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

Of Microfungi, Music, Conservation & More

Remembering Martha Christensen.

In 1982, when I started as a grad student in botany at the University of Wyoming, my familiarity with fungi was limited. I knew of only two kinds: mushrooms and yucky crud (like athlete’s foot). But that’s not why I took Mycology. Few botany courses were offered that would fulfill my grad requirements, so when someone told me Mycology was “a really good class,” I signed up. It was a great choice, one that has benefitted me for 35 years.

By the time the semester ended, we had been immersed in the mind-boggling taxonomy of fungi, and exposed to the many critical roles fungi play in plant growth and ecosystem health. We experienced economic mycology: bread, beer (beer in class didn’t raise eyebrows then), cheese, tempeh and more. Especially intriguing to me was the discovery that soil microfungi in Wyoming basins include tundra species! These are Pleistocene periglacial relics, from times not so long ago (circa 10,000 years) when today’s short-grass prairies were permafrost and tundra.

But the best part of Mycology was the instructor, Dr. Martha Christensen. On the first day of class, we were taken in by her passion for the subject and her sense of humor. It was a semester filled with new knowledge, camaraderie, and lots of fun. I went on to take Martha’s Algae and Bryophytes, and was her teaching assistant for Man, Agriculture and Civilization, a non-majors course. I don't remember exactly what was taught in that course, but I’ve thought of it many times in the 30+ years since, because of one very useful piece of advice. We were frantically preparing for lab while the clock raced towards 1:10, when Martha noted with a smile: “This is just like fixing dinner for lots of guests: get as much done as you can, then quit worrying and enjoy it!”

The next year, when my advisor announced he wouldn't be available for my defense and seminar, Martha agreed to serve as committee chair. I’m not sure why I was so lucky, probably just timing, but it felt like Fortune had kindly intervened.

Those grad student days were the start of a long enjoyable friendship. But then last week Martha shocked everyone by passing away. She was 85, but still so full of enthusiasm and energy, and so busy with life, that death was unimaginable. The days since have been a time of reminiscing and sharing stories.

Martha had a long list of academic achievements. When I read her obituary and a recent tribute by one of her colleagues, I realized how little I knew about her career. That’s because our friendship was based on other mutual interests: outdoor recreation, conservation, and music. Martha’s interests were broad, and though an academic, she found time for them all. Sometimes it seems those days are gone. Is academic pressure now too great? Is there no longer time for the arts, public service, advocacy?

Martha played the viola, as do I. I love her story—told with her characteristic hearty chuckle—about how being a violist helped her land a professorship in the Botany Department. She was sure she was hired partly because several faculty members and their wives were fans of classical music and supporters of the University symphony orchestra—which was in desperate need of a good violist. Martha found herself sitting first chair (in a section of three!) and would play with the UWSO for thirty years. Though she loved classical music, and was especially fond of opera, she was no snob. Martha also played the saw!—entertaining us at departmental Christmas parties.

There was another side to Martha that we appreciated very much … and still do. She was a major advocate for public lands conservation in Wyoming, contributing both time and financial support. This is a tough place to be a conservationist; it’s easy to get burned out. But Martha persisted. That she loved nature and the out-of-doors was always clear. In retirement, she took great pleasure in visiting natural areas in the US and other parts of the world, always exploring, always learning. I looked forward to hearing of her latest adventures in our annual Christmas correspondence, for her contagious enthusiasm never disappeared!

Martha was one of the conservationists profiled in Ahead of their Time; Wyoming Voices for Wilderness.

A memorial service for Dr. Martha Christensen will be held on Saturday afternoon, April 1, 2017, at the Heritage Congregational Church, 3102 Prairie Road in Madison, Wisconsin. Family members will greet her friends at 1:00. A service of remembrance will begin at 2:00.

In September (date to be set), Martha's many colleagues, students and friends will gather in Laramie to celebrate her life. More information will be provided on the University of Wyoming Botany Department website.