Fungi Page 8
Some of the mutualistic relationships examined in this chapter are bewilderingly complex. Mushroom farming by ants and termites seems particularly intricate because it is dependent on so many physical and molecular interactions between the participants. But we misread biology by treating symbiosis as an exceptional phenomenon. No species exists without benefit from interactions with many other organisms. Fungi, along with other microbes, associate with every animal and plant. Many of these relationships are not as obvious as the growth of algae inside lichens or the development of sheaths of mycorrhizal fungi around root tips, but they are every bit as intimate. Insect guts may seem an unlikely place for complicated symbioses, but they teem with fungi. Researchers have identified hundreds of new yeast species inside beetles and know very little about what these fungi are doing. Some of them may be commensals, benefiting from food in the host digestive system without causing any negative effects, but mutualistic interactions are probably very common too. Detrimental relationships between pathogenic fungi and plants are similarly diverse and these are the subject of Chapter 5.
Chapter 5
Fungi as parasites of plants
Global impact
Parasitic fungi that grow on plants have reshaped the biosphere and caused the deaths of millions of people since the beginning of agriculture. Dutch elm disease and chestnut blight are examples of fungal pandemics that resulted in widespread ecological changes in the 20th century. These diseases destroyed billions of trees, remodelled the urban landscape in Europe and North America, and ravaged the broadleaf forests of the Eastern United States. Recent pandemics include ash dieback in Europe, and needle blights of pines in Europe and North America. The appearance of these tree diseases is a consequence of global commerce and the unwitting introduction of fungi that can attack plant species with no resistance to foreign pathogens. Climate change may be a contributing factor in the vulnerability of trees to fungal infection and is a major concern for forest management. The sight of dying trees is disturbing, but the wider ecological consequences attract little lasting attention. This is the way with the continuous remodelling of forests and other ecosystems by disease and human activity. People born after a destructive phase in forest history overlook the changes because they have no experience of the earlier richer environment.
Fungi that infect crops have more immediate and lasting effects on human populations. Crop failures have caused starvation, economic collapse, social conflict, warfare, and mass emigration. Rusts and smuts that attack cereals have been a source of immense misery throughout history and comparable suffering has resulted from other kinds of fungi that destroy rice. As the human population swells, scientists are engaged in a global initiative to understand and combat fungi that infect staple crops. Farmers and consumers are affected by fungi that damage fruit crops including cacao, citrus, coffee, and grapes, and a wider range of commodities including natural rubber. The study of fungal diseases of domesticated and wild plants is part of the wider field of plant pathology that also includes research on viruses, bacteria, protists, nematodes, and insects.
Rusts
Stripe rust is a highly destructive disease of wheat that poses a significant threat to global food security. It is widespread across wheat-growing regions and has been called the ‘polio of agriculture’. Stripe rust, also known as yellow rust, is caused by the rust fungus Puccinia striiformis. This microorganism feeds on wheat and a thorny shrub called barberry, alternating between these plant hosts according to its stage of development (Figure 22).
Stripe rust on wheat produces lines of yellow blisters between the leaf veins that are filled with spores. The spores in the blisters are urediniospores (also called urediospores and uredospores) and spread the infection through a crop when they are dispersed by wind. When urediniospores germinate on wheat, their filamentous hyphae extend over the leaf surface and are capable of detecting tiny ripples associated with the underlying cells. The sensitivity of the fungus allows it to angle its growth across the leaf rather than along the length of the blade. By growing in this direction, the fungus maximizes the likelihood of finding open breathing pores, or stomata, which offer easy access to the interior of the plant. Germination of the spores is timed to coincide with the cooler morning temperatures when the stomata are open. Wheat plants close their stomata in late morning to reduce water loss.
22. The complex life cycle of a cereal rust.
As the cereal infection progresses, the rust begins to produce a second type of spore called the teliospore in the same blisters. Teliospores are dark brown. These spores do not infect wheat. They serve instead as a reservoir for the disease, surviving in the dead leaves or the soil. When environmental conditions are suitable, the teliospores germinate and produce a third type of spore. These are basidiospores. This developmental cycle is very complicated, but the challenge of writing and reading this step-by-step description is necessary for an understanding of the biology of the rust fungi. On a positive note, comprehension of the rust life cycle makes everything else in fungal biology seem quite straightforward.
Rust basidiospores are formed by the same process that produces spores on the surface of mushroom gills. This similarity in development is not surprising because genetic evidence shows that rusts and mushrooms are related and mycologists group both kinds of fungi in the basidiomycetes. When the rust basidiospores are dispersed in air they infect the alternate host, the barberry shrub. Rather than searching for open stomata on barberry, the rust punches its way straight through the leaf surface. This direct penetration process is widespread among fungi that infect plants. The subsequent damage done to barberry does not concern cereal growers directly. The problem with the shrub is that the fungus uses its leaves as a platform for producing a fourth type of spore, called the aeciospore, which infects wheat.
The formation of aeciospores occurs after two strains of the rust unite on the barberry leaves. Rather than growing towards one another and fusing like mushroom colonies, however, cells of the rust are carried by insects that fly from shrub to shrub. The rusts produce sugary nectar that attracts flies and the cells, called spermatia (or pycniospores), stick to the body of the insects as they feed. This is comparable to the process of insect pollination in flowers. After ‘pollination’, aeciospores are formed and are shed from the underside of the barberry leaves and infect wheat leaves. Each aeciospore carries a pair of nuclei, one from each of the strains brought together by the insects. This means that the aeciospores are heterokaryotic, like the mycelia of mushrooms whose compartments contain pairs of nuclei after two homokaryons fuse in the soil.
In a more remarkable instance of fungal pollination, the rust Puccinia monoica prevents flowering in mustard plants and turns the green stem and leaves of its host into bright yellow imitation flowers. Bees and other insects are attracted by the yellow coloration and aromatic molecules released from the infected tissues. As they feed on nectar associated with the fungus, they become covered with its spermatia and carry them to other ‘flowers’ where the pollination process is completed. After pollination the rust produces airborne aeciospores that infect grasses, which are its alternate hosts.
The formation of urediniospores, teliospores, basidiospores, spermatia, and aeciospores may seem a fantastically convoluted way of life, but each phase of development serves a critical function in perpetuating the rust fungus. Rust pollination creates new combinations of nuclei from compatible mating types of the rust and these are transmitted through the urediniospores and teliospores. Fusion of nuclei and meiosis in the teliospores produces basidiospores whose single nuclei contain novel combinations of the genes from the two mating types. Again, these events are comparable with the formation of homokaryons, heterokaryons, and spores in mushrooms described in Chapter 3.
Intensive agriculture has allowed cereal rusts to sidestep the barberry part of their life cycles. With the cultivation of summer and winter wheat, the fungus has a source of food for most of the year and can attack successive
crops using urediniospores alone. Warmer temperatures associated with climate change may be exacerbating this problem. In regions where winter temperatures are low enough to kill the urediniospores, the barberry stage can still be omitted by the spread of spores from infected wheat in warmer areas. Over many growing seasons, the edited life cycle may weaken the fungus by preventing the genetic recombination that takes place on barberry. The high levels of genetic variation among rusts suggest that they avoid this handicap by maintaining a background of barberry infection even when their urediniospores spread over long distances. This intermittent growth on barberry allows the fungus to adapt quickly to the introduction of new disease-resistant varieties of wheat developed through crop breeding programmes.
Airborne urediniospores spread stripe rust over thousands of kilometres in a stepwise fashion from crop to crop of susceptible plants. In North America, for example, cereal rusts spread northward along an established ‘Puccinia pathway’ that runs from Mexico to Canada. In a stripe rust epidemic in the 1950s, for example, the disease spread 2,400 kilometres from northern Mexico to North Dakota in six months. Movement of spores according to weather conditions and the availability of susceptible crops allows cereal rusts to spread in other wheat-growing regions. In China, for example, stripe rust disperses across wheat-growing provinces on easterly winds, creating a wave of epidemic disease over hundreds of kilometres of farmland. Rare cases of disease introduction also occur via a single-step invasion when a fungus moves over a great distance without infecting crops on the way. Stripe rust was carried from Europe to Australia on infected plants, or possibly on clothing, in the 1970s and then spread to New Zealand by windblown spores in 1980.
Black stem rust, caused by Puccinia graminis, was the probable culprit for the destruction of crops in the Roman Empire of the 1st century ad. These epidemics occurred during a period of wet and cooler weather and the resulting food shortages played a part in the decline of Roman civilization. Disease resistant varieties of wheat have been effective at reducing the impact of this disease, but the fungus continues to cause crop losses. A highly virulent strain of black stem rust discovered in Uganda in 1999 has spread to other wheat-growing countries in Africa and to Yemen and Iran. The evolution of new virulent strains of this rust is a relentless process. Our reliance on monocultures of cereals, and other crops, means that a single race of a fungus that can overcome the defences of its host has the potential to destroy a commodity that is grown over a wide geographical area.
Rusts are examples of biotrophic pathogens that feed on living plant cells without killing the host. Biotrophy enables the fungus to withdraw nutrients for days or weeks while it keeps producing spores at a feverish rate. The dependence of rusts on living host tissues is so unwavering that they cannot be grown in the laboratory on culture plates. Necrotrophs kill plant cells and feed on their contents. Necrotrophic growth is responsible for chestnut blight and Dutch elm disease (both caused by ascomycete fungi). Many fungi confuse this simple categorization by starting with a biotrophic interaction and shifting to necrotrophic behaviour as the disease progresses.
Parasite and pathogen are catch-all terms that many mycologists apply to biotrophs and necrotrophs. Rusts form colonies of branching hyphae that grow between leaf cells and absorb nutrients through structures called haustoria that protrude into the cells. Haustoria are similar to the arbuscules produced by mycorrhizal fungi because they dimple the membrane of the plant cell without breaking it. The resulting interface is like a hand (the haustorium) inside a glove (the membrane of the plant cell) and the fungus absorbs food across this tight connection.
Plants mount an immune response to attack by rusts. The plant is furnished with receptors that induce a cascade of defences when they are activated by molecules released by the fungus. There are two defence systems: a non-specific response to a common family of chemicals released by all microbes, and a specific response to fungi recognized by the plant. These are analogous to the innate and adaptive immune systems that have evolved in animals. One of the specific defence reactions is called the hypersensitive response. This triggers the death of plant cells in the immediate vicinity of the early infection, which has the effect of creating a barrier of dead cells that obstructs the spread of the fungus. In a continuing arms race between pathogens and hosts, an array of molecular processes has evolved in the rusts to thwart the plant defences.
More than 7,000 species of rusts have been described with a host range that extends from cereals to other flowering plants, conifers, and ferns. Many rusts do not engage in the complex life cycle described for the cereal rusts and only infect one plant species. The fungi that cause Asian soybean rust (Phakopsora pachyrhizi) and coffee rust (Hemileia vastatrix) are examples of rusts with this kind of truncated life cycle. They infect the leaves of their hosts with urediniospores and do not seem to engage in the pollination process and aeciospore formation on another plant. This is strange, because both of these rusts form teliospores and shed basidiospores into the air. It is possible that the basidiospores infect another plant species and that this cryptic phase of the life cycle has not been found. Logical places to search for these missing hosts would be East Asia, for soybean rust, and Ethiopia, for coffee rust, where the target crops originated.
Smuts
The smuts are another group of basidiomycetes that cause plant disease. Most of the 1,400 species of smuts infect grasses, including cereals, and sedges. Each smut is dedicated to killing a single plant species or handful of related plants and does not switch to an alternate host to complete its life cycle. Smuts do not produce as many spore types as the rusts. Sugar cane smut, caused by Sporisorium scitamineum, occurs in all areas where the crop is cultivated. The use of sugar cane in the production of biofuel ethanol has increased the interest in this pathogen. Infected plants bear a blackened stalk called a smut whip that is filled with teliospores. These spores can be spread to other plants or deposited in the soil.
When the smut teliospores germinate they form a short outgrowth from which a second spore type is produced. These spores are similar to the basidiospores of rusts, but they are called ‘sporidia’ by experts on smuts. Sporidia bud to form yeast cells and fusion of two of these yeast cells from different strains creates the invasive form of the fungus that penetrates the sugar cane plant. The smut induces the premature formation of flowering tassels by upsetting the normal hormonal balance in the plant. The normal tassel is a tall feathery structure called an arrow, but the fungus transforms this into the smut whip.
Similar growth processes play out in head smut of corn and covered smut of sorghum caused by other species of Sporisorium. The related smut, Ustilago maydis, infects the ovaries of corn and converts the kernels into swollen bags of teliospores. Infected corn kernels are used as a flavourful ingredient called huitlacoche in Mexican cooking. Huitlacoche was part of Aztec, Hopi, and Zuni cuisine long before the Spanish conquests in the 16th century. The yeast phase of the smut grows in culture, which makes it easier to manipulate than rusts that cannot be grown separately from their plant hosts. Ustilago maydis has been used as a model for cancer research. Disruption of a gene in the smut fungus called brh2, which is related to the human tumour suppressor gene BRCA2, results in a deficiency in DNA repair mechanisms. This is consistent with a mechanistic link between mutations in the human gene and an increased risk of developing breast cancer.
Some smuts show astonishing finesse in the way that they control the development of their hosts. A beautiful example of this parasitic manipulation is seen in the infection of campion flowers by the smut Microbotryum violaceum. When the fungus infects the female flowers it suppresses the formation of the ovaries and stimulates the production of the male organs called stamens. Normal stamens bear anthers that hold pollen grains, but the fungus replaces the pollen with its teliospores. This subversion of floral development allows the smut to make use of butterflies and other insect pollinators to disperse its spores.
Ascomycetes and o
ther plant pathogens
Trees are plagued by a staggering number of fungi. Chestnut blight and Dutch elm disease are caused by ascomycetes that destroy the vascular tissues that convey water and nutrients through trees. Cryphonectria parasitica is the chestnut blight pathogen, whose spores are spread by wind, insects, and birds. Bark beetles that chew tunnels in the sapwood of elm trees transmit the spores of Ophiostoma ulmi and Ophiostoma novo-ulmi, responsible for Dutch elm disease. Ash dieback, which was first identified in Britain in 2012, is caused by windblown spores of Hymenoscyphus pseudoalbidus (also known as Chalara fraxinea). Symptoms include leaf loss and dieback of branches and twigs. Needle blights of conifers are produced by ascomycetes that do not spread beyond the needles. They do not kill trees outright, but debilitate the host slowly by damaging the foliage year after year. Ascomycetes that produce anthracnose diseases of broadleafed trees have the same effect.
Powdery mildews are ascomycetes that attack plant species in many different families, and damage crops including wheat and barley, grapes, onions, apples and pears, cucumbers, and strawberries. The common name refers to the formation of chains of spores that coat infected leaves in a white powder. Powdery mildews produce haustoria in the outermost cells of the leaf and develop an extensive mycelium on the surface of the host. Most species do not penetrate deeper into the plant tissues. But despite the superficial nature of the invasion, powdery mildews cripple their hosts by diverting nutrients to support the mycelium. They suck the plants dry. The haustoria of some mildews are simple knobs, but Blumeria graminis, that infects barley and other grasses, forms haustoria with long finger-like extensions.