Nature is ridden with exceptions. To biologist Peter Schlögelhofer, the case of an exotic sedge is a classic fit to the adage. The plant’s unusual type of chromosomes makes cell division in sex cells rather challenging. But the flourishing species has found a solution, just as unusual, to the formidable problem.
There’s one ulterior reason to why organisms love sex. Besides zapping our pleasure centers, sex allows a species to sustain itself against the odds. By increasing genetic diversity, it ensures that at least some individuals can cope with changing environments and protract the prevalence of a species.
A seminal event in sexual reproduction is meiosis – a special type of cell division that gives rise to sex cells namely, the sperm and the egg. Meiosis is distinct from cell divisions of somatic cells in the way the chromosomes – the seat of genetic information – are distributed to daughter cells. First, it fosters shuffling of parental DNAs, in a process dubbed recombination, and thus increases genetic variability. Second, it halves the chromosomal content so that the offspring receives two sets of chromosomes, one from each parent. These steps make but round one of meiosis (M-I), the so-called ‘reductional’ division. The process is complete only after the daughter cells of M-I go through round II (M-II), which resembles the canonical ‘equational’ division seen in somatic cells.
Most sexually reproducing organisms ditto the classical meiotic sequence, as even subtle deviations can have dire effects in the offspring. In humans, for instance, chromosomal errors can cause cognitive disability such as in Down’s patients or infertility as in Turner’s, while in plants, they account for sterility and stunted growth among others.
The sedge, a grass-like plant native to tropical lands, is however an exception. Hailing from the family Cyperaceae, sedges of the Rhynchospora genus sport atypical chromosomes that are incapable of enduring conventional meiosis. This would normally throttle breeding success, but surprisingly, these plants flourish in hot, Brazilian wetlands. Peter Schlögelhofer, a group head in the Department of Chromosome Biology, Max F. Perutz Laboratories, Austria, uncovers in his latest paper (Nat Comm 5:5070) how the quirky grass procreates using a quirkier solution.
Cut-copy-paste in sex cells
The Schlögelhofer lab’s decade-long interest has been to understand meiotic recombination – the cut, copy, and paste of genetic material – between homologs, pairs of maternal and paternal chromosomes, in plants.
Soon after DNA replication and at the onset of meiosis, duplicated chromosomes or ‘sister’ chromatids – conjoined all along their lengths by ring-like protein complexes – line up next to their duplex homolog, setting the stage for recombination. Genetic exchange between homologous non-sister chromatids initiates when the DNA gets a cut in the chromosomal arms. The protrusive strand at the cut invades the homolog and uses the latter’s complementary sequence as a template to bandage its severed end in a repair process. Peter explains, “during DNA repair, maternal and paternal chromatids become chemically linked at the cross-over site, termed chiasma, and mutually exchange chromosomal parts giving rise to new, chimeric genetic combinations”. This repeats at several chiasmata giving rise to patches of maternal and paternal DNAs on both homologs.
In their previous work, the Austrian group unveiled some of the molecular players in the repair process in the model plant Arabidopsis. Peter elaborates, “it’s not just about repairing the break, but about shifting the repair to the homologous chromosome and in the end, connecting maternal and paternal chromosomal strands. Some of our work has been addressing this aspect.”
The sedge paradox
Once the homologs have swapped their DNAs, it’s time for them to segregate into different daughter cells. To enable this, the glue along the chromosomal arms dissolves, freeing the homologs, while sisters are still joined at a region called the centromere. Molecular ropes or microtubules (MTs), from the two ends of the cell, latch on to the centromere via a protein complex called the kinetochore. The MTs now pull the attached sister chromatids to one pole of the dividing cell, while the homologous non-sister chromatids are simultaneously drawn to the opposite pole. “In classical meiosis, homologs are separated at M-I while sister chromatids are still joined at the centromere and migrate together. At M-II, the cohesion between sister chromatids that remained in the region of the centromeres is lost and the sisters now separate”, elaborates Peter.
The successive loss of the glue, first along the chromosome arms and then at the centromeres, is what preserves this meiotic sequence and ensures that the chromosomes are segregated in correct numbers and as correct sets.
“Our latest paper was inspired by a shared student Gabriella. She brought two species of Rhynchospora – R.pubera and R.tenius from her hometown in Brazil. They do not have the typical monocentric chromosomes but instead exhibit holocentricity”. Conventional meiosis works for monocentric chromosomes (MCs) with a single centromeric region and localized kinetochore. “Here, the arms are free of kinetic activity and can engage in cross-over, loosen up from the homologs and trail behind the centromere when sister chromatids rise towards the poles”, Peter explains. Holocentric chromosomes (HCs), on the other hand, bind kinetochore proteins all along their lengths. “Cross-overs are problematic here [in HCs]…The recombined DNA should not be attached to kinetic activity but be able to move around freely. Besides there’s difficulty with proper segregation if everything is connected all the time”, he continues. For the right chromosomes to be packed into the right cells, it is important for homologs to first pair up and sort out and then, in a second round, have the sister chromatids separate.
Nature’s quirky solution
Rhynchospora are not the only organisms with HCs. HCs have shown up time and again, in both plants and animals, during evolution. It is not known which came first – the HCs or the MCs. Besides, how HCs cross-over and sort out during meiosis has puzzled scientists. There is some evidence for alternative routes to canonical meiosis in these species. “It’s likely that the holocentric chromosomes still behave as monocentrics, as in the worm C. elegans. But a more interesting possibility is that they engage in inverted meiosis, though there is only vague support for this from insect studies”, Peter draws attention to a novel form of meiosis in which the sequence of events is reversed.
When they probed into the distribution of chromosomes in R.pubera at M-I, the Austrian group instantly realized what they were getting at. For an organism with five pairs of chromosomes, R.pubera should exhibit five pairs of sister chromatids at each pole. But instead, there were up to ten individual chromatids at either pole. This meant that the sister chromatids are already separated at M-I in a likely inverted meiosis. These chromatids mostly stayed connected to their homologs by visible DNA threads. The connections were presumably pivotal to the proper segregation of the homologous non-sister chromatids at M-II.
In an elegant experiment using a heteromorphic chromosome pair, the group bolstered their findings. “The main moment came when we generated plants with a broken homolog for chromosome 2”, Peter recollects. The two fragments of the fractured homolog were replicated normally and could be readily followed by DNA staining. If sisters separated first, they expected to see equal number of stained structures in both M-I daughter cells; whereas, if homologs separated first, the structures would be distributed unequally, with one cell receiving the intact and the other, the fragmented version of chromosome 2. It was clearly the first case, so they safely concluded that R.pubera indeed exhibits an upside-down meiosis.
“Step away from models”
“We always thought inverted meiosis was amiss. There’s been very little evidence in favor of it. But our studies on R.pubera and R.tenius have both confirmed that it does exist in nature”. R.tenius – another species of the same genus – is even more peculiar. It displays an achiasmatic inverted meiosis, with no signs of genetic exchange between homologs. “Besides these examples, Andreas Houben from Gatersleben has demonstrated inverted meiosis in yet another plant Luzula elegans”, Peter summons another paper, published in the same issue as theirs with similar findings. “We now appreciate that inverted meiosis is a specific adaptation of sexually reproducing organisms with holocentric chromosomes to distribute their chromosomes correctly during meiosis”.
It’s fascinating that nature comes up with novel solutions to quaint problems, but why does it create them in the first place? Peter responds wittily, “it’s just nature’s way to reconcile innovation and tradition”. But he agrees that we do not yet completely understand the implications of such bizarreness. “We lack the resources for comparative analysis of the biology of exotic species, to see how different they are from our own. A part of the problem is the over-reliance on model organisms for research. These models do not represent the entire biodiversity. But all our tools are derived from and represent only these prototypes”, he shirks. However, he ends with an optimistic note, “novel technologies such as deep sequencing of DNA and CRISPR/Cas9 may make it easier for us to expand our studies into diverse organisms”.
Published in LabTimes 01/15
Photo courtesy: White-beak sedge (Rhynchospora sp.) via Creative Commons