Rust never sleeps

16 August 2013 by Malcolm Campbell, posted in Biology

There’s more to the picture, than meets the eye." from Hey Hey, My My (Into the Black) off the album Rust Never Sleeps (1979) by Neil Young (1945- )

When you look down, it’s as though you are seeing the feet of Tin Woodman in his introductory scene from The Wonderful Wizard of Oz.

Rusted.

Coated in a fine orange dust.

And dusty it is.

If you merely walk through the grass, let alone stomp your feet, clouds of fine, rust-coloured powder swirl about your feet. The powder gently settles onto neighbouring plants, adding to the sunset hues of the normally green grass.

You are looking at the handiwork of a rust fungus. In keeping with their name, rust fungi release spores that bestow a rust-like appearance wherever they come to rest. And, just as their metallic counterpart can cause machinery to seize up, fungal rust can similarly bring plant growth and reproduction to a grinding halt.

Rust fungi are a major cause of plant disease. They are obligate parasites, in that they require a living plant host in order to complete their life cycle. While there are some generalist rust fungi that can infect a broad range of plants, most of the 7000 or so species of rust fungi are relatively specialised pathogens. That is, most rust fungi species have a rather limited range of plants that they can infect.

Rust infection is yet another wonder of nature.

The orange spores that festoon shoes are spread by wind, water or animals. When they come into contact with a plant surface, they adhere to it by producing a specialised mucous-like “glue”.

When it has adhered to the plant surface, a spore produces a finger-like protrusion, a germ tube. Just like a finger, the germ tube “feels” its way across the plant surface, probing for points of entry into the plant. The favoured points of entry are stomata, pores located on leaf surfaces. Stomata are like tiny mouths on leaf surfaces, enabling the exchange of water and carbon dioxide, so that photosynthesis can take place within the leaf. They are an ideal entry point for the fungus to push in between cells, to enter the plant tissues and gain access to the nutrients that they need there.

When a germ tube identifies an individual stoma, it flattens to form a specialised fungal structure, the appressorium. The appressorium is like a launching pad for a full on assault of the plant. The appressorium produces another specialised fungal structure, the infection peg. Like a minute wedge, the infection peg pushes between the plant’s epidermal cells to enter the tissues beneath. There it makes yet another specialised fungal structure, the haustorium.

The haustorium enables the fungus to pirate plant resources. The haustorium surface is peppered with specialised transporters. These transporters capture sugars and amino acids made by the plant, so that they can be used by the fungus.

The fungus makes use of the pirated plant nutrients to complete the fungal life cycle. It utilises plant-derived nutrients to build pustules. These pustules contain new spores that will themselves spread to new hosts, beginning the life cycle all over again. The entire cycle can be completed every 10-14 days, resulting in a dramatic spread of the fungus in areas where susceptible host plants reside.

The remarkable rust fungus life cycle is reliant on the perception of plant-derived cues. These cues inform the fungus when to generate the distinct infection structures. Specifically, the cues function to direct changes in the manner in which fungal genes are used. Some genes are brought into action, while the activity of others is quelled. These orchestrated changes in gene function ensure that the fungus invests its energies into appropriate activities, like appressorium formation, at the right place and time.

Clearly, it is disadvantageous to the plant to provide cues to the fungus that result in the loss of plant resources. In fact, it would be a great advantage to the plant if it could provide no cues, or minimally, miscues or misdirections, so as to outmanoeuvre the fungus. Alternatively, and perhaps even better, if the plant were able to produce an active defence, by recognising when it was under attack from the fungus, it could prevent the fungus from doing its dirty work.

Not surprisingly, the interests of the plant are at odds with the interests of the rust fungus. The fungus aims to capture plant resources, while the plant aims to protect those same resources. Given that this conflict of interest has been in existence since plants have been available as a source of nutrients for fungi, how is it possible that rust fungi are still able to infect plants? Shouldn’t plants have been able to find ways to outmanoeuvre rust fungi?

It turns out that evolution has equipped plants with a means by which to outmanoeuvre rust fungi. The mechanism in question is resistance genes. Resistance genes, known as R genes, reside in the genomes of potential host plants. R genes enable potential host plants to recognise invading fungi and mount a defence against infection.

R genes encode proteins that generally detect some component of the fungal infection machinery. That component might be a component of the fungal cell wall, or a specific protein that the fungus uses to gain entry to the plant’s resources. The plant’s R gene product can be thought of like a lock, and the fungal product it recognises as a key. If the key fits in the lock, the plant unleashes its defences against the fungus.

But here’s the thing.

Plants will only be resistant to those fungi for which it has R genes that enable recognition of those fungi. And evolution doesn’t just work in the plant’s favour.

Just as evolution can give rise to R genes that help the plant recognise a fungal invader, evolution can also provide the fungus with altered features and proteins that either mask it from detection, or provide it with a new mode for entering the plant. If evolution equips the fungus with a means by which to evade an R gene, it will be able to pirate the plant’s resources once more.

And that is precisely what has happened over evolutionary time.

Plants are resistant to those fungi where the R gene product recognises a fungal feature. This fungal feature is said to be an avirulence factor, the product of an avr gene. The avr gene prevents the fungus from being virulent. Specific combinations of plant R genes and fungal avr genes result in plant resistance. But every now and then, fungi evolve a new virulence factor that enables them to be an effective pathogen again.

The plants and fungi are involved in an evolutionary arms race. R genes and virulence genes are constantly deployed in a battle to one-up each other – to detect or to evade detection. The consequence of these arms races is incredible specificity of fungal pathogens. Fungal evolution works, generation over generation, to overcome the latest R gene, to pathogenise their putative host.

This arms race is encapsulated in the gene-for-gene model, originally proposed by Harold Henry Flor in the middle of the last century from his studies of fungal rust pathogens of flax. In keeping with Flor’s original model, specific interactions between R-gene products and avr gene products have been shown to underpin flax resistance to rust fungi.

What is truly amazing is that we can see the rust fungus-plant arms race in action within our lifetimes.

In 1998, a virulent rust pathogen emerged that infected wheat. This new fungal strain of wheat stem rust, called Ug99, arose in Uganda (providing the “Ug” designation). Ug99 has wreaked havoc on wheat production in Africa, because it is virulent even in the face of the R genes spread across 90% of cultivated wheat varieties. As such, Ug99 is a significant threat to global food security.

Ug99 provides evidence of the ongoing arms race between wheat stem rust fungi and wheat. Fortunately, our knowledge of how these arms races work also gives us reason for hope. While Ug99 emerged as an evolutionary innovation to overcome R genes in many cultivated wheat varieties, it may be that there are R genes in other plants for which the Ug99 virulence gene is, instead, an avr gene.

As reported in today’s edition of Science, two research groups have identified two different R genes, Sr33 and Sr35, that confer resistance to Ug99.  Both R genes were identified in wheat species that are different from bread wheat and pasta wheat species. Sr33 was identified in a wheat species that is a progenitor to bread wheat; whereas, Sr35 was found in a more distantly related wheat species. In both cases, the R gene products look like receptors for Ug99 avr gene products, but it is not yet know what these Ug99-derived avirulence factors may be.

Importantly, evolution has provided two distinct R genes that enable the recognition of Ug99. When either Sr33 or Sr35 was introduced, by genetic engineering, into wheat cultivars normally susceptible to Ug99, the acquisition of the new R gene was sufficient to confer resistance to Ug99.  It is hoped that the two R genes may be used together to provide highly robust resistance to Ug99 in cultivated wheat varieties in the future. Making use of the products of evolution, scientists can give susceptible plants an edge in the ongoing plant-pathogen arms race, and provide some additional insurance against disease-related food crop losses.

We tend to think of evolution as a rather static process, because we often don’t see it in action within a human lifespan. We generally map evolutionary processes onto geological timescales. The rust fungus-plant arms race shows us that evolution is constantly in play. Like rust, evolution never sleeps.

References:

Dodds PN et al. (2006) Direct protein interaction underlies gene-for-gene specificity and coevolution of the flax resistance genes and flax rust avirulence genes. Proceedings of the National Academy of Sciences 103: 8888-8893

Flor HH (1942) Inheritance of pathogenicity in Melampsora lini. Phytopathology 32: 653-669

Flor HH (1947) Inheritance of reaction to rust in flax. Journal of Agricultural Research 74: 241-262

Flor HH (1955) Host-parasite interaction in flax rust - its genetics and other implications. Phytopathology 45: 680-685

Flor HH (1971) Current status of the gene-for-gene concept. Annual Review of Phytopathology 9: 275-296

Periyannan S et al. (2013) The gene Sr33, an ortholog of barley Mla genes, encodes resistance to wheat stem rust race Ug99. Science 341: 786-788

Saintenac C, Zhang W, Salcedo A, Rouse MN, Trick HN, Akhunov E & Dubcovsky, J (2013) Identification of wheat gene Sr35 that confers resistance to Ug99 stem rust race group. Science 341: 783-786

Singh RP et al. (2011) The emergence of Ug99 races of the stem rust fungus is a threat to world wheat production. Annual Review of Phytopathology 49: 465-481

Images: All photographs by Malcolm M. Campbell.

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