Epigenetic Patterns in Genetically Imbalanced Polyploid Dog Rose Hybrids (<i>Rosa</i> L. sect. <i>Caninae</i> (DC.) Ser.) Revealed by <scp>c</scp>DNA–Amplified Fragment Length Polymorphisms and Methylation-Sensitive Amplified Polymorphisms

Vogt, Janina C.; Herklotz, Veit; Ritz, Christiane M.

doi:10.1086/680725

Cited by 5 publications

(4 citation statements)

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“…Within each subsection several micro‐species are distinguished by fruit characters (Henker, ). Previous studies at the site revealed that some micro‐species represent spontaneous F1‐hybrids between subsections (Herklotz and Ritz, ; Vogt et al ., ). In this study we analysed three hybrid plants: one 5x (2 n = 5x = 35) individual of R. dumalis Bechst.…”

Section: Methodsmentioning

confidence: 97%

“…These studies focussed either on established dogroses species or on synthetic hybrids; however, also ongoing spontaneous hybridization is frequent and contributes substantially to the diversity of extant dogroses (Schanzer and Vagina, ; Schanzer and Kutlunina, ; Ritz and Wissemann, ; Herklotz and Ritz, , ). Expression patterns of anonymous markers (cDNA‐AFLPs and MSAPs) in such a hybrid population were mostly additive, but also tissue‐specific effects were observed (Vogt et al ., ).…”

Section: Introductionmentioning

confidence: 97%

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The fate of ribosomal RNA genes in spontaneous polyploid dogrose hybrids [Rosa L. sect. Caninae (DC.) Ser.] exhibiting non‐symmetrical meiosis

et al. 2018

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Dogroses represent an exceptional system for studying the effects of genome doubling and hybridization: their asymmetrical meiosis enables recombination in bi-parentally inherited chromosomes but prevents it in maternally inherited ones. We employed fluorescent in situ hybridization, genome skimming, amplicon sequencing of genomic and cDNA as well as conventional cloning of nuclear ribosomal DNA in two phylogenetically distinct pentaploid (2n = 5x = 35) species, Rosa canina and Rosa inodora, and their naturally occurring reciprocal hybrids, Rosa dumalis (5x) and Rosa agrestis (5x, 6x). Both progenitor species differed in composition, meiotic behaviour and expression of rDNA loci: R. canina (five 18S and 5-8 5S loci) was dominated by the Canina ribotypes, but R. inodora (four 18S loci and 7-8 5S loci) by the Rubiginosa ribotype. The co-localized 5S/18S loci occurred on either bivalent-forming (R. canina) or univalent-forming (R. inodora) chromosomes. Ribosomal DNA loci were additively inherited; however, the Canina ribotypes were dominantly expressed, even in genotypes with relatively low copy number of these genes. Moreover, we observed rDNA homogenization towards the paternally transmitted Canina ribotype in 6x R. agrestis. The here-observed variation in arrangement and composition of rDNA types between R. canina and R. inodora suggests the involvement of different genomes in bivalent formation. This results supports the hypothesis that the asymmetrical meiosis arose at least twice by independent ancient hybridization events.

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Section: Methodsmentioning

confidence: 97%

Section: Introductionmentioning

confidence: 97%

The fate of ribosomal RNA genes in spontaneous polyploid dogrose hybrids [Rosa L. sect. Caninae (DC.) Ser.] exhibiting non‐symmetrical meiosis

et al. 2018

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“…display retarded migration compared with that of bivalents in the first meiotic division. The expression activity of genes located on univalent chromosomes has been debated considerably ( Darlington, 1965 ; Khaitová et al , 2010 ; Ritz et al , 2011 ; Vogt et al , 2015 ). Earlier studies suggested these chromosomes to be primarily inactive and heterochromatic ( Darlington, 1965 ), whereas more recent studies revealed transcriptional activity of genes encoded by chromosomes forming univalents ( Ritz et al , 2011 ; Herklotz et al , 2018 ).…”

Section: Introductionmentioning

confidence: 99%

Epigenetic histone H3 phosphorylation marks discriminate between univalent- and bivalent-forming chromosomes during canina asymmetrical meiosis

Kalfusová,

Herklotz,

Kumke

et al. 2023

Annals of Botany

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Background and aims Dogroses (Rosa sect. Caninae) are mostly pentaploid, bearing 2n = 5x = 35 chromosomes in somatic cells. They evolved a unique form of asymmetrical meiosis characterized by two types of chromosomes: (i) chromosomes forming bivalents and distributed in the normal sexual way and (ii) chromosomes occurring as univalents and transferred by a female gamete only. In the mature pollen of pentaploid species, seven bivalent-derived chromosomes are transmitted to offspring, while 21 unpaired univalent chromosomes are eliminated during microsporogenesis. To discriminate between bivalent- and univalent-forming chromosomes, we studied histone H3 phosphorylation patterns regulating meiotic chromosome condensation and segregation. Methods We analysed histone modification patterns during male canina meiosis in two representative dogrose species, 5x Rosa canina and 5x R. rubiginosa, by immunohistochemical and molecular cytogenetics approaches. Immunostaining of meiotic cells included alpha-tubulin, histone H3 phosphorylation (H3S10p, H3S28p, H3T3p) and methylation (H3K4me3, H3K27me3) marks. In addition, fluorescent in situ hybridization (FISH) was carried out with an 18S rDNA probe. Key results In the first meiotic division, univalent chromosomes underwent equational division into chromatids, while homologues in bivalents were segregated as regular dyads. In diakinesis, bivalent chromosomes displayed strong H3 phosphorylation signals in proximal regions, spreading to the rest of the chromosome. In contrast, in univalents, the H3 phosphorylation signals were weaker, occurring mostly outside proximal regions largely overlapping with the H3K4me3 signals. Reduced phosphorylation was associated with relative under condensation of the univalent chromosomes, particularly at early diakinesis. Conclusions We hypothesize that the absence of pairing and/or recombination in univalent chromosomes negatively affects the histone H3 phosphorylation of their chromatin and perhaps the loading of meiotic-specific cohesins. This apparently destabilizes cohesion of sister chromatids, leading to their premature split in the first meiotic division.

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“…The mechanism of asymmetric meiosis remains unresolved in ACAs, despite the comprehensive investigation of chromosome inheritance, morphological and genetic patterns, at least in the dog rose Rosa canina complex (33)(34)(35)(36)(37)(38). On the one hand, asymmetric meiosis ensures reassortment of some of the genetic material and preserves correct chromosome composition in the male and female gametes; on the other hand, it ensures a mixed karyotype in the progeny.…”

Section: Introductionmentioning

confidence: 99%

Flow cytometric seed screen data are consistent with models of chromosome inheritance in asymmetrically compensating allopolyploids

Kolarčik¹,

Kocová²,

Vašková³

2018

Cytometry Pt A

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Angiosperms have evolved a mechanism of double fertilization, which results in the production of a separate embryo (new individual) and endosperm (nutritive tissue). The flow cytometric seed screen (FCSS) was developed to infer plant reproduction modes based on endosperm-to-embryo DNA content ratio (P ). A ratio of 1.5 indicates sexual reproduction, whereas higher values of ≥2.0 are consistent with apomixis. Although FCSS has been successfully applied to the study of sexual and asexual plants, the limits of FCSS and particularly its potential for determination of reproduction modes in hemisexual plants have not been explored. Here, we evaluated the application of FCSS to the study of reproduction modes in two asymmetrically compensating allopolyploids (ACAs), Onosma arenaria and Rosa canina. These two species are characterized by the presence of asexually inherited univalent-forming and sexually inherited bivalent-forming chromosome sets. They both use asymmetric meiosis, which eliminates univalent-forming chromosome sets from the male gamete and retains them in the female gamete. Different chromosomal behavior in male and female meiosis in these plants is reflected in different theoretically derived P values, which deviate from a sexual 1.5 value. Here, we determined P FCSS-based values in seeds of ACAs, and compared the results to sexual species. As expected, we determined that the mean P is 1.51, 1.52, and 1.52 in the sexual plants, that is, Capsella bursa-pastoris, Crataegus monogyna, and O. pseudoarenaria, respectively. In the ACAs, different mean P values were determined for O. arenaria (1.61) and R. canina (1.82). These values are consistent with the theoretical P values determined based on models of chromosome inheritance. This study highlights the precision of flow cytometry in determining DNA content and it's utility in screening reproduction modes. Additionally, it advocates for more in-depth investigations into rapid screening of accessions where the P ratio has deviated from the 1.5 value typical of sexual species, which may indicate meiotic irregularities.

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Epigenetic Patterns in Genetically Imbalanced Polyploid Dog Rose Hybrids (Rosa L. sect. Caninae (DC.) Ser.) Revealed by cDNA–Amplified Fragment Length Polymorphisms and Methylation-Sensitive Amplified Polymorphisms

Cited by 5 publications

References 62 publications

The fate of ribosomal RNA genes in spontaneous polyploid dogrose hybrids [Rosa L. sect. Caninae (DC.) Ser.] exhibiting non‐symmetrical meiosis

The fate of ribosomal RNA genes in spontaneous polyploid dogrose hybrids [Rosa L. sect. Caninae (DC.) Ser.] exhibiting non‐symmetrical meiosis

Epigenetic histone H3 phosphorylation marks discriminate between univalent- and bivalent-forming chromosomes during canina asymmetrical meiosis

Flow cytometric seed screen data are consistent with models of chromosome inheritance in asymmetrically compensating allopolyploids

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