Proper regulation of a sperm-specific <i>cis</i>-nat-siRNA is essential for double fertilization in <i>Arabidopsis</i>

Ron, Mily; Saez, Monica Alandete; Williams, Leor Eshed; Fletcher, Jennifer; McCormick, Susan P.

doi:10.1101/gad.1882810

Cited by 160 publications

(195 citation statements)

References 57 publications

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“…The kpl-1, tt16-2, tt16-3, ProFIS:FIS-GUS, and ProMEA:MEA-GUS lines are in the Ws-2 accession (Luo et al, 2000;Nesi et al, 2002;Ron et al, 2010). The agl62-2/+, mc1, lsd1, fie-12/+, msi1-1/+, fis2-5/+, goa-1, and ProFWA:FWA-GUS lines are in the Col-0 accession (Kinoshita et al, 2004;Coll et al, 2010;Prasad et al, 2010;Roszak and Köhler, 2011).…”

Section: Plant and Genetic Materialsmentioning

confidence: 99%

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Endosperm and Nucellus Develop Antagonistically in Arabidopsis Seeds

et al. 2016

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In angiosperms, seed architecture is shaped by the coordinated development of three genetically different components: embryo, endosperm, and maternal tissues. The relative contribution of these tissues to seed mass and nutrient storage varies considerably among species. The development of embryo, endosperm, or nucellus maternal tissue as primary storage compartments defines three main typologies of seed architecture. It is still debated whether the ancestral angiosperm seed accumulated nutrients in the endosperm or the nucellus. During evolution, plants shifted repeatedly between these two storage strategies through molecular mechanisms that are largely unknown. Here, we characterize the regulatory pathway underlying nucellus and endosperm tissue partitioning in Arabidopsis thaliana. We show that Polycomb-group proteins repress nucellus degeneration before fertilization. A signal initiated in the endosperm by the AGAMOUS-LIKE62 MADS box transcription factor relieves this Polycomb-mediated repression and therefore allows nucellus degeneration. Further downstream in the pathway, the TRANSPARENT TESTA16 (TT16) and GORDITA MADS box transcription factors promote nucellus degeneration. Moreover, we demonstrate that TT16 mediates the crosstalk between nucellus and seed coat maternal tissues. Finally, we characterize the nucellus cell death program and its feedback role in timing endosperm development. Altogether, our data reveal the antagonistic development of nucellus and endosperm, in coordination with seed coat differentiation.

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Section: Plant and Genetic Materialsmentioning

confidence: 99%

“…To investigate the role of each of the two fertilization events independently, we examined nucellus degeneration in the Arabidopsis kokopelli (kpl) mutant (Ron et al, 2010). kpl plants display random single-fertilization events that result in seeds carrying either the endosperm or the embryo.…”

Section: Fertilization Of the Central Cell Generates A Signal That Trmentioning

confidence: 99%

Endosperm and Nucellus Develop Antagonistically in Arabidopsis Seeds

et al. 2016

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“…In the RdDM pathway, both PolV-dependent nascent scaffold transcripts and hc-siRNAs are essential to guide de novo cytosine DNA methylation, which maintains the silencing of repeats (Wierzbicki et al, 2008;Wierzbicki et al, 2009). Nat-siRNAs are products of processed natural antisense transcripts and have been shown to be involved in plant stress resistance and reproduction (Borsani et al, 2005;Katiyar-Agarwal et al, 2006;Ron et al, 2010). ta-siRNAs are initiated by DCL1-dependent miRNA-guided cleavage of noncoding transcripts, which are then stabilized by SUPPRESSOR OF GENE SILENCING3 (SGS3) and converted to double-stranded RNA (dsRNA) by the actions of RDR6 (Peragine et al, 2004;Vazquez et al, 2004;Xie et al, 2004;Allen et al, 2005;Yoshikawa et al, 2005;Axtell et al, 2006).…”

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confidence: 99%

Roles of DICER-LIKE and ARGONAUTE Proteins in TAS-Derived Small Interfering RNA-Triggered DNA Methylation

2012

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Trans-acting small interfering RNAs (ta-siRNAs; TAS) emerge as a class of plant-specific small RNAs that are initiated from microRNA-mediated cleavage of TAS gene transcripts. It has been revealed that ta-siRNAs are generated by the sequential activities of SUPPRESSOR OF GENE SILENCING3 (SGS3), RNA-DEPENDENT RNA POLYMERASE6 (RDR6), and DICER-LIKE4 (DCL4), and loaded into ARGONAUTE1 (AGO1) proteins to posttranscriptionally regulate several target genes by messenger RNA cleavage in trans. Here, we showed a high cytosine DNA methylation status at ta-siRNA-generating loci in Arabidopsis (Arabidopsis thaliana), which is dependent on RDR6, SGS3, and DNA-DIRECTED RNA POLYMERASE V (PolV). More important, we found that DCL1 is the only DCL protein that is required for TAS3 loci DNA methylation, and all four DCLs exert combinatory functions in the methylation of TAS1 loci, suggesting a previously unknown role for DCL1 in directly processing TAS gene transcripts. Furthermore, we demonstrated that AGO4/6 complexes rather than AGO1 are responsible for TAS siRNA-guided DNA methylation. Based upon these findings, we propose a novel ta-siRNA pathway that acts at both the messenger RNA and chromatin level.

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“…The nat-siRNA biogenesis is dependent on DCL1, DCL2, and RDR6 (Borsani et al, 2005;Ron et al, 2010). Zhang et al (2012) also found that some nat-siRNAs were dependent on DCL1, DCL3, and RDR2.…”

Section: Mapping Srnas To Cis-natsmentioning

confidence: 97%

Protein-Coding cis-Natural Antisense Transcripts Have High and Broad Expression in Arabidopsis

Zhan

Lukens

2013

Plant Physiology

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Pairs of genes within eukaryotic genomes are often located on opposite DNA strands such that transcription generates cisnatural sense antisense transcripts (cis-NATs). This orientation of genes has been associated with the biogenesis of splice variants and natural antisense small RNAs. Here, in an analysis of currently available data, we report that within Arabidopsis (Arabidopsis thaliana), protein-coding cis-NATs are also characterized by high abundance, high coexpression, and broad expression. Our results suggest that a permissive chromatin environment may have led to the proximity of these genes. Compared with other genes, cis-NAT-encoding genes have enriched low-nucleosome-density regions, high levels of histone H3 lysine-9 acetylation, and low levels of H3 lysine-27 trimethylation. Promoters associated with broadly expressed genes are preferentially found in the 59 regulatory sequences of cis-NAT-encoding genes. Our results further suggest that natural antisense small RNA production from cis-NATs is limited. Small RNAs sequenced from natural antisense small RNA biogenesis mutants including dcl1, dcl2, dcl3, and rdr6 map to cis-NATs as frequently as small RNAs sequenced from wild-type plants. Future work will investigate if the positive transcriptional regulation of overlapping protein-coding genes contributes to the prevalence of these genes within other eukaryotic genomes.

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Proper regulation of a sperm-specific cis-nat-siRNA is essential for double fertilization in Arabidopsis

Cited by 160 publications

References 57 publications

Endosperm and Nucellus Develop Antagonistically in Arabidopsis Seeds

Endosperm and Nucellus Develop Antagonistically in Arabidopsis Seeds

Roles of DICER-LIKE and ARGONAUTE Proteins in TAS-Derived Small Interfering RNA-Triggered DNA Methylation

Protein-Coding cis-Natural Antisense Transcripts Have High and Broad Expression in Arabidopsis

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