Epigenetics

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    Epigenetic regulation of N-hydroxypipecolic acid biosynthesis by the AIPP3-PHD2-CPL2 complex
    Jiameng Lan, Siyu Chen, Joana Pico, Kevin Ao, Shitou Xia, Shucai Wang, Xin Li, Simone D. Castellarin and Yuelin Zhang
    J Integr Plant Biol 2023, 65 (12): 2660-2671.  
    DOI: 10.1111/jipb.13577
    Abstract (Browse 148)  |   Save
    N-Hydroxypipecolic acid (NHP) is a signaling molecule crucial for systemic acquired resistance (SAR), a systemic immune response in plants that provides long-lasting and broad-spectrum protection against secondary pathogen infections. To identify negative regulators of NHP biosynthesis, we performed a forward genetic screen to search for mutants with elevated expression of the NHP biosynthesis gene FLAVIN-DEPENDENT MONOOXYGENASE 1 (FMO1). Analysis of two constitutive expression of FMO1 (cef) and one induced expression of FMO1 (ief) mutants revealed that the AIPP3-PHD2-CPL2 protein complex, which is involved in the recognition of the histone modification H3K27me3 and transcriptional repression, contributes to the negative regulation of FMO1 expression and NHP biosynthesis. Our study suggests that epigenetic regulation plays a crucial role in controlling FMO1 expression and NHP levels in plants.
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    Conserved H3K27me3-associated chromatin looping mediates physical interactions of gene clusters in plants
    Linhua Sun, Yuxin Cao, Zhu Li, Yi Liu, Xiaochang Yin, Xing Wang Deng, Hang He and Weiqiang Qian
    J Integr Plant Biol 2023, 65 (8): 1966-1982.  
    DOI: 10.1111/jipb.13502
    Abstract (Browse 215)  |   Save
    Higher-order chromatin organization is essential for transcriptional regulation, genome stability maintenance, and other genome functions. Increasing evidence has revealed significant differences in 3D chromatin organization between plants and animals. However, the extent, pattern, and rules of chromatin organization in plants are still unclear. In this study, we systematically identified and characterized long-range chromatin loops in the Arabidopsis 3D genome. We identified hundreds of long-range cis chromatin loops and found their anchor regions are closely associated with H3K27me3 epigenetic modifications. Furthermore, we demonstrated that these chromatin loops are dependent on Polycomb group (PcG) proteins, suggesting that the Polycomb repressive complex 2 (PRC2) complex is essential for establishing and maintaining these novel loops. Although most of these PcG-medicated chromatin loops are stable, many of these loops are tissue-specific or dynamically regulated by different treatments. Interestingly, tandemly arrayed gene clusters and metabolic gene clusters are enriched in anchor regions. Long-range H3K27me3-marked chromatin interactions are associated with the coregulation of specific gene clusters. Finally, we also identified H3K27me3-associated chromatin loops associated with gene clusters in Oryza sativa and Glycine max, indicating that these long-range chromatin loops are conserved in plants. Our results provide novel insights into genome evolution and transcriptional coregulation in plants.
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    Conserved noncoding sequences correlate with distant gene contacts in Arabidopsis and Brassica
    Lei Zhang, Jian Wu, Jianli Liang, Runmao Lin, Chao Sun, Qirui Dai, Lupeng Zhang, Huiling Guo, Ranze Zhao and Xiaowu Wang
    J Integr Plant Biol 2023, 65 (6): 1467-1478.  
    doi: 10.1111/jipb.13465
    Abstract (Browse 235)  |   Save
    Physical contact between genes distant on chromosomes is a potentially important way for genes to coordinate their expressions. To investigate the potential importance of distant contacts, we performed high-throughput chromatin conformation capture (Hi-C) experiments on leaf nuclei isolated from Brassica rapa and Brassica oleracea. We then combined our results with published Hi-C data from Arabidopsis thaliana. We found that distant genes come into physical contact and do so preferentially between the proximal promoter of one gene and the downstream region of another gene. Genes with higher numbers of conserved noncoding sequences (CNSs) nearby were more likely to have contact with distant genes. With more CNSs came higher numbers of transcription factor binding sites and more histone modifications associated with the activity. In addition, for the genes we studied, distant contacting genes with CNSs were more likely to be transcriptionally coordinated. These observations suggest that CNSs may enrich active histone modifications and recruit transcription factors, correlating with distant contacts to ensure coordinated expression. This study advances our knowledge of gene contacts and provides insights into the relationship between CNSs and distant gene contacts in plants.
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    Histone deacetylase OsHDA706 increases salt tolerance via H4K5/K8 deacetylation of OsPP2C49 in rice
    Kai Liu, Jijin Chen, Shang Sun, Xu Chen, Xinru Zhao, Yingying Hu, Guoxiao Qi, Xiya Li, Bo Xu, Jun Miao, Chao Xue, Yong Zhou and Zhiyun Gong
    J Integr Plant Biol 2023, 65 (6): 1394-1407.  
    DOI: 10.1111/jipb.13470
    Abstract (Browse 345)  |   Save
    High salt is a major environmental factor that threatens plant growth and development. Increasing evidence indicates that histone acetylation is involved in plant responses to various abiotic stress; however, the underlying epigenetic regulatory mechanisms remain poorly understood. In this study, we revealed that the histone deacetylase OsHDA706 epigenetically regulates the expression of salt stress response genes in rice (Oryza sativa L.). OsHDA706 localizes to the nucleus and cytoplasm and OsHDA706 expression is significantly induced under salt stress. Moreover, oshda706 mutants showed a higher sensitivity to salt stress than the wild-type. In vivo and in vitro enzymatic activity assays demonstrated that OsHDA706 specifically regulates the deacetylation of lysines 5 and 8 on histone H4 (H4K5 and H4K8). By combining chromatin immunoprecipitation and mRNA sequencing, we identified the clade A protein phosphatase 2 C gene, OsPP2C49, which is involved in the salt response as a direct target of H4K5 and H4K8 acetylation. We found that the expression of OsPP2C49 is induced in the oshda706 mutant under salt stress. Furthermore, the knockout of OsPP2C49 enhances plant tolerance to salt stress, while its overexpression has the opposite effect. Taken together, our results indicate that OsHDA706, a histone H4 deacetylase, participates in the salt stress response by regulating the expression of OsPP2C49 via H4K5 and H4K8 deacetylation.
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    Bracelet salt glands of the recretohalophyte Limonium bicolor: Distribution, morphology, and induction
    Boqing Zhao, Yingli Zhou, Xiangmei Jiao, Xi Wang, Baoshan Wang and Fang Yuan
    J Integr Plant Biol 2023, 65 (4): 950-966.  
    doi: 10.1111/jipb.13417
    Abstract (Browse 177)  |   Save
    Halophytes complete their life cycles in saline environments. The recretohalophyte Limonium bicolor has evolved a specialized salt secretory structure, the salt gland, which excretes Na+ to avoid salt damage. Typical L. bicolor salt glands consist of 16 cells with four fluorescent foci and four secretory pores. Here, we describe a special type of salt gland at the base of the L. bicolor leaf petiole named bracelet salt glands due to their beaded‐bracelet‐ like shape of blue auto‐fluorescence. Bracelet salt glands contain more than 16 cells and more than four secretory pores. Leaf disc secretion measurements and non‐invasive micro‐test techniques indicated that bracelet salt glands secrete more salt than normal salt glands, which helps maintain low Na+ levels at the leaf blade to protect the leaf. Cytokinin treatment induced bracelet salt gland differentiation, and the developed ones showed no further differentiation when traced with a living fluorescence microscopy imager, even though new salt gland development and leaf expansion were observed. Transcriptome revealed a NAC transcription factor gene that participates in bracelet salt gland development, as confirmed by its genome editing and overexpression in L. bicolor. These findings shed light on bracelet salt gland development and may facilitate the engineering of salt‐tolerant crops.
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    Interplay of phytohormones and epigenetic regulation: A recipe for plant development and plasticity
    Kai Jiang, Hongwei Guo and Jixian Zhai
    J Integr Plant Biol 2023, 65 (2): 381-398.  
    doi: 10.1111/jipb.13384
    Abstract (Browse 228)  |   Save
    Both phytohormone signaling and epigenetic mechanisms have long been known to play crucial roles in plant development and plasticity in response to ambient stimuli. Indeed, diverse signaling pathways mediated by phytohormones and epigenetic processes integrate multiple upstream signals to regulate various plant traits. Emerging evidence indicates that phytohormones and epigenetic processes interact at multiple levels. In this review, we summarize the current knowledge of the interplay between phytohormones and epigenetic processes from the perspective of phytohormone biology. We also review chemical regulators used in epigenetic studies and propose strategies for developing novel regulators using multidisciplinary approaches.
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    AtMCM10 promotes DNA replication-coupled nucleosome assembly in Arabidopsis
    Xinjie Zhao, Jingyi Wang, Dan Jin, Jinkui Cheng, Hui Chen, Zhen Li, Yu Wang, Huiqiang Lou, Jian-Kang Zhu, Xuan Du, Zhizhong Gong
    J Integr Plant Biol 2023, 65 (1): 203-222.  
    DOI: 10.1111/jipb.13438
    Abstract (Browse 175)  |   Save
    Minichromosome Maintenance protein 10 (MCM10) is essential for DNA replication initiation and DNA elongation in yeasts and animals. Although the functions of MCM10 in DNA replication and repair have been well documented, the detailed mechanisms for MCM10 in these processes are not well known. Here, we identified AtMCM10 gene through a forward genetic screening for releasing a silenced marker gene. Although plant MCM10 possesses a similar crystal structure as animal MCM10, AtMCM10 is not essential for plant growth or development in Arabidopsis. AtMCM10 can directly bind to histone H3-H4 and promotes nucleosome assembly in vitro. The nucleosome density is decreased in Atmcm10, and most of the nucleosome density decreased regions in Atmcm10 are also regulated by newly synthesized histone chaperone Chromatin Assembly Factor-1 (CAF-1). Loss of both AtMCM10 and CAF-1 is embryo lethal, indicating that AtMCM10 and CAF-1 are indispensable for replication-coupled nucleosome assembly. AtMCM10 interacts with both new and parental histones. Atmcm10 mutants have lower H3.1 abundance and reduced H3K27me1/3 levels with releasing some silenced transposons. We propose that AtMCM10 deposits new and parental histones during nucleosome assembly, maintaining proper epigenetic modifications and genome stability during DNA replication.
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    Structural basis for histone H3 recognition by NASP in Arabidopsis
    Yanhong Liu, Liu Chen, Na Wang, Baixing Wu, Hongyu Bao and Hongda Huang
    J Integr Plant Biol 2022, 64 (12): 2309-2313.  
    doi: 10.1111/jipb.13277
    Abstract (Browse 216)  |   Save

    The structural basis for histone recognition by the histone chaperone nuclear autoantigenic sperm protein (NASP) remains largely unclear. Here, we showed that Arabidopsis thaliana AtNASP is a monomer and displays robust nucleosome assembly activity in vitro. Examining the structure of AtNASP complexed with a histone H3 α3 peptide revealed a binding mode that is conserved in human NASP. AtNASP recognizes the H3 N-terminal region distinct from human NASP. Moreover, AtNASP forms a co-chaperone complex with ANTI-SILENCING FUNCTION 1 (ASF1) by binding to the H3 N-terminal region. Therefore, we deciphered the structure of AtNASP and the basis of the AtNASP–H3 interaction.

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    The H3K9me2-binding protein AGDP3 limits DNA methylation and transcriptional gene silencing in Arabidopsis
    Xuelin Zhou, Mengwei Wei, Wenfeng Nie, Yue Xi, Li Peng, Qijie Zheng, Kai Tang, Viswanathan Satheesh, Yuhua Wang, Jinyan Luo, Xuan Du, Rui Liu, Zhenlin Yang, Honggui La, Yingli Zhong, Yu Yang, Jian‐Kang Zhu, Jiamu Du and Mingguang Lei
    J Integr Plant Biol 2022, 64 (12): 2385-2395.  
    doi: 10.1111/jipb.13369
    Abstract (Browse 259)  |   Save

    DNA methylation, a conserved epigenetic mark, is critical for tuning temporal and spatial gene expression. The Arabidopsis thaliana DNA glycosylase/lyase REPRESSOR OF SILENCING 1 (ROS1) initiates active DNA demethylation and is required to prevent DNA hypermethylation at thousands of genomic loci. However, how ROS1 is recruited to specific loci is not well understood. Here, we report the discovery of Arabidopsis AGENET Domain Containing Protein 3 (AGDP3) as a cellular factor that is required to prevent gene silencing and DNA hypermethylation. AGDP3 binds to H3K9me2 marks in its target DNA via its AGD12 cassette. Analysis of the crystal structure of the AGD12 cassette of AGDP3 in complex with an H3K9me2 peptide revealed that dimethylated H3K9 and unmodified H3K4 are specifically anchored into two different surface pockets. A histidine residue located in the methyllysine binding aromatic cage provides AGDP3 with pH-dependent H3K9me2 binding capacity. Our results uncover a molecular mechanism for the regulation of DNA demethylation by the gene silencing mark H3K9me2.

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    Chromatin architectural alterations due to null mutation of a major CG methylase in rice
    Jinbin Wang, Xiaochong Li, Qianli Dong, Changping Li, Juzuo Li, Ning Li, Baoxu Ding, Xiaofei Wang, Yanan Yu, Tianya Wang, Zhibin Zhang, Yiyang Yu, Man Lang, Zixian Zeng, Bao Liu and Lei Gong
    J Integr Plant Biol 2022, 64 (12): 2396-2410.  
    doi: 10.1111/jipb.13378
    Abstract (Browse 214)  |   Save

    Associations between 3D chromatin architectures and epigenetic modifications have been characterized in animals. However, any impact of DNA methylation on chromatin architecture in plants is understudied, which is confined to Arabidopsis thaliana. Because plant species differ in genome size, composition, and overall chromatin packing, it is unclear to what extent findings from A. thaliana hold in other species. Moreover, the incomplete chromatin architectural profiles and the low-resolution high-throughput chromosome conformation capture (Hi-C) data from A. thaliana have hampered characterizing its subtle chromatin structures and their associations with DNA methylation. We constructed a high-resolution Hi-C interaction map for the null OsMET1-2 (the major CG methyltransferase in rice) mutant (osmet1-2) and isogenic wild-type rice (WT). Chromatin structural changes occurred in osmet1-2, including intra-/inter-chromosomal interactions, compartment transition, and topologically associated domains (TAD) variations. Our findings provide novel insights into the potential function of DNA methylation in TAD formation in rice and confirmed DNA methylation plays similar essential roles in chromatin packing in A. thaliana and rice.

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    DEMETHYLATION REGULATOR 1 regulates DNA demethylation of the nuclear and mitochondrial genomes
    Zhen Wang, Hao Zheng, Jinguang Huang, Guodong Yang, Kang Yan, Shizhong Zhang, Changai Wu, Chengchao Zheng
    J Integr Plant Biol 2022, 64 (12): 2344-2360.  
    doi: 10.1111/jipb.13386
    Abstract (Browse 248)  |   Save

    Active DNA demethylation effectively modulates gene expression during plant development and in response to stress. However, little is known about the upstream regulatory factors that regulate DNA demethylation. We determined that the demethylation regulator 1 (demr1) mutant exhibits a distinct DNA methylation profile at selected loci queried by methylation-sensitive polymerase chain reaction and globally based on whole-genome bisulfite sequencing. Notably, the transcript levels of the DNA demethylase gene REPRESSOR OF SILENCING 1 (ROS1) were lower in the demr1 mutant. We established that DEMR1 directly binds to the ROS1 promoter in vivo and in vitro, and the methylation level in the DNA methylation monitoring sequence of ROS1 promoter decreased by 60% in the demr1 mutant. About 40% of the hyper-differentially methylated regions (DMRs) in the demr1 mutant were shared with the ros1-4 mutant. Genetic analysis indicated that DEMR1 acts upstream of ROS1 to positively regulate abscisic acid (ABA) signaling during seed germination and seedling establishment stages. Surprisingly, the loss of DEMR1 function also caused a rise in methylation levels of the mitochondrial genome, impaired mitochondrial structure and an early flowering phenotype. Together, our results show that DEMR1 is a novel regulator of DNA demethylation of both the nuclear and mitochondrial genomes in response to ABA and plant development in Arabidopsis.

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    Evolution of lmiRNAs and their targets from MITEs for rice adaptation
    Tianxiao Huang, Yan Li, Wei Wang, Le Xu, Jingrui Li and Yijun Qi
    J Integr Plant Biol 2022, 64 (12): 2411-2424.  
    doi: 10.1111/jipb.13413
    Abstract (Browse 197)  |   Save

    Twenty-four nucleotide long microRNAs (lmiRNAs) direct DNA methylation at target genes and regulate their transcription. The evolutionary origin of lmiRNAs and the range of lmiRNA-mediated regulation remain obscure. Here, we reannotated lmiRNAs and their targets in rice by applying stringent criteria. We found that the majority of lmiRNAs are derived from Miniature Inverted-repeat Transposable Elements (MITEs) and most sites targeted by MITE-derived lmiRNAs reside within MITEs, suggesting co-evolution of lmiRNAs and their targets through MITE amplification. lmiRNAs undergo dynamically changes under stress conditions and the genes targeted by lmiRNAs show an enrichment for stress-responsive genes, suggesting that lmiRNAs are widely involved in plant responses to stresses. We constructed the evolutionary histories of lmiRNAs and their targets. Nearly half of lmiRNAs emerged before or when the AA genome was diverged, while the emergence of lmiRNA targets coincided with or followed the emergence of lmiRNAs. Furthermore, we found that the sequences of a lmiRNA target site underwent variations, coincident with the divergence of rice accessions and the distribution of rice accessions in different geographical locations and climatic conditions. Our findings highlight MITEs as an important origin of lmiRNAs and suggest that the evolution of lmiRNA-target regulatory modules may contribute to rice adaptation to environmental changes.

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    From molecular basics to agronomic benefits: Insights into noncoding RNA-mediated gene regulation in plants
    Yuqiu Wang, Xing Wang Deng and Danmeng Zhu
    J Integr Plant Biol 2022, 64 (12): 2290-2308.  
    doi: 10.1111/jipb.13420
    Abstract (Browse 446)  |   Save

    The development of plants is largely dependent on their growth environment. To better adapt to a particular habitat, plants have evolved various subtle regulatory mechanisms for altering gene expression. Non coding RNAs (ncRNAs) constitute a major portion of the transcriptomes of eukaryotes. Various ncRNAs have been recognized as important regulators of the expression of genes involved in essential biological processes throughout the whole life cycles of plants. In this review, we summarize the current understanding of the biogenesis and contributions of small nucle olar RNA (snoRNA)- and regulatory long non coding RNA (lncRNA)-mediated gene regulation in plant development and environmental responses. Many regulatory ncRNAs appear to be associated with increased yield, quality and disease resistance of various species and cultivars. These ncRNAs may potentially be used as genetic resources for improving agronomic traits and for molecular breeding. The challenges in understanding plant ncRNA biology and the possibilities to make better use of these valuable gene resources in the future are discussed in this review.

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    DNA methylation dynamics during germline development
    Shengbo He and Xiaoqi Feng
    J Integr Plant Biol 2022, 64 (12): 2240-2251.  
    doi: 10.1111/jipb.13422
    Abstract (Browse 154)  |   Save

    DNA methylation plays essential homeostatic functions in eukaryotic genomes. In animals, DNA methylation is also developmentally regulated and, in turn, regulates development. In the past two decades, huge research effort has endorsed the understanding that DNA methylation plays a similar role in plant development, especially during sexual reproduction. The power of whole-genome sequencing and cell isolation techniques, as well as bioinformatics tools, have enabled recent studies to reveal dynamic changes in DNA methylation during germline development. Furthermore, the combination of these technological advances with genetics, developmental biology and cell biology tools has revealed functional methylation reprogramming events that control gene and transposon activities in flowering plant germlines. In this review, we discuss the major advances in our knowledge of DNA methylation dynamics during male and female germline development in flowering plants.

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    Celebrating the discovery of DNA demethylase
    Zhizhong Gong and Jian-Kang Zhu
    J Integr Plant Biol 2022, 64 (12): 2215-2216.  
    doi: 10.1111/jipb.13424
    Abstract (Browse 228)  |   Save

    Maintaining correct DNA methylation patterns entails the addition of methyl groups by DNA methyltransferases and the active removal of methylation from DNA. Removing a methyl group from 5-methylcytosine requires breaking a strong C–C bond, suggesting that demethylation might occur by an alternative mechanism that does not involve severing this bond. Indeed, the discovery of the 5-methylcytosine DNA glycosylase (also known as DNA demethylase) REPRESSOR OF SILENCING 1 (ROS1) by (Gong et al., 2002) revolutionized thinking in this field, as the study of ROS1 revealed a mechanism by which 5-methylcytosine is excised and replaced by the DNA repair machinery. This special issue celebrates the 20th anniversary of the discovery of ROS1 and the remarkable research that followed.

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    HEXOKINASE1 forms a nuclear complex with the PRC2 subunits CURLY LEAF and SWINGER to regulate glucose signaling
    Yutong Liu, Yunshu Bai, Ning Li, Mengting Li, Wenxin Liu, Dae‐Jin Yun, Bao Liu and Zheng‐Yi Xu
    J Integr Plant Biol 2022, 64 (6): 1168-1180.  
    DOI: 10.1111/jipb.13261
    Abstract (Browse 248)  |   Save

    The glucose sensor HEXOKINASE1 (HXK1) integrates myriad external and internal signals to regulate gene expression and development in Arabidopsis thaliana. However, how HXK1 mediates glucose signaling in the nucleus remains unclear. Here, using immunoprecipitation-coupled mass spectrometry, we show that two catalytic subunits of Polycomb Repressive Complex 2, SWINGER (SWN) and CURLY LEAF (CLF), directly interact with catalytically active HXK1 and its inactive forms (HXK1G104D and HXK1S177A) via their evolutionarily conserved SANT domains. HXK1, CLF, and SWN target common glucose-responsive genes to regulate glucose signaling, as revealed by RNA sequencing. The glucose-insensitive phenotypes of the Arabidopsis swn-1 and clf-50 mutants were similar to that of hxk1, and genetic analysis revealed that CLF, SWN, and HXK1 function in the same genetic pathway. Intriguingly, HXK1 is required for CLF- and SWN-mediated histone H3 lysine 27 (H3K27me3) deposition and glucose-mediated gene repression. Moreover, CLF and SWN affect the recruitment of HXK1 to its target chromatin. These findings support a model in which HXK1 and epigenetic modifiers form a nuclear complex to cooperatively mediate glucose signaling, thereby affecting the histone modification and expression of glucose-regulated genes in plants.

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    MicroProteins: Dynamic and accurate regulation of protein activity
    Qingqing Wu, Shangwei Zhong and Hui Shi
    J Integr Plant Biol 2022, 64 (4): 812-820.  
    DOI: 10.1111/jipb.13229
    Abstract (Browse 313)  |   Save

    Proteins usually assemble oligomers or high-order complexes to increase their efficiency and specificity in biological processes. The dynamic equilibrium of complex formation and disruption imposes reversible regulation of protein function. MicroProteins are small, single-domain proteins that directly bind target protein complexes and disrupt their assembly. Growing evidence shows that microProteins are efficient regulators of protein activity at the post-translational level. In the last few decades, thousands of plant microProteins have been predicted by computational approaches, but only a few have been experimentally validated. Recent studies highlighted the mechanistic working modes of newly-identified microProteins in Arabidopsis and other plant species. Here, we review characterized microProteins, including their biological roles, regulatory targets, and modes of action. In particular, we focus on microProtein-directed allosteric modulation of key components in light signaling pathways, and we summarize the biogenesis and evolutionary trajectory of known microProteins in plants. Understanding the regulatory mechanisms of microProteins is an important step towards potential utilization of microProteins as versatile biotechnological tools in crop bioengineering.

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    The immunophilin CYCLOPHILIN28 affects PSII-LHCII supercomplex assembly and accumulation in Arabidopsis thaliana
    Weining Zhu, Linqing Xu, Xiaoxia Yu and Ying Zhong
    J Integr Plant Biol 2022, 64 (4): 915-929.  
    DOI: 10.1111/jipb.13235
    Abstract (Browse 188)  |   Save

    In plant chloroplasts, photosystem II (PSII) complexes, together with light-harvesting complex II (LHCII), form various PSII-LHCII supercomplexes (SCs). This process likely involves immunophilins, but the underlying regulatory mechanisms are unclear. Here, by comparing Arabidopsis thaliana mutants lacking the chloroplast lumen-localized immunophilin CYCLOPHILIN28 (CYP28) to wild-type and transgenic complemented lines, we determined that CYP28 regulates the assembly and accumulation of PSII-LHCII SCs. Compared to the wild type, cyp28 plants showed accelerated leaf growth, earlier flowering time, and enhanced accumulation of high molecular weight PSII-LHCII SCs under normal light conditions. The lack of CYP28 also significantly affected the electron transport rate. Blue native-polyacrylamide gel electrophoresis analysis revealed more Lhcb6 and less Lhcb4 in M-LHCII-Lhcb4-Lhcb6 complexes in cyp28 versus wild-type plants. Peptidyl-prolyl cis/trans isomerase (PPIase) activity assays revealed that CYP28 exhibits weak PPIase activity and that its K113 and E187 residues are critical for this activity. Mutant analysis suggested that CYP28 may regulate PSII-LHCII SC accumulation by altering the configuration of Lhcb6 via its PPIase activity. Furthermore, the Lhcb6-P139 residue is critical for PSII-LHCII SC assembly and accumulation. Therefore, our findings suggest that CYP28 likely regulates PSII-LHCII SC assembly and accumulation by altering the configuration of P139 of Lhcb6 via its PPIase activity.

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    Crop phenotyping in a context of global change: What to measure and how to do it
    Jose Luis Araus, Shawn Carlisle Kefauver, Omar Vergara‐Díaz, Adrian Gracia‐Romero, Fatima Zahra Rezzouk, Joel Segarra, Maria Luisa Buchaillot, Melissa Chang‐Espino, Thomas Vatter, Rut Sanchez‐Bragado, José Armando Fernandez‐Gallego, Maria Dolores Serret and Jordi Bort
    J Integr Plant Biol 2022, 64 (2): 592-618.  
    doi: 10.1111/jipb.13191
    Abstract (Browse 230)  |   Save
    High-throughput crop phenotyping, particularly under field conditions, is nowadays perceived as a key factor limiting crop genetic advance. Phenotyping not only facilitates conventional breeding, but it is necessary to fully exploit the capabilities of molecular breeding, and it can be exploited to predict breeding targets for the years ahead at the regional level through more advanced simulation models and decision support systems. In terms of phenotyping, it is necessary to determined which selection traits are relevant in each situation, and which phenotyping tools/methods are available to assess such traits. Remote sensing methodologies are currently the most popular approaches, even when lab-based analyses are still relevant in many circumstances. On top of that, data processing and automation, together with machine learning/deep learning are contributing to the wide range of applications for phenotyping. This review addresses spectral and red–green–blue sensing as the most popular remote sensing approaches, alongside stable isotope composition as an example of a lab-based tool, and root phenotyping, which represents one of the frontiers for field phenotyping. Further, we consider the two most promising forms of aerial platforms (unmanned aerial vehicle and satellites) and some of the emerging data-processing techniques. The review includes three Boxes that examine specific case studies.
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    Shaping polyploid wheat for success: Origins, domestication, and the genetic improvement of agronomic traits
    Jie Liu, Yingyin Yao, Mingming Xin, Huiru Peng, Zhongfu Ni and Qixin Sun
    J Integr Plant Biol 2022, 64 (2): 536-563.  
    doi: 10.1111/jipb.13210
    Abstract (Browse 322)  |   Save
    Bread wheat (Triticum aestivum L., AABBDD, 2n = 6x = 42), which accounts for most of the cultivated wheat crop worldwide, is a typical allohexaploid with a genome derived from three diploid wild ancestors. Bread wheat arose and evolved via two sequential allopolyploidization events and was further polished through multiple steps of domestication. Today, cultivated allohexaploid bread wheat has numerous advantageous traits, including adaptive plasticity, favorable yield traits, and extended end-use quality, which have enabled its cultivation well beyond the ranges of its tetraploid and diploid progenitors to become a global staple food crop. In the past decade, rapid advances in wheat genomic research have considerably accelerated our understanding of the bases for the shaping of complex agronomic traits in this polyploid crop. Here, we summarize recent advances in characterizing major genetic factors underlying the origin, evolution, and improvement of polyploid wheats. We end with a brief discussion of the future prospects for the design of gene cloning strategies and modern wheat breeding.
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    Roles of MEM1 in safeguarding Arabidopsis genome against DNA damage, inhibiting ATM/SOG1-mediated DNA damage response, and antagonizing global DNA hypermethylation
    Qianqian Wang, Yumei La, Huihui Xia, Shaoxia Zhou, Zhaoyu Zhai and Honggui La
    J Integr Plant Biol 2022, 64 (1): 87-104.  
    doi: 10.1111/jipb.13200
    Abstract (Browse 201)  |   Save
    Arabidopsis methylation elevated mutant 1 (mem1) mutants have elevated levels of global DNA methylation. In this study, such mutant alleles showed increased sensitivity to methyl methanesulfonate (MMS). In mem1 mutants, an assortment of genes engaged in DNA damage response (DDR), especially DNA-repair-associated genes, were largely upregulated without MMS treatment, suggestive of activation of the DDR pathway in them. Following MMS treatment, expression levels of multiple DNA-repair-associated genes in mem1 mutants were generally lower than in Col-0 plants, which accounted for the MMS-sensitive phenotype of the mem1 mutants. A group of DNA methylation pathway genes were upregulated in mem1 mutants under non-MMS-treated conditions, causing elevated global DNA methylation, especially in RNA-directed DNA methylation (RdDM)-targeted regions. Moreover, MEM1 seemed to help ATAXIA-TELANGIECTASIA MUTATED (ATM) and/or SUPPRESSOR OF GAMMA RESPONSE 1 (SOG1) to fully activate/suppress transcription of a subset of genes regulated simultaneously by MEM1 and ATM and/or SOG1, because expression of such genes decreased/increased consistently in mem1 and atm and/or sog1 mutants, but the decreases/increases in the mem1 mutants were not as dramatic as in the atm and/or sog1 mutants. Thus, our studies reveals roles of MEM1 in safeguarding genome, and interrelationships among DNA damage, activation of DDR, DNA methylation/demethylation, and DNA repair.
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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 307)  |   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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    Cytosine methylation of the FWA promoter promotes direct in vitro shoot regeneration in Arabidopsis thaliana
    Xuehuan Dai, Jing Wang, Yuguang Song, Zhenhua Liu, Tao Xue, Meng Qiao, Yanchong Yu, Wei Xin and Fengning Xiang
    J Integr Plant Biol 2021, 63 (8): 1491-1504.  
    doi: 10.1111/jipb.13156
    Abstract (Browse 269)  |   Save
    Epigenetic modifications within promoter sequences can act as regulators of gene expression. Shoot regeneration is influenced by both DNA methylation and histone methylation, but the mechanistic basis of this regulation is obscure. Here, we identified 218 genes related to the regeneration capacity of callus that were differentially transcribed between regenerable calli (RC) and non-regenerable calli (NRC) in Arabidopsis thaliana. An analysis of the promoters of five of the differentially expressed genes (FWA, ACC1, TFL1, MAX3, and GRP3) pointed to an inverse relationship between cytosine methylation and transcription. The FWA promoter was demethylated and highly expressed in NRC, whereas it was methylated and expressed at low levels in RC. Explants of the hypomethylation mutants fwa-1 and fwa-2 showed strong levels of FWA expression and regenerated less readily than the wild type, suggesting that FWA inhibits direct in vitro shoot regeneration. WUSCHEL-RELATED HOMEOBOX 9 (WOX9), which is required for shoot apical meristem formation, was directly repressed by FWA. Overexpressing WOX9 partly rescued the shoot regeneration defect of fwa-2 plants. These findings suggest that cytosine methylation of the FWA promoter forms part of the regulatory system governing callus regenerability and direct in vitro shoot regeneration.
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    SIZ1 negatively regulates aluminum resistance by mediating the STOP1–ALMT1 pathway in Arabidopsis
    Jiameng Xu, Jiayong Zhu, Jiajia Liu, Junxia Wang, Zhaojun Ding and Huiyu Tian
    J Integr Plant Biol 2021, 63 (6): 1147-1160.  
    DOI: 10.1111/jipb.13091
    Abstract (Browse 408)  |   Save
    Sensitive to proton rhizotoxicity 1 (STOP1) functions as a crucial regulator of root growth during aluminum (Al) stress. However, how this transcription factor is regulated by Al stress to affect downstream genes expression is not well understood. To explore the underlying mechanisms of the function and regulation of STOP1, we employed a yeast two hybrid screen to identify STOP1-interacting proteins. The SUMO E3 ligase SIZ1, was found to interact with STOP1 and mainly facilitate its SUMO modification at K40 and K212 residues. Simultaneous introduction of K40R and K212R substitutions in STOP1 enhances its transactivation activity to upregulate the expression of aluminum-activated malate transporter 1 (ALMT1) via increasing the association with mediator 16 (MED16) transcriptional co-activator. Loss of function of SIZ1 causes highly increased expression of ALMT1, thus enhancing Al-induced malate exudation and Al tolerance. Also, we found that the protein level of SIZ1 is reduced in response to Al stress. Genetic evidence demonstrates that STOP1/ALMT1 is epistatic to SIZ1 in regulating root growth response to Al stress. This study suggests a mechanism about how the SIZ1–STOP1–ALMT1 signaling module is involved in root growth response to Al stress.
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    Recognition of H3K9me1 by maize RNA-directed DNA methylation factor SHH2
    Yuhua Wang, Xuelin Zhou, Jinyan Luo, Suhui Lv, Rui Liu, Xuan Du, Bei Jia, Fengtong Yuan, Heng Zhang and Jiamu Du
    J Integr Plant Biol 2021, 63 (6): 1091-1096.  
    doi: 10.1111/jipb.13103
    Abstract (Browse 305)  |   Save
    RNA-directed DNA methylation (RdDM) is a plant-specific de novo DNA methylation pathway, which has extensive cross-talk with histone modifications. Here, we report that the maize RdDM regulator SAWADEE HOMEODOMAIN HOMOLOG 2 (SHH2) is an H3K9me1 reader. Our structural studies reveal that H3K9me1 recognition is achieved by recognition of the methyl group via a classic aromatic cage and hydrogen-bonding and salt-bridge interactions with the free protons of the mono-methyllysine. The di- and tri-methylation states disrupt the polar interactions, decreasing the binding affinity. Our study reveals a mono-methyllysine recognition mechanism which potentially links RdDM to H3K9me1 in maize.
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    NF-YCs modulate histone variant H2A.Z deposition to regulate photomorphogenic growth in Arabidopsis
    Chunyu Zhang, Qian Qian, Xiang Huang, Wenbin Zhang, Xu Liu and Xingliang Hou
    J Integr Plant Biol 2021, 63 (6): 1120-1132.  
    DOI: 10.1111/jipb.13109
    Abstract (Browse 243)  |   Save
    In plants, light signals trigger a photomorphogenic program involving transcriptome changes, epigenetic regulation, and inhibited hypocotyl elongation. The evolutionarily conserved histone variant H2A.Z, which functions in transcriptional regulation, is deposited in chromatin by the SWI2/SNF2-RELATED 1 complex (SWR1c). However, the role of H2A.Z in photomorphogenesis and its deposition mechanism remain unclear. Here, we show that in Arabidopsis thaliana, H2A.Z deposition at its target loci is induced by light irradiation via NUCLEAR FACTOR-Y, subunit C (NF-YC) proteins, thereby inhibiting photomorphogenic growth. NF-YCs physically interact with ACTIN-RELATED PROTEIN6 (ARP6), a key component of the SWR1c that is essential for depositing H2A.Z, in a light-dependent manner. NF-YCs and ARP6 function together as negative regulators of hypocotyl growth by depositing H2A.Z at their target genes during photomorphogenesis. Our findings reveal an important role for the histone variant H2A.Z in photomorphogenic growth and provide insights into a novel transcription regulatory node that mediates H2A.Z deposition to control plant growth in response to changing light conditions.
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    The E3 ligase XBAT35 mediates thermoresponsive hypocotyl growth by targeting ELF3 for degradation in Arabidopsis
    Lin‐Lin Zhang, Wei Li, Ying‐Ying Tian, Seth Jon Davis and Jian‐Xiang Liu
    J Integr Plant Biol 2021, 63 (6): 1097-1103.  
    doi: 10.1111/jipb.13107
    Abstract (Browse 370)  |   Save
    Plants are capable of coordination of their growth and development with ambient temperatures. EARLY FLOWERING3 (ELF3), an essential component of the plant circadian clock, is also involved in ambient temperature sensing, as well as in inhibiting the expression and protein activity of the thermoresponsive regulator phytochrome interacting factor 4 (PIF4). The ELF3 activity is subjected to attenuation in response to warm temperature; however, how the protein level of ELF3 is regulated at warm temperature remains less understood. Here, we report that the E3 ligase XB3 ORTHOLOG 5 IN ARABIDOPSIS THALIANA, XBAT35, mediates ELF3 degradation. XBAT35 interacts with ELF3 and ubiquitinates ELF3. Loss-of-function mutation of XBAT35 increases the protein level of ELF3 and confers a short-hypocotyl phenotype under warm temperature conditions. Thus, our findings establish that XBAT35 mediates ELF3 degradation to lift the inhibition of ELF3 on PIF4 for promoting thermoresponsive hypocotyl growth in plants.
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    Phytochrome B interacts with SWC6 and ARP6 to regulate H2A.Z deposition and photomorphogensis in Arabidopsis
    Xuxu Wei, Wanting Wang, Peng Xu, Wenxiu Wang, Tongtong Guo, Shuang Kou, Minqing Liu, Yake Niu, Hong‐Quan Yang and Zhilei Mao
    J Integr Plant Biol 2021, 63 (6): 1133-1146.  
    DOI: 10.1111/jipb.13111
    Abstract (Browse 313)  |   Save
    Light serves as a crucial environmental cue which modulates plant growth and development, and which is controlled by multiple photoreceptors including the primary red light photoreceptor, phytochrome B (phyB). The signaling mechanism of phyB involves direct interactions with a group of basic helix-loop-helix (bHLH) transcription factors, PHYTOCHROME-INTERACTING FACTORS (PIFs), and the negative regulators of photomorphogenesis, COP1 and SPAs. H2A.Z is an evolutionarily conserved H2A variant which plays essential roles in transcriptional regulation. The replacement of H2A with H2A.Z is catalyzed by the SWR1 complex. Here, we show that the Pfr form of phyB physically interacts with the SWR1 complex subunits SWC6 and ARP6. phyB and ARP6 co-regulate numerous genes in the same direction, some of which are associated with auxin biosynthesis and response including YUC9, which encodes a rate-limiting enzyme in the tryptophan-dependent auxin biosynthesis pathway. Moreover, phyB and HY5/HYH act to inhibit hypocotyl elongation partially through repression of auxin biosynthesis. Based on our findings and previous studies, we propose that phyB promotes H2A.Z deposition at YUC9 to inhibit its expression through direct phyB-SWC6/ARP6 interactions, leading to repression of auxin biosynthesis, and thus inhibition of hypocotyl elongation in red light.
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    Roles of DEMETER in regulating DNA methylation in vegetative tissues and pathogen resistance
    Wenjie Zeng, Huan Huang, Xueqiang Lin, Chen Zhu, Ken‐ichi Kosami, Chaofeng Huang, Huiming Zhang, Cheng‐Guo Duan, Jian‐Kang Zhu and Daisuke Miki
    J Integr Plant Biol 2021, 63 (4): 691-706.  
    doi: 10.1111/jipb.13037
    Abstract (Browse 325)  |   Save
    DNA methylation is an epigenetic mark important for genome stability and gene expression. In Arabidopsis thaliana, the 5‐methylcytosine DNA glycosylase/demethylase DEMETER (DME) controls active DNA demethylation during the reproductive stage; however, the lethality of loss‐of‐function dme mutations has made it difficult to assess DME function in vegetative tissues. Here, we edited DME using clustered regularly interspaced short palindromic repeats (CRISPR) /CRISPR‐associated protein 9 and created three weak dme mutants that produced a few viable seeds. We also performed central cell‐specific complementation in a strong dme mutant and combined this line with mutations in the other three Arabidopsis demethylase genes to generate the dme ros1 dml2 dml3 (drdd) quadruple mutant. A DNA methylome analysis showed that DME is required for DNA demethylation at hundreds of genomic regions in vegetative tissues. A transcriptome analysis of the drdd mutant revealed that DME and the other three demethylases are important for plant responses to biotic and abiotic stresses in vegetative tissues. Despite the limited role of DME in regulating DNA methylation in vegetative tissues, the dme mutants showed increased susceptibility to bacterial and fungal pathogens. Our study highlights the important functions of DME in vegetative tissues and provides valuable genetic tools for future investigations of DNA demethylation in plants.
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    A novel protein complex that regulates active DNA demethylation in Arabidopsis
    Pan Liu, Wen‐Feng Nie, Xiansong Xiong, Yuhua Wang, Yuwei Jiang, Pei Huang, Xueqiang Lin, Guochen Qin, Huan Huang, Qingfeng Niu, Jiamu Du, Zhaobo Lang, Rosa Lozano‐Duran and Jian‐Kang Zhu
    J Integr Plant Biol 2021, 63 (4): 772-786.  
    doi: 10.1111/jipb.13045
    Abstract (Browse 398)  |   Save
    Active DNA demethylation is critical for altering DNA methylation patterns and regulating gene expression. The 5‐methylcytosine DNA glycosylase/lyase ROS1 initiates a base‐excision repair pathway for active DNA demethylation and is required for the prevention of DNA hypermethylation at 1 000s of genomic regions in Arabidopsis. How ROS1 is regulated and targeted to specific genomic regions is not well understood. Here, we report the discovery of an Arabidopsis protein complex that contains ROS1, regulates ROS1 gene expression, and likely targets the ROS1 protein to specific genomic regions. ROS1 physically interacts with a WD40 domain protein (RWD40), which in turn interacts with a methyl‐DNA binding protein (RMB1) as well as with a zinc finger and homeobox domain protein (RHD1). RMB1 binds to DNA that is methylated in any sequence context, and this binding is necessary for its function in vivo. Loss‐of‐function mutations in RWD40, RMB1, or RHD1 cause DNA hypermethylation at several tested genomic regions independently of the known ROS1 regulator IDM1. Because the hypermethylated genomic regions include the DNA methylation monitoring sequence in the ROS1 promoter, plants mutated in RWD40, RMB1, or RHD1 show increased ROS1 expression. Importantly, ROS1 binding to the ROS1 promoter requires RWD40, RMB1, and RHD1, suggesting that this complex dictates ROS1 targeting to this locus. Our results demonstrate that ROS1 forms a protein complex with RWD40, RMB1, and RHD1, and that this novel complex regulates active DNA demethylation at several endogenous loci in Arabidopsis.
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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 317)  |   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 574)  |   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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    Genome‐wide distribution and functions of the AAE complex in epigenetic regulation in Arabidopsis
    Yi‐Zhe Zhang, Juncheng Lin, Zhizhong Ren, Chun‐Xiang Chen, Daisuke Miki, Si‐Si Xie, Jian Zhang, Ya‐Nan Chang, Jing Jiang, Jun Yan, Qingshun Q. Li, Jian‐Kang Zhu and Cheng‐Guo Duan
    J Integr Plant Biol 2021, 63 (4): 707-722.  
    DOI: 10.1111/jipb.13068
    Abstract (Browse 236)  |   Save
    Heterochromatin is widespread in eukaryotic genomes and has diverse impacts depending on its genomic context. Previous studies have shown that a protein complex, the ASI1‐AIPP1‐EDM2 (AAE) complex, participates in polyadenylation regulation of several intronic heterochromatin‐containing genes. However, the genome‐wide functions of AAE are still unknown. Here, we show that the ASI1 and EDM2 mostly target the common genomic regions on a genome‐wide level and preferentially interacts with genetic heterochromatin. Polyadenylation (poly(A) sequencing reveals that AAE complex has a substantial influence on poly(A) site usage of heterochromatin‐containing genes, including not only intronic heterochromatin‐containing genes but also the genes showing overlap with heterochromatin. Intriguingly, AAE is also involved in the alternative splicing regulation of a number of heterochromatin‐overlapping genes, such as the disease resistance gene RPP4. We provided evidence that genic heterochromatin is indispensable for the recruitment of AAE in polyadenylation and splicing regulation. In addition to conferring RNA processing regulation at genic heterochromatin‐containing genes, AAE also targets some transposable elements (TEs) outside of genes (including TEs sandwiched by genes and island TEs) for epigenetic silencing. Our results reveal new functions of AAE in RNA processing and epigenetic silencing, and thus represent important advances in epigenetic regulation.
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    N4‐methylcytidine ribosomal RNA methylation in chloroplasts is crucial for chloroplast function, development, and abscisic acid response in Arabidopsis
    Le Nguyen Tieu Ngoc, Su Jung Park, Trinh Thi Huong, Kwang Ho Lee and Hunseung Kang
    J Integr Plant Biol 2021, 63 (3): 570-582.  
    doi: 10.1111/jipb.13009
    Abstract (Browse 339)  |   Save
    Although the essential role of messenger RNA methylation in the nucleus is increasingly understood, the nature of ribosomal RNA (rRNA) methyltransferases and the role of rRNA methylation in chloroplasts remain largely unknown. A recent study revealed that CMAL (for Chloroplast mr aW‐ Like) is a chloroplast‐localized rRNA methyltransferase that is responsible for N4‐methylcytidine (m4C) in 16S chloroplast rRNA in Arabidopsis thaliana. In this study, we further examined the role of CMAL in chloroplast biogenesis and function, development, and hormone response. The cmal mutant showed reduced chlorophyll biosynthesis, photosynthetic activity, and growth‐defect phenotypes, including severely stunted stems, fewer siliques, and lower seed yield. The cmal mutant was hypersensitive to chloroplast translation inhibitors, such as lincomycin and erythromycin, indicating that the m4C‐methylation defect in the 16S rRNA leads to a reduced translational activity in chloroplasts. Importantly, the stunted stem of the cmal mutant was partially rescued by exogenous gibberellic acid or auxin. The cmal mutant grew poorer than wild type, whereas the CMAL‐overexpressing transgenic Arabidopsis plants grew better than wild type in the presence of abscisic acid. Altogether, these results indicate that CMAL is an indispensable rRNA methyltransferase in chloroplasts and is crucial for chloroplast biogenesis and function, photosynthesis, and hormone response during plant growth and development.
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    Histone deacetylase HDA710 controls salt tolerance by regulating ABA signaling in rice
    Farhan Ullah, Qiutao Xu, Yu Zhao and Dao‐Xiu Zhou
    J Integr Plant Biol 2021, 63 (3): 451-467.  
    doi: 10.1111/jipb.13042
    Abstract (Browse 722)  |   Save
    Plants have evolved numerous mechanisms that assist them in withstanding environmental stresses. Histone deacetylases (HDACs) play crucial roles in plant stress responses; however, their regulatory mechanisms remain poorly understood. Here, we explored the function of HDA710/OsHDAC2, a member of the HDAC RPD3/HDA1 family, in stress tolerance in rice (Oryza sativa). We established that HDA710 localizes to both the nucleus and cytoplasm and is involved in regulating the acetylation of histone H3 and H4, specifically targeting H4K5 and H4K16 under normal conditions. HDA710 transcript accumulation levels were strongly induced by abiotic stresses including drought and salinity, as well as by the phytohormones jasmonic acid (JA) and abscisic acid (ABA). hda710 knockout mutant plants showed enhanced salinity tolerance and reduced ABA sensitivity, whereas transgenic plants overexpressing HDA710 displayed the opposite phenotypes. Moreover, ABA‐ and salt‐stress‐responsive genes, such as OsLEA3, OsABI5, OsbZIP72, and OsNHX1, were upregulated in hda710 compared with wild‐type plants. These expression differences corresponded with higher levels of histone H4 acetylation in gene promoter regions in hda710 compared with the wild type under ABA and salt‐stress treatment. Collectively, these results suggest that HDA710 is involved in regulating ABA‐ and salt‐stress‐responsive genes by altering H4 acetylation levels in their promoters.
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    Chromatin remodeling factors regulate environmental stress responses in plants
    Ze‐Ting Song, Jian‐Xiang Liu and Jia‐Jia Han
    J Integr Plant Biol 2021, 63 (3): 438-450.  
    doi: 10.1111/jipb.13064
    Abstract (Browse 460)  |   Save
    Environmental stress from climate change and agricultural activity threatens global plant biodiversity as well as crop yield and quality. As sessile organisms, plants must maintain the integrity of their genomes and adjust gene expression to adapt to various environmental changes. In eukaryotes, nucleosomes are the basic unit of chromatin around which genomic DNA is packaged by condensation. To enable dynamic access to packaged DNA, eukaryotes have evolved Snf2 (sucrose nonfermenting 2) family proteins as chromatin remodeling factors (CHRs) that modulate the position of nucleosomes on chromatin. During plant stress responses, CHRs are recruited to specific genomic loci, where they regulate the distribution or composition of nucleosomes, which in turn alters the accessibility of these loci to general transcription or DNA damage repair machinery. Moreover, CHRs interplay with other epigenetic mechanisms, including DNA methylation, histone modifications, and deposition of histone variants. CHRs are also involved in RNA processing at the post‐transcriptional level. In this review, we discuss major advances in our understanding of the mechanisms by which CHRs function during plants’ response to environmental stress.
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    The Class III peroxidase gene OsPrx30, transcriptionally modulated by the AT‐hook protein OsATH1, mediates rice bacterial blight‐induced ROS accumulation
    Hao Liu, Shuangyu Dong, Ming Li, Fengwei Gu, Guili Yang, Tao Guo, Zhiqiang Chen and Jiafeng Wang
    J Integr Plant Biol 2021, 63 (2): 393-408.  
    doi: 10.1111/jipb.13040
    Abstract (Browse 474)  |   Save
    Class III peroxidases (CIII Prxs) play critical roles in plant immunity by scavenging reactive oxygen species (ROS). However, the functions of CIII Prxs in rice (Oryza sativa L.) immunity are largely unexplored. Here, we report a Prx precursor, OsPrx30, that is responsive to the bacterial blight Xanthomonas oryzae pv. oryzae (Xoo). OsPrx30 was primarily expressed in rice roots, leaves, and stems, and its protein product was mainly localized at the endoplasmic reticulum. Overexpression of OsPrx30 enhanced the plant's susceptibility to Xoo by maintaining a high level of peroxidase (POD) activity and reducing the content of H2O2, whereas depletion of OsPrx30 had the opposite effects. Furthermore, we identified an AT‐hook transcription factor, OsATH1, that is specifically bound to the OsPrx30 promoter. As observed in plants overexpressing OsPrx30, depletion of OsATH1 enhanced susceptibility to Xoo. Finally, we demonstrated that depletion of OsATH1 increased histone H3 acetylation at the AT‐rich region of the OsPrx30 promoter. Taken together, these results reveal a mechanism underlying the POD‐induced natural resistance to bacterial diseases and suggest a model for transcription regulation of Prx genes in rice.
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    Contribution of phenylpropanoid metabolism to plant development and plant–environment interactions
    Nai-Qian Dong and Hong-Xuan Lin
    J Integr Plant Biol 2021, 63 (1): 180-209.  
    doi: 10.1111/jipb.13054
    Abstract (Browse 793)  |   Save
    Phenylpropanoid metabolism is one of the most important metabolisms in plants, yielding more than 8,000 metabolites contributing to plant development and plant–environment interplay. Phenylpropanoid metabolism materialized during the evolution of early freshwater algae that were initiating terrestrialization and land plants have evolved multiple branches of this pathway, which give rise to metabolites including lignin, flavonoids, lignans, phenylpropanoid esters, hydroxycinnamic acid amides, and sporopollenin. Recent studies have revealed that many factors participate in the regulation of phenylpropanoid metabolism, and modulate phenylpropanoid homeostasis when plants undergo successive developmental processes and are subjected to stressful environments. In this review, we summarize recent progress on elucidating the contribution of phenylpropanoid metabolism to the coordination of plant development and plant–environment interaction, and metabolic flux redirection among diverse metabolic routes. In addition, our review focuses on the regulation of phenylpropanoid metabolism at the transcriptional, post‐transcriptional, post‐translational, and epigenetic levels, and in response to phytohormones and biotic and abiotic stresses.
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    Genome editing for plant research and crop improvement
    Xiangqiang Zhan, Yuming Lu, Jian-Kang Zhu and Jose Ramon Botella
    J Integr Plant Biol 2021, 63 (1): 3-33.  
    doi: 10.1111/jipb.13063
    Abstract (Browse 818)  |   Save
    The advent of clustered regularly interspaced short palindromic repeat (CRISPR) has had a profound impact on plant biology, and crop improvement. In this review, we summarize the state‐of‐the‐art development of CRISPR technologies and their applications in plants, from the initial introduction of random small indel (insertion or deletion) mutations at target genomic loci to precision editing such as base editing, prime editing and gene targeting. We describe advances in the use of class 2, types II, V, and VI systems for gene disruption as well as for precise sequence alterations, gene transcription, and epigenome control.
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    RNA-directed DNA methylation has an important developmental function in Arabidopsis that is masked by the chromatin remodeler PICKLE
    Rong Yang, Li He, Huan Huang, Jian-Kang Zhu, Rosa Lozano-Duran and Heng Zhang
    J Integr Plant Biol 2020, 62 (11): 1647-1652.  
    doi: 10.1111/jipb.12979
    Abstract (Browse 514)  |   Save
    In Arabidopsis, RNA‐directed DNA methylation (RdDM) is required for the maintenance of CHH methylation, and for de novo methylation in all (CG, CHG, and CHH) contexts, but no obvious effect of RdDM deficiency on plant development has been found to date. We show that the combination of mutations in the chromatin remodeler PKL and RdDM components results in developmental alterations, which appear in a SUPPRESSOR OF DRM1 DRM2 CMT3 (SDC)‐dependent manner.
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