Hypomethylated Pollen Bypasses the Interploidy Hybridization Barrier in<i>Arabidopsis</i>

Schatlowski, Nicole; Wolff, Philip; Santos‐González, Juan; Schoft, Vera K.; Siretskiy, Alexey; Scott, Rod; Tamaru, Hisashi; Köhler, Claudia

doi:10.1105/tpc.114.130120

Cited by 55 publications

(69 citation statements)

References 57 publications

Supporting

Mentioning

Contrasting

Unclassified

Order By: Relevance

“…Although we cannot rule out the possibility that the relative genome dosages of the two fertilization products to the maternal tissues or even to the female gametophyte (Birchler 2014) cause the seed defects of interploidy cross, it has been speculated that the unbalanced parental genomes cause arrested embryo and disruptive seed development primarily via the unbalanced contributions of parentally expression-biased genes (imprinted genes) and altered endosperm development, as indicated by a detailed genetic analysis in maize and Arabidopsis (Lin 1984; Scott et al 1998). This notion is also supported by the studies in Arabidopsis where knocking-out endosperm specific imprinted genes or regulators of imprinting can alleviate endosperm abortion and promote seed viability in interploidy crosses (Erilova et al 2009; Kradolfer et al 2013a; 2013b; Schatlowski et al 2014). Our observations support the differential roles of the maternal and paternal genomes in endosperm development (Haig and Westoby 1989; 1991; Dilkes and Comai 2004): excess maternal genome drives the precocious endosperm cellularization and excess paternal genome delays or disrupts cellularization, implying the possible roles of imprinting involved in mediating parent-of-origin effects on seed development in different species.…”

Section: Discussionmentioning

confidence: 86%

“…Increasing the ploidy level of one parent in an interspecific cross was able to improve the viability of hybrid seeds (Johnston et al 1980; Josefsson et al 2006), suggesting that there are common mechanisms underlying endosperm abortion in response to both interploidy and interspecific crosses (Haig and Westoby 1991; Schatlowski and Köhler 2012). Imprinting and epigenetic mechanisms regulating imprinting are the promising mechanisms controlling both interspecific and interploidy postzygotic hybridization barrier (Haig and Westoby 1991; Erilova et al 2009; Kradolfer et al 2013a; Schatlowski et al 2014). We reason that low conservation of imprinted genes across species (Luo et al 2011; Waters et al 2011; Wolff et al 2011) contributes to reproductive isolation between related species.…”

Section: Discussionmentioning

confidence: 99%

See 1 more Smart Citation

Parental Genome Imbalance Causes Post-Zygotic Seed Lethality and Deregulates Imprinting in Rice

Zhang

Luo

Johnson

et al. 2016

Rice

View full text Add to dashboard Cite

BackgroundReproductive isolation between rice of different ploidy levels is manifested as endosperm and embryo abortion in seeds produced by interploidy crosses. Genomic imprinting is considered to be the underlying mechanism establishing the post-zygotic hybridization barrier. We characterized disrupted seed development in reciprocal crosses between a diploid Japonica rice and a tetraploid Indica rice.ResultsTriploid seeds from these crosses had aborted development and could not germinate in soil but could be rescued in culture medium with significantly more seeds developing to seedlings in the 4n × 2n (♀-♂) cross with excess maternal genomes than in the 2n × 4n cross with excess paternal genome. Consistent with previous findings, precocious endosperm cellularization and bigger embryos were observed in the seeds from the maternal excess cross, whereas absence of cellularization and arrested globular embryos were found in the seeds from the paternal excess cross, supporting the idea that endosperm cellularization is an important transition for embryo development. Moreover, we found that starch granules were persistently deposited in the pericarp parenchyma cells of the paternal excess cross, while pericarp starch gradually decreased and relocated to the developing endosperm in balanced and maternal excess crosses in which cellularization and starch deposition occur in endosperm, suggesting that parental genome balance influences pericarp starch relocation via cellularization and starch deposition. Loss of imprinting, or altered expression of imprinted genes and epigenetic regulators, OsFIE2 and OsMET1b were observed, implying the potential role of imprinting and epigenetic mechanisms in regulating the differential parental genome dosage effects on endosperm development.ConclusionsOur results support the hypothesis that the maternal genome dosage promotes endosperm cellularization and the paternal genome dosage delays or inhibits cellularization via contributing different sets of imprinted genes.Electronic supplementary materialThe online version of this article (doi:10.1186/s12284-016-0115-4) contains supplementary material, which is available to authorized users.

show abstract

Section: Discussionmentioning

confidence: 86%

Section: Discussionmentioning

confidence: 99%

Parental Genome Imbalance Causes Post-Zygotic Seed Lethality and Deregulates Imprinting in Rice

Zhang

Luo

Johnson

et al. 2016

Rice

View full text Add to dashboard Cite

show abstract

“…The data of 6-DAP bisulfite-treated samples have been published previously (Schatlowski et al 2014). RNA sequencing data used in this study have been published previously (Wolff et al 2015).…”

Section: Bioinformatic Analysismentioning

confidence: 99%

Ectopic application of the repressive histone modification H3K9me2 establishes post-zygotic reproductive isolation inArabidopsis thaliana

et al. 2017

Self Cite

View full text Add to dashboard Cite

Hybrid seed lethality as a consequence of interspecies or interploidy hybridizations is a major mechanism of reproductive isolation in plants. This mechanism is manifested in the endosperm, a dosage-sensitive tissue supporting embryo growth. Deregulated expression of imprinted genes such as ADMETOS (ADM) underpin the interploidy hybridization barrier in Arabidopsis thaliana; however, the mechanisms of their action remained unknown. In this study, we show that ADM interacts with the AT hook domain protein AHL10 and the SET domain-containing SU (VAR)3-9 homolog SUVH9 and ectopically recruits the heterochromatic mark H3K9me2 to AT-rich transposable elements (TEs), causing deregulated expression of neighboring genes. Several hybrid incompatibility genes identified in Drosophila encode for dosage-sensitive heterochromatin-interacting proteins, which has led to the suggestion that hybrid incompatibilities evolve as a consequence of interspecies divergence of selfish DNA elements and their regulation. Our data show that imbalance of dosage-sensitive chromatin regulators underpins the barrier to interploidy hybridization in Arabidopsis, suggesting that reproductive isolation as a consequence of epigenetic regulation of TEs is a conserved feature in animals and plants.

show abstract

“…Retention of CG gene body methylation on the paternal alleles of PEGs (Figure 4) could possibly protect them from gain of CHG methylation. Interestingly, gain of gene body CHG methylation was also recently shown to occur in both A. thaliana endosperm and embryos when wild type plants were pollinated by diploid hypomethylated pollen 26 . Diploid pollen creates triploid seeds with tetraploid endosperm that usually abort, but seed abortion is suppressed when the pollen is hypomethylated due to mutations in met1 .…”

mentioning

confidence: 94%

Conserved imprinting associated with unique epigenetic signatures in the Arabidopsis genus

2016

View full text Add to dashboard Cite

In plants, imprinted gene expression occurs in endosperm seed tissue and is sometimes associated with differential DNA methylation between maternal and paternal alleles1. Imprinting is theorized to have been selected for because of conflict between parental genomes in offspring2, but most studies of imprinting have been conducted in Arabidopsis thaliana, an inbred primarily self-fertilizing species that should have limited parental conflict. We examined embryo and endosperm allele-specific expression and DNA methylation genome-wide in the wild outcrossing species Arabidopsis lyrata. Here we show that the majority of A. lyrata imprinted genes also exhibit parentally-biased expression in A. thaliana, suggesting that there is evolutionary conservation in gene imprinting. Surprisingly, we discovered substantial interspecies differences in methylation features associated with paternally expressed imprinted genes (PEGs). Unlike in A. thaliana, the maternal allele of many A. lyrata PEGs was hypermethylated in the CHG context. Increased maternal allele CHG methylation was associated with increased expression bias in favor of the paternal allele. We propose that CHG methylation maintains or reinforces repression of maternal alleles of PEGs. These data suggest that while the genes subject to imprinting are largely conserved, there is flexibility in the epigenetic mechanisms employed between closely related species to maintain monoallelic expression. This supports the idea that imprinting of specific genes is a functional phenomenon, and not simply a byproduct of seed epigenomic reprogramming.

show abstract

Hypomethylated Pollen Bypasses the Interploidy Hybridization Barrier inArabidopsis

Cited by 55 publications

References 57 publications

Parental Genome Imbalance Causes Post-Zygotic Seed Lethality and Deregulates Imprinting in Rice

Parental Genome Imbalance Causes Post-Zygotic Seed Lethality and Deregulates Imprinting in Rice

Ectopic application of the repressive histone modification H3K9me2 establishes post-zygotic reproductive isolation inArabidopsis thaliana

Conserved imprinting associated with unique epigenetic signatures in the Arabidopsis genus

Contact Info

Product

Resources

About