The genes in one organism’s cells, then, can have extended phenotypic influence on the living body of another organism.
—Dawkins, Richard. 1999. The Extended Phenotype: The Long Reach of the Gene. Oxford University Press.
note to self: get a better header image
As a young child I spent many of my holidays in Groomsport, a small coastal town on the northern coast of Down. My memory is of the gently rocky coastline that fringes much of the Ards Peninsula, encrusted with Spring Squill Tractema verna, Sea Campion Silene uniflora, and Lesser Bird's-foot Trefoil Lotus corniculatus. These coastal grasslands defined my early experiences of botany and Spring Squill is one of those plants that makes a place feel like home.
One year, I remember the Spring Squill looked strange. It was dirty with brown powder that covered the petals. Every plant I looked at that year had this strange powder in every flower. I think I remember somehow knowing that the word for this was “smut”; it must have been mentioned in one of my guides to fungi, which I was into at the time. This early encounter with Antherospora tractemae, and another smut in the genus Microbotryum on Sea Campion, are my earliest memories of plant pathogens, when I was around eight or nine. Unbeknownst to be, around the same time, it was described as a new species to science, having been previous considered part of A. vaillantii1. I never saw A. tractemae again at Groomsport, or at all until I started visiting Killard Point National Nature Reserve a few years ago.
“Classic” smut fungi like Antherospora and Microbotryum alter their hosts' flowers so much as to be unavoidably noticeable. They aren't the only pathogens to infect flowers though. It is a strategy that works: by focusing spore production on a part of the plant that is visited by pollinating animals, they take advantage of the existing adaptations of the host plant to spread its own pollen. A given spore that is picked up by a pollinator is more likely to meet another host plant than if it was spread by the wind. This means floricolous pathogens can use their resources more efficiently.
Some floricolous downy mildews don't just produce conidiophores on their host's flowers. They change the structure of the flower fundamentally. Anecdotally,
The smut fungi includes a large number that infect grasses and sedges. These plants are not pollinated by animals, but by the wind. These smut fungi do not receive a big advantage in their dispersal by producing their spores in the plant's flowers, other than that the flowers of these plants are the parts that are highest in the air and most exposed to the wind.
One grass smut that has a particular importance to human culture is the Corn Smut Mycosarcoma maydis. It infects the female spikes of Maize Zea mays, causing the kernels to swell into large bluish grey tumours. These mature and release blackish brown spores, which spread on the wind. The immature infected kernels are eaten as a delicacy in Mexico, where it is known as huitlacoche, a name that comes from Nāhuatl.
A few rust species go beyond just hijacking their hostplant's flowers. They have reinvented the flower from first principles, transforming the shoot of their hosts into a pseudoflower, a yellow landing pad for pollinating insects. They produce sugary liquid to attract insects, and this liquid contains haploid male gametes (reproductive cells) which are then spread to other pseudoflowers by the insects2,3. These male gametes fuse with female gametes in the other pseudoflower, forming a diploid cell which goes on to produce the next stage in the rust life cycle. In this way, pollinators facilitate the recombination of rust DNA, just as they facilitate the recombination of plant DNA by spreading pollen between plants.
Pseudoflowers have evolved at least twice in rusts, in the American Puccinia monoica on Brassicaceae and the European Uromyces pisi agg. on Euphorbiaceae. These are just two small clades in the huge group that is the rust fungi, which have some of the most complex life cycles of any organism on Earth. In the next chapter, we'll look at these life cycles in all their intricacy.
