Similarity of the Domain Structure of Proteins as a Basis for the Conservation of Meiosis¹

Meiosis is conserved in all eucaryotic kingdoms, and homologous rows of variability are revealed for the cytological traits of meiosis. To find the nature of these phenomenons, we reviewed the most‐studied meiosis‐specific proteins and studied them with the methods of bioinformatics. We found that synaptonemal complex proteins have no homology of amino‐acid sequence, but are similar in the domain organization and three‐dimensional (3D) structure of functionally important domains in budding yeast, nematode, Drosophila, Arabidopsis, and human. Recombination proteins of Rad51/Dmc1 family are conserved to the extent which permits them to make filamentous single‐strand deoxyribonucleic acid (ssDNA)‐protein intermediates of meiotic recombination. The same structural principles are valid for conservation of the ultrastructure of kinetochores, cell gap contacts, and nuclear pore complexes, such as in the cases when ultrastructure 3D parameters are important for the function. We suggest that self‐assembly of protein molecules plays a significant role in building‐up of all biological structures mentioned.

Introduction

It is well known that the general scheme of meiosis is evolutionarily conserved. The cytological pattern of meiosis is essentially similar in protists, fungi, plants, and animals, although some details vary. Mutations of specific meiotic genes have been found in representatives of all these kingdoms. Such mutations cause morphologically similar cell phenotypes, that is, meiotic abnormalities with similar cytological expression at the light‐microscopic and ultrastructural levels. What are the cytological and molecular events occurring in the meiotic cell that are advantageous for meiosis to the extent of determining their existence for thousands and millions of years and their fixation in all kingdoms of eukaryotes?

The molecular basis of meiosis is provided by several tightly associated events, which distinguish meiosis from mitosis and occur in the first meiotic division (meiosis I). The events include (1) synapsis and recombination of homologous chromosomes; (2) the formation of chiasmata, physically linking two nonsister chromatids; and (3) the lack of centromere splitting in meiosis I. The cytological consequences of these events are nondisjunction of sister chromatids and segregation of homologous chromosomes in meiosis I. As a result, cells carrying replicated chromosomes are haploidized. Meiosis II does not require chromosome replication; it leads to segregation of sister chromatids with recombinant alleles located distally of a single (or an odd) chiasma.

It is possible to consider conservation of morphological traits of meiosis as an example of the general biological law of homologous series of variation, which N. I. Vavilov formulated in the 1920s and continued to refine and improve for about 10 more years. This fundamental biological law was formulated on the basis of studies on the variation in plants. More recently, Vavilov extended the law to the animal world. In 1930, one of his formulations described a homologous series as “a biological phenomenon consisting in the fact that different species and even genera of plants or animals include repeating, analogous, parallel series of forms (i.e., forms similar in morphological and physiological features)” (Vavilov, 1987). In his book Law of Homologous Series in Hereditary Variation (Vavilov, 1935; reissued as Vavilov, 1987), Vavilov noted that this law is true for larger taxa (families and classes), and gave examples of the homology of morphogenetic processes in ascomycetes and basidiomycetes, in the class Infusoria, in fossil cephalopods, and in insects, amphibians, and mammals (Vavilov, 1935; reissued as Vavilov, 1987).

In all these cases, homology was deduced from the similarity of variation of features, namely, from discrete changes that formed series. This description of the fundamental phenomenon of homology implied the homology of genes. Of real interest is the question as to how the similarity of intracellular structures in taxonomically distant organisms is ensured at the molecular level. This question concerns all cell structures from chromosomes to all organelles involved in cell division. Rapidly progressing genomics has already developed its own understanding of this problem and quantitative estimation of homology. The homology of genes is considered essential when their nucleotide sequences coincide by no less than 80% (Chervitz 1998, Rubin 2000). Such homology is characteristic of genes coding for functionally important proteins, enzymes in particular, and is, as a rule, followed within the limits of a taxonomic class.

Homology of proteins, especially those fulfilling morphogenetic functions rather than that of genes, is more important for the purpose of this paper. In view of the redundancy of genetic codes, one could expect that the nucleotide sequences of homologous genes are more variable than amino‐acid sequences of their products in various organisms. There are mutations that change the course of meiosis, including mutations of specific meiotic genes. Tens of such genes have been identified in model organisms studied to the greatest extent. Judging by the data for Saccharomyces cerevisiae, the best‐studied model species, meiosis should be governed by hundreds of genes, including those common for meiosis and mitosis (common genes of cell division) and those specific for each of these processes (Bogdanov, 2003). Table I lists specific meiotic genes identified so far in various species. Meiotic mutations are similar in phenotypic expression in different species. Published data on morphological changes in the picture of meiosis allow us to speak about homologous series of variation in meiotic features in a wide range of taxa, including the kingdoms (Bogdanov, 2003). It is possibly more correct to speak about homomorphism of these features. Let us consider several examples.