Emerging Fungal Threats to Plants and Animals Challenge Agriculture and Ecosystem Resilience

Abstract

While fungi can make positive contributions to ecosystems and agro-ecosystems, for example, in mycorrhizal associations, they can also have devastating impacts as pathogens of plants and animals. In undisturbed ecosystems, most such negative interactions will be limited through the coevolution of fungi with their hosts. In this article, we explore what happens when pathogenic fungi spread beyond their natural ecological range and become invasive on naïve hosts in new ecosystems. We will see that such invasive pathogens have been problematic to humans and their domesticated plant and animal species throughout history, and we will discuss some of the most pressing fungal threats of today.

FIGURE 1

Mass mortalities of midwife toads, Alytes obstetricans, caused by Batrachochytrium dendrobatidis (photo: Matthew C. Fisher).

FIGURE 2

Mass mortalities of little brown bats, Myotis lucifugus (photo: Alan Hicks).

FIGURE 3

Factors influencing the emergence of infectious diseases of crop plants. These include features of the pathogens themselves as well as changes forced by the opportunities given to and pressures placed upon pathogens externally, as a result of human activity. Pathogen features prompting the emergence of new diseases include specialized genomes, sexual reproduction, large populations, and plentiful variation, which contribute to evolutionary potential. Invasiveness is key to the appearance of new emerging infectious diseases. This pathogen trait has natural components including high virulence and the capacity to infect multiple hosts and to transmit vertically, as well as such traits as long-distance dispersal and a propensity to undergo host shifts and jumps. Such traits may be natural or appear as a result of opportunities provided by anthropogenic changes to the environment. Such anthropogenic opportunities include climate change and trade and transport, introducing pathogens to new places, niches, and hosts. They may also take the form of pressures placed on pathogens by the continuous cultivation of a single crop year-round leading to genetic uniformity of available hosts over large areas. Such elite varieties are the product of artificial selection, which is the main driver of host evolution when the host is a domesticated crop. Host evolution can then drive pathogen evolution, leading to the appearance of new emerging infectious diseases and subsequent selection of new, resistant elite varieties. In addition, during the domestication of a crop, pathogens may be directly domesticated, short-cutting their adaptation to a particular host.

FIGURE 4

The wheat pathogen, Zymoseptoria tritici. (a) Scanning electron micrograph showing Z. tritici (green) on the surface of a wheat leaf. False color image. (b) Confocal fluorescence micrograph showing green-fluorescent protein-tagged Z. tritici (turquoise) beginning to colonize mesophyll tissues of a wheat leaf (purple). False-color image. (c) Confocal fluorescence micrograph showing Z. tritici (turquoise) proliferating with a wheat leaf at a late stage of infection. The fungal mass on the right of the image is a nascent pycnidium, the structure in which sporulation takes place. (d) Severely diseased wheat leaf showing Z. tritici symptoms, including mature pycnidia (black). Each black spot can release hundreds of spores. (Photos: Helen Fones; GFP-tagged Z. tritici: reference .)

FIGURE 5

Fusarium oxysporum f. sp. cubense race 4 (Panama disease). Culture on potato-dextrose agar in a laboratory, showing characteristic purple coloring. (Photo: Helen Fones.)

FIGURE 6

Hymenoscyphus fraxineus on ash. Left, hyphae (green; stained with fluorescein isothiocyanate-labeled wheat-germ agglutinin) of H. fraxineus, visualized by confocal microscopy, growing over and out of the vascular tissue of an ash leaf (red; stained with propidium iodide). Right, ash die-back symptoms on an ash seedling under laboratory conditions. (Photos: Helen Fones.)