Sedge plant has sex but produces clones, study finds

Researchers studying Rhynchospora tenuis, a small perennial beak-sedge that grows in seasonally wet grasslands across tropical and subtropical America, found that it undergoes a form of sexual reproduction that does not include the genetic shuffling normally central to sex. In most sexually reproducing organisms, chromosomes pair up during the cell division that makes eggs and sperm (or, in plants, pollen and seed cells), a process called meiosis, and swap segments of DNA in an event called a crossover. Crossovers scramble genetic material between the two copies of each chromosome an organism inherited from its parents, which is why offspring are not identical to either parent. R. tenuis, the study found, forms no crossovers at all, in either its male or female reproductive cells, a condition called achiasmy. This total, two-sex absence of crossing over has not been documented before in a sexually reproducing species, according to the researchers.

The plant is unusual in other ways too. It has just two chromosomes per set, the lowest number known in any flowering plant, and its chromosomes are "holocentric," meaning the structure that pulls chromosomes apart during division is spread along their whole length rather than concentrated at one point. It also performs its two division steps in reverse order compared with most organisms: sister strands separate first, and the two parental copies of each chromosome separate only in the second step. The combination let the researchers ask a question earlier cytology work had raised but not settled: without any crossovers to shuffle genes, how does the plant still segregate chromosomes accurately and stay fertile.

The team assembled genomes for nine populations of R. tenuis collected across Brazil, sequencing both chromosome copies (haplotypes) separately for each. They found that the two copies within a single plant differ from each other far more than expected for a species that mostly self-fertilizes, and more than the two copies typically differ in a related, outcrossing sedge. Much of the difference comes from an uneven buildup of transposable elements, DNA sequences that can copy and insert themselves elsewhere in the genome, which piled up differently on each copy and made one consistently larger than the other. Comparing the two copies across a plant's genome produced a pattern that normally shows up only in species that reproduce asexually: because non-recombining chromosome copies build up separate mutations, one copy from any given plant should end up looking more like the same copy from an unrelated plant than like its own partner copy. That is exactly the pattern the researchers saw, even though R. tenuis is not asexual.

Tracing the plant's evolutionary history, the researchers found that its two-chromosome genome arose through a series of end-to-end fusions of an ancestral set of five chromosomes, first producing an intermediate arrangement of three and then, in R. tenuis itself, the final pair. Layered on top of that history are smaller, population-specific translocations, exchanges of DNA segments between the ends of chromosomes, which differ from one Brazilian population to another. During reproduction, larger chromosomes carrying more of these transposable-element insertions were passed on more often than smaller ones, a pattern known as segregation distortion, or meiotic drive. Seeds only developed successfully, the researchers found, when the sperm and egg cells that fused carried translocations compatible with each other; combinations that did not match were eliminated. That selective elimination, combined with the drive favoring larger chromosomes, is what the researchers say restores the parent's original heterozygous genotype in each generation despite ongoing fertilization.

Plants that produce offspring genetically identical to the mother are usually described using a different term: apomixis, in which the plant skips both meiosis and fertilization to form seeds directly, without ever mixing genetic material from a father. Apomixis is well documented in some grasses, including species of Paspalum, and is of long-standing interest to plant breeders because it lets a valuable hybrid genotype be reproduced through seed indefinitely without losing its traits. Reviews of apomixis describe it as bypassing "the most fundamental aspects of sexual reproduction – meiosis and fertilization." R. tenuis does neither of those things: it completes meiosis, even without crossovers, and its seeds form through fertilization between egg and sperm cells. What is distinct about R. tenuis, according to the researchers, is that it reaches an apomixis-like outcome, offspring matching the mother's genotype, through an entirely different route: post-meiotic selection against incompatible chromosome combinations rather than a skipped division.

The researchers tried to estimate how long the plant's two chromosome copies have been evolving independently, using three separate methods, and got three different answers. A molecular-clock estimate based on mutation rates in protein-coding genes put the split at roughly 1.7 million years ago. Estimating instead from the ages of transposable-element insertions specific to each chromosome copy gave a more recent range, between about 400,000 and 600,000 years ago. A third method, based on the density of single-letter DNA differences in matching regions, gave narrower and more recent ranges still, roughly 230,000 to 310,000 years for one chromosome and 220,000 to 275,000 years for the other. The paper does not resolve which estimate is most accurate, only that reconciling them requires further discussion, leaving the precise age of this reproductive arrangement an open question.