Nondisjunction in Favor of a Chromosome: The Mechanism of Rye B Chromosome Drive during Pollen Mitosis

Banaei-Moghaddam, Ali Mohammad; Schubert, Veit; Kumke, Katrin; Weiβ, Oda; Klemme, Sonja; Nagaki, Kiyotaka; Macas, Jiří; González‐Sánchez, Mónica; Heredia, Victoria; Gómez-Revilla, Diana; González-García, M.; Vega, Maximiliano Rodrigo; Puertas, M. J.; Houben, Andreas

doi:10.1105/tpc.112.105270

Cited by 77 publications

(95 citation statements)

References 77 publications

Supporting

Mentioning

Contrasting

Unclassified

Order By: Relevance

“…In E. plorans , B chromosomes carrying active CIP2A and KIF20A genes could potentially influence the course of cell division for their own benefit, thus revealing their true parasitic nature. In rye, the presence of repetitive DNA sequences in the short arm of the B chromosome promotes mitotic nondisjunction which is the basis for its drive mechanism53. In E. plorans , B chromosome drive takes place during female meiosis2728, and the possibility of manipulating it through gene expression might be the basis for the high success of B chromosomes in this species, as they are present in almost all natural populations hitherto analyzed24.…”

Section: Discussionmentioning

confidence: 99%

Protein-coding genes in B chromosomes of the grasshopper Eyprepocnemis plorans

Navarro-Domínguez

Ruiz‐Ruano

Cabrero

et al. 2017

Sci Rep

View full text Add to dashboard Cite

For many years, parasitic B chromosomes have been considered genetically inert elements. Here we show the presence of ten protein-coding genes in the B chromosome of the grasshopper Eyprepocnemis plorans. Four of these genes (CIP2A, GTPB6, KIF20A, and MTG1) were complete in the B chromosome whereas the six remaining (CKAP2, CAP-G, HYI, MYCB2, SLIT and TOP2A) were truncated. Five of these genes (CIP2A, CKAP2, CAP-G, KIF20A, and MYCB2) were significantly up-regulated in B-carrying individuals, as expected if they were actively transcribed from the B chromosome. This conclusion is supported by three truncated genes (CKAP2, CAP-G and MYCB2) which showed up-regulation only in the regions being present in the B chromosome. Our results indicate that B chromosomes are not so silenced as was hitherto believed. Interestingly, the five active genes in the B chromosome code for functions related with cell division, which is the main arena where B chromosome destiny is played. This suggests that B chromosome evolutionary success can lie on its gene content.

show abstract

Section: Discussionmentioning

confidence: 99%

Protein-coding genes in B chromosomes of the grasshopper Eyprepocnemis plorans

Navarro-Domínguez

Ruiz‐Ruano

Cabrero

et al. 2017

Sci Rep

View full text Add to dashboard Cite

show abstract

“…Chromatin condensation has been shown to increase during pollen development and after microspore reprogramming and embryo cell differentiation [Testillano et al, 2000Seguí-Simarro et al, 2011;. Different patterns of chromatin condensation, DNA methylation, histone H3K9 methylation, and some H3 variants have also been found between the generative and the vegetative nuclei of mature pollen in different species [Houben et al, 2011;Seguí-Simarro et al, 2011;Banaei-Moghaddam et al, 2012;Solís et al, 2012;Hoffmann and Palmgren, 2013;González-Sánchez et al, this issue]. These differences have been related to different transcriptional activities and fates of both cells.…”

Section: Increase Of H3k9me2 During Microspore Embryogenesis Occurs Cmentioning

confidence: 99%

Changes in Histone Methylation and Acetylation during Microspore Reprogramming to Embryogenesis Occur Concomitantly with BnHKMT and BnHAT Expression and Are Associated with Cell Totipotency, Proliferation, and Differentiation in Brassica napus

Rodríguez-Sanz

Moreno‐Romero

Solís

et al. 2014

Cytogenet Genome Res

View full text Add to dashboard Cite

In response to stress treatments, microspores can be reprogrammed to become totipotent cells that follow an embryogenic pathway producing haploid and double-haploid embryos which are important biotechnological tools in plant breeding. Recent studies have revealed the involvement of DNA methylation in regulating this process, but no information is available on the role of histone modifications in microspore embryogenesis. Histone modifications are major epigenetic marks controlling gene expression during plant development and in response to environmental changes. Lysine methylation of histones, accomplished by histone lysine methyltransferases (HKMTs), can occur on different lysine residues, with histone H3K9 methylation being mainly associated with transcriptionally silenced regions. In contrast, histone H3 and H4 acetylation is carried out by histone acetyltransferases (HATs) and is associated with actively transcribed genes. In this work, we analyzed 3 different histone epigenetic marks: dimethylation of H3K9 (H3K9me2) and acetylation of H3 and H4 (H3Ac and H4Ac) during microspore embryogenesis in Brassica napus by Western blot and immunofluorescence assays. The expression patterns of histone methyltransferase BnHKMT and histone acetyltransferase BnHAT genes have also been analyzed by qPCR. Our results revealed different spatial and temporal distribution patterns for methylated and acetylated histone variants during microspore embryogenesis and their similarity with the expression profiles of BnHKMT and BnHAT, respectively. The data presented suggest the participation of H3K9me2 and HKMT in embryo cell differentiation and heterochromatinization events, whereas H3Ac, H4Ac, and HAT would be involved in transcriptional activation, totipotency, and proliferation events during cell reprogramming and embryo development.

show abstract

“…Based on these results, we have studied the patterns of H3K4me3 and H3K27me3 immunolabeling during microgametogenesis in rye plants with and without Bs. The interest on studying the possible effect of Bs is based on their special behavior during pollen mitosis, because rye Bs undergo nondisjunction directed to the generative pole, being present in a higher than Mendelian number in both sperm cells of the mature pollen grain [Muntzing, 1946;Banaei-Moghaddam et al, 2012]. The presence of Bs does not affect rye plant vigor but strongly affects fertility [Jiménez et al, 1994;Gonzá-lez-Sánchez et al, 2004a]; therefore it is reasonable to hypothesize possible differences in histone modifications between 0B and +B plants during pollen grain development, but there are not many effects in somatic tissues.…”

Section: Discussionmentioning

confidence: 99%

“…The B chromatids are normally included in both poles at the second pollen mitosis [Jones, 1991;Puertas, 2002]. Nondisjunction is not caused by inactivity of the B centromeres, because they show anti-CENH3 signals with the same intensity as the A centromeres during pollen mitosis [Banaei-Moghaddam et al, 2012]. Nondisjunction is likely caused by extended cohesion of the B sister chromatids.…”

mentioning

confidence: 99%

“…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 the first pollen mitosis results in the accumulation of Bs in the generative nucleus and therefore ensures their transmission at a higher than Mendelian rate to the next generation [Banaei-Moghaddam et al, 2012].…”

mentioning

confidence: 99%

See 1 more Smart Citation

Rye B Chromosomes Influence the Dynamics of Histone H3 Methylation during Microgametogenesis

González‐Sánchez

Heredia²,

Díez³

et al. 2014

Cytogenet Genome Res

Self Cite

View full text Add to dashboard Cite

We have studied the trimethylation dynamics of lysines 4 and 27 of histone H3 in rye with and without B chromosomes (Bs) in root tip mitosis, meiosis, and pollen grain mitosis by immunostaining. In root meristems, H3K4me3 immunolabeling was homogeneous along the chromosome arms of the normal complement (As), with the exception of the pericentromeric and subtelomeric regions which were unlabeled. On the contrary, a signal was observed on the long arm of the B chromosome, in the region where most of the B-specific repeats are located. H3K27me3 immunosignals were observed on the subtelomeric heterochromatic region of the As and the Bs and some interstitial bands of the As. Thus, the terminal region of the Bs showed both signals, whereas the subtelomeric region of the As showed H3K27me3 immunosignals only. During meiosis and first pollen grain mitosis, the immunosignals were observed distributed as in the root tip mitosis in plants with or without Bs. However, we observed remarkable changes in the immunolabeling patterns during the second pollen grain mitosis between 0B and +B plants. In 0B plants, H3K4me3 immunosignals were similarly distributed in the vegetative and generative nuclei. In B-carrying plants, the vegetative nucleus showed a lighter signal than the generative one. In 0B plants, all nuclei of the microgametophyte showed H3K27me3 immunosignals. In B-carrying plants, the generative nucleus and, correspondingly, the second metaphase, anaphase, and sperm nuclei did not show any signal. When the Bs were lost as micronuclei, they did not show any H3K4me3 or H3K27me3 signal. Most remarkably, Bs are able to change the pattern of H3 methylation on K4 and K27 during the second pollen mitosis, resulting in differently labeled sperm nuclei in 0 and +B plants.

show abstract

Nondisjunction in Favor of a Chromosome: The Mechanism of Rye B Chromosome Drive during Pollen Mitosis

Cited by 77 publications

References 77 publications

Protein-coding genes in B chromosomes of the grasshopper Eyprepocnemis plorans

Protein-coding genes in B chromosomes of the grasshopper Eyprepocnemis plorans

Changes in Histone Methylation and Acetylation during Microspore Reprogramming to Embryogenesis Occur Concomitantly with Bn<b><i>HKMT</i></b> and Bn<b><i>HAT</i></b> Expression and Are Associated with Cell Totipotency, Proliferation, and Differentiation in <b><i>Brassica napus</i></b>

Rye B Chromosomes Influence the Dynamics of Histone H3 Methylation during Microgametogenesis

Contact Info

Product

Resources

About