Increased Maternal Genome Dosage Bypasses the Requirement of the FIS Polycomb Repressive Complex 2 in Arabidopsis Seed Development

Kradolfer, David; Hennig, Lars; Köhler, Claudia

doi:10.1371/journal.pgen.1003163

Cited by 60 publications

(77 citation statements)

References 53 publications

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“…repressive chromatin modification H3K27me3 (18,19,48). Transcriptome profiling analysis on siliques suggested that CKX2 could respond to both parental genome balance and fis1/mea mutation (49).…”

Section: Resultsmentioning

confidence: 99%

“…The expression of MEA and FIS2 becomes imbalanced in response to maternal excess, and it was proposed that genes targeted by PRC2 depositing the repressive modification trimethylated lysine 27 on histone H3 (H3K27me3) might be responsible for the restriction of endosperm and seed growth (18). However, additional results have questioned this idea and proposed rather that the dosage of AGL62 and associated AGLs are primarily involved in responses to maternal dosage excess (19).…”

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confidence: 99%

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Integration of epigenetic and genetic controls of seed size by cytokinin in Arabidopsis

Nie

Tan

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

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The development of seeds in flowering plants is placed under complex interactions between maternal tissues, the embryo, and the endosperm. The endosperm plays a major role in the regulation of seed size. In Arabidopsis thaliana, endosperm size depends on the coordination of the genetic pathway HAIKU (IKU) with epigenetic controls comprising genome dosage, DNA methylation, and trimethylated lysine 27 on histone H3 (H3K27me3) deposition. However, the effectors that integrate these pathways have remained unknown. Here, we identify a target of the IKU pathway, the cytokinin oxidase CKX2, that affects cytokinin signaling. CKX2 expression is activated by the IKU transcription factor WRKY10 directly and promotes endosperm growth. CKX2 expression also depends on H3K27me3 deposition, which fluctuates in response to maternal genome dosage imbalance and DNA demethylation of male gametes. Hence, the control of endosperm growth by CKX2 integrates genetic and epigenetic regulations. In angiosperms, cytokinins are highly active in endosperm, and we propose that IKU effectors coordinate environmental and physiological factors, resulting in modulation of seed size.

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Section: Resultsmentioning

confidence: 99%

mentioning

confidence: 99%

Integration of epigenetic and genetic controls of seed size by cytokinin in Arabidopsis

Nie

Tan

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

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“…Perturbation of the machinery that contributes to gene expression in the endosperm can lead to alterations in seed size (Xiao et al 2006;Kradolfer et al 2013;Li et al 2013). To quantify the effect of PKL and/or PKR2 on seed size, we scored the mean seed areas of WT, pkl, pkr2, and pkl pkr2 seeds as described previously (Herridge et al 2011).…”

Section: Pkl and Pkr2 Antagonistically Influence Seed Sizementioning

confidence: 99%

“…However, we found no evidence of differences in embryo development or seed set in pkl pkr2 plants relative to pkl plants ( Figure S5 and Table S6). Thus, rather than observing phenotypic enhancement by the loss of both paralogs, our data indicated that these traits are not PKR2 dependent.Perturbation of the machinery that contributes to gene expression in the endosperm can lead to alterations in seed size (Xiao et al 2006;Kradolfer et al 2013;Li et al 2013). To quantify the effect of PKL and/or PKR2 on seed size, we scored the mean seed areas of WT, pkl, pkr2, and pkl pkr2 seeds as described previously (Herridge et al 2011).…”

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confidence: 99%

Cross-Talk Between Sporophyte and Gametophyte Generations Is Promoted by CHD3 Chromatin Remodelers inArabidopsis thaliana

et al. 2016

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Angiosperm reproduction requires the integrated development of multiple tissues with different genotypes. To achieve successful fertilization, the haploid female gametophytes and diploid ovary must coordinate their development, after which the male gametes must navigate through the maternal sporophytic tissues to reach the female gametes. After fertilization, seed development requires coordinated development of the maternal diploid integuments, the triploid endosperm, and the diploid zygote. Transcription and signaling factors contribute to communication between these tissues, and roles for epigenetic regulation have been described for some of these processes. Here we identify a broad role for CHD3 chromatin remodelers in Arabidopsis thaliana reproductive development. Plants lacking the CHD3 remodeler, PICKLE, exhibit various reproductive defects including abnormal development of the integuments, female gametophyte, and pollen tube, as well as delayed progression of ovule and embryo development. Genetic analyses demonstrate that these phenotypes result from loss of PICKLE in the maternal sporophyte. The paralogous gene PICKLE RELATED 2 is preferentially expressed in the endosperm and acts antagonistically with respect to PICKLE in the seed: loss of PICKLE RELATED 2 suppresses the large seed phenotype of pickle seeds. Surprisingly, the alteration of seed size in pickle plants is sufficient to determine the expression of embryonic traits in the seedling primary root. These findings establish an important role for CHD3 remodelers in plant reproduction and highlight how the epigenetic status of one tissue can impact the development of genetically distinct tissues. KEYWORDS PICKLE; PKR2; ovule; pollen tube; seed size D EVELOPMENT in multicellular organisms requires coordinated morphogenesis and communication between tissues with distinct gene expression profiles and occasionally distinct genotypes. Mutations in epigenetic regulators can perturb mutually dependent cell types and therefore complicate interpretation of the resulting phenotypes. The reproductive system of flowering plants presents an attractive context in which to distinguish autonomous phenotypes from those arising from defects in ancillary tissues. The haploid male and female gametophyte generation is contained within the diploid sporophyte, and development of these genetically distinct tissues is highly interdependent (Ma and Sundaresan 2010;Niklas and Kutschera 2010). The female gametophyte develops within the sporophytic ovary, where it forms into an embryo sac as it is surrounded by the diploid sporophytic integuments of the ovule (Bencivenga et al. 2011;Chevalier et al. 2011). Characterization of ovule-defective mutants in Arabidopsis thaliana has revealed that female gametophyte development is dependent on the sporophyte, particularly integument development, and has also identified a variety of factors that contribute to this relationship including transcription factors, kinases, and components of plant hormone signal transduction pathwa...

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“…In interploidy hybridizations, the parental genome contributions are altered, adding either one additional maternal or paternal copy to the embryo and endosperm, thereby creating either maternal or paternal excess hybridizations depending on whether the ovule donor or the pollen donor has a higher ploidy level. The parental genome dosage affects endosperm cellularization, a process essential for the formation of viable seeds (Scott et al, 1998;Hehenberger et al, 2012;Kradolfer et al, 2013a).…”

Section: Introductionmentioning

confidence: 99%

Hypomethylated Pollen Bypasses the Interploidy Hybridization Barrier inArabidopsis

et al. 2014

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Plants of different ploidy levels are separated by a strong postzygotic hybridization barrier that is established in the endosperm. Deregulated parent-of-origin specific genes cause the response to interploidy hybridizations, revealing an epigenetic basis of this phenomenon. In this study, we present evidence that paternal hypomethylation can bypass the interploidy hybridization barrier by alleviating the requirement for the Polycomb Repressive Complex 2 (PRC2) in the endosperm. PRC2 epigenetically regulates gene expression by applying methylation marks on histone H3. Bypass of the barrier is mediated by suppressed expression of imprinted genes. We show that the hypomethylated pollen genome causes de novo CHG methylation directed to FIS-PRC2 target genes, suggesting that different epigenetic modifications can functionally substitute for each other. Our work presents a method for the generation of viable triploids, providing an impressive example of the potential of epigenome manipulations for plant breeding.

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Increased Maternal Genome Dosage Bypasses the Requirement of the FIS Polycomb Repressive Complex 2 in Arabidopsis Seed Development

Cited by 60 publications

References 53 publications

Integration of epigenetic and genetic controls of seed size by cytokinin in Arabidopsis

Integration of epigenetic and genetic controls of seed size by cytokinin in Arabidopsis

Cross-Talk Between Sporophyte and Gametophyte Generations Is Promoted by CHD3 Chromatin Remodelers inArabidopsis thaliana

Hypomethylated Pollen Bypasses the Interploidy Hybridization Barrier inArabidopsis

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