AGO104 is a RdDM effector of paramutation at the maize b1 locus

Aubert, Juliette; Bellegarde, Fanny; Oltehua-Lopez, Omar; Leblanc, Olivier; Arteaga-Vázquez, Mario; Martienssen, Robert A.; Grimanelli, Daniel

doi:10.1371/journal.pone.0273695

Cited by 4 publications

(3 citation statements)

References 48 publications

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“…AGO4 and its paralogs (AGO6 and AGO9) have been extensively studied in Arabidopsis using mutants (Havecker et al 2010 ; Duan et al 2015 ; Wang et al 2023 ). Contrarily, in monocotyledons, only rice and maize orthologs have been experimentally studied (Nonomura et al 2007 ; Kapoor et al 2008 ; Qian et al 2011 ; Yang et al 2013 ; Li et al 2019 ; Zhai et al 2019 ; Aubert et al 2022 ). Rice was found to have four different members of the AGO4 clade, namely AGO4A, AGO4B, AGO15, and AGO16.…”

Section: Introductionmentioning

confidence: 99%

Barley AGO4 proteins show overlapping functionality with distinct small RNA-binding properties in heterologous complementation

Miloro,

Kis,

Havelda

et al. 2024

Plant Cell Rep

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Key message Barley AGO4 proteins complement expressional changes of epigenetically regulated genes in Arabidopsis ago4-3 mutant and show a distinct affinity for the 5′ terminal nucleotide of small RNAs, demonstrating functional conservation and divergence. Abstract The function of Argonaute 4 (AGO4) in Arabidopsis thaliana has been extensively characterized; however, its role in monocots, which have large genomes abundantly supplemented with transposable elements (TEs), remains elusive. The study of barley AGO4 proteins can provide insights into the conserved aspects of RNA-directed DNA methylation (RdDM) and could also have further applications in the field of epigenetics or crop improvement. Bioinformatic analysis of RNA sequencing data identified two active AGO4 genes in barley, HvAGO4a and HvAGO4b. These genes function similar to AtAGO4 in an Arabidopsis heterologous complementation system, primarily binding to 24-nucleotide long small RNAs (sRNAs) and triggering methylation at specific target loci. Like AtAGO4, HvAGO4B exhibits a preference for binding sRNAs with 5′ adenine residue, while also accepting 5′ guanine, uracil, and cytosine residues. In contrast, HvAGO4A selectively binds only sRNAs with a 5′ adenine residue. The diverse binding capacity of barley AGO4 proteins is reflected in TE-derived sRNAs and in their varying abundance. Both barley AGO4 proteins effectively restore the levels of extrachromosomal DNA and transcript abundancy of the heat-activated ONSEN retrotransposon to those observed in wild-type Arabidopsis plants. Our study provides insight into the distinct binding specificities and involvement in TE regulation of barley AGO4 proteins in Arabidopsis by heterologous complementation.

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Section: Introductionmentioning

confidence: 99%

Barley AGO4 proteins show overlapping functionality with distinct small RNA-binding properties in heterologous complementation

Miloro,

Kis,

Havelda

et al. 2024

Plant Cell Rep

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“…Together, these genetic studies show that, similar to other cases of maize paramutation ( Dorweiler et al 2000 ; Alleman et al 2006 ; Erhard et al 2009 ; Stonaker et al 2009 ), establishment of p1 paramutation depends on RNA-mediated silencing mechanisms, while maintenance of P1-rr′ silencing has distinct genetic requirements that would benefit from additional studies. These additional studies may include factors that have been shown to regulate pl1 and b1 paramutations, including but not limited to PICKLE-like chromodomain DNA-binding 3 (CHD3) protein that is required to maintain pl1 paramutation but is dispensable for maintenance of b1 paramutation ( Deans et al 2020 ) and AGO104 that disrupts b1 paramutation ( Aubert et al 2022 ).…”

Section: Introductionmentioning

confidence: 99%

Transcribed enhancer sequences are required for maize p1 paramutation

Sidorenko,

Chandler,

Wang

et al. 2024

Genetics

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Paramutation is a transfer of heritable silencing states between interacting endogenous alleles or between endogenous alleles and homologous transgenes. Prior results demonstrated that paramutation occurs at the P1-rr (red pericarp and red cob) allele of the maize p1 (pericarp color 1) gene when exposed to a transgene containing a 1.2-kb enhancer fragment (P1.2) of P1-rr. The paramutable P1-rr allele undergoes transcriptional silencing resulting in a paramutant light-pigmented P1-rr′ state. To define more precisely the sequences required to elicit paramutation, the P1.2 fragment was further subdivided, and the fragments transformed into maize plants and crossed with P1-rr. Analysis of the progeny plants showed that the sequences required for paramutation are located within a ∼600-bp segment of P1.2 and that this segment overlaps with a previously identified enhancer that is present in 4 direct repeats in P1-rr. The paramutagenic segment is transcribed in both the expressed P1-rr and the silenced P1-rr′. Transcription is sensitive to α-amanitin, indicating that RNA polymerase II mediates most of the transcription of this sequence. Although transcription within the paramutagenic sequence was similar in all tested genotypes, small RNAs were more abundant in the silenced P1-rr′ epiallele relative to the expressed P1-rr allele. In agreement with prior results indicating the association of RNA-mediated DNA methylation in p1 paramutation, DNA blot analyses detected increased cytosine methylation of the paramutant P1-rr′ sequences homologous to the transgenic P1.2 subfragments. Together these results demonstrate that the P1-rr enhancer repeats mediate p1 paramutation.

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“…Additional proteins implicated in the repression of B´ include a putative maize ortholog of Arabidopsis ARGONAUTE9 (AGO9) (a member of the AGO4 clade), ZmAGO104, [ 43 ] and a novel protein isoform encoded by the unstable factor for orange1 ( ufo1 ) locus [ 44 , 45 ]. A dominant Ufo1-1 allele enhances the expression of both repressed B´ and p1 alleles through an unknown mechanism [ 44 ].…”

Section: Introductionmentioning

confidence: 99%

Paramutation at the maize pl1 locus is associated with RdDM activity at distal tandem repeats

Deans,

Talbot,

et al. 2024

PLoS Genet

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Exceptions to Mendelian inheritance often highlight novel chromosomal behaviors. The maize Pl1-Rhoades allele conferring plant pigmentation can display inheritance patterns deviating from Mendelian expectations in a behavior known as paramutation. However, the chromosome features mediating such exceptions remain unknown. Here we show that small RNA production reflecting RNA polymerase IV function within a distal downstream set of five tandem repeats is coincident with meiotically-heritable repression of the Pl1-Rhoades transcription unit. A related pl1 haplotype with three, but not one with two, repeat units also displays the trans-homolog silencing typifying paramutations. 4C interactions, CHD3a-dependent small RNA profiles, nuclease sensitivity, and polyadenylated RNA levels highlight a repeat subregion having regulatory potential. Our comparative and mutant analyses show that transcriptional repression of Pl1-Rhoades correlates with 24-nucleotide RNA production and cytosine methylation at this subregion indicating the action of a specific DNA-dependent RNA polymerase complex. These findings support a working model in which pl1 paramutation depends on trans-chromosomal RNA-directed DNA methylation operating at a discrete cis-linked and copy-number-dependent transcriptional regulatory element.

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AGO104 is a RdDM effector of paramutation at the maize b1 locus

Cited by 4 publications

References 48 publications

Barley AGO4 proteins show overlapping functionality with distinct small RNA-binding properties in heterologous complementation

Barley AGO4 proteins show overlapping functionality with distinct small RNA-binding properties in heterologous complementation

Transcribed enhancer sequences are required for maize p1 paramutation

Paramutation at the maize pl1 locus is associated with RdDM activity at distal tandem repeats

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