Confrontation, Consolidation, and Recognition: The Oocyte’s Perspective on the Incoming Sperm

Abstract

From the oocyte's perspective, the incoming sperm poses a significant challenge. Despite (usually) arising from a male of the same species, the sperm is a "foreign" body that may carry with it additional, undesirable factors such as transposable elements (mainly retroposons) into the egg. These factors can arise either during spermatogenesis or while the sperm is moving through the epididymis or the female genital tract. Furthermore, in addition to the paternal genome, the sperm also carries its own complex repertoire of RNAs into the egg that includes mRNAs, lncRNAs, and sncRNAs. Last, the paternal genome itself is efficiently packaged into a protamine (nucleo-toroid) and histone (nucleosome)-based chromatin scaffold within which much of the RNA is embedded. Taken together, the sperm delivers a far more complex package to the egg than was originally thought. Understanding this complexity, at both the compositional and structural level, depends largely on investigating sperm chromatin from both the genomic (DNA packaging) and epigenomic (RNA carriage and extant histone modifications) perspectives. Why this complexity has arisen and its likely purpose requires us to look more closely at what happens in the oocyte when the sperm gains entry and the processes that then take place preparing the paternal (and maternal) genomes for syngamy.

Epigenetic inheritance of acquired traits through sperm RNAs and sperm RNA modifications

“…Whether sperm RNAs are necessary for early embryonic development remains controversial 129–131 , particularly given the recent generation of parthenogenetic mice with appreciable survival rates 132,133 ; nonetheless, their potential synergistic action with maternal RNAs have been discussed with interest 134 . Thus far, the most significant biological functions identified for sperm RNAs are their involvement in non-Mendelian inheritance in mammals, such as the paramutation phenomenon in mice (BOX 2), and their contribution to the intergenerational inheritance of paternally acquired traits, including mental and nutritional stresses 9,24–26 .…”

Gamete-mediated mate choice: towards a more inclusive view of sexual selection

“…Mature sperm cells contain complex 'populations' of different RNA subtypes, known to be important for fertilization and early embryo development [82]. Interestingly, it has been suggested that small non-coding RNAs, piRNA and micro-RNA, may play important roles in the verification of the cytoplasmic and genetic compatibility of gametes prior to fertilization [83]. In this process, non-coding sperm RNAs may recognize their respective binding sites in oocyte RNAs.…”

Analysis of the small non-protein-coding RNA profile of mouse spermatozoa reveals specific enrichment of piRNAs within mature spermatozoa

“…5 Nevertheless, the presence of such a diverse RNA profile takes on added significance in view of their potential to be delivered to the oocyte, along with the paternal genome, whereupon they may contribute to fertilization and embryo development and fitness. 3,[9][10][11] This implies that, rather than simply being a legacy of the spermatogenic process, these transcripts may actually have fitness consequences and potentially adaptive value. 12 As an extension of this hypothesis, it has recently been proposed that sperm RNA could encode information about the paternal environment, with males having the capacity to modify the RNA content of their sperm under different conditions to prime the embryo to develop appropriately within the prevailing environment.…”