Plant diseases

To truly understand the evolution and ecology of diseases, they must be studied not only in human-made environments such as laboratories or agricultural fields, but also in natural populations.

Like animals, plants also suffer from infectious diseases caused by microbes, including viruses, bacteria, protists, and fungi.

In order to really understand the evolution and ecology of diseases, they have to be studied in natural populations in addition to the human-made environments such as laboratories or fields. Like animals, plants have microbial, viral, protozoan and fungal infections. Furthermore, working on plants is not as limited by ethical questions as animal or human research. Ethical restrictions are further reduced if the disease cannot infect crop plants, as is the case with powdery mildew of ribwort plantain. As sessile organisms, plant populations and their disease status can be easily followed from year to year. The disease research conducted on ribwort plantain populations in the Åland Islands, and the long-term dataset collected through it, are in their scope unique even on a global scale.

The biology of the mildew

Powdery mildews are fairly common plant diseases both in cultivated environments and in nature. Powdery mildew can be seen with the naked eye as a powdery layer on the surface of leaves, formed by fungal hyphae, spores, or both. From the surface, the mildew develops structures that penetrate the plant’s tissues, through which it absorbs nutrients. Some powdery mildews are able to infect several plant species, while others are specialized to a single host species.

The ribwort plantain powdery mildew occurring in the meadow network of the Åland Islands (Podosphaera plantaginis) is specialized to live on ribwort plantain. The fungus does not kill its host plant, but it can hinder its growth and reduce its ability to cope with other environmental stress factors. During the growing season, the mildew spreads from plant to plant and from population to population by means of small asexual spores. Toward autumn, it increasingly produces sexual resting spores, which can be distinguished as dark dots on the leaf surface. With the help of these resting spores, the mildew survives the winter and infects its host again the following summer.

Both ribwort plantain and the mildew are relatively easy to work with in laboratory and greenhouse experiments. Mildew infection can be reliably detected with the naked eye, unlike, for example, viral diseases, which facilitates observations in nature. The ribwort plantain powdery mildew also completes its entire life cycle on ribwort plantain, which simplifies the construction of ecological models.

Powdery mildew

Powdery mildew infections in ribwort plantain populations in the Åland Islands are surveyed every autumn together with the Glanville fritillary survey. During the mildew survey, the surveyors visually inspect the leaves of ribwort plantain for mildew and record their observations for each population. The proportion of infected populations among all surveyed populations has varied between less than five percent and about thirty percent during the years 2001–2024. This is a good example of how rare it is to encounter devastating epidemics in natural populations that are typical of fields or other human-made monocultures.

Using the data collected in the surveys, it has been possible to show that infection by mildew is significantly influenced by the proximity of populations to one another. One might expect more diseases to spread between populations that are closely connected.In fact, more mildew has been observed ribwort plantain populations that are more isolated. Close connections between populations increase gene flow among host plants and thus their evolutionary potential and the development of disease resistance. Laboratory tests have confirmed that this effect is indeed due to the resistance of the host plants. Genetic diversity plays a key role in the evolution of resistance. Habitat fragmentation isolates populations from one another and can therefore increase their susceptibility to diseases.

Genetic samples have revealed that the powdery mildew of ribwort plantain is highly diverse in the Åland Islands. Laboratory studies have shown that mildew strains vary in their life cycle speed and optimal growth temperatures as well as their susceptibility to their mycoparasite Ampelomyces. Both abiotic and biotic environmental factors are likely to increase the diversity of the mildew in nature, because the most advantageous traits depend on the prevailing conditions and vary from one situation to another. It is therefore not sufficient to study the disease only in the laboratory.

Phomopsis fungus

Phomopsis ordinaria is another fungal disease occurring on ribwort plantain in the Åland Islands. While powdery mildew takes its nutrients from living leaf tissue, Phomopsis exploits dead tissue. Phomopsis  spreads from plant to plant via beetles belonging to the weevil group and infects the flowering stems of ribwort plantain. The disease kills the developing seeds or even the entire plant. Phomopsis is common in ribwort plantain populations, but epidemics are small, often involving fewer than ten infected plants.

During the autumn survey in 2018, Phomopsis was also surveyed, although only in 261 populations. As many as 47% of the populations studied were infected. In most populations fewer than ten percent of individuals plants were infected. The severity of the disease on individual plants, that is, its virulence, was also examined by calculating the proportion of infected flowering stems. In populations where more than ten percent of the plants were infected, the disease was also highly virulent.

This disease can also help us understand the evolution of pathogens and their hosts. Relevant questions include: Why the epidemics remain so small  and why does this fungus kill its host? 

Viruses

Research on plant viruses often focuses on crop species, and the prevalence and diversity of viruses in natural environments are less well known, even though viruses can move between wild and cultivated plants. The adoption of new methods, such as metagenomic analyses and the use of small RNAs, has made it possible to investigate these phenomena in greater detail than before. Studying the diversity of pathogenic microbes in nature can provide insight into the factors that influence the long-term coexistence of hosts and parasites, and thus help to predict when and where disease risk is highest.

DNA and RNA samples collected from the Åland Islands have been used to study viruses occurring in ribwort plantain. The prevalence and diversity of viruses vary among populations, but infections have been detected in nearly all of the populations examined. In infected plants, more than one virus species is fairly common. In the 2013 dataset, twenty percent of the virus infections were polymicrobial. Viruses are more common in symptomatic plants, but they also occur in asymptomatic individuals. In addition, five new virus species have been discovered in these studies, which has generated interest in the international level. One of them (Plantago lanceolata latent virus, PlLV) has already been detected elsewhere in the world: in France, Italy, Spain, and Iran.

Mycorrhiza

Mycorrhizae are symbioses formed between fungi and plants, which are usually mutualistic, meaning that both the plant and the fungus benefit from the relationship. Fungal hyphae are more efficient than plant roots at acquiring nutrients and water, and the plant takes some of these resources collected by the fungus for its own use. In return, the fungus receives carbohydrates produced by the plant through photosynthesis. Mycorrhizae play a very important role in plant ecology, and almost all plants in the world form such symbioses.

In one study, root samples were collected from ribwort plantain populations in the Åland Islands that differed in their history of powdery mildew infection. Genetic samples were used to determine the structure of the fungal community in the root system. By comparing healthy and infected populations, it is possible to assess whether fungal diseases of the aboveground parts affect the fungal community of the roots. Such interactions between the microbiota of roots and shoots have been rarely studied only rarely in natural populations.

The genetic samples have also been used to examine the presence of pathogenic and mutualistic fungi in the roots of ribwort plantain. In addition, the roots are examined under a microscope for mycorrhizae. A higher abundance of mycorrhizae is generally beneficial for the plant. Mutualistic fungi in the root system may strengthen the plant’s own defense against diseases.

Preliminary findings indicate that there is variation in the root fungal communities among ribwort plantain populations. The community appears to be influenced at least by the plant population itself and to some extent also by the population’s history of powdery mildew infection. The next step is to determine whether the proportions of pathogenic and mutualistic root fungi differ between mildew-infected and mildew-free populations, and whether some belowground fungi are more common in populations affected by mildew.