AIP1 is a novel Agenet/Tudor domain protein from Arabidopsis that interacts with regulators of DNA replication, transcription and chromatin remodeling

Brasil, Juliana Nogueira; Cabral, Luiz Mors; Eloy, Núbia Barbosa; Primo, Luiza M. F.; Barroso-Neto, Ito L.; Grangeiro, Letícia P. Perdigão; González, Nathalie; Inzé, Dirk; Ferreira, Paulo Cavalcanti Gomes; Hemerly, Adriana S.

doi:10.1186/s12870-015-0641-z

Cited by 20 publications

(26 citation statements)

References 64 publications

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“…5). Secondary-structure modeling studies suggest that the Agenet domains of EML proteins contain four ␤ sheets that form a Tudor-like ␤ barrel fold (17). Thus, while EML1 and EML3 Agenet domains contain the four ␤ strands needed to make the characteristic ␤ barrel of Royal Family domains, the aromatic cage may be incomplete, allowing promiscuous target recognition.…”

Section: Discussionmentioning

confidence: 99%

“…A structurally conserved group known as the Royal Family is largely responsible for recognizing methylated lysine and arginine residues (15,16). In Arabidopsis, there are 32 proteins that collectively contain 71 copies of the Royal Family Agenet domain, a structural homolog of animal Tudor domains (17,18). Until recently, only two proteins with Agenet or Agenet-like domains have been linked to a specific histone PTM target.…”

mentioning

confidence: 99%

“…The tandem Tudor-like fold of the SAWADEE domain of SAWADEE HOMEODOMAIN HOMOLOGUE 1 (SHH1) recognizes H3K9me2 and recruits RNA polymerase IV, a component of the RNA-directed DNA methylation (RdDM) pathway, to silenced loci (19,20). The Agenet domain-containing ABAP1 INTERACTING PROTEIN 1 (AIP1), important for flowering, is believed to interact with unmodified histones (17,21).…”

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confidence: 99%

“…Four Arabidopsis EMSY-LIKE (EML) proteins have recently been identified as potential histone readers based on their Agenet domain-containing structure (17). EML proteins are characterized by a central Agenet domain and an EMSY N-terminal (ENT) domain.…”

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confidence: 99%

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Arabidopsis Histone Reader EMSY-LIKE 1 Binds H3K36 and Suppresses Geminivirus Infection

Coursey

Milutinovic

Regedanz

et al. 2018

J Virol

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Histone posttranslational modifications (PTMs) impart information that regulates chromatin structure and activity. Their effects are mediated by histone reader proteins that bind specific PTMs to modify chromatin and/or recruit appropriate effectors to alter the chromatin landscape. Despite their crucial juxtaposition between information and functional outcome, relatively few plant histone readers have been identified, and nothing is known about their impact on viral chromatin and pathogenesis. We used the geminivirus (CaLCuV) as a model to functionally characterize two recently identified reader proteins, EMSY-LIKE 1 (EML1) and EML3, which contain Tudor-like Agenet domains predictive of histone PTM binding function. Here, we show that mutant plants exhibit contrasting hypersusceptible () and tolerant () responses to CaLCuV infection and that EML1 deficiency correlates with RNA polymerase II (Pol II) enrichment on viral chromatin and upregulated viral gene expression. Consistent with reader activity, EML1 and EML3 associate with nucleosomes and with CaLCuV chromatin, suggesting a direct impact on pathogenesis. We also demonstrate that EML1 and EML3 bind peptides containing histone H3 lysine 36 (H3K36), a PTM usually associated with active gene expression. The interaction encompasses multiple H3K36 PTMs, including methylation and acetylation, suggesting nuanced regulation. Furthermore, EML1 and EML3 associate with similar regions of viral chromatin, implying possible competition between the two readers. Regions of EML1 and EML3 association correlate with sites of trimethylated H3K36 (H3K36me3) enrichment, consistent with regulation of geminivirus chromatin by direct EML targeting. Histone PTMs convey information that regulates chromatin compaction and DNA accessibility. Histone reader proteins bind specific PTMs and translate their effects by modifying chromatin and/or by recruiting effectors that alter chromatin structure or activity. In this study, CaLCuV was used to characterize the activities of two Agenet domain histone readers, EML1 and EML3. We show that mutants are hypersusceptible to CaLCuV, whereas plants are more tolerant of infection than wild-type plants. We also demonstrate that EML1 and EML3 associate with histones and viral chromatin and that both proteins bind peptides containing H3K36, a PTM associated with active gene expression. Consistent with antiviral activity, EML1 suppresses CaLCuV gene expression and reduces Pol II access to viral chromatin. By linking EML1 and EML3 to pathogenesis, these studies have expanded our knowledge of histone reader proteins and uncovered an additional level of viral chromatin regulation.

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Section: Discussionmentioning

confidence: 99%

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confidence: 99%

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confidence: 99%

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confidence: 99%

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Arabidopsis Histone Reader EMSY-LIKE 1 Binds H3K36 and Suppresses Geminivirus Infection

Coursey

Milutinovic

Regedanz

et al. 2018

J Virol

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“…RIF1 is characterized by the presence of ENT (EMSY-like N-terminal) and Agenet (Tudor-like) domains. Agenet/Tudor-like domains are chromatin-binding domains present in chromatin remodelers and histone readers [109]. The proposed RIF1 histone reading function has been related to the 'activating' H3K9/14ac marks and requires R [108].…”

Section: Anthocyanin Biosynthesis Depends On the Activity Of Rif1 A mentioning

confidence: 99%

Combinatorial control of plant gene expression

Brkljačić

Grotewold

2017

Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanism

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Combinatorial gene regulation provides a mechanism by which relatively small numbers of transcription factors can control the expression of a much larger number of genes with finely tuned temporal and spatial patterns. This is achieved by transcription factors assembling into complexes in a combinatorial fashion, exponentially increasing the number of genes that they can target. Such an arrangement also increases the specificity and affinity for the cis-regulatory sequences required for accurate target gene expression. Superimposed on this transcription factor combinatorial arrangement is the increasing realization that histone modification marks expand the regulatory information, which is interpreted by histone readers and writers that are part of the regulatory apparatus. Here, we review the progress in these areas from the perspective of plant combinatorial gene regulation, providing examples of different regulatory solutions and comparing them to other metazoans. This article is part of a Special Issue entitled: Plant Gene Regulatory Mechanisms and Networks, edited by Dr. Erich Grotewold and Dr. Nathan Springer.

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QTL analysis of four yield-related traits for Brassica napus L. in multiple environments

et al. 2019

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AIP1 is a novel Agenet/Tudor domain protein from Arabidopsis that interacts with regulators of DNA replication, transcription and chromatin remodeling

Cited by 20 publications

References 64 publications

Arabidopsis Histone Reader EMSY-LIKE 1 Binds H3K36 and Suppresses Geminivirus Infection

Arabidopsis Histone Reader EMSY-LIKE 1 Binds H3K36 and Suppresses Geminivirus Infection

Combinatorial control of plant gene expression

QTL analysis of four yield-related traits for Brassica napus L. in multiple environments

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