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Uniparental chromosome elimination occurs in several interspecific hybrids of plants. We studied the mechanism underlying selective elimination of the paternal chromosomes during the early development of Hordeum vulgare x Hordeum bulbosum embryos. The following conclusions regarding the role of the centromere-specific histone H3 variant (CENH3) in the process of chromosome elimination were drawn: (i) centromere inactivity of H. bulbosum chromosomes triggers the mitosis-dependent process of uniparental chromosome elimination in unstable H. vulgare x H. bulbosum hybrids; (ii) centromeric loss of CENH3 protein rather than uniparental silencing of CENH3 genes causes centromere inactivity; (iii) in stable species combinations, cross-species incorporation of CENH3 occurs despite centromere-sequence differences, and not all CENH3 variants get incorporated into centromeres if multiple CENH3s are present in species combinations; and (iv) diploid barley species encode two CENH3 variants, the proteins of which are intermingled within centromeres throughout mitosis and meiosis.

Holocentric chromosomes occur in a number of independent eukaryotic lineages. They form holokinetic kinetochores along the entire poleward chromatid surfaces, and owing to this alternative chromosome structure, species with holocentric chromosomes cannot use the two-step loss of cohesion during meiosis typical for monocentric chromosomes. Here we show that the plant Luzula elegans maintains a holocentric chromosome architecture and behaviour throughout meiosis, and in contrast to monopolar sister centromere orientation, the unfused holokinetic sister centromeres behave as two distinct functional units during meiosis I, resulting in sister chromatid separation. Homologous non-sister chromatids remain terminally linked after metaphase I, by satellite DNA-enriched chromatin threads, until metaphase II. They then separate at anaphase II. Thus, an inverted sequence of meiotic sister chromatid segregation occurs. This alternative meiotic process is most likely one possible adaptation to handle a holocentric chromosome architecture and behaviour during meiosis. Conventionally, meiosis depends on a two-step loss of chromosome cohesion that requires distinction between chromosome arms and sister centromeres. Heckmann et al. show that a plant that lacks a single defined centromere overcomes this problem by inverting the sequence of meiotic segregation events.

silene latifolia (white campion) is a dioecious plant with heteromorphic sex chromosomes (24, XX in females and 24, XY in males), and a genetically degenerated Y chromosome that is 1.4 times larger than the X chromosome. Although the two sex chromosomes differ in their DNA content, information about epigenetic histone marks and evidence of their function are scarce. We performed immunolabeling experiments using antibodies specific for active and suppressive histone modifications as well as pericentromere-specific histone modifications. We show that the Y chromosome is partially depleted of histone modifications important for transcriptionally active chromatin, and carries these marks only in the pseudo-autosomal region, but that it is not enriched for suppressive and pericentromere histone marks. We also show that two of the active marks are specifically enriched in one of the X chromosomes in females and in the X chromosome in males. Our data support recent findings that genetic imprinting mediates dosage compensation of sex chromosomes in S. latifolia.

Centromeres are essential for kinetochore assembly and spindle attachment. While chromosomes of most species are monocentric with a single centromere, a minority exhibit holocentricity, with a centromere along the chromatid length. Sporadic emergence of holocentricity suggests multiple independent transitions. To explore this, we compare the centromere and (epi)genome organization of two sister genera with contrasting centromere types: Chamaelirium luteum with large macro-monocentromeres and Chionographis japonica with holocentromeres. Both exhibit chromosome-wide histone phosphorylation patterns distinct from typical monocentric species. Kinetochore analysis reveals similar chimeric Borealin in both species, with additional KNL2 loss and NSL1 chimerism in Cha. luteum . The broad-scale synteny between both genomes supports de novo holocentromere formation in Chi. japonica . Despite sharing features with both centromere types, macro-monocentromeres do not represent a direct link between mono- and holocentromeres. We propose a model for the divergent evolution involving kinetochore gene mutations, altered histone phosphorylation patterns, and centromeric satellite DNA amplification. Centromeres ensure chromosome segregation. Analyzed sister species with distinct centromere types show that kinetochore mutations, histone modifications, and centromeric DNA amplification underlie the process of mono- to holocentromere evolution.

Microgametogenesis in angiosperms results in two structurally and functionally different cells, one generative cell, which subsequently forms the sperm cells, and the vegetative cell. We analysed the chromatin properties of both types of nuclei after first and second pollen mitosis in rye ( Secale cereale ). The condensed chromatin of generative nuclei is earmarked by an enhanced level of histone H3K4/K9 dimethylation and H3K9 acetylation. The less condensed vegetative nuclei are RNA polymerase II positive. Trimethylation of H3K27 is not involved in transcriptional downregulation of genes located in generative nuclei as H3K27me3 was exclusively detected in the vegetative nuclei. The global level of DNA methylation does not differ between both types of pollen nuclei. In rye, unlike in Arabidopsis thaliana (Ingouff et al. Curr Biol 17:1032–1037 2007 ; Schoft et al. EMBO Rep 10:1015–1021 2009 ), centromeric histone H3 is not excluded from the chromatin of the vegetative nucleus and the condensation degree of centromeric and subtelomeric regions did not differ between the generative and vegetative nuclei. Differences between rye and A. thaliana data suggest that the chromatin organization in mature nuclei of pollen grains is not universal across angiosperms.

B chromosomes (Bs) are supernumerary components of the genome and do not confer any advantages on the organisms that harbor them. The maintenance of Bs in natural populations is possible by their transmission at higher than Mendelian frequencies. Although drive is the key for understanding B chromosomes, the mechanism is largely unknown. We provide direct insights into the cellular mechanism of B chromosome drive in the male gametophyte of rye (Secale cereale). We found that nondisjunction of Bs is accompanied by centromere activity and is likely caused by extended cohesion of the B sister chromatids. The B centromere originated from an A centromere, which accumulated B-specific repeats and rearrangements. Because of unequal spindle formation at the first pollen mitosis, nondisjoined B chromatids preferentially become located toward the generative pole. The failure to resolve pericentromeric cohesion is under the control of the B-specific nondisjunction control region. Hence, a combination of nondisjunction and unequal spindle formation at first pollen mitosis results in the accumulation of Bs in the generative nucleus and therefore ensures their transmission at a higher than expected rate to the next generation.

B chromosomes (Bs) are dispensable components of the genomes of numerous species. To test whether the transcriptome of a host is influenced by Bs, we looked for differences in expression in response to additional Bs. Comparative complementary DNA amplified fragment length polymorphism experiments resulted in the identification of 16 putative B-chromosome-associated transcripts. This comprises 0.7% of the total transcript number and indicates a low activity of Bs. We also provide evidence that B chromosome influences in trans the transcription of A chromosome sequences. The B-specific transcribed sequences B1334, B8149, and B2465 belong to high-copy families with similarity to mobile elements. For all analyzed B-chromosome-derived transcripts, similar A chromosome-encoded sequences were found which supports an A-derived origin of rye B chromosomes.

The B chromosome (B) is a dispensable component of the genome in many species. To evaluate the impact of Bs on the transcriptome of the standard A chromosomes (A), comparative RNA-seq analyses of rye and wheat anthers with and without additional rye Bs were conducted. In both species, 5–6% of the A-derived transcripts across the entire genomes were differentially expressed in the presence of  2Bs. The GO term enrichment analysis revealed that Bs influence A chromosome encoded processes like “gene silencing”; “DNA methylation or demethylation”; “chromatin silencing”; “negative regulation of gene expression, epigenetic”; “post-embryonic development”; and “chromosome organization.” 244 B chromosome responsive A-located genes in + 2B rye and + B wheat shared the same biological function. Positively correlated with the number of Bs, 939 and 1391 B-specific transcripts were identified in + 2B and + 4B wheat samples, respectively. 85% of B-transcripts in + 2B were also found in + 4B transcriptomes. 297 B-specific transcripts were identified in + 2B rye, and 27% were common to the B-derived transcripts identified in + B wheat. Bs encode mobile elements and housekeeping genes, but most B-transcripts were without detectable similarity to known genes. Some of these genes are involved in cell division-related functions like Nuf2 and might indicate their importance in maintaining Bs. The transcriptome analysis provides new insights into the complex interrelationship between standard A chromosomes and supernumerary B chromosomes.

B chromosomes (Bs) are dispensable, less-transcriptionally active components of the genomes of numerous species. Little information is available on the chromatin composition of Bs and whether it differs in any way from that of the A chromosomes. Methylated isoforms of histone H3 are of particular interest because of their role in eu/heterochromatin formation. Immunofluorescence using site-specific antibodies demonstrates that the chromatin in A and both types of Bs of B. dichromosomatica differs markedly in euchromatic histone H3 methylation marks. While A chromosomes are labelled brightly, the micro B and large B chromosomes are faintly labelled with antibodies against H3K4me2/3, H3K9me3 and H3K27me2/3. The heteropycnotic, tandem-repeat enriched micro Bs were even less labelled with euchromatic histone H3 methylation marks than large Bs, most probably due to different DNA composition. No differences in immunolabelling intensity between A and B chromosomes were found as to the heterochromatic marks H3K9me1/2 and H3K27me1, indicating that Bs are not additionally labelled by heterochromatin typical histone H3 modifications. Analysis of DNA replication timing suggests that micro Bs are replicating throughout S-phase.