Flowering

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    TaZIM-A1 negatively regulates flowering time in common wheat (Triticum aestivum L.)
    Hong Liu, Tian Li, Yamei Wang, Jun Zheng, Huifang Li, Chenyang Hao and Xueyong Zhang
    J Integr Plant Biol 2019, 61 (3): 359-376.  
    doi: 10.1111/jipb.12720
    Abstract (Browse 245)  |   Save
    Flowering time is a critical determinant of regional adaptation for crops and has strong effects on crop yields. Here, we report that TaZIM-A1, an atypical GATA-like transcription factor, is a negative regulator of flowering in wheat. TaZIM-A1 possessed weak transcriptional repression activity, with its CCT domain functioning as the major inhibitory region. TaZIM-A1 expression exhibited a typical circadian oscillation pattern under various light regimes. Overexpression of TaZIM-A1 caused a delay in flowering time and a decrease in thousand-kernel weight (TKW) in wheat under long-day conditions. Moreover, TaZIM-A1 directly bound to the promoters of TaCO-1 and TaFT-1 and downregulated their expression. Sequence analysis of a collection of common wheat cultivars identified three and two haplotypes for TaZIM-A1 and TaZIM-B1, respectively. Association analysis revealed that TaZIM-A1-HapI/-HapIII and TaZIM-B1-HapI have undergone strong positive selection during modern wheat breeding, likely due to their association with earlier heading and higher TKW. Diagnostic markers were developed for these haplotypes that can be used for wheat cultivar improvement, via marker-assisted breeding.
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    Control of flowering in rice through synthetic microProteins
    Tenai Eguen, Jorge Gomez Ariza, Vittoria Brambilla, Bin Sun, Kaushal Kumar Bhati, Fabio Fornara and Stephan Wenkel
    J Integr Plant Biol 2020, 62 (6): 730-736.  
    doi: 10.1111/jipb.12865
    Abstract (Browse 422)  |   Save

    Photoperiod‐dependent flowering in rice is regulated by HEADING DATE 1 (Hd1), which acts as both an activator and repressor of flowering in a daylength‐dependent manner. To investigate the use of microProteins as a tool to modify rice sensitivity to the photoperiod, we designed a synthetic Hd1 microProtein (Hd1miP) capable of interacting with Hd1 protein, and overexpressed it in rice. Transgenic OX‐Hd1miP plants flowered significantly earlier than wild type plants when grown in non‐inductive long day conditions. Our results show the potential of microProteins to serve as powerful tools for modulating crop traits and unraveling protein function.

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    Flowering phenology as a core domestication trait in soybean
    Zhizhong Gong
    J Integr Plant Biol 2020, 62 (5): 546-549.  
    doi: 10.1111/jipb.12934
    Abstract (Browse 307)  |   Save

    Flowering time variation in soybean is well characterized within domesticated germplasms and is critical for modern production, but its importance during domestication is unclear. Recently, Lu et al. (Nature Genetics, 2020) reported that two homeologous pseudo‐response‐regulator genes, Tof12 and Tof11, were sequentially selected in early soybean evolution for ancient flowering time adaptation and intensification of crop cultivation.

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    WRKY transcription factors WRKY12 and WRKY13 interact with SPL10 to modulate age-mediated flowering
    Zhenbing Ma, Wei Li, Houping Wang and Diqiu Yu
    J Integr Plant Biol 2020, 62 (11): 1659-1673.  
    DOI: 10.1111/jipb.12946
    Abstract (Browse 379)  |   Save

    WRKY12 and WRKY13 are two WRKY transcription factors that play important roles in the control of flowering time under short‐day (SD) conditions. The temporally regulated expression of WRKY12 and WRKY13 indicates that they may be involved in the age‐mediated flowering pathway. However, their roles in this pathway are poorly understood. Here, we show that the transcription of WRKY12 and WRKY13 is directly regulated by SQUAMOSA PROMOTER BINDING–LIKE 10 (SPL10), a transcription factor downstream of the age pathway. Binding and activation analyses revealed that SPL10 functions as a positive regulator of WRKY12 and a negative regulator of WRKY13. Further mechanistic investigation revealed that WRKY12 and WRKY13 physically interact with SPL10 and that both of them bind to the promoter of miR172b. Thus, the WRKY12‐SPL10 and WRKY13‐SPL10 interactions facilitate and inhibit SPL10 transcriptional function, respectively, to regulate miR172b expression. Together, our results show that WRKY12 and WRKY13 participate in the control of age‐mediated flowering under SD conditions though physically interacting with SPLs and co‐regulating the target gene miR172b.

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    Soybean AP1 homologs control flowering time and plant height
    Liyu Chen, Haiyang Nan, Lingping Kong, Lin Yue, Hui Yang, Qingsong Zhao, Chao Fang, Haiyang Li, Qun Cheng, Sijia Lu, Fanjiang Kong, Baohui Liu and Lidong Dong
    J Integr Plant Biol 2020, 62 (12): 1868-1879.  
    DOI: 10.1111/jipb.12988
    Abstract (Browse 357)  |   Save

    Flowering time and plant height are key agronomic traits that directly affect soybean (Glycine max) yield. APETALA1 (AP1) functions as a class A gene in the ABCE model for floral organ development, helping to specify carpel, stamen, petal, and sepal identities. There are four AP1 homologs in soybean, all of which are mainly expressed in the shoot apex. Here, we used clustered regularly interspaced short palindromic repeats (CRISPR) – CRISPR‐associated protein 9 technology to generate a homozygous quadruple mutant, gmap1, with loss‐of‐function mutations in all four GmAP1 genes. Under short‐day (SD) conditions, the gmap1 quadruple mutant exhibited delayed flowering, changes in flower morphology, and increased node number and internode length, resulting in plants that were taller than the wild type. Conversely, overexpression of GmAP1a resulted in early flowering and reduced plant height compared to the wild type under SD conditions. The gmap1 mutant and the overexpression lines also exhibited altered expression of several genes related to flowering and gibberellic acid metabolism, thereby providing insight into the role of GmAP1 in the regulatory networks controlling flowering time and plant height in soybean. Increased node number is the trait with the most promise for enhancing soybean pod number and grain yield. Therefore, the mutant alleles of the four AP1 homologs described here will be invaluable for molecular breeding of improved soybean yield.

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    Global analysis of CCT family knockout mutants identifies four genes involved in regulating heading date in rice
    Jia Zhang, Xiaowei Fan, Yong Hu, Xiangchun Zhou, Qin He, Liwen Liang and Yongzhong Xing
    J Integr Plant Biol 2021, 63 (5): 913-923.  
    DOI: 10.1111/jipb.13013
    Abstract (Browse 413)  |   Save
    Many genes encoding CCT domain‐containing proteins regulate flowering time. In rice (Oryza sativa), 41 such genes have been identified, but only a few have been shown to regulate heading date. Here, to test whether and how additional CCT family genes regulate heading date in rice, we classified these genes into five groups based on their diurnal expression patterns. The expression patterns of genes in the same subfamily or in close phylogenetic clades tended to be similar. We generated knockout mutants of the entire gene family via CRISPR/Cas9. The heading dates of knockout mutants of only 4 of 14 genes previously shown to regulate heading date were altered, pointing to functional redundancy of CCT family genes in regulating this trait. Analysis of mutants of four other genes showed that OsCCT22, OsCCT38, and OsCCT41 suppress heading under long‐day conditions and promote heading under short‐day conditions. OsCCT03 promotes heading under both conditions and upregulates the expression of Hd1 and Ehd1, a phenomenon not previously reported for other such genes. To date, at least 18 CCT domain‐containing genes involved in regulating heading have been identified, providing diverse, flexible gene combinations for generating rice varieties with a given heading date.
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    Molecular mechanisms for the photoperiodic regulation of flowering in soybean
    Xiaoya Lin, Baohui Liu, James L. Weller, Jun Abe and Fanjiang Kong
    J Integr Plant Biol 2021, 63 (6): 981-994.  
    doi: 10.1111/jipb.13021
    Abstract (Browse 460)  |   Save
    Photoperiodic flowering is one of the most important factors affecting regional adaptation and yield in soybean (Glycine max). Plant adaptation to long-day conditions at higher latitudes requires early flowering and a reduction or loss of photoperiod sensitivity; adaptation to short-day conditions at lower latitudes involves delayed flowering, which prolongs vegetative growth for maximum yield potential. Due to the influence of numerous major loci and quantitative trait loci (QTLs), soybean has broad adaptability across latitudes. Forward genetic approaches have uncovered the molecular basis for several of these major maturity genes and QTLs. Moreover, the molecular characterization of orthologs of Arabidopsis thaliana flowering genes has enriched our understanding of the photoperiodic flowering pathway in soybean. Building on early insights into the importance of the photoreceptor phytochrome A, several circadian clock components have been integrated into the genetic network controlling flowering in soybean: E1, a repressor of FLOWERING LOCUS T orthologs, plays a central role in this network. Here, we provide an overview of recent progress in elucidating photoperiodic flowering in soybean, how it contributes to our fundamental understanding of flowering time control, and how this information could be used for molecular design and breeding of high-yielding soybean cultivars.
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    A recent retrotransposon insertion of J caused E6 locus facilitating soybean adaptation into low latitude
    Chao Fang, Jun Liu, Ting Zhang, Tong Su, Shichen Li, Qun Cheng, Lingping Kong, Xiaoming Li, Tiantian Bu, Haiyang Li, Lidong Dong, Sijia Lu, Fanjiang Kong and Baohui Liu
    J Integr Plant Biol 2021, 63 (6): 995-1003.  
    doi: 10.1111/jipb.13034
    Abstract (Browse 364)  |   Save
    Soybean (Glycine max) is an important legume crop that was domesticated in temperate regions. Soybean varieties from these regions generally mature early and exhibit extremely low yield when grown under inductive short-day (SD) conditions at low latitudes. The long-juvenile (LJ) trait, which is characterized by delayed flowering and maturity, and improved yield under SD conditions, allowed the cultivation of soybean to expand to lower latitudes. Two major loci control the LJ trait: J and E6. In the current study, positional cloning, sequence analysis, and transgenic complementation confirmed that E6 is a novel allele of J, the ortholog of Arabidopsis thaliana EARLY FLOWERING 3 (ELF3). The mutant allele e6PG, which carries a Ty1/Copia-like retrotransposon insertion, does not suppress the legume-specific flowering repressor E1, allowing E1 to inhibit Flowering Locus T (FT) expression and thus delaying flowering and increasing yields under SD conditions. The e6PG allele is a rare allele that has not been incorporated into modern breeding programs. The dysfunction of J might have greatly facilitated the adaptation of soybean to low latitudes. Our findings increase our understanding of the molecular mechanisms underlying the LJ trait and provide valuable resources for soybean breeding.
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    The CBP/p300 histone acetyltransferases function as plant‐specific MEDIATOR subunits in Arabidopsis
    Jing Guo, Long Wei, Shan‐Shan Chen, Xue‐Wei Cai, Yin‐Na Su, Lin Li, She Chen and Xin‐Jian He
    J Integr Plant Biol 2021, 63 (4): 755-771.  
    DOI: 10.1111/jipb.13052
    Abstract (Browse 285)  |   Save
    In eukaryotes, MEDIATOR is a conserved multi‐subunit complex that links transcription factors and RNA polymerase II and that thereby facilitates transcriptional initiation. Although the composition of MEDIATOR has been well studied in yeast and mammals, relatively little is known about the composition of MEDIATOR in plants. By affinity purification followed by mass spectrometry, we identified 28 conserved MEDIATOR subunits in Arabidopsis thaliana, including putative MEDIATOR subunits that were not previously validated. Our results indicated that MED34, MED35, MED36, and MED37 are not Arabidopsis MEDIATOR subunits, as previously proposed. Our results also revealed that two homologous CBP/p300 histone acetyltransferases, HAC1 and HAC5 (HAC1/5) are in fact plant‐specific MEDIATOR subunits. The MEDIATOR subunits MED8 and MED25 (MED8/25) are partially responsible for the association of MEDIATOR with HAC1/5, MED8/25 and HAC1/5 co‐regulate gene expression and thereby affect flowering time and floral development. Our in vitro observations indicated that MED8 and HAC1 form liquid‐like droplets by phase separation, and our in vivo observations indicated that these droplets co‐localize in the nuclear bodies at a subset of nuclei. The formation of liquid‐like droplets is required for MED8 to interact with RNA polymerase II. In summary, we have identified all of the components of Arabidopsis MEDIATOR and revealed the mechanism underlying the link of histone acetylation and transcriptional regulation.
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    A histone H3K27me3 reader cooperates with a family of PHD finger‐containing proteins to regulate flowering time in Arabidopsis
    Feng Qian, Qiu‐Yuan Zhao, Tie‐Nan Zhang, Yu‐Lu Li, Yin‐Na Su, Lin Li, Jian‐Hua Sui, She Chen and Xin‐Jian He
    J Integr Plant Biol 2021, 63 (4): 787-802.  
    DOI: 10.1111/jipb.13067
    Abstract (Browse 533)  |   Save
    Trimethylated histone H3 lysine 27 (H3K27me3) is a repressive histone marker that regulates a variety of developmental processes, including those that determine flowering time. However, relatively little is known about the mechanism of how H3K27me3 is recognized to regulate transcription. Here, we identified BAH domain‐containing transcriptional regulator 1 (BDT1) as an H3K27me3 reader. BDT1 is responsible for preventing flowering by suppressing the expression of flowering genes. Mutation of the H3K27me3 recognition sites in the BAH domain disrupted the binding of BDT1 to H3K27me3, leading to de‐repression of H3K27me3‐enriched flowering genes and an early‐flowering phenotype. We also found that BDT1 interacts with a family of PHD finger‐containing proteins, which we named PHD1–6, and with CPL2, a Pol II carboxyl terminal domain (CTD) phosphatase responsible for transcriptional repression. Pull‐down assays showed that the PHD finger‐containing proteins can enhance the binding of BDT1 to the H3K27me3 peptide. Mutations in all of the PHD genes caused increased expression of flowering genes and an early‐flowering phenotype. This study suggests that the binding of BDT1 to the H3K27me3 peptide, which is enhanced by PHD proteins, is critical for preventing early flowering.
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    FT5a interferes with the Dt1-AP1 feedback loop to control flowering time and shoot determinacy in soybean
    Lin Yue, Xiaoming Li, Chao Fang, Liyu Chen, Hui Yang, Jie Yang, Zhonghui Chen, Haiyang Nan, Linnan Chen, Yuhang Zhang, Haiyang Li, Xingliang Hou, Zhicheng Dong, James L. Weller, Jun Abe, Baohui Liu and Fanjiang Kong
    J Integr Plant Biol 2021, 63 (6): 1004-1020.  
    doi: 10.1111/jipb.13070
    Abstract (Browse 525)  |   Save
    Flowering time and stem growth habit determine inflorescence architecture in soybean, which in turn influences seed yield. Dt1, a homolog of Arabidopsis TERMINAL FLOWER 1 (TFL1), is a major controller of stem growth habit, but its underlying molecular mechanisms remain unclear. Here, we demonstrate that Dt1 affects node number and plant height, as well as flowering time, in soybean under long-day conditions. The bZIP transcription factor FDc1 physically interacts with Dt1, and the FDc1-Dt1 complex directly represses the expression of APETALA1 (AP1). We propose that FT5a inhibits Dt1 activity via a competitive interaction with FDc1 and directly upregulates AP1. Moreover, AP1 represses Dt1 expression by directly binding to the Dt1 promoter, suggesting that AP1 and Dt1 form a suppressive regulatory feedback loop to determine the fate of the shoot apical meristem. These findings provide novel insights into the roles of Dt1 and FT5a in controlling the stem growth habit and flowering time in soybean, which determine the adaptability and grain yield of this important crop.
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    MYB106 is a negative regulator and a substrate for CRL3BPM E3 ligase in regulating flowering time in Arabidopsis thaliana
    Liu Hong, Fangfang Niu, Youshun Lin, Shuang Wang, Liyuan Chen and Liwen Jiang
    J Integr Plant Biol 2021, 63 (6): 1104-1119.  
    DOI: 10.1111/jipb.13071
    Abstract (Browse 475)  |   Save
    Flowering time is crucial for successful reproduction in plants, the onset and progression of which are strictly controlled. However, flowering time is a complex and environmentally responsive history trait and the underlying mechanisms still need to be fully characterized. Post-translational regulation of the activities of transcription factors (TFs) is a dynamic and essential mechanism for plant growth and development. CRL3BPM E3 ligase is a CULLIN3-based E3 ligase involved in orchestrating protein stability via the ubiquitin proteasome pathway. Our study shows that the mutation of MYB106 induced early flowering phenotype while over-expression of MYB106 delayed Arabidopsis flowering. Transcriptome analysis of myb106 mutants reveals 257 differentially expressed genes between wild type and myb106-1 mutants, including Flowering Locus T (FT) which is related to flowering time. Moreover, in vitro electrophoretic mobility shift assays (EMSA), in vivo chromatin immunoprecipitation quantitative polymerase chain reaction (ChIP-qPCR) assays and dual luciferase assays demonstrate that MYB106 directly binds to the promoter of FT to suppress its expression. Furthermore, we confirm that MYB106 interacts with BPM proteins which are further identified by CRL3BPM E3 ligases as the substrate. Taken together, we have identified MYB106 as a negative regulator in the control of flowering time and a new substrate for CRL3BPM E3 ligases in Arabidopsis.
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    A domesticated Harbinger transposase forms a complex with HDA6 and promotes histone H3 deacetylation at genes but not TEs in Arabidopsis
    Xishi Zhou, Junna He, Christos N. Velanis, Yiwang Zhu, Yuhan He, Kai Tang, Mingku Zhu, Lisa Graser, Erica deLeau, Xingang Wang, Lingrui Zhang, W. Andy Tao, Justin Goodrich, Jian‐Kang Zhu and Cui‐Jun Zhang
    J Integr Plant Biol 2021, 63 (8): 1462-1474.  
    doi: 10.1111/jipb.13108
    Abstract (Browse 263)  |   Save
    In eukaryotes, histone acetylation is a major modification on histone N-terminal tails that is tightly connected to transcriptional activation. HDA6 is a histone deacetylase involved in the transcriptional regulation of genes and transposable elements (TEs) in Arabidopsis thaliana. HDA6 has been shown to participate in several complexes in plants, including a conserved SIN3 complex. Here, we uncover a novel protein complex containing HDA6, several Harbinger transposon-derived proteins (HHP1, SANT1, SANT2, SANT3, and SANT4), and MBD domain-containing proteins (MBD1, MBD2, and MBD4). We show that mutations of all four SANT genes in the sant-null mutant cause increased expression of the flowering repressors FLC, MAF4, and MAF5, resulting in a late flowering phenotype. Transcriptome deep sequencing reveals that while the SANT proteins and HDA6 regulate the expression of largely overlapping sets of genes, TE silencing is unaffected in sant-null mutants. Our global histone H3 acetylation profiling shows that SANT proteins and HDA6 modulate gene expression through deacetylation. Collectively, our findings suggest that Harbinger transposon-derived SANT domain-containing proteins are required for histone deacetylation and flowering time control in plants.
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    ERF1 delays flowering through direct inhibition of FLOWERING LOCUS T expression in Arabidopsis
    Yanli Chen, Liping Zhang, Haiyan Zhang, Ligang Chen and Diqiu Yu
    J Integr Plant Biol 2021, 63 (10): 1712-1723.  
    DOI: 10.1111/jipb.13144
    Abstract (Browse 416)  |   Save
    ETHYLENE RESPONSE FACTOR1 (ERF1) is a key component in ethylene signaling, playing crucial roles in both biotic and abiotic stress responses. Here, we demonstrate that ERF1 also has an important role during floral initiation in Arabidopsis thaliana. Knockdown or knockout of ERF1 accelerated floral initiation, whereas overexpression of ERF1 dramatically delayed floral transition. These contrasting phenotypes were correlated with opposite transcript levels of FLOWERING LOCUS T (FT). Chromatin immunoprecipitation (ChIP) assays revealed that ERF1 associates with genomic regions of the FT gene to repress its transcription. ft-10/ERF1RNAi plants showed a similar flowering phenotype to the ft-10 mutant, whereas the flowering of FTox/ERF1ox mimicked that of FTox plants, suggesting that ERF1 acts upstream of FT during floral initiation. Similarly, altered floral transition in ethylene-related mutants was also correlated with FT expression. Further analysis suggested that ERF1 also participates in delay in flowering-time control mediated by the ethylene precursor 1-aminocyclopropane-1-carboxylic acid. Thus, ERF1 may act as a negative modulator of flowering-time control by repressing FT transcription in Arabidopsis.
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