Origin and function of meiosis

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The origin and function of meiosis are currently not well understood scientifically, and would provide fundamental insight into the evolution of sexual reproduction in eukaryotes. There is no current consensus among biologists on the questions of how sex in eukaryotes arose in evolution, what basic function sexual reproduction serves, and why it is maintained, given the basic two-fold cost of sex. It is clear that it evolved over 1.2 billion years ago, and that almost all species which are descendants of the original sexually reproducing species are still sexual reproducers, including plants, fungi, and animals.

Contents

Meiosis is a key event of the sexual cycle in eukaryotes. It is the stage of the life cycle when a cell gives rise to haploid cells (gametes) each having half as many chromosomes as the parental cell. Two such haploid gametes, ordinarily arising from different individual organisms, fuse by the process of fertilization, thus completing the sexual cycle.

Meiosis is ubiquitous among eukaryotes. It occurs in single-celled organisms such as yeast, as well as in multicellular organisms, such as humans. Eukaryotes arose from prokaryotes more than 2.2 billion years ago [1] and the earliest eukaryotes were likely single-celled organisms. To understand sex in eukaryotes, it is necessary to understand (1) how meiosis arose in single celled eukaryotes, and (2) the function of meiosis.

Origin of meiosis

There are two conflicting theories on how meiosis arose. One is that meiosis evolved from prokaryotic sex (bacterial recombination) as eukaryotes evolved from prokaryotes. [2] [3] The other is that meiosis arose from mitosis. [4]

From prokaryotic sex

In prokaryotic sex, DNA from one prokaryote is taken up by another prokaryote and its information integrated into the DNA of the recipient prokaryote. In extant prokaryotes the donor DNA can be transferred either by transformation or conjugation. [2] [3] Transformation in which DNA from one prokaryote is released into the surrounding medium and then taken up by another prokaryotic cell may have been the earliest form of sexual interaction. One theory on how meiosis arose is that it evolved from transformation. [2] According to this view, the evolutionary transition from prokaryotic sex to eukaryotic sex was continuous.

Transformation, like meiosis, is a complex process requiring the function of numerous gene products. A key similarity between prokaryotic sex and eukaryotic sex is that DNA originating from two different individuals (parents) join up so that homologous sequences are aligned with each other, and this is followed by exchange of genetic information (a process called genetic recombination). After the new recombinant chromosome is formed it is passed on to progeny.

When genetic recombination occurs between DNA molecules originating from different parents, the recombination process is catalyzed in prokaryotes and eukaryotes by enzymes that have similar functions and that are evolutionarily related. One of the most important enzymes catalyzing this process in bacteria is referred to as RecA, and this enzyme has two functionally similar counterparts that act in eukaryotic meiosis, RAD51 and DMC1. [5]

Support for the theory that meiosis arose from prokaryotic transformation comes from the increasing evidence that early diverging lineages of eukaryotes have the core genes for meiosis. This implies that the precursor to meiosis was already present in the prokaryotic ancestor of eukaryotes. For instance the common intestinal parasite Giardia intestinalis , a simple eukaryotic protozoan was, until recently, thought to be descended from an early diverging eukaryotic lineage that lacked sex. However, it has since been shown that G. intestinalis contains within its genome a core set of genes that function in meiosis, including five genes that function only in meiosis. [6] In addition, G. intestinalis was recently found to undergo a specialized, sex-like process involving meiosis gene homologs. [7] This evidence, and other similar examples, suggest that a primitive form of meiosis, was present in the common ancestor of all eukaryotes, an ancestor that arose from an antecedent prokaryote. [2] [8]

From mitosis

Mitosis is the normal process in eukaryotes for cell division; duplicating chromosomes and segregating one of the two copies into each of the two daughter cells, in contrast with meiosis. The mitosis theory states that meiosis evolved from mitosis. [9] According to this theory, early eukaryotes evolved mitosis first, became established, and only then did meiosis and sexual reproduction arise.

Supporting this idea are observations of some features, such as the meiotic spindles that draw chromosome sets into separate daughter cells upon cell division, as well as processes regulating cell division that employ the same, or similar molecular machinery. Yet there is no compelling evidence for a period in the early evolution of eukaryotes, during which meiosis and accompanying sexual capability did not yet exist.

In addition, as noted by Wilkins and Holliday, [9] there are four novel steps needed in meiosis that are not present in mitosis. These are: (1) pairing of homologous chromosomes, (2) extensive recombination between homologs; (3) suppression of sister chromatid separation in the first meiotic division; and (4) avoiding chromosome replication during the second meiotic division. Although the introduction of these steps seems to be complicated, Wilkins and Holliday argue that only one new step, homolog synapsis, was particularly initiated in the evolution of meiosis from mitosis. Meanwhile, two of the other novel features could have been simple modifications, and extensive recombination could have evolved later. [9]

Coevolution with mitosis

If meiosis arose from prokaryotic transformation, during the early evolution of eukaryotes, mitosis and meiosis could have evolved in parallel. Both processes use shared molecular components, where mitosis evolved from the molecular machinery used by prokaryotes for DNA replication and segregation, and meiosis evolved from the prokaryotic sexual process of transformation. However, meiosis also made use of the evolving molecular machinery for DNA replication and segregation.

Function

Stress-induced sex

Abundant evidence indicates that facultative sexual eukaryotes tend to undergo sexual reproduction under stressful conditions. For instance, the budding yeast Saccharomyces cerevisiae (a single-celled fungus) reproduces mitotically (asexually) as diploid cells when nutrients are abundant, but switches to meiosis (sexual reproduction) under starvation conditions. [10] The unicellular green alga, Chlamydomonas reinhardtii grows as vegetative cells in nutrient rich growth medium, but depletion of a source of nitrogen in the medium leads to gamete fusion, zygote formation and meiosis. [11] The fission yeast Schizosaccharomyces pombe , treated with H2O2 to cause oxidative stress, substantially increases the proportion of cells which undergo meiosis. [12] The simple multicellular eukaryote Volvox carteri undergoes sex in response to oxidative stress [13] or stress from heat shock. [14] These examples, and others, suggest that, in simple single-celled and multicellular eukaryotes, meiosis is an adaptation to respond to stress.

Prokaryotic sex also appears to be an adaptation to stress. For instance, transformation occurs near the end of logarithmic growth, when amino acids become limiting in Bacillus subtilis, [15] or in Haemophilus influenzae when cells are grown to the end of logarithmic phase. [16] In Streptococcus mutans and other streptococci, transformation is associated with high cell density and biofilm formation. [17] In Streptococcus pneumoniae, transformation is induced by the DNA damaging agent mitomycin C. [18] These, and other, examples indicate that prokaryotic sex, like meiosis in simple eukaryotes, is an adaptation to stressful conditions. This observation suggests that the natural selection pressures maintaining meiosis in eukaryotes are similar to the selective pressures maintaining prokaryotic sex. This similarity suggests continuity, rather than a gap, in the evolution of sex from prokaryotes to eukaryotes.

Stress is, however, a general concept. What is it specifically about stress that needs to be overcome by meiosis? And what is the specific benefit provided by meiosis that enhances survival under stressful conditions?

DNA repair

In one theory, meiosis is primarily an adaptation for repairing DNA damage. Environmental stresses often lead to oxidative stress within the cell, which is well known to cause DNA damage through the production of reactive forms of oxygen, known as reactive oxygen species (ROS). DNA damages, if not repaired, can kill a cell by blocking DNA replication, or transcription of essential genes.

When only one strand of the DNA is damaged, the lost information (nucleotide sequence) can ordinarily be recovered by repair processes that remove the damaged sequence and fill the resulting gap by copying from the opposite intact strand of the double helix. However, ROS also cause a type of damage that is difficult to repair, referred to as double-strand damage. One common example of double-strand damage is the double-strand break. In this case, genetic information (nucleotide sequence) is lost from both strands in the damaged region, and proper information can only be obtained from another intact chromosome homologous to the damaged chromosome. The process that the cell uses to accurately accomplish this type of repair is called recombinational repair.

Meiosis is distinct from mitosis in that a central feature of meiosis is the alignment of homologous chromosomes followed by recombination between them. The two chromosomes which pair are referred to as non-sister chromosomes, since they did not arise simply from the replication of a parental chromosome. Recombination between non-sister chromosomes at meiosis is known to be a recombinational repair process that can repair double-strand breaks and other types of double-strand damage. [2] In contrast, recombination between sister chromosomes cannot repair double-strand damages arising prior to the replication which produced them. Thus on this view, the adaptive advantage of meiosis is that it facilitates recombinational repair of DNA damage that is otherwise difficult to repair, and that occurs as a result of stress, particularly oxidative stress. [19] [20] If left unrepaired, this damage would likely be lethal to gametes and inhibit production of viable progeny.

Even in multicellular eukaryotes, such as humans, oxidative stress is a problem for cell survival. In this case, oxidative stress is a byproduct of oxidative cellular respiration occurring during metabolism in all cells. In humans, on average, about 50 DNA double-strand breaks occur per cell in each cell generation. [21] Meiosis, which facilitates recombinational repair between non-sister chromosomes, can efficiently repair these prevalent damages in the DNA passed on to germ cells, and consequently prevent loss of fertility in humans. Thus with the theory that meiosis arose from prokaryotic sex, recombinational repair is the selective advantage of meiosis in both single celled eukaryotes and multicellular eukaryotes, such as humans.

An argument against this hypothesis is that adequate repair mechanisms including those involving recombination already exist in prokaryotes. [22] Prokaryotes do have DNA repair mechanism enriched with recombination al repair, [23] and the existence of prokaryotic life in severe environment indicates the extreme efficiency of this mechanism to help them survive many DNA damages related to the environment. This implies that an extra costly repair in the form of meiosis would be unnecessary. However, most of these mechanisms cannot be as accurate as meiosis and are possibly more mutagenic than the repair mechanism provided by meiosis. They primarily do not require a second homologous chromosome for the recombination that promotes a more extensive repair. Thus, despite the efficiency of recombinational repair involving sister chromatids, the repair still needs to be improved, and another type of repair is required. [24] Moreover, due to the more extensive homologous recombinational repair in meiosis in comparison to the repair in mitosis, meiosis as a repair mechanism can accurately remove any damage that arises at any stage of the cell cycle more than mitotic repair mechanism can do [25] and was, therefore, naturally selected. In contrast, the sister chromatid in mitotic recombination could have been exposed to similar amount of stress, and, thus, this type of recombination, instead of eliminating the damage, could actually spread the damage [24] and decrease fitness.

Prophase I arrest

Female mammals and birds are born possessing all the oocytes needed for future ovulations, and these oocytes are arrested at the prophase I stage of meiosis. [26] In humans, as an example, oocytes are formed between three and four months of gestation within the fetus and are therefore present at birth. During this prophase I arrested stage (dictyate), which may last for many years, four copies of the genome are present in the oocytes. The arrest of ooctyes at the four genome copy stage was proposed to provide the informational redundancy needed to repair damage in the DNA of the germline. [26] The repair process used likely involves homologous recombinational repair. [26] [27] Prophase arrested oocytes have a high capability for efficient repair of DNA damages. [27] The adaptive function of the DNA repair capability during meiosis appears to be a key quality control mechanism in the female germ line and a critical determinant of fertility. [27]

Genetic diversity

Another hypothesis to explain the function of meiosis is that stress is a signal to the cell that the environment is becoming adverse. Under this new condition, it may be beneficial to produce progeny that differ from the parent in their genetic make up. Among these varied progeny, some may be more adapted to the changed condition than their parents. Meiosis generates genetic variation in the diploid cell, in part by the exchange of genetic information between the pairs of chromosomes after they align (recombination). Thus, on this view, [28] an advantage of meiosis is that it facilitates the generation of genomic diversity among progeny, allowing adaptation to adverse changes in the environment.

However, in the presence of a fairly stable environment, individuals surviving to reproductive age have genomes that function well in their current environment. This raises the question of why such individuals should risk shuffling their genes with those of another individual, as occurs during meiotic recombination? Considerations such as this have led many investigators to question whether genetic diversity is a major adaptive advantage of sex.

See also

Related Research Articles

<span class="mw-page-title-main">Meiosis</span> Type of cell division in sexually-reproducing organisms used to produce gametes

Meiosis is a special type of cell division of germ cells in sexually-reproducing organisms that produces the gametes, such as sperm or egg cells. It involves two rounds of division that ultimately result in four cells with only one copy of each chromosome (haploid). Additionally, prior to the division, genetic material from the paternal and maternal copies of each chromosome is crossed over, creating new combinations of code on each chromosome. Later on, during fertilisation, the haploid cells produced by meiosis from a male and female will fuse to create a cell with two copies of each chromosome again, the zygote.

<span class="mw-page-title-main">Cell division</span> Process by which living cells divide

Cell division is the process by which a parent cell divides, when a mother cell divides into two or more daughter cells. Cell division usually occurs as part of a larger cell cycle. In eukaryotes, there are two distinct types of cell division; a vegetative division, whereby each daughter cell is genetically identical to the parent cell (mitosis), and a reproductive cell division, whereby the number of chromosomes in the daughter cells is reduced by half to produce haploid gametes (meiosis). In cell biology, mitosis (/maɪˈtoʊsɪs/) is a part of the cell cycle, in which, replicated chromosomes are separated into two new nuclei. Cell division gives rise to genetically identical cells in which the total number of chromosomes is maintained. In general, mitosis is preceded by the S stage of interphase and is often followed by telophase and cytokinesis; which divides the cytoplasm, organelles, and cell membrane of one cell into two new cells containing roughly equal shares of these cellular components. The different stages of mitosis all together define the mitotic (M) phase of animal cell cycle—the division of the mother cell into two genetically identical daughter cells. Meiosis results in four haploid daughter cells by undergoing one round of DNA replication followed by two divisions. Homologous chromosomes are separated in the first division, and sister chromatids are separated in the second division. Both of these cell division cycles are used in the process of sexual reproduction at some point in their life cycle. Both are believed to be present in the last eukaryotic common ancestor.

<span class="mw-page-title-main">Chromosomal crossover</span> Cellular process

Chromosomal crossover, or crossing over, is the exchange of genetic material during sexual reproduction between two homologous chromosomes' non-sister chromatids that results in recombinant chromosomes. It is one of the final phases of genetic recombination, which occurs in the pachytene stage of prophase I of meiosis during a process called synapsis. Synapsis begins before the synaptonemal complex develops and is not completed until near the end of prophase I. Crossover usually occurs when matching regions on matching chromosomes break and then reconnect to the other chromosome.

<span class="mw-page-title-main">Prophase</span> First phase of cell division in both mitosis and meiosis

Prophase is the first stage of cell division in both mitosis and meiosis. Beginning after interphase, DNA has already been replicated when the cell enters prophase. The main occurrences in prophase are the condensation of the chromatin reticulum and the disappearance of the nucleolus.

<span class="mw-page-title-main">Genetic recombination</span> Production of offspring with combinations of traits that differ from those found in either parent

Genetic recombination is the exchange of genetic material between different organisms which leads to production of offspring with combinations of traits that differ from those found in either parent. In eukaryotes, genetic recombination during meiosis can lead to a novel set of genetic information that can be further passed on from parents to offspring. Most recombination occurs naturally and can be classified into two types: (1) interchromosomal recombination, occurring through independent assortment of alleles whose loci are on different but homologous chromosomes ; & (2) intrachromosomal recombination, occurring through crossing over.

<span class="mw-page-title-main">Unicellular organism</span> Organism that consists of only one cell

A unicellular organism, also known as a single-celled organism, is an organism that consists of a single cell, unlike a multicellular organism that consists of multiple cells. Organisms fall into two general categories: prokaryotic organisms and eukaryotic organisms. All prokaryotes are unicellular and are classified into bacteria and archaea. Many eukaryotes are multicellular, but some are unicellular such as protozoa, unicellular algae, and unicellular fungi. Unicellular organisms are thought to be the oldest form of life, with early protocells possibly emerging 3.8–4.0 billion years ago.

<span class="mw-page-title-main">Homologous chromosome</span> Chromosomes that pair in fertilization

A couple of homologous chromosomes, or homologs, are a set of one maternal and one paternal chromosome that pair up with each other inside a cell during fertilization. Homologs have the same genes in the same loci where they provide points along each chromosome which enable a pair of chromosomes to align correctly with each other before separating during meiosis. This is the basis for Mendelian inheritance which characterizes inheritance patterns of genetic material from an organism to its offspring parent developmental cell at the given time and area.

<span class="mw-page-title-main">Biological life cycle</span> Series of stages of an organism

In biology, a biological life cycle is a series of changes in form that an organism undergoes, returning to the starting state. "The concept is closely related to those of the life history, development and ontogeny, but differs from them in stressing renewal." Transitions of form may involve growth, asexual reproduction, or sexual reproduction.

<span class="mw-page-title-main">Evolution of sexual reproduction</span> How sexually reproducing multicellular organisms could have evolved from a common ancestor species

Sexual reproduction is an adaptive feature which is common to almost all multicellular organisms and various unicellular organisms, with some organisms being incapable of asexual reproduction. Prior to the advent of sexual reproduction, the adaptation process whereby genes would change from one generation to the next happened very slowly and randomly. Sex evolved as an extremely efficient mechanism for producing variation, and this had the major advantage of enabling organisms to adapt to changing environments. Sex did, however, come with a cost. In reproducing asexually, no time nor energy needs to be expended in choosing a mate. And if the environment has not changed, then there may be little reason for variation, as the organism may already be well adapted. Sex also halves the amount of offspring a given population is able to produce. Sex, however, has evolved as the most prolific means of species branching into the tree of life. Diversification into the phylogenetic tree happens much more rapidly via sexual reproduction than it does by way of asexual reproduction.

RecQ helicase is a family of helicase enzymes initially found in Escherichia coli that has been shown to be important in genome maintenance. They function through catalyzing the reaction ATP + H2O → ADP + P and thus driving the unwinding of paired DNA and translocating in the 3' to 5' direction. These enzymes can also drive the reaction NTP + H2O → NDP + P to drive the unwinding of either DNA or RNA.

<span class="mw-page-title-main">Homologous recombination</span> Genetic recombination between identical or highly similar strands of genetic material

Homologous recombination is a type of genetic recombination in which genetic information is exchanged between two similar or identical molecules of double-stranded or single-stranded nucleic acids. It is widely used by cells to accurately repair harmful breaks that occur on both strands of DNA, known as double-strand breaks (DSB), in a process called homologous recombinational repair (HRR). Homologous recombination also produces new combinations of DNA sequences during meiosis, the process by which eukaryotes make gamete cells, like sperm and egg cells in animals. These new combinations of DNA represent genetic variation in offspring, which in turn enables populations to adapt during the course of evolution. Homologous recombination is also used in horizontal gene transfer to exchange genetic material between different strains and species of bacteria and viruses.

<span class="mw-page-title-main">Synapsis</span> Biological phenomenon in meiosis

Synapsis is the pairing of two chromosomes that occurs during meiosis. It allows matching-up of homologous pairs prior to their segregation, and possible chromosomal crossover between them. Synapsis takes place during prophase I of meiosis. When homologous chromosomes synapse, their ends are first attached to the nuclear envelope. These end-membrane complexes then migrate, assisted by the extranuclear cytoskeleton, until matching ends have been paired. Then the intervening regions of the chromosome are brought together, and may be connected by a protein-RNA complex called the synaptonemal complex. During synapsis, autosomes are held together by the synaptonemal complex along their whole length, whereas for sex chromosomes, this only takes place at one end of each chromosome.

<span class="mw-page-title-main">Mating of yeast</span> Biological process

The yeast Saccharomyces cerevisiae is a simple single-celled eukaryote with both a diploid and haploid mode of existence. The mating of yeast only occurs between haploids, which can be either the a or α (alpha) mating type and thus display simple sexual differentiation. Mating type is determined by a single locus, MAT, which in turn governs the sexual behaviour of both haploid and diploid cells. Through a form of genetic recombination, haploid yeast can switch mating type as often as every cell cycle.

<span class="mw-page-title-main">Natural competence</span> Ability of cells to alter their own genetics by taking up extracellular DNA

In microbiology, genetics, cell biology, and molecular biology, competence is the ability of a cell to alter its genetics by taking up extracellular ("naked") DNA from its environment in the process called transformation. Competence may be differentiated between natural competence, a genetically specified ability of bacteria which is thought to occur under natural conditions as well as in the laboratory, and induced or artificial competence, which arises when cells in laboratory cultures are treated to make them transiently permeable to DNA. Competence allows for rapid adaptation and DNA repair of the cell. This article primarily deals with natural competence in bacteria, although information about artificial competence is also provided.

<span class="mw-page-title-main">Sister chromatids</span> Two identical copies of a chromosome joined at the centromere

A sister chromatid refers to the identical copies (chromatids) formed by the DNA replication of a chromosome, with both copies joined together by a common centromere. In other words, a sister chromatid may also be said to be 'one-half' of the duplicated chromosome. A pair of sister chromatids is called a dyad. A full set of sister chromatids is created during the synthesis (S) phase of interphase, when all the chromosomes in a cell are replicated. The two sister chromatids are separated from each other into two different cells during mitosis or during the second division of meiosis.

<span class="mw-page-title-main">Sister chromatid exchange</span>

Sister chromatid exchange (SCE) is the exchange of genetic material between two identical sister chromatids.

Recombinases are genetic recombination enzymes.

Microbial genetics is a subject area within microbiology and genetic engineering. Microbial genetics studies microorganisms for different purposes. The microorganisms that are observed are bacteria, and archaea. Some fungi and protozoa are also subjects used to study in this field. The studies of microorganisms involve studies of genotype and expression system. Genotypes are the inherited compositions of an organism. Genetic Engineering is a field of work and study within microbial genetics. The usage of recombinant DNA technology is a process of this work. The process involves creating recombinant DNA molecules through manipulating a DNA sequence. That DNA created is then in contact with a host organism. Cloning is also an example of genetic engineering.

Chromosome segregation is the process in eukaryotes by which two sister chromatids formed as a consequence of DNA replication, or paired homologous chromosomes, separate from each other and migrate to opposite poles of the nucleus. This segregation process occurs during both mitosis and meiosis. Chromosome segregation also occurs in prokaryotes. However, in contrast to eukaryotic chromosome segregation, replication and segregation are not temporally separated. Instead segregation occurs progressively following replication.

<span class="mw-page-title-main">Sexual reproduction</span> Reproduction process that creates a new organism by combining the genetic material of two organisms

Sexual reproduction is a type of reproduction that involves a complex life cycle in which a gamete with a single set of chromosomes combines with another gamete to produce a zygote that develops into an organism composed of cells with two sets of chromosomes (diploid). This is typical in animals, though number of chromosome sets and how that number changes in sexual reproduction varies, especially among plants, fungi, and other eukaryotes.

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  27. 1 2 3 Stringer JM, Winship A, Zerafa N, Wakefield M, Hutt K (May 2020). "Oocytes can efficiently repair DNA double-strand breaks to restore genetic integrity and protect offspring health". Proceedings of the National Academy of Sciences of the United States of America. 117 (21): 11513–11522. doi:10.1073/pnas.2001124117. PMC   7260990 . PMID   32381741.
  28. ↑ Otto SP, Gerstein AC (August 2006). "Why have sex? The population genetics of sex and recombination". Biochemical Society Transactions. 34 (Pt 4): 519–22. doi:10.1042/BST0340519. PMID   16856849.
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