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Article ; Online: Chromatin dynamics and RNA metabolism are double-edged swords for the maintenance of plant genome integrity.

Bergis-Ser, Clara / Reji, Meega / Latrasse, David / Bergounioux, Catherine / Benhamed, Moussa / Raynaud, Cécile

Nature plants

2024

Abstract: Maintenance of genome integrity is an essential process in all organisms. Mechanisms avoiding the formation of DNA lesions or mutations are well described in animals because of their relevance to human health and cancer. In plants, they are of growing ... ...

Abstract	Maintenance of genome integrity is an essential process in all organisms. Mechanisms avoiding the formation of DNA lesions or mutations are well described in animals because of their relevance to human health and cancer. In plants, they are of growing interest because DNA damage accumulation is increasingly recognized as one of the consequences of stress. Although the cellular response to DNA damage is mostly studied in response to genotoxic treatments, the main source of DNA lesions is cellular activity itself. This can occur through the production of reactive oxygen species as well as DNA processing mechanisms such as DNA replication or transcription and chromatin dynamics. In addition, how lesions are formed and repaired is greatly influenced by chromatin features and dynamics and by DNA and RNA metabolism. Notably, actively transcribed regions or replicating DNA, because they are less condensed and are sites of DNA processing, are more exposed to DNA damage. However, at the same time, a wealth of cellular mechanisms cooperate to favour DNA repair at these genomic loci. These intricate relationships that shape the distribution of mutations along the genome have been studied extensively in animals but much less in plants. In this Review, we summarize how chromatin dynamics influence lesion formation and DNA repair in plants, providing a comprehensive view of current knowledge and highlighting open questions with regard to what is known in other organisms.
Language	English
Publishing date	2024-04-24
Publishing country	England
Document type	Journal Article ; Review
ISSN	2055-0278
ISSN (online)	2055-0278
DOI	10.1038/s41477-024-01678-z
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Article ; Online: CRUMPLED LEAF supports plastid OUTER ENVELOPE PROTEIN OF 80 KDA complex formation in Arabidopsis.

Yoshimura, Ryo / Minamikawa, Syun / Suzuki, Takamasa / Goto, Kotaro / Latrasse, David / Sicar, Sanchari / Raynaud, Cécile / Benhamed, Moussa / Yoshioka, Yasushi

Plant physiology

2024 Volume 194, Issue 4, Page(s) 2422–2433

Abstract: Embedded β-barrel proteins in the outer envelope membrane mediate most cellular trafficking between the cytoplasm and plastids. Although the TRANSLOCON AT THE OUTER ENVELOPE MEMBRANE OF CHLOROPLASTS 75-V (TOC75-V)/OUTER ENVELOPE PROTEIN OF 80 KDA (OEP80) ...

Abstract	Embedded β-barrel proteins in the outer envelope membrane mediate most cellular trafficking between the cytoplasm and plastids. Although the TRANSLOCON AT THE OUTER ENVELOPE MEMBRANE OF CHLOROPLASTS 75-V (TOC75-V)/OUTER ENVELOPE PROTEIN OF 80 KDA (OEP80) complex has been implicated in the insertion and assembly of β-barrel proteins in the outer envelope membrane of Arabidopsis (Arabidopsis thaliana) chloroplasts, relatively little is known about this process. CRUMPLED LEAF (CRL) encodes a chloroplast outer envelope membrane-localized protein, and its loss-of-function mutation results in pleiotropic defects, including altered plant morphogenesis, growth retardation, suppression of plastid division, and spontaneous light intensity-dependent localized cell death. A suppressor screen conducted on mutagenized crl mutants revealed that a missense mutation in OEP80 suppresses the pleiotropic defects of crl. Furthermore, we found that OEP80 complex formation is compromised in crl. Additionally, we demonstrated that CRL interacts with OEP80 in vivo and that a portion of CRL is present at the same molecular weight as the OEP80 complex. Our results suggest that CRL interacts with OEP80 to facilitate its complex formation. CRL is involved in plastid protein import; therefore, the pleiotropic defects in crl are likely due to the combined effects of decreased plastid protein import and altered membrane integration of β-barrel proteins in the outer envelope membrane. This study sheds light on the mechanisms that allow β-barrel protein integration into the plastid outer envelope membrane and the importance of this finding for plant cellular processes.
MeSH term(s)	Arabidopsis/metabolism ; Arabidopsis Proteins/genetics ; Arabidopsis Proteins/metabolism ; Chloroplast Proteins/metabolism ; Chloroplasts/metabolism ; Membrane Proteins/metabolism ; Plastids/genetics ; Plastids/metabolism ; Protein Transport
Chemical Substances	Arabidopsis Proteins ; Chloroplast Proteins ; CRUMPLED LEAF protein, Arabidopsis ; Membrane Proteins ; OEP80 protein, Arabidopsis
Language	English
Publishing date	2024-01-03
Publishing country	United States
Document type	Journal Article
ZDB-ID	208914-2
ISSN	1532-2548 ; 0032-0889
ISSN (online)	1532-2548
ISSN	0032-0889
DOI	10.1093/plphys/kiae005
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Article ; Online: Histone Modification ChIP-seq on

Ramirez-Prado, Juan S / Latrasse, David / Benhamed, Moussa

Bio-protocol

2021 Volume 11, Issue 21, Page(s) e4211

Abstract: Characterizing the molecular mechanisms regulating gene expression is crucial for understanding the regulatory processes underlying physiological responses to environmental and developmental signals in eukaryotes. The covalent modification of histones ... ...

Abstract	Characterizing the molecular mechanisms regulating gene expression is crucial for understanding the regulatory processes underlying physiological responses to environmental and developmental signals in eukaryotes. The covalent modification of histones contributes to the compaction levels of chromatin, as well as the recruitment of the transcriptional machinery to specific loci, facilitating metastable changes in gene activity. ChIP-seq (Chromatin Immunoprecipitation followed by sequencing) has become the gold standard method for determining histone modification profiles among different organisms, tissues, and genotypes. In the current protocol, we describe a highly robust method for performing ChIP-seq of histone modifications in
Language	English
Publishing date	2021-11-05
Publishing country	United States
Document type	Journal Article
ZDB-ID	2833269-6
ISSN	2331-8325 ; 2331-8325
ISSN (online)	2331-8325
ISSN	2331-8325
DOI	10.21769/BioProtoc.4211
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Article ; Online: The plant POLYMERASE-ASSOCIATED FACTOR1 complex links transcription and H2B monoubiquitination genome wide.

Blanco-Touriñán, Noel / Pérez-Alemany, Jaime / Bourbousse, Clara / Latrasse, David / Ait-Mohamed, Ouardia / Benhamed, Moussa / Barneche, Fredy / Blázquez, Miguel A / Gallego-Bartolomé, Javier / Alabadí, David

Plant physiology

2024 Volume 195, Issue 1, Page(s) 640–651

Abstract: The evolutionarily conserved POLYMERASE-ASSOCIATED FACTOR1 complex (Paf1C) participates in transcription, and research in animals and fungi suggests that it facilitates RNA POLYMERASE II (RNAPII) progression through chromatin. We examined the genomic ... ...

Abstract	The evolutionarily conserved POLYMERASE-ASSOCIATED FACTOR1 complex (Paf1C) participates in transcription, and research in animals and fungi suggests that it facilitates RNA POLYMERASE II (RNAPII) progression through chromatin. We examined the genomic distribution of the EARLY FLOWERING7 (ELF7) and VERNALIZATION INDEPENDENCE3 subunits of Paf1C in Arabidopsis (Arabidopsis thaliana). The occupancy of both subunits was confined to thousands of gene bodies and positively associated with RNAPII occupancy and the level of gene expression, supporting a role as a transcription elongation factor. We found that monoubiquitinated histone H2B, which marks most transcribed genes, was strongly reduced genome wide in elf7 seedlings. Genome-wide profiling of RNAPII revealed that in elf7 mutants, RNAPII occupancy was reduced throughout the gene body and at the transcription end site of Paf1C-targeted genes, suggesting a direct role for the complex in transcription elongation. Overall, our observations suggest a direct functional link between Paf1C activity, monoubiquitination of histone H2B, and the transition of RNAPII to productive elongation. However, for several genes, Paf1C may also act independently of H2Bub deposition or occupy these genes more stable than H2Bub marking, possibly reflecting the dynamic nature of Paf1C association and H2Bub turnover during transcription.
MeSH term(s)	Histones/metabolism ; Arabidopsis/genetics ; Arabidopsis/metabolism ; Ubiquitination ; Arabidopsis Proteins/genetics ; Arabidopsis Proteins/metabolism ; RNA Polymerase II/metabolism ; RNA Polymerase II/genetics ; Transcription, Genetic ; Gene Expression Regulation, Plant ; Genome, Plant ; Transcription Factors/metabolism ; Transcription Factors/genetics
Chemical Substances	Histones ; Arabidopsis Proteins ; RNA Polymerase II (EC 2.7.7.-) ; Transcription Factors
Language	English
Publishing date	2024-01-29
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	208914-2
ISSN	1532-2548 ; 0032-0889
ISSN (online)	1532-2548
ISSN	0032-0889
DOI	10.1093/plphys/kiae041
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Article ; Online: RTEL1 is required for silencing and epigenome stability.

Olivier, Margaux / Hesketh, Amy / Pouch-Pélissier, Marie-Noëlle / Pélissier, Thierry / Huang, Ying / Latrasse, David / Benhamed, Moussa / Mathieu, Olivier

Nucleic acids research

2023 Volume 51, Issue 16, Page(s) 8463–8479

Abstract: Transcriptional silencing is an essential mechanism for controlling the expression of genes, transgenes and heterochromatic repeats through specific epigenetic marks on chromatin that are maintained during DNA replication. In Arabidopsis, silenced ... ...

Abstract	Transcriptional silencing is an essential mechanism for controlling the expression of genes, transgenes and heterochromatic repeats through specific epigenetic marks on chromatin that are maintained during DNA replication. In Arabidopsis, silenced transgenes and heterochromatic sequences are typically associated with high levels of DNA methylation, while silenced genes are enriched in H3K27me3. Reactivation of these loci is often correlated with decreased levels of these repressive epigenetic marks. Here, we report that the DNA helicase REGULATOR OF TELOMERE ELONGATION 1 (RTEL1) is required for transcriptional silencing. RTEL1 deficiency causes upregulation of many genes enriched in H3K27me3 accompanied by a moderate decrease in this mark, but no loss of DNA methylation at reactivated heterochromatic loci. Instead, heterochromatin exhibits DNA hypermethylation and increased H3K27me3 in rtel1. We further find that loss of RTEL1 suppresses the release of heterochromatin silencing caused by the absence of the MOM1 silencing factor. RTEL1 is conserved among eukaryotes and plays a key role in resolving DNA secondary structures during DNA replication. Inducing such aberrant DNA structures using DNA cross-linking agents also results in a loss of transcriptional silencing. These findings uncover unappreciated roles for RTEL1 in transcriptional silencing and in stabilizing DNA methylation and H3K27me3 patterns.
MeSH term(s)	Arabidopsis/metabolism ; Arabidopsis Proteins/metabolism ; DNA Methylation/genetics ; Epigenome ; Gene Silencing ; Heterochromatin/genetics ; Heterochromatin/metabolism ; Histones/genetics ; Histones/metabolism ; Telomere/metabolism ; DNA Helicases/metabolism
Chemical Substances	Arabidopsis Proteins ; Heterochromatin ; Histones ; RTEL1 protein, Arabidopsis (EC 3.6.4.-) ; DNA Helicases (EC 3.6.4.-)
Language	English
Publishing date	2023-09-08
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	186809-3
ISSN	1362-4962 ; 1362-4954 ; 0301-5610 ; 0305-1048
ISSN (online)	1362-4962 ; 1362-4954
ISSN	0301-5610 ; 0305-1048
DOI	10.1093/nar/gkad610
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Article ; Online: Distinctive and complementary roles of E2F transcription factors during plant replication stress responses.

Nisa, Maherun / Eekhout, Thomas / Bergis, Clara / Pedroza-Garcia, Jose-Antonio / He, Xiaoning / Mazubert, Christelle / Vercauteren, Ilse / Cools, Toon / Brik-Chaouche, Rim / Drouin-Wahbi, Jeannine / Chmaiss, Layla / Latrasse, David / Bergounioux, Catherine / Vandepoele, Klaas / Benhamed, Moussa / De Veylder, Lieven / Raynaud, Cécile

Molecular plant

2023 Volume 16, Issue 8, Page(s) 1269–1282

Abstract: Survival of living organisms is fully dependent on their maintenance of genome integrity, being permanently threatened by replication stress in proliferating cells. Although the plant DNA damage response (DDR) regulator SOG1 has been demonstrated to cope ...

Abstract	Survival of living organisms is fully dependent on their maintenance of genome integrity, being permanently threatened by replication stress in proliferating cells. Although the plant DNA damage response (DDR) regulator SOG1 has been demonstrated to cope with replication defects, accumulating evidence points to other pathways functioning independent of SOG1. Here, we report the roles of the Arabidopsis E2FA and EF2B transcription factors, two well-characterized regulators of DNA replication, in plant response to replication stress. Through a combination of reverse genetics and chromatin immunoprecipitation approaches, we show that E2FA and E2FB share many target genes with SOG1, providing evidence for their involvement in the DDR. Analysis of double- and triple-mutant combinations revealed that E2FB, rather than E2FA, plays the most prominent role in sustaining plant growth in the presence of replication defects, either operating antagonistically or synergistically with SOG1. Conversely, SOG1 aids in overcoming the replication defects of E2FA/E2FB-deficient plants. Collectively, our data reveal a complex transcriptional network controlling the replication stress response in which E2Fs and SOG1 act as key regulatory factors.
MeSH term(s)	Arabidopsis Proteins/genetics ; Arabidopsis Proteins/metabolism ; Arabidopsis/metabolism ; Transcription Factors/metabolism ; E2F Transcription Factors/genetics ; E2F Transcription Factors/metabolism ; Gene Expression Regulation, Plant/genetics
Chemical Substances	Arabidopsis Proteins ; Transcription Factors ; E2F Transcription Factors ; SOG1 protein, Arabidopsis
Language	English
Publishing date	2023-07-06
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2393618-6
ISSN	1752-9867 ; 1674-2052
ISSN (online)	1752-9867
ISSN	1674-2052
DOI	10.1016/j.molp.2023.07.002
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Article ; Online: The Arabidopsis APOLO and human UPAT sequence-unrelated long noncoding RNAs can modulate DNA and histone methylation machineries in plants.

Fonouni-Farde, Camille / Christ, Aurélie / Blein, Thomas / Legascue, María Florencia / Ferrero, Lucía / Moison, Michaël / Lucero, Leandro / Ramírez-Prado, Juan Sebastián / Latrasse, David / Gonzalez, Daniel / Benhamed, Moussa / Quadrana, Leandro / Crespi, Martin / Ariel, Federico

Genome biology

2022 Volume 23, Issue 1, Page(s) 181

Abstract: Background: RNA-DNA hybrid (R-loop)-associated long noncoding RNAs (lncRNAs), including the Arabidopsis lncRNA AUXIN-REGULATED PROMOTER LOOP (APOLO), are emerging as important regulators of three-dimensional chromatin conformation and gene ... ...

Abstract	Background: RNA-DNA hybrid (R-loop)-associated long noncoding RNAs (lncRNAs), including the Arabidopsis lncRNA AUXIN-REGULATED PROMOTER LOOP (APOLO), are emerging as important regulators of three-dimensional chromatin conformation and gene transcriptional activity. Results: Here, we show that in addition to the PRC1-component LIKE HETEROCHROMATIN PROTEIN 1 (LHP1), APOLO interacts with the methylcytosine-binding protein VARIANT IN METHYLATION 1 (VIM1), a conserved homolog of the mammalian DNA methylation regulator UBIQUITIN-LIKE CONTAINING PHD AND RING FINGER DOMAINS 1 (UHRF1). The APOLO-VIM1-LHP1 complex directly regulates the transcription of the auxin biosynthesis gene YUCCA2 by dynamically determining DNA methylation and H3K27me3 deposition over its promoter during the plant thermomorphogenic response. Strikingly, we demonstrate that the lncRNA UHRF1 Protein Associated Transcript (UPAT), a direct interactor of UHRF1 in humans, can be recognized by VIM1 and LHP1 in plant cells, despite the lack of sequence homology between UPAT and APOLO. In addition, we show that increased levels of APOLO or UPAT hamper VIM1 and LHP1 binding to YUCCA2 promoter and globally alter the Arabidopsis transcriptome in a similar manner. Conclusions: Collectively, our results uncover a new mechanism in which a plant lncRNA coordinates Polycomb action and DNA methylation through the interaction with VIM1, and indicates that evolutionary unrelated lncRNAs with potentially conserved structures may exert similar functions by interacting with homolog partners.
MeSH term(s)	Arabidopsis/genetics ; Arabidopsis/metabolism ; Arabidopsis Proteins/genetics ; Arabidopsis Proteins/metabolism ; CCAAT-Enhancer-Binding Proteins/genetics ; CCAAT-Enhancer-Binding Proteins/metabolism ; DNA/metabolism ; DNA Methylation ; Histones/metabolism ; Humans ; Indoleacetic Acids/metabolism ; Plants/genetics ; RNA, Long Noncoding/genetics ; RNA, Long Noncoding/metabolism ; Ubiquitin-Protein Ligases/genetics ; Ubiquitin-Protein Ligases/metabolism
Chemical Substances	Arabidopsis Proteins ; CCAAT-Enhancer-Binding Proteins ; Histones ; Indoleacetic Acids ; RNA, Long Noncoding ; DNA (9007-49-2) ; UHRF1 protein, human (EC 2.3.2.27) ; Ubiquitin-Protein Ligases (EC 2.3.2.27)
Language	English
Publishing date	2022-08-29
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2040529-7
ISSN	1474-760X ; 1474-760X
ISSN (online)	1474-760X
ISSN	1474-760X
DOI	10.1186/s13059-022-02750-7
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Article ; Online: The matrix revolutions: towards the decoding of the plant chromatin three-dimensional reality.

Huang, Ying / Rodriguez-Granados, Natalia Yaneth / Latrasse, David / Raynaud, Cecile / Benhamed, Moussa / Ramirez-Prado, Juan Sebastian

Journal of experimental botany

2020 Volume 71, Issue 17, Page(s) 5129–5147

Abstract: In recent years, we have witnessed a significant increase in studies addressing the three-dimensional (3D) chromatin organization of the plant nucleus. Important advances in chromatin conformation capture (3C)-derived and related techniques have allowed ... ...

Abstract	In recent years, we have witnessed a significant increase in studies addressing the three-dimensional (3D) chromatin organization of the plant nucleus. Important advances in chromatin conformation capture (3C)-derived and related techniques have allowed the exploration of the nuclear topology of plants with large and complex genomes, including various crops. In addition, the increase in their resolution has permitted the depiction of chromatin compartmentalization and interactions at the gene scale. These studies have revealed the highly complex mechanisms governing plant nuclear architecture and the remarkable knowledge gaps in this field. Here we discuss the state-of-the-art in plant chromosome architecture, including our knowledge of the hierarchical organization of the genome in 3D space and regarding other nuclear components. Furthermore, we highlight the existence in plants of topologically associated domain (TAD)-like structures that display striking differences from their mammalian counterparts, proposing the concept of ICONS-intergenic condensed spacers. Similarly, we explore recent advances in the study of chromatin loops and R-loops, and their implication in the regulation of gene activity. Finally, we address the impact that polyploidization has had on the chromatin topology of modern crops, and how this is related to phenomena such as subgenome dominance and biased gene retention in these organisms.
MeSH term(s)	Animals ; Cell Nucleus/genetics ; Chromatin/genetics ; Chromosomes, Plant ; Genome ; Plants/genetics
Chemical Substances	Chromatin
Language	English
Publishing date	2020-07-27
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2976-2
ISSN	1460-2431 ; 0022-0957
ISSN (online)	1460-2431
ISSN	0022-0957
DOI	10.1093/jxb/eraa322
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Article ; Online: The Seed Development Factors

Jacob, Pierre / Brisou, Gwilherm / Dalmais, Marion / Thévenin, Johanne / van der Wal, Froukje / Latrasse, David / Suresh Devani, Ravi / Benhamed, Moussa / Dubreucq, Bertrand / Boualem, Adnane / Lepiniec, Loic / Immink, Richard G H / Hirt, Heribert / Bendahmane, Abdelhafid

Genes

2021 Volume 12, Issue 5

Abstract: HEAT SHOCK FACTOR ... ...

Abstract	HEAT SHOCK FACTOR A2
MeSH term(s)	Arabidopsis ; Arabidopsis Proteins/genetics ; Arabidopsis Proteins/metabolism ; DNA-Binding Proteins/genetics ; DNA-Binding Proteins/metabolism ; Gene Expression Regulation, Plant ; Heat Shock Transcription Factors/genetics ; Heat Shock Transcription Factors/metabolism ; Heat-Shock Response ; Loss of Function Mutation ; Seeds/genetics ; Seeds/growth & development ; Transcriptome
Chemical Substances	Arabidopsis Proteins ; Atmyb5 protein, Arabidopsis ; DNA-Binding Proteins ; HSFA2 protein, Arabidopsis ; Heat Shock Transcription Factors ; TT2 protein, Arabidopsis
Language	English
Publishing date	2021-05-15
Publishing country	Switzerland
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2527218-4
ISSN	2073-4425 ; 2073-4425
ISSN (online)	2073-4425
ISSN	2073-4425
DOI	10.3390/genes12050746
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Article ; Online: The canonical E2Fs together with RETINOBLASTOMA-RELATED are required to establish quiescence during plant development.

Communications biology

2023 Volume 6, Issue 1, Page(s) 903

Abstract: Maintaining stable and transient quiescence in differentiated and stem cells, respectively, requires repression of the cell cycle. The plant RETINOBLASTOMA-RELATED (RBR) has been implicated in stem cell maintenance, presumably by forming repressor ... ...

Abstract	Maintaining stable and transient quiescence in differentiated and stem cells, respectively, requires repression of the cell cycle. The plant RETINOBLASTOMA-RELATED (RBR) has been implicated in stem cell maintenance, presumably by forming repressor complexes with E2F transcription factors. Surprisingly we find that mutations in all three canonical E2Fs do not hinder the cell cycle, but similarly to RBR silencing, result in hyperplasia. Contrary to the growth arrest that occurs when exit from proliferation to differentiation is inhibited upon RBR silencing, the e2fabc mutant develops enlarged organs with supernumerary stem and differentiated cells as quiescence is compromised. While E2F, RBR and the M-phase regulatory MYB3Rs are part of the DREAM repressor complexes, and recruited to overlapping groups of targets, they regulate distinct sets of genes. Only the loss of E2Fs but not the MYB3Rs interferes with quiescence, which might be due to the ability of E2Fs to control both G1-S and some key G2-M targets. We conclude that collectively the three canonical E2Fs in complex with RBR have central roles in establishing cellular quiescence during organ development, leading to enhanced plant growth.
MeSH term(s)	Humans ; Retinoblastoma/genetics ; Cell Division ; Cell Cycle/genetics ; Plant Development ; Retinal Neoplasms
Language	English
Publishing date	2023-09-04
Publishing country	England
Document type	Journal Article ; Research Support, U.S. Gov't, Non-P.H.S. ; Research Support, Non-U.S. Gov't
ISSN	2399-3642
ISSN (online)	2399-3642
DOI	10.1038/s42003-023-05259-2
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