The dynamics of histone H3 modifications is species-specific in plant meiosis

Abstract

Different histone modifications often modify DNA-histone interactions affecting both local and global structure of chromatin, thereby providing a vast potential for functional responses. Most studies have focused on the role of several modifications in gene transcription regulation, being scarce on other aspects of eukaryotic chromosome structure during cell division, mainly in meiosis. To solve this issue we have performed a cytological analysis to determine the chromosomal distribution of several histone H3 modifications throughout all phases of both mitosis and meiosis in different plant species. We have chosen Aegilops sp. and Secale cereale (monocots) and Arabidopsis thaliana (dicots) because they differ in their phylogenetic affiliation as well as in content and distribution of constitutive heterochromatin. In the species analyzed, the patterns of H3 acetylation and methylation were held constant through mitosis, including modifications associated with "open chromatin". Likewise, the immunolabeling patterns of H3 methylation remained invariable throughout meiosis in all cases. On the contrary, there was a total loss of acetylated H3 immunosignals on condensed chromosomes in both meiotic divisions, but only in monocot species. Regarding the phosphorylation of histone H3 at Ser10, present on condensed chromosomes, although we did not observe any difference in the dynamics, we found slight differences between the chromosomal distribution of this modification between Arabidopsis and cereals (Aegilops sp. and rye). Thus far, in plants chromosome condensation throughout cell division appears to be associated with a particular combination of H3 modifications. Moreover, the distribution and dynamics of these modifications seem to be species-specific and even differ between mitosis and meiosis in the same species.

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

“…The results of this work coincide with previous reports on rye plants in mitosis and meiosis [Carchilan et al, 2007;Oliver et al, 2013], irrespective of the presence of Bs. However, we report that the rye Bs produce a remarkably different pattern of H3K4me3 and H3K27me3 immunolabeling during microgametogenesis, from the stage of bicellular pollen onwards.…”

“…Most studies on histone H3 modifications in plants have been reported in somatic cells [Fuchs et al, 2006], but references to epigenetic modifications during meiosis [Oliver et al, 2013] and particularly during microgametogenesis are scarce. The immunolabeling technique, which uses specific antibodies for localizing different types of histone modifications in situ, is extremely useful to be applied to mitotic or meiotic cells but difficult to apply to anthers during pollen grain mitosis.…”

DNA Crossover Motifs Associated with Epigenetic Modifications Delineate Open Chromatin Regions in Arabidopsis

“…Thus, some reprogramming of epigenetic marks during meiosis, which might have affected our analysis, cannot be ruled out. However, some degree of conservation of the epigenetic patterns and especially of H3 methylations during plant development, including during meiosis, is expected (Feng et al, 2010;Oliver et al, 2013), in contrast to the extensive epigenetic reprogramming found in animals during meiosis (Sasaki and Matsui, 2008).…”

Histone Phosphorylation: Its Role during Cell Cycle and Centromere Identity in Plants

“…At metaphase, the pericentromeric region shows the most intense phosphorylation signals in mono-and dicot plants (Hordeum vulgare , Secale cereale , Vicia faba) [Houben et al, 1999]. Meanwhile, H3S10ph is initiated at the transition from leptotene to zygotene and terminated toward interkinesis during the first meiotic division; it only occurs at pericentromeric regions from prophase II until telophase II in rye (S. cereale) and wheat (Triticum aestivum) [Manzanero et al, 2000;Oliver et al, 2013]. By using an antibody that specifically recognizes H3S10ph in maize, Kaszás and Cande [2000] found that only pericentromeric regions are stained and very few signals are present on the chromosome arm during mitosis.…”

“…During meiosis, H3T3ph first appears in diakinesis and extends to AI, whereas in the second division the signals are visible at MII through AII. However, the dephosphorylation occurs at AI and AII in A. thaliana [Caperta et al, 2008;Oliver et al, 2013]. H3T3ph occurs along entire chromosome arms in plants and is associated with mitotic and meiotic chromosome condensation [Houben et al, 2007].…”