A null allele of the pol <scp>IV</scp> second subunit impacts stature and reproductive development in <i>Oryza sativa</i>

Chakraborty, Tania; Trujillo, Joshua T.; Kendall, Timmy; Mosher, Rebecca A.

doi:10.1111/tpj.15848

Cited by 10 publications

(12 citation statements)

References 64 publications

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“…Considering how RDR2 is linked to pol IV transcription, this observation is not surprising. Further, we observed that the nrp(d/e)2 sRNA datasets (Chakraborty et al 2022) indeed retained the pol IV suppressed loci, suggesting only a minor role of pol V in altering the chromatin state and the accumulation of these sRNAs (Fig. 3A).…”

Section: Resultsmentioning

confidence: 79%

Plant Polymerase IV sensitizes chromatin through histone modifications to preclude spread of silencing into protein-coding domains

G¹,

Swetha²,

Basu³

et al. 2021

Preprint

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Heterochromatin is the predominant architectural feature of genomes that ensures genomic stability across eukaryotes. It mostly functions in restricting expression of repeats, mobile elements such as transposons and other regions. The establishment, maintenance and spreading of heterochromatin requires several factors including chromatin modifiers. However, how exactly heterochromatin formation is avoided in protein-coding domains is poorly understood. Here we show that a plant specific paralogue of RNA polymerase (pol) II, named pol IV, is involved in avoidance of facultative heterochromatic marks in protein coding genes, in addition to silencing the repeats and transposons forming constitutive heterochromatin. In its absence, H3K27 trimethylation mark intrudes the protein coding genes, more profoundly in genes embedded with repeats. In a subset of genes that lack the compensatory silencing, spurious transcriptional activity results in small(s)RNA production leading to post-transcriptional gene silencing. We show that such effects are significantly pronounced in rice, a plant with larger genome with distributed heterochromatin when compared to Arabidopsis. Our results indicate the surprising division of labour among plant-specific polymerases, not just in establishing effective silencing via small RNAs and epigenetics, but also in influencing chromatin boundaries.

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Section: Resultsmentioning

confidence: 79%

Plant Polymerase IV sensitizes chromatin through histone modifications to preclude spread of silencing into protein-coding domains

G¹,

Swetha²,

Basu³

et al. 2021

Preprint

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“…3D). We also measured sRNA and DNA methylation levels using published datasets of several RdDM mutants (Wang et al, 2022; Hu et al, 2022; Chakraborty et al, 2022). We found that RdDM mutants such as rdr2 and nrp(d/e)2 show reduction of MITE derived sRNAs in the OsCLSY3 promoter, whereas, as expected, MITE derived sRNAs were unaltered in polv (Fig.…”

Section: Resultsmentioning

confidence: 99%

“…In rice too, RdDM pathway genes such as PolIV, RDR2, PolV regulate important agronomic traits such as panicle development, seed setting, pollen development etc. (Hari Sundar G et al, 2023; Wang et al, 2022; Higo et al, 2020; Zheng et al, 2021; Chakraborty et al, 2022). The guides for sRNA production in plants are a family of chromatin remodelers named CLSYs that regulate DNA methylation in a tissue- and locus-specific manner (Zhou et al, 2018, 2022).…”

Section: Discussionmentioning

confidence: 99%

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Upstream regulator of genomic imprinting in rice endosperm is a small RNA-associated chromatin remodeler

Pal,

Sundar G,

et al. 2023

Preprint

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Genomic imprinting is observed in endosperm, a placenta-like seed tissue, where transposable elements (TEs) and repeat-derived small(s)RNAs mediate epigenetic changes in plants. In imprinting, uniparental gene expression arises due to parent-specific epigenetic marks on one allele but not on the other. The importance of sRNAs and their regulation in endosperm development or in imprinting is poorly understood in crops. Here we show that a previously uncharacterized CLASSY (CLSY)-family chromatin remodeler named OsCLSY3 is essential for rice endosperm development and imprinting, acting as an upstream player in sRNA pathway. Comparative transcriptome and genetic analysis indicated its endosperm-preferred expression and its paternally imprinted nature. These important features were modulated by RNA-directed DNA methylation (RdDM) of tandemly arranged TEs in its promoter. Upon perturbation of OsCLSY3 in transgenic lines we observed defects in endosperm development and loss of around 70% of all sRNAs. Interestingly, well-conserved endosperm-specific sRNAs (siren) that are vital for reproductive fitness in angiosperms were dependent on OsCLSY3. We also observed many imprinted genes and seed development-associated genes under the control of CLSY3-dependent RdDM. These results support an essential role of OsCLSY3 in rice endosperm development and imprinting, and propose similar regulatory strategies involving CLSY3 homologs among other cereals.

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“…In contrast, Brassica rapa RdDM mutants are almost completely sterile and produce seeds that are smaller than wild type (Grover et al, 2018). Reproductive defects are also among the pleiotropic phenotypes observed in RdDM mutants of maize, tomato, and rice (Erhard et al, 2009; Gouil and Baulcombe, 2016; Xu et al, 2020; Zheng et al, 2021; Chakraborty et al, 2022; Wang et al, 2022).…”

Section: Introductionmentioning

confidence: 99%

Mating system is associated with seed phenotypes upon loss of RNA-directed DNA Methylation in Brassicaceae

Dew-Budd

Chow

Kendall

et al. 2023

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In plants, de novo DNA methylation is guided by 24-nt short interfering (si)RNAs in a process called RNA-directed DNA methylation (RdDM). Primarily targeted at transposons, RdDM causes transcriptional silencing and can indirectly influence expression of neighboring genes. During reproduction, a small number of siRNA loci are dramatically upregulation in the maternally-derived seed coat, suggesting that RdDM might have a special function during reproduction. However, the developmental consequence of RdDM has been difficult to dissect because disruption of RdDM does not result in overt phenotypes in Arabidopsis thaliana, where the pathway has been most thoroughly studied. In contrast, Brassica rapa mutants lacking RdDM have a severe seed production defect, which is determined by the maternal sporophytic genotype. To explore the factors that underlie the different phenotypes of these closely-related species, we produced RdDM mutations in three additional members of the Brassicaceae family: Camelina sativa, Capsella rubella, and Capsella grandiflora. Among these three species, only mutations in Capsella grandiflora displayed a seed production defect similar to Brassica rapa mutants, suggesting that mating system is a key determinant for reproductive phenotypes in RdDM mutants.

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A null allele of the pol IV second subunit impacts stature and reproductive development in Oryza sativa

Cited by 10 publications

References 64 publications

Plant Polymerase IV sensitizes chromatin through histone modifications to preclude spread of silencing into protein-coding domains

Plant Polymerase IV sensitizes chromatin through histone modifications to preclude spread of silencing into protein-coding domains

Upstream regulator of genomic imprinting in rice endosperm is a small RNA-associated chromatin remodeler

Mating system is associated with seed phenotypes upon loss of RNA-directed DNA Methylation in Brassicaceae

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