Exploring Plant Reproduction - How Chromosomes Mix and Match

André Marques and his team are curious about how chromosomes work and how they control genetic exchange during meiosis in plants.
 

High yields, delicious flavour and resistance to disease are just some of the characteristics we want from the ideal crop plant. The aim of plant breeding is therefore to combine all these positive characteristics in a single plant.

Gregor Mendel (1822-1884), the pioneer of the theory of heredity, once believed that all the characteristics of a plant can be inherited independently of each other. But the reality is different. Nowadays, plant breeders often encounter the problem that genes for positive or negative traits are in regions that cannot be exchanged.

DNA Mixing for diversity

Some biological processes are so fundamental to survival that they have changed little over the course of evolution. Meiosis is one of them. This specialised form of cell division takes place in most species that reproduce sexually. Although it has existed for a long time, it still harbours great potential for the targeted creation of new genetic diversity - an enormous advantage for plant breeding.

In every cell, DNA, the fundamental material of life, is tightly packed with proteins to form structures called chromosomes. These chromosomes usually take on the familiar X-shape, which is due to a special connection point called the centromere. The centromere serves as a link between two identical copies of the chromosome, known as sister chromatids, which are made during DNA replication.

During reproduction, chromosomes that are similar in shape and genetic content, called homologous chromosomes, come together and swap genetic material. This swapping of DNA is called crossing-over, and it mixes genetic material from both parents to ensure diversity in their offspring. This is what makes us all unique.

But here's the twist: crossing-over doesn't happen evenly along the chromosome. It's less likely to occur near the centromere and more often in regions farther away. This phenomenon, known as the 'centromere effect', suggests that the centromere itself might influence the occurrence and distribution of crossing-over events.

But how exactly does it all work?

Chromosomes with hundreds of centromeres

To learn more about the 'centromere effect', the researchers do so by studying a plant called beak-sedge (Rhynchospora spp.), which is like a grass-looking plant. It's a great plant model for studying how genes mix and match naturally.

Rather than having a single centromere like most chromosomes, the beak-sedge chromosome has hundreds of centromeres scattered along its entire length. This creates a structure known as “holocentric”, which is different from the typical "monocentric" chromosome structure with just a single centromere.

The team discovered that genes in holocentric chromosomes are uniformly spread throughout the entire length, unlike monocentric chromosomes where genes are often found away from the centromere.

In species with monocentric chromosomes, extensive interactions between chromosomes occur during cell division. But in beak-sedge plants, with their different chromosome organization, this interaction between chromosomes is less, meaning that chromosomes occupy distinct regions within the nucleus.

Having these special chromosomes not only changes where genes are located, but also how chromosomes act when cells divide.

Distribution and frequency of genetic exchange

The team created a map of genetic recombination, studying how crossing-over happens in holocentric chromosomes.

By using these chromosomes, the researchers excluded the influence of a single centralized centromere and the compartmentalized structure of a monocentric chromosome.

Some crossing-over took indeed place near the centromeres – so this area was not excluded as it is in monocentric plants. Interestingly, though, they found that crossing-over wasn't evenly spread across the chromosomes, as one could expect from the uniform gene distribution, but instead happened more often towards the ends.

Marques believes that the centromere isn't a main factor controlling the overall crossing-over distribution. The main reason influencing the way genes mix and match in plants is possibly due to how chromosomes come together and link up during cell division. It's not so much about the genes themselves or the arrangement of centromeres.

Engineering of gene exchange

The team wants to find and characterize the genes in holocentric plants responsible for the crossing-over activity near the centromere.

With this knowledge in place, it may be possible in the future to increase gene exchange in monocentric crop plants close to the centromere. This would allow plant breeders to exchange the genes for both favourable and unfavourable traits, independent from their location on the chromosome.

References

Paulo G. Hofstatter, Gokilavani Thangavel, Thomas Lux et al. Repeat-based holocentromeres influence genome architecture and karyotype evolution. Cell 185, Issue 17, 3153-3168.e18 (2022)
https://www.sciencedirect.com/science/article/pii/S0092867422007978

Marco Castellani, Meng Zhang, Gokilavani Thangavel, Yennifer Mata Sucre, Thomas Lux, José A. Campoy, Magdalena Marek, Bruno Huettel, Hequan Sun, Klaus F. X. Mayer, Korbinian Schneeberger and André Marques. Meiotic recombination dynamics in plants with repeat-based holocentromeres shed light on the primary drivers of crossover patterning. Nature Plants, February 9, 2024
https://www.nature.com/articles/s41477-024-01625-y