As climate change and population growth threaten to destabilize global food security, plant breeders are ramping up efforts to create better, more productive crops. But in order to introduce new traits, breeding techniques typically rely on rare genetic recombination events during meiosis.
Now, a study published in Nature Plants demonstrates that inactivating a single gene called RECQ4 can triple the number of recombination events during meiosis in a variety of distantly-related crop species, including rice (Oryza sativa), pea (Pisum sativum), and tomato (Solanum lycopersicum).
Such meiotic manipulation has been demonstrated before, but not in crop species. “These mutations were around in Arabidopsis for several years. And then suddenly to see that this all works in crops. That’s fantastic,” says Erik Wijnker, a plant biotechnologist at Wageningen University and Research in the Netherlands who was not involved in the study.
During meiosis, parental chromosomes move close enough to partially overlap and hundreds of breaks form in their double-stranded DNA. Repair machinery inspects the chromosomes and fixes these breaks before the chromosomes separate into gametes.
But on rare occasion—only about one to two times per chromosome—these breaks do not get repaired in the usual way, and recombination, or crossover, occurs. Recombination produces gametes with a much greater diversity of gene alleles than the original parental chromosomes. The more crossover events that occur, the more varied the gametes will be. But low recombination rates severely limit breeding efficiency. Inactivating the DNA repair pathways may offer a workaround.
The study follows up on three others published in PNAS in 2015, 2017, and 2018 by members of the same team. Those studies first identified RECQ4 as a major pathway that normally prevents meiotic crossover in the non-crop plant Arabidopsis thaliana. The researchers showed that inactivating the RECQ4 pathway genes increased meiotic recombination more than three-fold and up to eight-fold when combined with mutations in other crossover control pathways. Without a functioning RECQ4 pathway, the only way to repair the breaks that occur during meiosis is to make a crossover.
The diversity of crop species tested in the recent Nature Plant study suggests the tool could be of use in nearly any plant species. “This RECQ4 mutation is likely a universal tool to increase recombination in whatever species you are interested in,” says study coauthor Raphaël Mercier, a plant geneticist at one of France’s National Institute of Agricultural Research centers, located in Versailles. “The next step is to implement this in true breeding schemes and see how efficient it is and how useful it is.”
But as both Mercier and Wijnker point out, increased recombination doesn’t necessarily produce a larger number of improved crop varieties. That’s because desirable traits, such as yield, can depend on the right combination of hundreds of genes. “It gives you more genetic combinations, but you don’t necessarily get higher phenotypic variation,” Wijnker says.
Inactivating the RECQ4 pathway also did not increase the recombination rate in parts of the chromosome that are resistant to it—those tightly packed regions around the centromere that make up as much as two-thirds of the chromosome. “These mutations increase the crossover level a lot, which is really cool,” Wijnker says. “But the crossover increase is all in this region where already there was recombination.”
Nor does the tool increase recombination in hybrids, which have low homology between the chromosomes of the different parental species. “What we want now is to go for those regions where you normally don’t have recombination,” Wijnker says.
Despite these limitations, the RECQ4 mutation tool appears to be a boon for gene mapping, which is also a vital tool in crop breeding. “The more recombination events I have in my population, the more precisely I can pinpoint the position of a gene. And then you can select the plants that have the right combination,” Wijnker explains. “That’s what this is most useful for—gene mapping.”
In its current form, the RECQ4 tool would be applied in the early phases of crop breeding. The idea would be to use RECQ4 to increase DNA mixing in the chromosomes so that you have more extreme phenotypes combining favorable alleles together. Plant breeders then select their favorite line. With this increased level of recombination, Mercier explains, breeders would be able to map genes using either a much smaller population of plants to reduce cost, or the same size population to achieve greater accuracy.