Pseudoflowers—Trick or Treat?

A flower-less rockcress.

Every spring some of our rockcresses forego flowering, and instead grow terminal clusters of fragrant yellow leaves dotted with sugary goo. But why? Generally plants produce color, fragrance and nectar to lure pollinators, which carry male gametes (pollen) off to where female gametes (ovules) await fertilization. But the yellow-leaved rockcresses have no flowers, no pollen, no ovules. And yet these plants are all about sex—fungal sex that is.

Rockcresses (Boechera spp.; formerly Arabis) are members of the mustard family. Most are perennials, with a few biennials. They usually produce white to pale pink or purple flowers, but the yellow-leaved versions are common enough to frequently confuse wild-flower enthusiasts.

“Almost every spring, someone brings me a picture or a plant of a strange little flower they’ve never seen before, and can’t key out or even begin to guess the family for.” Irene Shonle

“Strange little flower” (source).

Normal rockcress, and infected rockcress with pseudoflowers (Cano et al. 2013).

The yellowed rockcresses are infected with Puccinia monoica—mustard flower rust. Rust fungi are obligate plant pathogens, and include some of the most destructive agricultural pests (e.g. wheatstem rust, coffee rust). Some have extremely complex life cycles, involving five spore types and multiple host species in a single life cycle! (details here)

The life of the mustard flower rust is simpler, requiring three spore types and one or two hosts (full story here). If a wind-blown basidospore (which has a single haploid nucleus) is lucky enough to land on a suitable host plant, it germinates. Hyphae grow into the stem, tapping into the plant’s nutrient supply. But living happily ever after on a rockcress is not part of the rust's plan. Sex is its goal. Mustard flower rust is heterothallic, meaning opposite mating types are produced by separate “individuals” (rust infections) on separate rockcress plants. Opposite mating types need to get together somehow.

Puccinia monoica solves this problem by creating pseudoflowers. Like real flowers, they attract pollinators (mostly insects) by way of fragrance and the promise of sweet reward. How impressive that a simple little fungus has evolved to to grow such features! … except that’s not what happens, at least not directly. The real story is even more amazing. The plant grows these novel features … under the direction of the rust!

In addition to siphoning off nutrients, the rust reprograms the host plant, somehow changing which genes are expressed when. As a result, the infected rockcress never makes the transition from vegetative growth to flowering. Instead it elongates, grows extra leaves, and produces yellow pigment, fragrant compounds, sugary liquid, and wax. The resulting structure looks, smells and tastes enough like a flower that foraging insects show up, partake of a bit of sugar, and hopefully carry off the spore-like spermatia to receptive hypha on other rockcresses.

Bumps are spermagonia, which contain spores waiting to be dispersed and super-sweet liquid.

Pseudoflowers may mimic other wildflowers, like this nearby sagebrush buttercup (speculation for now).

With today’s molecular analysis techniques and model organisms (Arabidopsis thaliana, the thale cress, is a close relative of rockcresses), it’s possible to delve deeply into pseudoflower biology. In 2013, Liliana Cano and her colleagues looked at developmental changes in rockcresses infected with mustard flower rust. They found that for at least 31 genes, activity was significantly altered (enhanced or reduced), affecting leaf, stem and flower development; metabolism and transport of sugars and lipids; synthesis of volatiles (fragrant compounds); and wax production.

These changes can be interpreted as beneficial to the mustard flower rust. For example, consider wax production. Cano and colleagues suggest that the waxy leaves induced by rust infection serve to reduce water stress. Water-stressed plants often have shorter stems and fewer leaves—not what the rust needs. Perhaps the waxy leaves of infected plants allow taller leafier growth.

Gravelly soil drains rapidly, making for dry habitat. Looks like waxy leaves weren't enough to compensate.

Whatever the mechanisms, by enabling fungal sex, infection clearly benefits the rust. And the rockcress clearly suffers—no flowers, no sex. But what about pollinators? Are they beneficiaries or unsuspecting dupes? Some botanists consider pseudoflowers to be tricksters, luring insects into service with little reward. However in a 1998 paper, Robert Raguso and Bitty Roy pointed out that the super sweet liquid of rockcress pseudoflowers is popular with many kinds of insects, including bees, ants, butterflies and flies. And given how many sugar-oozing spermagonia there are on each yellow leaf, infected rockcresses may actually produce more yummy calories than uninfected plants. If so, then for pollinators, pseudoflowers are not a trick but a treat.

Foraging ant (in a hurry).

Puccinia monoica on Boechera sp. is the latest addition to my iNaturalist project, Plants of the Southern Laramie Mountains (two observations—one for the rust, one for the plant). To identify the rockcress to species, I have to wait until uninfected individuals are in fruit.

I found infected rockcresses scattered through this sagebrush grassland.

It’s still early spring at Blair (8000 feet elevation)—not much flower action.

Sources

Thanks to Elio Schaechter of Small Things Considered who recently blogged about Boechera pseudoflowers, which I’ve long ignored.

Caro, LM, et al. 2013. Major transcriptome reprogramming underlies floral mimicry induced by the rust fungus Puccinia monoica in Boechera stricta. PLoS ONE 8(9): e75293. http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0075293 (free).

Raguso, RA, and Roy, BA. 1998. ‘Floral’ scent production by Puccinia rust fungi that mimic flowers. Molecular Ecology (1998) 7, 1127-1136.
http://onlinelibrary.wiley.com/doi/10.1046/j.1365-294x.1998.00426.x/abstract