The WD40 Domain Protein MSI1 Functions in a Histone Deacetylase Complex to Fine-Tune Abscisic Acid Signaling

Mehdi, Saher; Derkacheva, Maria; Ramström, Margareta; Kralemann, Lejon E. M.; Bergquist, Jonas; Hennig, Lars

doi:10.1105/tpc.15.00763

Cited by 138 publications

(141 citation statements)

References 77 publications

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“…However, it is possible that each HDAC may control the response to salt stress in a different manner among class I HDACs. hda9 and hda19 knockdown lines lead to the derepression of salt stress-responsive genes (Mehdi et al, 2016;Zheng et al, 2016). Considering the previous results from the functional analysis of HDA9 and the hda19 mutants in this study, both of which belong to class I HDACs, HDA9 and HDA19 negatively regulate salt stress-responsive genes.…”

Section: Discussionsupporting

confidence: 66%

“…Some HDACs, such as HDA14 and SRT2, are actually targeted to organelles (Alinsug et al, 2012;König et al, 2014), suggesting that HDACs might be involved in the acetylation of nonhistone protein and regulate enzymatic activity or protein stability like HDA6. Furthermore, HDA19 forms a complex with Histone Deacetylase Complex1 and MSl1, and they control HDA19 activity in stress responses (Perrella et al, 2013;Mehdi et al, 2016;Asensi-Fabado et al, 2017). It is also reported that the BES1/TPL/HDA19 repressor complex mediates the inhibitory action of brassinosteroids on abscisic acid responses (Ryu et al, 2014).…”

Section: Discussionmentioning

confidence: 98%

“…For example, HDA9 and HD2D negatively regulate the salt response (Han et al, 2016;Zheng et al, 2016), whereas HDA6 and HD2C positively regulate it Luo et al, 2012). In the case of HDA19, previous studies reported controversial data demonstrating that an hda19 knockout mutant in the Wassilewskija (Ws) background shows sensitivity to salt stress, whereas an hda19 knockdown mutant in the Columbia-0 (Col-0) background exhibits the opposite phenotype Mehdi et al, 2016). Taking these previous results into consideration, HDACs appear to activate positive and negative responses in salinity stress, with some discrepancies.…”

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confidence: 99%

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The Distinct Roles of Class I and II RPD3-Like Histone Deacetylases in Salinity Stress Response

et al. 2017

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ORCID IDs: 0000-0002-7750-6056 (M.U.); 0000-0002-3979-3947 (A.M.); 0000-0001-8288-0467 (M.S.).Histone acetylation is an essential process in the epigenetic regulation of diverse biological processes, including environmental stress responses in plants. Previously, our research group identified a histone deacetylase (HDAC) inhibitor (HDI) that confers salt tolerance in Arabidopsis (Arabidopsis thaliana). In this study, we demonstrate that class I HDAC (HDA19) and class II HDACs (HDA5/14/15/18) control responses to salt stress through different pathways. The screening of 12 different selective HDIs indicated that seven newly reported HDIs enhance salt tolerance. Genetic analysis, based on a pharmacological study, identified which HDACs function in salinity stress tolerance. In the wild-type Columbia-0 background, hda19 plants exhibit tolerance to high-salinity stress, while hda5/14/15/18 plants exhibit hypersensitivity to salt stress. Transcriptome analysis revealed that the effect of HDA19 deficiency on the response to salinity stress is distinct from that of HDA5/14/15/18 deficiencies. In hda19 plants, the expression levels of stress tolerance-related genes, late embryogenesis abundant proteins that prevent protein aggregation and positive regulators such as ABI5 and NAC019 in abscisic acid signaling, were induced strongly relative to the wild type. Neither of these elements was up-regulated in the hda5/14/15/18 plants. The mutagenesis of HDA19 by genome editing in the hda5/14/15/18 plants enhanced salt tolerance, suggesting that suppression of HDA19 masks the phenotype caused by the suppression of class II HDACs in the salinity stress response. Collectively, our results demonstrate that HDIs that inhibit class I HDACs allow the rescue of plants from salinity stress regardless of their selectivity, and they provide insight into the hierarchal regulation of environmental stress responses through HDAC isoforms.Histones are DNA-packaging proteins that provide stability to the genome by preventing physical genotoxicity (e.g. DNA breaks; Luger et al., 1997;Downs et al., 2007). They also have been considered to originally function as regulators of mRNA expression before the divergence of the Archaea and Eukarya (Ammar et al., 2012). A variety of chemical modifications (acetylation, methylation, phosphorylation, etc.) to the N tails of histones are one of the properties that enable the regulation of mRNA expression, which is generally conserved in eukaryotes (Jenuwein and Allis, 2001;Kouzarides, 2007). Chromatin possesses a diverse array of chemical moieties that allows it to contain and transmit information that is independent of the genetic code (i.e. epigenetic) and regulate gene expression levels. Epigenetic regulation is considered to be profoundly associated with plant development and adaptation to the environment. A complete understanding of the coordinated regulation of gene expression by histone modifications, however, is still lacking in plants. The role of epigenetic regulation in the abiotic stress response...

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Section: Discussionsupporting

confidence: 66%

Section: Discussionmentioning

confidence: 98%

mentioning

confidence: 99%

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The Distinct Roles of Class I and II RPD3-Like Histone Deacetylases in Salinity Stress Response

et al. 2017

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“…Transgenic MSI1 cosuppression lines (msi1-cs), in which MSI1 expression is reduced to 5% of that in wild-type plants, lose repression of some EMF2-target genes and show strong defects in vegetative and reproductive development leading to sterility Köhler et al, 2003). Recently, Mehdi et al (2016) reported that MSI1 interacts with HDA19 to form a histone deacetylase complex involved in the suppression of ABA receptor gene expression, which is thought to attenuate ABA signaling in Arabidopsis. Thus, MSI1 may have functions outside of the classical PRC2 context.…”

Section: Introductionmentioning

confidence: 99%

HSI2/VAL1 Silences AGL15 to Regulate the Developmental Transition from Seed Maturation to Vegetative Growth in Arabidopsis

et al. 2018

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Gene expression during seed development in Arabidopsis thaliana is controlled by transcription factors including LEAFY COTYLEDON1 (LEC1) and LEC2, ABA INSENSITIVE3 (ABI3), FUSCA3 (FUS3), known as LAFL proteins, and AGAMOUS-LIKE15 (AGL15). The transition from seed maturation to germination and seedling growth requires the transcriptional silencing of these seed maturation-specific factors leading to downregulation of structural genes including those that encode seed storage proteins, oleosins, and dehydrins. During seed germination and vegetative growth, B3-domain protein HSI2/VAL1 is required for the transcriptional silencing of LAFL genes. Here, we report chromatin immunoprecipitation analysis indicating that HSI2/VAL1 binds to the upstream sequences of the AGL15 gene but not at LEC1, ABI3, FUS3, or LEC2 loci. Functional analysis indicates that the HSI2/VAL1 B3 domain interacts with two RY elements upstream of the AGL15 coding region and at least one of them is required for HSI2/VAL1-dependent AGL15 repression. Expression analysis of the major seed maturation regulatory genes LEC1, ABI3, FUS3, and LEC2 in different genetic backgrounds demonstrates that HSI2/VAL1 is epistatic to AGL15 and represses the seed maturation regulatory program through downregulation of AGL15 by deposition of H3K27me3 at this locus. This hypothesis is further supported by results that show that HSI2/VAL1 physically interacts with the Polycomb Repressive Complex 2 component protein MSI1, which is also enriched at the AGL15 locus.

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“…HDA19 and HDC1 are components of the histone deacetylase complex, which epigenetically controls gene expression through repressive function of histone deacetylation (Perrella et al, 2013). HDA19 and HDC1 are involved in plant's response to abscisic acid, abiotic stresses, and in seed germination, among other functions (Perrella et al, 2013;Mehdi et al, 2016). Altered translation of HDA19 and HDC1 mRNAs might have contributed to the MRF-deficient phenotypes in DS.…”

Section: Discussionmentioning

confidence: 99%

MRF Family Genes Are Involved in Translation Control, Especially under Energy-Deficient Conditions, and Their Expression and Functions Are Modulated by the TOR Signaling Pathway

et al. 2017

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Dynamic control of protein translation in response to the environment is essential for the survival of plant cells. Target of rapamycin (TOR) coordinates protein synthesis with cellular energy/nutrient availability through transcriptional modulation and phosphorylation of the translation machinery. However, mechanisms of TOR-mediated translation control are poorly understood in plants. Here, we report that Arabidopsis thaliana MRF (MA3 DOMAIN-CONTAINING TRANSLATION REGULATORY FACTOR) family genes encode translation regulatory factors under TOR control, and their functions are particularly important in energy-deficient conditions. Four MRF family genes (MRF1-MRF4) are transcriptionally induced by dark and starvation (DS). Silencing of multiple MRFs increases susceptibility to DS and treatment with a TOR inhibitor, while MRF1 overexpression decreases susceptibility. MRF proteins interact with eIF4A and cofractionate with ribosomes. MRF silencing decreases translation activity, while MRF1 overexpression increases it, accompanied by altered ribosome patterns, particularly in DS. Furthermore, MRF deficiency in DS causes altered distribution of mRNAs in sucrose gradient fractions and accelerates rRNA degradation. MRF1 is phosphorylated in vivo and phosphorylated by S6 kinases in vitro. MRF expression and MRF1 ribosome association and phosphorylation are modulated by cellular energy status and TOR activity. We discuss possible mechanisms of the function of MRF family proteins under normal and energy-deficient conditions and their functional link with the TOR pathway.

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The WD40 Domain Protein MSI1 Functions in a Histone Deacetylase Complex to Fine-Tune Abscisic Acid Signaling

Cited by 138 publications

References 77 publications

The Distinct Roles of Class I and II RPD3-Like Histone Deacetylases in Salinity Stress Response

The Distinct Roles of Class I and II RPD3-Like Histone Deacetylases in Salinity Stress Response

HSI2/VAL1 Silences AGL15 to Regulate the Developmental Transition from Seed Maturation to Vegetative Growth in Arabidopsis

MRF Family Genes Are Involved in Translation Control, Especially under Energy-Deficient Conditions, and Their Expression and Functions Are Modulated by the TOR Signaling Pathway

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