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By Jeff Ellis 14 May 2021 6 min read

Rust is a formidable and agile opponent for wheat breeders.

A little over one hundred years since Ilya Metchnikoff and Paul Ehrlich were awarded the Nobel Prize for pioneering work on the animal immune system and establishing the field of immunology. During the last 12 months the Covid-19 pandemic has strongly refocused peoples’ attention on immunology and its applications to society and human health and we have been amazed by the rapid progress made in developing several effective vaccines against the disease.

Apart from human diseases, it is easy to overlook that our health also depends on appropriate nutrition, much of which is derived from plants. Crops also suffer disease, sometimes occurring in their own pandemics, which threaten regional and international food supplies and can lead to political unrest and large death tolls.

At about the same time as the development of the field of animal immunology, Rowland Biffen used classical Mendelian genetic analysis to show that plants also have an immune system. His work showed that single gene differences could determine whether wheat was resistant or susceptible to the fungal disease rust. These genes are referred to as rust resistance genes.

Because wheat supplies 20 per cent of human food and rust diseases are among the most serious of wheat causing major yield losses, plant breeders were quick to adopt Biffen’s discovery to breed rust resistant wheat varieties for farmers.

Over the last 25 years there has been an explosion of basic knowledge about how the plant immune system functions, and we are now at a point where this knowledge is flowing into practical applications in agriculture.

Wheat rust resistance seen in the field, with a five gene stack wheat line (green plants on the right) compared with a susceptible line (dead plants on left).

New developments in crop breeding required

Although initially highly effective, by the mid-20th century it was clear that rust resistance in wheat is frequently short-lived because new strains of the rust pathogen soon evolve that break the genetic barrier of resistance. The challenge faced by wheat farmers/breeders is similar to the medical problem of evolution of antibiotic resistance in bacteria which has eroded many previously successful therapies.

As a result, preventing rust in wheat has become a continuous, laborious and repetitive process for plant breeders. It involves discovering new rust resistance genes and transferring them into new wheat varieties while simultaneously maintaining grain yield and quality. Some of the rust resistance genes used by breeders have been brought into wheat from other cereals like rye and even from wild grasses. This process has involved complex chromosome manipulation techniques, an early and widely applied form of genetic engineering that has not generated the same concern among consumers as newer technologies involving gene cloning.

However, two earlier discoveries have increased and lengthened the effectiveness of rust resistant wheat varieties giving plant breeders some brief breathing space before new pathogen strains evolve. First, breeders try to include several different rust resistance genes, each effective against the prevailing rust strains. This process is called resistance gene stacking which has proven effective in slowing evolution of new pathogen strains. Second, epidemiologists realised that the speed of evolution of virulent rust strains increased with the pathogen population size. So farmers are encouraged to grow only rust resistant wheat varieties which greatly reduce the population size and evolution of the rust pathogens. This is an example of the recently much-discussed term “herd immunity”.

In a major breakthrough starting 25 years ago, rust resistance genes were cloned and their protein products identified. We now know that rust resistance proteins possess the ability to detect the presence of invaders and then trigger the expression of resistance responses that block the growth of the pathogen.

A microscope image of wheat rust growing in a wheat leaf. The green stained material is fungal hyphae growing inside the leaf. The smaller circular objects in the centre of the image are spores that are produced by the fungal infection site which have erupted through the leaf surface and will be dispersed by the wind to reinfect more wheat plants. This image shows the infection site that grows after a single spore has infected the leaf.

New breakthroughs herald a new age in plant disease resistance

These basic advances have provided insights into the fundamental basis of rust resistance but have not so far been translated into practical disease control in agriculture. However, this is now changing.

Important advances in wheat genome sequences over last five years have allowed rapid cloning of many rust resistance genes and also techniques to transfer these genes into wheat to deliver rust resistance of practical value.

These advances have been highlighted in the recently published work of an international team of scientists led by the CSIRO. These scientists have taken five highly effective rust resistance genes cloned from wheat and its relatives, linked these genes together in one large gene stack and transferred the stack into a variety of wheat that was susceptible to rust.

The resulting transformed wheat plants have been tested under greenhouse and field conditions and have high levels of resistance to several strains of the wheat rust fungus including some of the recently evolved highly virulent strains that have seriously threatened world wheat production. This represents a major advance that opens the door to a step change in protecting wheat from rust.

Using traditional breeding methods, stacked genes occur at different locations on plant chromosomes. Therefore, assembly of gene stacks is laborious and slow and when the resulting wheat variety is used in further breeding for additional varietal improvements the hard-gained gene stacks fall apart due to the process known as random genetic assortment of chromosomes.

In contrast, the gene stacks assembled in the laboratory and transferred to wheat occur at a single location on one chromosome and in subsequent breeding are inherited as a unit. This will greatly facilitate development of new varieties by simplifying and speeding up the breeding process allowing wheat breeders to focus more heavily on other critical characters like yield and drought resistance.

Additionally, this approach can be used to include resistance genes for many other crop types and against other pathogen diseases such as rice blast and potato blight. It would also have the added benefit of reducing the need for farmers to spray their crops against disease, saving them time, money and improving environmental outcomes.

A diagram of a five gene stack. Each gene is called Sr, for stem rust resistance, and given a unique identifying number. The box labelled hyg indicates a gene that was used to create transgenic wheat plants in tissue culture. It confers resistance to a chemical called hygromycin.

Out of the labs and into the fields

The plan is now to clone many rust resistance genes, assemble them into a variety of different gene stacks and transfer them to wheat. These stacks can then be transferred by traditional breeding methods into new wheat varieties to provide high levels of rust resistance.

The gene stacks could be released simultaneously to provide a diversity of resistance or more probably released singly and sequentially to replace varieties when gene stacks are eventually overcome by pathogen evolution. While in theory gene stacks should provide durable rust resistance, this can only be confirmed by long term experience and not experiments.

In the continuing struggle against rust evolution the ‘street wisdom’ is never bet against the pathogen but these new technologies will greatly improve the odds wheat breeders face.

These new developments in rust control use what is popularly referred to as genetic engineering. There has been strong push-back against this technology and at present there is no commercial production of genetically engineered wheat. Nevertheless, resistance gene stack technology is being used in the US and more recently in Africa to control the Irish Famine disease, late blight in potato.

Just as with Covid-19, it may take an unprecedented rust pandemic that threatens global wheat production with all the serious political and societal flow-ons to propel the application of basic research into practical applications for food security. And just as with the rapid development of vaccines against Covid-19, the results of study of the plant immune system and the pre-commercial practical developments are already on the shelf ready for when the desire and need for application arises.

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