Histone H3 Methylation and Autosomal vs. Sex Chromosome Segregation During Male Meiosis in Heteroptera

María Ayelen Toscani,Alba G Papeschi,María José Bressa,María Inés Pigozzi

doi:10.3389/fevo.2022.836786

Abstract

Heteropteran insects exhibit a remarkable diversity of meiotic processes, including coexistence of different chromosomes types with different behavior during the first meiotic division, non-chiasmatic segregation, and inverted meiosis. Because of this diversity they represent suitable models to study fundamental questions about the mechanisms of chromosome behavior during cell division. All heteropteran species possess holokinetic chromosomes and in most of them the autosomal chromosomes synapse, recombine, and undergoe pre-reductional meiosis. In contrast, the sex chromosomes are achiasmatic, behave as univalents at metaphase I and present an inverted or post-reductional meiosis. An exception to this typical behavior is found in Pachylis argentinus, where both the autosomes and the X-chromosome divide reductionally at anaphase I and then divide equationally at anaphase II. In the present report, we analyzed the distribution of histones H3K9me2 and H3K9me3 in P. argentinus and in five species that have simple and multiple sex chromosome systems with typical chromosome segregation, Belostoma elegans, B. oxyurum, Holhymenia rubiginosa, Phthia picta, and Oncopeltus unifasciatellus. We found that H3K9me3 is a marker for sex-chromosomes from early prophase I to the end of the first division in all the species. H3K9me2 also marks the sex chromosomes since early prophase but shows different dynamics at metaphase I depending on the sex-chromosome segregation: it is lost in species with equationally dividing sex chromosomes but remains on one end of the X chromosome of P. argentinus, where chromatids migrate together at anaphase I. It is proposed that the loss of H3K9me2 from the sex chromosomes observed at metaphase I may be part of a set of epigenetic signals that lead to the reductional or equational division of autosomes and sex chromosomes observed in most Heteroptera. The present observations suggest that the histone modifications analyzed here evolved in Heteroptera as markers for asynaptic and achiasmatic sex chromosomes during meiosis to allow the distinction from the chiasmatic autosomal chromosomes.

Highlights

Post-transcriptional modifications (PTMs) of histones are related to basic biological processes such as transcriptional activation/inactivation, chromosome packaging, mitosis, meiosis, apoptosis, and DNA damage/repair (Bannister and Kouzarides, 2011; Tessarz and Kouzarides, 2014)
We present the results of the cytogenetic analyses of the male meiosis in the six species, organized as follows: (1) karyotype and meiotic chromosome behavior, (2) amount and distribution of constitutive heterochromatin, and (3) immunolocalization of modified histone H3
The diploid chromosome number and male meiosis of Belostoma elegans, B. oxyurum, Holhymenia rubiginosa, Pachylis argentinus, and Phthia picta have been described in detail previously (Papeschi and Bidau, 1985; Papeschi, 1992; Papeschi et al, 2003; Bressa et al, 2005, 2008; Table 1)

Summary

Introduction

Post-transcriptional modifications (PTMs) of histones are related to basic biological processes such as transcriptional activation/inactivation, chromosome packaging, mitosis, meiosis, apoptosis, and DNA damage/repair (Bannister and Kouzarides, 2011; Tessarz and Kouzarides, 2014). Several histone modifications participate in meiosis acting individually or collectively to regulate a variety of meiotic events (Ivanovska and Orr-Weaver, 2006; Wang et al, 2017; Lam et al, 2019). In many cases, these histone marks can be detected at cytogenetic acting on whole chromosome or large chromosome segments. In mouse meiotic cells its tri-methylated form (H3K9me3) is a constitutive marker of pericentromeric heterochromatin and it is essential for normal synapsis and segregation (Peters et al, 2001). Its di-methylated form (H3K9me2) is present with other epigenetic markers on the heterochromatic “XY body” within the pachytene spermatocyte nucleus (Khalil et al, 2004; Sciurano and Solari, 2014). In Heteroptera immunostaining of H3K9me in two pentatomid species showed that this modification is present at heterochromatic regions of autosomal bivalents and on the sex chromosomes X and Y throughout the first meiotic prophase, suggesting a role for meiotic silencing of the sex pair (Viera et al, 2009a; Viera et al, 2016)

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Conclusion