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How Do Hybrid Species Overcome Genome Shock?


The cotton used to make our clothes comes from a hybrid species. Credit: zhuda/iStockphoto

By Murray Cox

How do hybrid species like cotton and ligers combine different genes, proteins and chromosomes, and can this knowledge be exploited for agriculture?

While individuals from one species usually cannot cross with members of a different species, these crosses do sometimes occur, including well-known examples such as mules (the offspring of donkeys and horses) and ligers (the offspring of lions and tigers).

While mules and ligers are relatively uncommon, other hybrid species are all around us. The cotton used to make our clothes comes from a hybrid species, as does the wheat in our bread. Hybrid species are also very common among the native plants of New Zealand and Australia, including several Eucalyptus species.

A major unanswered question in biology is how these hybrids arise, persist and thrive. Species are always competing. They can only survive by being extremely well adapted to their environment, and this is also true for the complex molecular machinery found in their cells. Like racing cars, species need a finely tuned engine to compete.

Most individuals inherit this well adapted molecular machinery from their parents, who come from the same species and therefore are broadly very similar. In contrast, hybrid species appear when cells from two very different parent species are suddenly thrown together. A new species forms instantaneously.

This suggests a problem. The two parent species of every hybrid are finely tuned. When their cells are merged together, the new hybrid carries two slightly different sets of proteins and protein complexes. Sometimes the different versions of these proteins still work well together, but often they do not. This leads to a process that the Nobel-winning scientist Barbara McClintock described as “genome shock”.

So how do hybrid species survive, and indeed, often thrive? My research group has found part of the answer to this question by studying a group of fungi that live in pasture grasses.

When thinking of fungi, the first image to spring to mind might be the green fuzz that grows on vegetables left too long in the fridge. But these fungi, called epichloe endophytes, are beneficial.

Epichloe fungi grow as an extensive network right throughout the grass plant. Fungal cells sit next to grass cells in a close symbiotic relationship: the plant gives the fungus a place to live, while the fungus produces chemicals that kill insects that try to eat the grass. This hidden relationship is a key reason behind the success of New Zealand and Australia’s dairy, cattle and sheep industries.

The epichloe endophytes include a large number of hybrid species. We focused on one of them, together with the two parent species that originally produced it.

In a paper published recently in PLOS Genetics we examined levels of RNA – the instruction sheets needed to build proteins. As a general rule, the more copies of RNA that exist for a particular protein, the more of that protein the cell makes. Because the amount of any given protein needed by the cell is finely tuned, so too are the number of RNA copies in the cell. By knowing how many RNA copies are present for any given gene, it is possible to observe how the overall molecular system of the cell is controlled and maintained.

Counting copies of RNA for every gene in a cell is technically challenging. We had to develop new statistical methods and computational tools to sequence, and then analyse, hundreds of millions of RNA molecules. By finding changes that distinguish the two versions derived from each parent species, every RNA molecule in the hybrid could be assigned to one parental version or the other.

Since cells contain two versions of RNA (and therefore two versions of every protein), how do hybrid species keep their cellular machinery working? One possible solution is simply to carry over levels of the two RNA copies from each parent species. If one parent expresses a lot of its copy while the other parent expresses very little, the hybrid species might produce the two versions in exactly the same ratio. We discovered that this does not happen.

Another solution could be to produce RNA at the average levels of the two parent species. If one parent expresses a lot of its copy while the other parent expresses very little, the hybrid species might produce both versions at some level between the two. This does not happen either.

Instead, we found that the hybrid produces both versions at a level found in either one parent or the other. In terms of the protein machinery, this means that one version of most proteins does not get made. Determining which version gets switched off follows a complex, but regular, pattern.

Due to the technical difficulty of this work, a similar analysis has been performed on only one other hybrid species – cotton. Surprisingly, the complex patterns that describe which RNA version is switched on and off in the epichloe endophyte are almost identical to the patterns found in cotton.

This is unexpected because these two species are radically different. To begin with, cotton is a plant while the epichloe endophyte is a fungus. The two species also have very different lifestyles and live in environments with very different challenges.

These shared patterns suggest that there are universal rules that describe how gene expression needs to behave for hybrid species to control their two sets of protein machinery – regardless of which exact species those hybrids are.

The presence of universal rules is important because it suggests that research on one hybrid can tell us how gene expression works in a completely different hybrid species. This is especially useful because hybrids are often poorly studied even though they make up a large part of the agricultural sector, and are increasingly being recognised in nature.

Research is now focusing on which molecular mechanisms produce these shared patterns, with two avenues looking particularly promising. The first is searching for shared changes in promoter regions, the molecular switches that encode how much a gene is expressed. The presence of universal rules suggests that promoter regions may change in similar ways across different hybrids. The second direction is determining whether conserved patterns of expressions correlate with shared changes in genome structure, particularly the order of genes along the chromosomes.

Even without understanding their molecular basis, the presence of universal rules is helping to jumpstart research on understudied hybrid species. This will be especially useful for developing new agricultural species, including epichloe endophytes with broader repertoires of chemicals that protect crops against insect damage.

Murray Cox is Rutherford Fellow at Massey University’s Institute of Fundamental Sciences.