How Is Sex Possible?

Meiosis must produce sex cells

Nature did not produce sex for our own pleasure, nor for us to have sick thoughts. Sex is the fuel of evolution; genetic material from parents recombines producing a unique new genome.

But how was sex possible?

Researchers at the Department of Energy's Lawrence Berkeley National Laboratory and the University of California at Berkeley have found clues about how the organism can form sex cells making studies on the nematode Caenorhabditis elegans. They have identified a group of genes and proteins that help bring C. elegans chromosomes together during meiosis, the specialized cell division that produces gametes (sex cells), each containing only one copy of each chromosome instead of paired chromosomes most cells carry.

For meiosis, corresponding chromosomes must first identify each other, then line up accurately and stay paired during the recombination process. In C. elegans, the task is initiated by regions called Pairing Centers, found near one end of each of the worm's six chromosomes.

Last year, the same team identified the function of a C. elegans protein called HIM-8. This protein brings together copies of the worm's sex chromosome (the X chromosome) to achieve pairing (synapsis). Now, the team has found three new genes - named zim-1, zim-2, and zim-3 - that perform the same task for the worm's five additional chromosomes. All four of these genes encode different but related "zinc-finger" proteins that usually recognize specific sequences of DNA, pairing one or two specific chromosomes among C. elegans's complete set of six.

The him and zim genes appear on a single chromosome. "There are many families of zinc-finger proteins involved in DNA transcription, all very rapidly evolving," says Abby Dernburg of Life Science Division. "Gene duplication is common throughout the genome in all species, but unless a duplicated gene quickly acquires a new function, it is not likely to be conserved. The group of related zinc-finger protein genes in C. elegans offers an opportunity to address the question of how and why new zinc-finger proteins acquire new functions."

C. elegans is a tiny worm, 1 mm in length, very suited to the study of meiosis because it is transparent and reproduces quickly, producing over 200 progeny within a few days. Most C. elegans are hermaphrodites, possessing two X chromosomes (XX), while some are males with a single X chromosome (X0).

The reproductive organs contain about half of the cells in an adult worm, and the process of meiosis can be observed at every stage. Failed pairing of X chromosomes results in a high incidence of males, with only one X chromosome. A mutant him-8 gene gives rise to a high incidence of males, hence the gene name. "In species where an X and Y chromosome make a male, only very small regions of these chromosomes require control for successful pairing. So even though we saw there were nearby genes similar to him-8" - which acts only on the C. elegans X chromosome - "at first we weren't sure they performed similar functions for the other chromosomes." said Dernburg.

By observing meiosis (and its failures), in worms with the three new genes knock-out, resulted that one produced pairing of the nonsex chromosomes II and III, one of chromosome V, and the third for chromosomes I and IV.

The researchers visualized the zinc-finger proteins during meiosis and how each protein binds specifically to the chromosomes they help to pair. During meiosis, each protein on each chromosome latches onto the cell's nuclear envelope. This activity is reminiscent of the way chromosomes attach to the nuclear envelope during meiosis in other organisms. "In most eukaryotic species - plants, mammals, fungi, and so on - the telomeres on the ends of the chromosomes anchor to the nuclear membrane in a transient structure called a 'meiotic bouquet,'" Dernburg says.

"In C. elegans it's the Pairing Centers, not telomeres, that attach to the nuclear envelope. They do so seemingly randomly, not in a single bunch; nevertheless, the association with the nuclear envelope seems to serve a similar function, which is to stabilize chromosome interactions during pairing."

"Zinc-finger proteins evolve rapidly because they are modular, so that combinations of elements allow them to move quickly to new binding sites on DNA, making the Pairing Centers of different chromosomes unique," she says.

"Telomeres, on the other hand, are all very much alike, no matter which chromosome they're on. It could be that C. elegans, which is hermaphroditic and grows to maturity in only three days, is under a lot of competitive pressure to reproduce quickly, and that different binding sites on different Pairing Centers makes for faster chromosome pairing and thus faster reproduction - unlike organisms that need to find a mate before they can reproduce, and mature more slowly."

When it comes to the evolution of sex in C. elegans and its relatives, "we haven't yet figured out what makes each chromosome unique," Dernburg says. But evidence is strong that the answer - as far as the worm is concerned - lies on the chromosomes Pairing Centers.

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