappa β

Nuclear factor kappa β (NFκB) is a well-defined redox-sensitive transcription factor that regulates the immune response and inflammation by controlling the expression of multiple genes activated by inflammatory mediators ( 55 – 57 ). Blocking NFκB can therefore improve outcomes of inflammatory diseases ( 58 ). NFκB is composed of p50 and p65 subunits, normally as an inactive cytoplasmic complex. The inhibitory proteins of the IκB family tightly bind the subunits of NFκB ( 59 ). Upon activation, the IκK complex phosphorylates IκBα, thus activating NFκB by detaching it from IkBα ( 60 – 62 ). Three IκK family members, α, β, and γ, are expressed in platelets, with β being the most abundant, and are reported to regulate platelet reactivity through non-transcriptional activity ( 9 , 10 , 63 ). For example, the pharmacological inhibition of IκKβ leads to reduced agonist-induced platelet activation, increased bleeding time, and prolonged thrombus formation in a mouse model ( 64 ). NF-κB has also been reported to be partially involved in the regulation of SERCA activity to regulate calcium homeostasis in platelets ( 65 ). IκKβ-deficient platelets lose the ability to shed the ectodomain of GP Ibα in response to ADP or collagen stimulations ( 66 ) but preserve thrombin-induced GP Ibα shedding ( 67 ). Collagen-induced p65 and IκKβ phosphorylation is blocked by inhibition of MAP kinase, but not by inhibition of ERK in platelets ( 68 ). The thrombin-induced GP Ibα shedding requires p38 mitogen-activated protein kinase (MAPK) and extracellular signal-regulated kinase (ERK) as its upstream and downstream molecules ( 68 , 69 ).

3.3. Peroxisome proliferator-activated receptors

The peroxisome proliferator-activated receptors (PPARs) are ligand-activated receptors in the nuclear hormone receptor family. They contain three subtypes (PPARα, PPARβ/δ, and PPARγ), which are essential in the regulation of cell differentiation, development, and metabolism ( 70 – 72 ). All PPARs heterodimerize with retinoid X receptor (RXR) and subsequently bind to a specific region of target genes called a peroxisome proliferator response element (PPRE) ( 73 ). PPARγ plays a transcription factor role in regulating platelet production from megakaryocytes, but the PPARγ ligand thiazolidinedione inhibits platelet aggregation induced by ADP under hydrostatic pressure and in diabetic mice ( 74 – 76 ). Similarly, activating PPARβ/δ also reduces platelet reactivity to ADP, thrombin, and collagen ( 77 , 78 ). However, PPARα is also required for platelet activation and thrombus formation, in which it regulates the dense granule secretion of platelets in hyperlipidemic mice ( 79 ). The reason for this apparent contradiction remains to be further investigated. PPARγ is recruited and phosphorylated by Syk to promote the recruitment of the protein called Linker for the Activation of T cells (LAT), which is necessary for collagen-induced platelet activation through glycoprotein VI ( 80 ).

While transcription factors are critically involved in megakaryocyte development and platelet production, they may also regulate platelet reactivity to conventional and specific platelet agonists ( Figure 1 ). The latter is independent of transcriptional activity, for which it is present but at a residual level. This non-transcriptional activity remains poorly understood and requires further investigation because it helps understanding how platelets are activated either by conventional agonists for hemostasis or as complications found in patients treated with drugs that block transcriptional activity of cells (e.g., cancer treatments). Such research will also play an important role in developing new therapeutics targeting these transcription factors to enhance or reduce platelet reactivity.

An external file that holds a picture, illustration, etc.
Object name is fimmu-14-1140501-g001.jpg

Transcription factors regulate platelet aggregation through non-transcriptional activities. (A) PPARγ is recruited and phosphorylated by Syk to promote the recruitment of LAT and enhance platelet aggregation; (B) NFκB is activated by upstream p38 mitogen-activated protein kinase (MAPK) and promotes platelet aggregation by regulating downstream extracellular signal-regulated kinase (ERK); (C) A complex of IL-6 with its soluble receptor IL-6R activates JAK2 to phosphorylate and dimerize STAT3, then the activated STAT3 serves as a protein scaffold to facilitate the catalytic interaction between the spleen tyrosine kinase (Syk) and its substrate PLCγ2 to promote platelet aggregation.

4. Transcription factors in extracellular vesicles released from platelets

Extracellular vesicles (EVs) are shed membrane fragments, intracellular organelles, and nuclear components from cells undergoing active microvesiculation ( 81 – 84 ) or apoptosis ( 85 – 87 ). The former is triggered by the activation of the cysteine protease calpain, which disrupts the membrane-cytoskeleton association ( 88 – 91 ). Platelets are the primary source of EVs circulating in blood, accounting for approximately 80% of total EVs ( 92 – 94 ). The subcellular size of EVs allows them to travel to areas where parental cells are unable to go. In additional to inherent functions from their parental cells, EVs also perform unique activities of their own because of molecules expressed on their surface and carried by them, the latter of which include transcription factors such as STAT3, STAT5, and PPARγ ( 95 ) as well as regulators of transcription factors ( 96 , 97 ). This EV-derived transcriptional activity has been scarcely reported but hold greats potential for influencing biological activities of target cells. For example, PPARγ in platelet EVs is taken up by monocytic THP-1 cells, where it induces the expression of fatty acid-binding protein-4 (FABP4). Monocytes receiving PPARγ-containing platelet EVs produce less inflammatory mediators and become more adherent through increased fibronectin production ( 95 ). Although reports on platelet-derived transcription factors remain very limited, a large body of evidence in the literature shows that platelet-derived EVs, especially EV-carried microRNAs, can change transcriptional activities, thus regulating the function of target cells. Platelet EV-carried NLR family pyrin domain containing 3 (NLRP3) stimulates endothelial cells to undergo pyroptosis through the NLRP3/nuclear factor (NF)-κB pathway ( 98 ). EVs from platelets stimulated with bacteria provoke proinflammatory activity of monocytes through the TRAF6/NFκB pathway ( 99 ). MicroRNA-142-3p carried by platelet-derived EVs promotes the proliferation of endothelial cells ( 100 ), whereas microRNA-126-3p-carrying platelet EVs can be internalized by macrophages to dose-dependently downregulate expression of target mRNA ( 101 ). These observations mostly pertain to phenotypic characterization with less information regarding the underlying pathways involved. Systemic studies of EV-carrying transcription factors and related mediators are therefore urgently needed.

5. Conclusion

Platelets lack a nucleus and de novo transcription, but a number of transcription factors are found in platelets and may have non-transcriptional activities that regulate platelet function. Transferring transcription factors between platelets and target cells through platelet EVs could also be a novel regulatory mechanism of cell-cell communications and a potential therapeutic target for a variety of pathologies.

Author contributions

HY and YL performed the literature search and compiled all the information from the researched articles and wrote the manuscript. ZZ, J-FD and JZ formulated, proposed, guided and wrote the manuscript. All authors contributed to the article and approved the submitted version.

Funding Statement

This study is supported by Young Scientists Award 82022020 from the National Natural Science Foundation of China (ZZ), National Natural Science Foundation of China 81971176 (ZZ), 81271361, 81271359 (JZ), 81102447 (HY), National Natural Science Foundation of China State Key Program Grant 81330029, National Natural Science Foundation of China Major International Joint Research Project 81720108015 (JZ), and Postdoctoral Science Foundation of China Grants 2013M541190 (HY).

Conflict of interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Publisher’s note

All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.

Single-Cell Chromatin Accessibility Analysis Reveals the Epigenetic Basis and Signature Transcription Factors for the Molecular Subtypes of Colorectal Cancers

Z. Liu, Y. Hu, H. Xie, and K. Chen contributed equally to this article.

Cancer Discov 2024;14:1082–105

Funder(s): National Natural Science Foundation of China (NSFC)
Award Id(s): 81972702
Funder(s): Beijing Nova Program
Award Id(s): 2022029
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Zhenyu Liu , Yuqiong Hu , Haoling Xie , Kexuan Chen , Lu Wen , Wei Fu , Xin Zhou , Fuchou Tang; Single-Cell Chromatin Accessibility Analysis Reveals the Epigenetic Basis and Signature Transcription Factors for the Molecular Subtypes of Colorectal Cancers. Cancer Discov 1 June 2024; 14 (6): 1082–1105. https://doi.org/10.1158/2159-8290.CD-23-1445

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Colorectal cancer is a highly heterogeneous disease, with well-characterized subtypes based on genome, DNA methylome, and transcriptome signatures. To chart the epigenetic landscape of colorectal cancers, we generated a high-quality single-cell chromatin accessibility atlas of epithelial cells for 29 patients. Abnormal chromatin states acquired in adenomas were largely retained in colorectal cancers, which were tightly accompanied by opposite changes of DNA methylation. Unsupervised analysis on malignant cells revealed two epigenetic subtypes, exactly matching the iCMS classification, and key iCMS-specific transcription factors (TFs) were identified, including HNF4A and PPARA for iCMS2 tumors and FOXA3 and MAFK for iCMS3 tumors. Notably, subtype-specific TFs bind to distinct target gene sets and contribute to both interpatient similarities and diversities for both chromatin accessibilities and RNA expressions. Moreover, we identified CpG-island methylator phenotypes and pinpointed chromatin state signatures and TF regulators for the CIMP-high subtype. Our work systematically revealed the epigenetic basis of the well-known iCMS and CIMP classifications of colorectal cancers.

Our work revealed the epigenetic basis of the well-known iCMS and CIMP classifications of colorectal cancers. Moreover, interpatient minor similarities and major diversities of chromatin accessibility signatures of TF target genes can faithfully explain the corresponding interpatient minor similarities and major diversities of RNA expression signatures of colorectal cancers, respectively.

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Transcription factor CaHDZ15 promotes pepper basal thermotolerance by activating HEAT SHOCK FACTORA6a

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Shaoliang Mou, Weihong He, Haitao Jiang, Qianqian Meng, Tingting Zhang, Zhiqin Liu, Ailian Qiu, Shuilin He, Transcription factor CaHDZ15 promotes pepper basal thermotolerance by activating HEAT SHOCK FACTORA6a , Plant Physiology , Volume 195, Issue 1, May 2024, Pages 812–831, https://doi.org/10.1093/plphys/kiae037

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High temperature stress (HTS) is a serious threat to plant growth and development and to crop production in the context of global warming, and plant response to HTS is largely regulated at the transcriptional level by the actions of various transcription factors (TFs). However, whether and how homeodomain-leucine zipper (HD-Zip) TFs are involved in thermotolerance are unclear. Herein, we functionally characterized a pepper ( Capsicum annuum ) HD-Zip I TF CaHDZ15. CaHDZ15 expression was upregulated by HTS and abscisic acid in basal thermotolerance via loss- and gain-of-function assays by virus-induced gene silencing in pepper and overexpression in Nicotiana benthamiana plants. CaHDZ15 acted positively in pepper basal thermotolerance by directly targeting and activating HEAT SHOCK FACTORA6a ( HSFA6a ), which further activated CaHSFA2 . In addition, CaHDZ15 interacted with HEAT SHOCK PROTEIN 70-2 (CaHsp70-2) and glyceraldehyde-3-phosphate dehydrogenase1 (CaGAPC1), both of which positively affected pepper thermotolerance. CaHsp70-2 and CaGAPC1 promoted CaHDZ15 binding to the promoter of CaHSFA6a , thus enhancing its transcription. Furthermore, CaHDZ15 and CaGAPC1 were protected from 26S proteasome-mediated degradation by CaHsp70-2 via physical interaction. These results collectively indicate that CaHDZ15, modulated by the interacting partners CaGAPC1 and CaHsp70-2, promotes basal thermotolerance by directly activating the transcript of CaHSFA6a . Thus, a molecular linkage is established among CaHsp70-2, CaGAPC1, and CaHDZ15 to transcriptionally modulate CaHSFA6a in pepper thermotolerance.

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Interaction of the transcription factors bes1/bzr1 in plant growth and stress response.

1. Introduction

2. interactors of bes1/bzr1 in plant growth and development, 2.1. interactors of bes1/bzr1 in skotomorphogenesis and photomorphogenesis, 2.2. interactors of bes1/bzr1 in root growth, 2.3. interactors of bes1/bzr1 in other developmental processes, 3. interactors of bes1/bzr1 in stress response, 3.1. interactors of bes1/bzr1 in abiotic stress response, 3.2. interactors of bes1/bzr1 in biotic stress response, 4. conclusions, author contributions, institutional review board statement, informed consent statement, data availability statement, conflicts of interest.

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Qi, G.; Chen, H.; Wang, D.; Zheng, H.; Tang, X.; Guo, Z.; Cheng, J.; Chen, J.; Wang, Y.; Bai, M.Y.; et al. The BZR1-EDS1 module regulates plant growth-defense coordination. Mol Plant 2021 , 14 , 2072–2087. [ Google Scholar ] [ CrossRef ] [ PubMed ]
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Click here to enlarge figure

Gene Name	Locus	Effect on Plant Growth through Interaction with BES1/BZR1	References
ARF6	AT1G30330	Promoting cell elongation and hypocotyl growth	[ ]
PIF4	AT2G43010	Promoting cell elongation and hypocotyl growth	[ ]
BIC1	AT3G52740	Promoting cell and hypocotyl elongation	[ ]
BLI	AT3G23980	Promoting hypocotyl elongation in darkness	[ ]
RGA	AT2G01570	Inhibiting cell elongation and BR-regulated plant growth	[ ]
HSP90	AT5G52640	Promoting hypocotyl elongation	[ ]
EIN3	AT3G20770	Promoting apical hook development	[ ]
SAUR17	AT4G09530	Promoting apical hook and closed cotyledon	[ ]
WAG2	AT3G14370	Inhibiting apical hook development	[ ]
GRF7	AT5G53660	Repressing chlorophyll biosynthesis promoting cell elongation	[ ]
phyB	AT2G18790	Repressing BR signaling	[ ]
CRY1	AT4G08920	Inhibiting hypocotyl elongation under blue light	[ , ]
UVR8	AT5G63860	Repressing BR-regulated photomorphogenesis	[ ]
BBX32	AT3G21150	Inhibiting cotyledon opening	[ ]
SHR	AT4G37650	Suppressing root lignification promoting periclinal division	[ , ]
BRAVO	AT5G17800	Suppressing root quiescent center division	[ ]
AGB1	AT4G34460	Promoting cell elongation	[ ]
PKL	AT2G25170	Promoting cell elongation	[ ]
C3H15	AT1G68200	Inhibiting cell elongation	[ ]
CYP20-2	AT5G13120	Promoting flowering	[ ]
ACO1	AT2G19590	Promoting fruit ripening	[ ]
OsWRKY53	Os05g0343400	Regulating rice architecture and increasing seed size	[ , ]
OsMED25	Os09g0306700	Regulating rice architecture	[ ]

Gene Name	Locus	Effect on Stress Tolerance through Interaction with BES1/BZR1	References
WRKY46	AT2G46400	Suppressing drought response	[ ]
WRKY54	AT2G40750	Suppressing drought response
WRKY70	AT3G56400	Suppressing drought response
RD26	AT4G27410	Inhibiting BR-regulated growth under drought condition	[ ]
TINY	AT5G25810	Inhibiting BR-regulated growth under drought condition	[ ]
HSFA1a	AT4G17750	Improving heat stress	[ ]
LBD37	AT5G67420	Promoting nitrogen response	[ ]
OsIDD10	Os04g47860	Improving nitrogen uptake	[ ]
phyB	AT2G18790	Inhibiting nitrogen uptake and sheath blight resistance	[ , ]
MYB34	AT5G60890	Suppressing insect defense	[ ]
MYB122	AT1G74080	Suppressing insect defense	[ ]
MYB51	AT1G18570	Suppressing insect defense	[ ]
EDS1	AT3G48090	Increasing pathogen resistance	[ ]
GhTINY2	GhD06G0642	Increased immune response	[ ]

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Share and Cite

Cao, X.; Wei, Y.; Shen, B.; Liu, L.; Mao, J. Interaction of the Transcription Factors BES1/BZR1 in Plant Growth and Stress Response. Int. J. Mol. Sci. 2024 , 25 , 6836. https://doi.org/10.3390/ijms25136836

Cao X, Wei Y, Shen B, Liu L, Mao J. Interaction of the Transcription Factors BES1/BZR1 in Plant Growth and Stress Response. International Journal of Molecular Sciences . 2024; 25(13):6836. https://doi.org/10.3390/ijms25136836

Cao, Xuehua, Yanni Wei, Biaodi Shen, Linchuan Liu, and Juan Mao. 2024. "Interaction of the Transcription Factors BES1/BZR1 in Plant Growth and Stress Response" International Journal of Molecular Sciences 25, no. 13: 6836. https://doi.org/10.3390/ijms25136836

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Lab on a Chip

An integrative temperature-controlled microfluidic system for budding yeast heat shock response analysis in single cell level.

Cells can respond and adapt to complex forms of environmental change. Budding yeast is wildly used as a model system for these stress response studies. In these studies, the precise control of the environment with high temporal resolution is most important. However, there is a lack of single-cell research platforms that enable precise control of the temperature and form of cell growth. This has hindered our understanding of cellular coping strategies in the face of diverse forms of temperature change. Here, we developed a novel temperature-controlled microfluidic platform that integrates a micro-heater(using liquid metal) and thermocouple(liquid metal vs conductive PDMS) on a chip. Three forms of temperature changes: step, gradient, and periodical oscillations were realized by automated equipment. The platform has the advantages of low cost and a simple fabrication process. Moreover, we investigated the nuclear entry and exit behaviors of the transcription factor Msn2 in yeast in response to heat stress (37°C) with different heating modes. The feasibility of this temperature-controlled platform for studying the protein dynamic behavior of yeast cells was demonstrated.

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J. Hong, H. He, Y. Xu, S. Wang and C. Luo, Lab Chip , 2024, Accepted Manuscript , DOI: 10.1039/D4LC00313F

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News : The 2024 HST graduation

Photo credit: Justin Knight

There were 57 clinician-scientists in this year’s graduating class, 40 attended the ceremony

Mindy Blodgett | IMES-HST

The 2024 graduating class of the Harvard-MIT Program in Health Sciences and Technology (HST) gathered on May 22, to celebrate their accomplishments with their families and friends, at the MIT Bartos Theater & Atrium. Also in attendance were HST alumni, faculty, and staff.

This 2024 graduation class includes 57 graduates: 35 MD graduates, and 25 Medical Engineering and Medical Physics (MEMP)PhDs; one Master of Science graduate, and one Graduate Education in Medical Sciences, or GEMS certificate, recipient. There were 40 graduates in attendance. HST MD graduates also participated in Harvard graduation events on May 23, and graduates of the HST Medical Engineering and Medical Physics (MEMP) PhD program participated in the MIT School of Engineering Advanced Degree Ceremony, and hooding event, on May 29.

All enjoyed congratulatory remarks from HST Associate Director Richard N. Mitchell, MD, PhD; Dean of the Harvard Medical School (HMS) George Q. Daley, MD (HST ’91), PhD; and Elazer Edelman, MD (HST ’83), PhD (HST ’84), Director of the Institute for Medical Engineering and Science (IMES). Also participating in the ceremony were Wolfram Goessling MD, PhD, the co-director of HST at Harvard, Collin M. Stultz, MD, (HST ’97), PhD, co-director of HST at MIT, and associate director of IMES (IMES is HST’s home at MIT), as well as Junne Kamihara, Associate Director, MD Advising, HST, and HST Associate Director, Matthew Frosch.

L to R, Junne Kamihara, Associate Director, MD Advising, HST; HST Associate Director Richard N. Mitchell, MD, PhD. Photo credit: Justin Knight

Dean Daley, an HST alumnus, called the occasion, a “spectacular achievement to graduate from the country’s pre-eminent program in translational biomedical science and engineering” and he praised the graduates’ “persistence in getting through the pandemic,” as Covid was at its height when many from the class began their studies in 2020. Daley observed that the graduates will witness “explosive developments” during their careers, in such areas as gene editing, artificial intelligence (AI) and the needs of an aging population.

Harvard Medical School (HMS) George Q. Daley, MD (HST ’91), PhD. Photo credit: Justin Knight.

Stultz called addressing the graduates “one of the best parts of my job,” remarking that “few individuals have achieved your level of accomplishments.”

Collin M. Stultz, MD, (HST ’97), PhD, co-director of HST at MIT, and associate director of IMES. Photo credit: Justin Knight.

Wolfram Goessling MD, PhD, the co-director of HST at Harvard, congratulated the graduates and their families and friends. Photo credit: Justin Knight.

Edelman, an HST alumnus, who is also a senior attending physician, Brigham and Women’s Hospital, shared a story about one of his patients, a middle school principal from Western Massachusetts, who was the “heart and soul” of his school, and of his small town. He said that the graduates were chosen for HST because “of what we saw in you…your heart and soul” and that “together, we can harness medicine to make the world a better place.”

Elazer Edelman, MD (HST ’83), PhD (HST ’84), Director of the Institute for Medical Engineering and Science (IMES). Photo credit: Justin Knight.

Abby Aymond, an HST MD graduate, was the 2024 class speaker. She praised the “exceptional sense of community and friendship” she had experienced while a student at HST. She said the some of the lessons she was taking from her years at HST were to “relax all the noise…focus only on the problem at hand…and to always be open to new information.”

Abby Aymond, HST MD graduate, was the 2024 class speaker. Photo credit: Justin Knight.

Elazer Edelman, left, and George Daley, right, address the graduates at the end of the ceremony, urging them to stay in touch. Photo credit: Justin Knight.

HST Associate Director Richard N. Mitchell donned the traditional Red Sox graduation cap, and applauded the graduates. Photo credit: Justin Knight.

The HST 2024 Graduates:

Doctor of Medicine

Medical Sciences

Abby Aymond, BS

Thesis Topic: Optimization of Ventricular Efficiency and Renal Artery Perfusion in a Bench Top Model System

Alaleh Azhir, BS

Thesis Topic: Chromosomes vs Hormones: Decoding the Expression Mosaic in Liver and Adipose Tissues

James Diao, BS

summa cum laude

The Seidman Prize for Outstanding HST Senior Medical Student Thesis

Richard C. Cabot Prize

Thesis Topic: The Use of Race in Clinical Algorithms

Christopher Michael Dietrich, BS

Thesis Topic: Towards Treat-Seq: Predicting Therapeutic Response from Transcriptomic Signatures

Jonah Issac Donnenfield, BA

magna cum laude

Thesis Topic: Transcriptomic Profiling of the Post-traumatic Porcine Knee: Degenerative Pathophysiology and Machine Learning Application

Micayla Flores, SB

Thesis Topic: Ambulatory and Delivery Obstetric Comorbidity Index (OB-CMI) for Identification of Pregnant Individuals at Risk for Severe Maternal Morbidity (SMM)

Allyson Freedy, BA, PhD

Leon Reznick Memorial Prize

HMS Multiculturalism Award

Thesis Topic: Uncovering the Biology of Chromatin Regulators with Drug Resistance Alleles

William Hao Ge, BS

Thesis Topic: Stereotypic Patterns and Genomic Correlates of Organotropism in Metastatic Melanoma

Blake Hauser, BSPH, PhD

Thesis Topic: Structure-Based Network Analysis Predicts Pathogenic Variants in Human Proteins Associated with Inherited Retinal Disease

Sofia Hu, BA, PhD

Thesis Topic: Transcription Factor Antagonism Regulates Heterogeneity in Embryonic Stem Cell States

Nauman Javed, BS, PhD

Thesis Topic: Strategies for Characterizing the Regulatory Code of the Human Genome

Tushar Vinod Kamath, SB, SM, PhD

Thesis Topic: Cell States and Neuronal Vulnerabilities in Neurodegenerative Diseases

Minjee Kim, BA

Thesis Topic: Transcriptional Antagonism by CDK8 Inhibition Improves Therapeutic Efficacy of MEK Inhibitors

Patrick Lenehan, BS, PhD

Thesis Topic: Investigating the Impact of Eosinophils on Pancreatic Cancer Growth and Metastasis

Claudio Macias Trevino, BS, PhD

Thesis Topic: Transcriptional Regulation of Esrp1 and its Role in Craniofacial Morphogenesis

Eliana Marostica, BA, MBMI

Thesis Topic: Systematic Quantification of Morphological Patterns in Surgical Specimens of Cancers

Eduardo Maury, SB, PhD

Thesis Topic: Somatic Mutations in the Human Brain: Tracing the Origins of Cancer and Schizophrenia

Elizabeth Minten, BS, PhD

Thesis Topic: Role of CDK12 in R-Loop Formation

Katherine Nabel Smith, BS, PhD

Thesis Topic: Molecular Mechanisms for Broad Neutralization of Emerging RNA Viruses

Julia E. Page, SB, PhD

Thesis Topic: Peptidoglycan Hydrolases, their Protein Partners, and Related Membrane Proteins in Staphylococcus Aureus

Deborah Plana, SB, PhD

Thesis Topic: Clinical Trial Data Science to Advance Precision Oncology

Sheridan Rea, BS, MS

Thesis Topic: Retrospective Cohort Analysis of Sociodemographic Factors and Postpartum Hemorrhage Outcomes

Sara Ann Rubin, BA, PhD

Thesis Topic: Zebrafish Immune Cell Development and Diversity in Health and Disease

Jamie Erin Shade, BS

Thesis Topic: Relationships Between Cardiac Magnetic Resonance-derived Myocardial, Hepatic, and Splenic Extracellular Volumes in Patients after the Fontan Operation

Bryce Filip Starr, BS

Thesis Topic: Generation and Validation of a Bileaflet Venous Valve for Single Ventricle Physiology

Hannah Jacqueline Szapary, BS, SM

Thesis Topic: Mechanical and Biologic Impact of Dynamic Loading on Bovine and Human Models of Osteoarthritis

Max Louis Valenstein, BS, MS, PhD

Thesis Topic: Integration of Amino Acid Signals by the mTORC1 Pathway

Sarah Weiss, SB, PhD

Thesis Topic: Deletion of an Exhaustion-specific PD-1 Enhancer Modulates CD8+ T Cell Fate and Function

Omar Yaghi, BS, PhD

Thesis Topic: Uncovering Stromal Cell Functions in Acute and Chronic Muscle Injuries

Katherine Young, SB, MEng

Thesis Topic: Transmission and Evolution of Staphylococcus Aureus in Families with Atopic Dermatitis

Doctor of Philosophy

Medical Engineering/Medical Physics

Jon Arizti Sanz, MNG

Thesis Topic: From Sample to Answer: Innovations in Sample Processing and CRISPR-based Diagnostics for Enhanced Clinical Translation and Field Deployment

Olivia Jane Arnold, SB

Thesis Topic: Therapeutic Applications of DNA Origami-based Progammable Nanoparticles

Rachel Bellisle, SB

Thesis Topic: A Wearable Countermeasure for Musculoskeletal Deconditioning in Human Spaceflight

Adam G. Berger, SB

Thesis Topic: Systematic Engineering of Controlled, Localized Oligonucleotide Delivery Systems for Wound Angiogenesis

Jennifer Dawkins, SB

Thesis Topic: Computational Prediction of Health Status from the Human Gut Microbiome and Metabolome

Brian Tshao Do, SB

Thesis Topic: Metabolic and Genetic Factors Guiding Hematopoietic Cell Fate

Mingjian He, SB

Thesis Topic: State-space Modeling of Neural Oscillations: Toward Assessing Alzheimer’s Disease Neuropathology with Sleep EEG

Brennan Leo Jackson, SB

Thesis Topic: The Impact of Gamma Stimulation on Neurological Phenotypes of Alzheimer's Dementia and Down Syndrome

Morgan Elizabeth Janes, SB

Thesis Topic: Engineering Translational Vaccine Delivery Systems with the Polyphenol Tannic Acid

Ashwin Srinivasan Kumar, BNG

Thesis Topic: Targeting B Cells to Improve Therapeutic Outcomes for Pediatric Medulloblastoma

Christian Landeros, SB

Thesis Topic: Machine-Guided Biopsy Analysis in Oncology: Facilitating Diagnostic Access and Biomedical Discovery Through Deep Learning

Ben D. Leaker, BNG

Thesis Topic: Biological and Biomechanical Effects of Direct Perturbation of Tissue Structure in the Cirrhotic Liver

Fiona Macleod, BNG

Thesis Topic: Investigating the Fidelity of Classic Cardiovascular Metrics in the Context of a Failing and Mechanically Supported Heart

Maria Carmen Martin Alonso, MNG

Thesis Topic: Amplifying Signals in the Tumor Microenvironment for Drug Development and Diagnostics

Eli Mattingly, SB

Thesis Topic: Design, Construction, and Validation of Magnetic Particle Imaging Systems for Rodent, Primate, and Human Functional Neuroimaging

Vincent Miao, BNG

Thesis Topic: Profiling Host Respiratory Responses to SARS-CoV-2 Infection

Allison Paige Porter, SB

Thesis Topic: Automation Framework for Exploration Medicine (AFEM): A Path for Integrating Automation into Autonomous Emergency Care

Rumya Raghavan, SB

Thesis Topic: Engineering Minimally Immunogenic Cargos and Delivery Modalities for Gene Therapy

Michelle Ramseier, SB

Thesis Topic: Cooptation of B Cell Developmental States in Malignancy and Autoimmunity

Luca Rosalia, MNG

Thesis Topic: Soft Robotic Platforms for the Simulation of Cardiovascular Disease and Device Development

Daphne Schlesinger, SB

Thesis Topic: Physiology-Inspired Deep Learning for Improved Heart Failure Management

Sydney Sherman, SB

Thesis Topic: Single-sided Magnetic Resonance Sensors for Clinical Detection of Volume Status

Nalini Singh, SB

Thesis Topic: Physics-Inspired Deep Learning for Inverse Problems in MRI

Anubhav Sinha, SB, MNG

Thesis Topic: Spatially Precise in situ Transcriptomics in Intact Biological Systems

Mingyu Yang, SB

Thesis Topic: Myelination Diseases of the Central Nervous System: Artificial Axons as in Vitro Models of Chemomechanical Cues

Master of Science

Health Sciences and Technology

Noah Stanley Warner, SB

Thesis Topic: A Framework for Detection and Observation of Radiation Chemistry Species on an MR-Linac

Certificate

Graduate Education in Medical Sciences

Akshay Kothakonda, BNG, SM

Thesis Topic: Engineering Mechanical Counter Pressure Spacesuits and Compression Garments: Active Pressurization and Design for Mobility

IMAGES

Transcription Factor Interplay
Caat Box, Transcriptional regulation, thesis Antithesis Synthesis
What are Transcription factors
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Transcription factor binding sites considered in this study. The
Unraveling Mechanisms of Transcription Factor-Mediated cDC1

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COMMENTS

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PDF Transcription factor binding motif analyses in two biological systems
scription factors. In this thesis, we focus on the binding of transcription factors to upstream region motifs to understand the mechanism of gene regulation. Sonic hedgehog (Shh) signals direct digit number and identity in the vertebrate limb via Gli transcription factors. We sought to identify key Gli binding motifs in
The SIX Family of Transcription Factors: Common Themes Integrating
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Hinojosa, Leetoria, Investigating the Localization of FOXO Transcription Factors in. Glioblastoma. Master of Sciences (MS), May, 2020, 32pp., 1 table, 7 figures, 17 references. The Phosphatidylinositol 3 Kinase (PI3K) pathway is an essential intracellular signaling. pathway that regulates cellular growth, survival, and fate.
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Transcription factor
Illustration of an activator. In molecular biology, a transcription factor (TF) (or sequence-specific DNA-binding factor) is a protein that controls the rate of transcription of genetic information from DNA to messenger RNA, by binding to a specific DNA sequence. The function of TFs is to regulate—turn on and off—genes in order to make sure that they are expressed in the desired cells at ...
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TRANSCRIPTION FACTOR BINDING SITES By LIANG ZHAO Bachelor of Science Zhejiang University Hangzhou, China 1992 . . Master of Engineering BetJmg Research Institute of Chemical Industry Beijing, China 1995 Submitted to the Faculty of the Graduate College of the Oklahoma State University in partial fulfillment of the requirements for the degree of
IJMS
Bri1-EMS Suppressor 1 (BES1) and Brassinazole Resistant 1 (BZR1) are two key transcription factors in the brassinosteroid (BR) signaling pathway, serving as crucial integrators that connect various signaling pathways in plants. Extensive genetic and biochemical studies have revealed that BES1 and BZR1, along with other protein factors, form a complex interaction network that governs plant ...
An integrative temperature-controlled microfluidic system for budding
Moreover, we investigated the nuclear entry and exit behaviors of the transcription factor Msn2 in yeast in response to heat stress (37°C) with different heating modes. The feasibility of this temperature-controlled platform for studying the protein dynamic behavior of yeast cells was demonstrated.
The 2024 HST graduation
Thesis Topic: Structure-Based Network Analysis Predicts Pathogenic Variants in Human Proteins Associated with Inherited Retinal Disease. Sofia Hu, BA, PhD. Thesis Topic: Transcription Factor Antagonism Regulates Heterogeneity in Embryonic Stem Cell States. Nauman Javed, BS, PhD

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The AP2/ERF transcription factor SmERF1L1 regulates the biosynthesis of tanshinones and phenolic acids in Salvia miltiorrhiza

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Characterization of YABBY transcription factors in Osmanthus fragrans and functional analysis of OfYABBY12 in floral scent formation and leaf morphology

Introduction

Materials and methods

Identification of O. fragrans YABBY transcription factors and protein physicochemical analysis

Gene structure, conserved motif, and cis-acting element analysis

Phylogenetic, chromosome localization, and gene duplication analysis

RNA extraction and quantitative reverse-transcription polymerase chain reaction (qRT-PCR) analyses

Subcellular localization and transactivation assay

Transformation of OfYABBY12 in N. tabacum

GC–MS volatile analysis

Scanning electron microscopy

RNA-Seq analysis

Dual-luciferase transient expression assay

Statistical analysis

Identification and classification of YABBY gene family members in O. fragrans

Phylogenetic analysis and gene duplication

Expression patterns of OfYABBYs

Subcellular localization and transcriptional activation activity of OfYABBYs

Phenotypes of transgenic N. tabacum overexpressing OfYABBY12

Detection of VOCs in transgenic N. tabacum overexpressing OfYABBY12

Overview of the YABBY gene family in O. fragrans

OfYABBY12 plays a negative role in VOC synthesis

OfYABBY12 is involved in the development of leaves and flowers

Data availability

Acknowledgements

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Additional information

Electronic supplementary material

Supplementary Material 1

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BMC Plant Biology

Transcription factors in megakaryocytes and platelets

Jianning Zhang

Zilong Zhao

1. Introduction

Table 1

2. Transcription factors in platelet production

2.2. GATA-binding protein 1

3. Non-transcriptional activity in platelets

3.2. Nuclear factor kappa β

3.3. Peroxisome proliferator-activated receptors

4. Transcription factors in extracellular vesicles released from platelets

5. Conclusion

Author contributions

Funding Statement

Conflict of interest

Publisher’s note

Single-Cell Chromatin Accessibility Analysis Reveals the Epigenetic Basis and Signature Transcription Factors for the Molecular Subtypes of Colorectal Cancers

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Transcription factor CaHDZ15 promotes pepper basal thermotolerance by activating HEAT SHOCK FACTORA6a

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