#130: Order Pucciniales, the Rust Fungi
Rust fungi – which are so named because of their characteristic, rust-colored spores – have the most complex life cycles of any fungi. These fungi are all obligate plant parasites and most have two hosts. To successfully cycle from one host to the other over the course of a year, rust fungi produce up to five different types of spores.
All rust fungi are placed in the order Pucciniales (phylum Basidiomycota, class Pucciniomycetes). Although in the same phylum as most mushrooms, none of the rust fungi form fruiting bodies large enough to be called mushrooms. The factor that ties them together with the other basidiomycetes is their sexual spore stage. Like all other members of the Basidiomycota that reproduce sexually, rust fungi produce sexual spores externally on structures called “basidia.”
Rust fungi are obligate plant parasites, which means they can only get nutrients from their plant host. Unlike other parasitic fungi, rusts produce structures called “haustoria” inside their host’s cells. Haustoria remove nutrients from the infected cell but are not designed to kill their host cell. However, cell death is often the eventual outcome of infection. Rust fungi have developed complex life cycles in order to maintain this balanced parasitism.
Before I describe the rust fungus life cycle, it will be useful to define the “primary host” and “alternate host.” The primary host is the host on which sexual spores (“basidiospores”) are produced. Mycologists have come up with a variety of terms for the primary host, including “definitive host” and “telial host.” I will use “primary host” because it is the most straightforward. The alternate host is the rust’s other host, i.e.: the one on which basidiospores are not produced.
The basic (which in this case means most complex) rust life cycle involves five stages and two plant hosts. Each stage is differentiated based on the host, the number of nuclei, and the function of the spores that are produced.
The rust life cycle begins in the spring, when a basidiospore lands on the alternate host. This spore germinates and – under the right conditions – infects the alternate host. Both the basidiospore and resulting mycelium have only one complete copy of chromosomes (n). Consequently, each fungal cell contains one haploid nucleus (monokaryotic). Summary: alternate host, n, alternate-infective spores.
Once the rust has established itself, it produces spores called spermatia on a structure called a spermagonium. The haploid, monokaryotic (n) spermatia are distributed to other spermagonia (by bugs, wind currents, etc.), where spores of different mating types have the opportunity to interact. If two spores with compatible mating types come into contact, they will fuse to create a dikaryotic (n+n) mycelium. In other words, this mycelium contains two dissimilar, haploid nuclei per cell. Summary: alternate host, n, mating spores.
The dikaryotic mycelium quickly sets about producing spores called “aeciospores” from structures called “aecia.” Since the new, dikaryotic mycelium is growing in the same place as the old mycelium, aecia often appear on the opposite side of the leaf from the structures produced earlier. This allows for some separation between the two stages. Aeciospores are dikaryotic (n+n) and are designed to infect the primary host. Large numbers of aeciospores are produced to increase the chances that one will land on a susceptible host. Summary: alternate host, n+n, primary-infective spores.
This is the main part of the rust’s life cycle. The rust aggressively infects its primary host, spreading within the host’s tissues as well as between hosts. Starting soon after infection and lasting until the end of the primary host’s growing season, the rust produces urediniospores on structures called “uredinia.” These spores are dikaryotic (n+n) and are designed to infect other susceptible primary host plants. Summary: primary host, n+n, primary-infective spores.
Towards the end of the primary host’s growing season, the rust starts producing teliospores from the uredinia, which are now called “telia.” Teliospores are thick-walled spores that cannot infect any plants but are designed to survive winter. At this point, the nuclei in each teliospore fuse together, resulting in diploid, monokaryotic (2n) spores. In the spring, each teliospore germinates and produces a structure called a “basidium.” Meiosis happens in the basidium, which then forms four basidiospores. These spores are carried by the wind to the rust’s alternate host to begin the cycle anew. Summary: primary host, 2n, resting (non-infective) spores.
Rusts have managed to modify this life cycle in a variety of ways. Some rusts may complete their life cycle on only one host, while others may skip one or more spore stages. For example, no alternate host has been found for Coffee Rust (Hemileia vastatrix), so it may be able to complete its life cycle on one host using only one spore type. A rust that uses only one host is called “autoecious,” while one that uses two hosts is termed “heteroecious.” Rust fungi are also diverse in their choice of host(s). Plant lineages infected by rusts include: angiosperms (flowering plants, including both monocots and dicots), gymnosperms (conifers, such as firs and cedars), and ferns. The primary and alternate hosts usually belong to two separate lineages. Cedar-Apple Rust (Gymnosporangium juniperi-virginianae), for example, alternates between a gymnosperm host and a dicot (angiosperm) host. Black Rust of Cereals (Puccinia graminis), however, sticks to the angiosperm lineage but alternates between monocot and dicot hosts.
One of the easiest modifications for rust fungi to make is the elimination of the alternate host. This would allow the fungus to infect its primary host when the alternate host is no longer available. An example of this modification is Puccinia spp. rusts on violets. These violet rusts likely once used various grasses as alternate hosts. However, violets in the forests are often not near any grasses. Dropping the alternate host would have allowed these rusts to expand their range into the forest. Without an alternate host, the rust may not need all five spore types to complete its life cycle. Therefore, it is not uncommon to find a rust that is missing one or more spore stages.
Rusts are an economically important lineage of fungi because some rusts are commercially significant plant pathogens. Black Rust of Cereals is a well-studied organism that can be especially problematic for wheat farmers. Coffee Rust is causing major problems for coffee growers in Central and South America. Cedar-Apple Rust is a significant but not worrying disease of apples.