Friday, April 21, 2017

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.


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. (free).

Raguso, RA, and Roy, BA. 1998. ‘Floral’ scent production by Puccinia rust fungi that mimic flowers. Molecular Ecology (1998) 7, 1127-1136.

Wednesday, April 12, 2017

Wyoming Native Plant Society helps liberate Plant Names for Creative Re-use

What's your pleasure?

Let’s say you’re writing an article about a plant, or your local flora, or a pioneering botanist. Now … close your eyes and imagine you’re in a huge library dedicated exclusively to biodiversity, with 200,000+ holdings (many rare) scattered across the globe. Next, imagine giving the name of your plant or botanist to a “librarian” who then piles all relevant books, articles, field notes, correspondence, etc., on your desk almost instantaneously! In fact, this library is not imaginary. It’s quite real, though in a virtual kind of way. It’s the Biodiversity Heritage Libraryheadquartered at the Smithsonian Institution in Washington DC, but easily accessible from your office, home, or favorite coffee house.

I discovered the BHL in 2014, while putting together a post about the history of the lanceleaf cottonwood (Populus acuminata). BHL soon became my go-to site for information about botanical exploration of the American West. What I like most is the quick easy access to lots of useful information. Documents that were difficult to access or even unavailable only a few years ago are now just a search and a click away.
Per Axel Rydberg’s Populus acuminata. From American Black Cottonwoods, 1893; BHL.
Edwin James’s Jamesia. From Curtis’s Botanical Magazine, 1875; BHL.
Fossilized palm frond (Powell palmetto perhaps?) collected near Rock Springs, Wyoming. From JS Newberry’s The later extinct floras of North America, 1898; BHL.

The BHL is a consortium of natural history and botanical libraries that are digitizing legacy biodiversity literature, making it easily accessible as part of a global “biodiversity commons.” Much of this literature has been available only in select libraries, mainly in the developed world, making limited access a major obstacle—for example in research, conservation and education. Providing it online free-of-charge is a radical and exciting change. “Free global access to digital literature repatriates information about the earth’s species to all parts of the world.”

Put another way, BHL is making biodiversity literature “freely accessible to a global audience … thereby liberating taxonomic names and bibliographic data associated with the content for creative re-use.” Among the plant names most recently liberated were those in our very own Castilleja, the newsletter of the Wyoming Native Plant Society.
In October 1994, the Wyoming Native Plant Society newsletter was given a name: Castilleja.

It all started last October when the BHL blog featured a post titled A Local Focus: The Native Plant Societies of the US. When I read that native plant society newsletters were being added to the collection, I contacted Project Investigator Susan Fraser at The New York Botanical Garden, asking if Castilleja were part of the plan. Indeed it was. “We would be thrilled to include Castilleja in the project,” she replied.

Incorporating native plant society newsletters into the BHL is part of Expanding Access to Biodiversity Literature—a two-year project designed to “preserve and provide access to small natural history and botanical collections and publications.” It’s conducted by the New York Botanical Garden in partnership with Harvard University, the Missouri Botanical Garden, and the Smithsonian Institution Libraries.
“We are grateful to the native plant societies who have generously shared their local expertise by making their newsletters available to researchers through BHL. In addition to the biodiversity information they contain, these publications are a wonderful snapshot of the small, dedicated groups of people working all over the U.S. to document and preserve our native plants.” –Patrick Randall, Community Manager, Expanding Access to Biodiversity Literature; Ernst Mayr Library, Harvard University

Before Castilleja issues could be processed, a permissions form had to be signed (the society President took care of this). Fortunately, PDFs were available for all issues; these were transmitted en masse to BHL. Then the techies worked their magic. Now, whenever someone searches BHL for Boechera pusilla or Yermo xanthocephalus, for example, relevant issues of Castilleja appear on the results list. We’ve hit the big time!

The image below shows one result from a BHL search for “yermo xanthocephalus”—the desert yellowhead, endemic to Wyoming. As I scrolled through Castilleja Volume 17 Number 4 (1998), scientific names on each page appeared in the box on the lower left. Note that contents can be printed or downloaded (either the entire work or selected pages). I’ve used the latter option many times. Usually the pages arrive well within the hour, whether from the newsletter of a neighboring native plant society, or from a rare old book in a library thousands of miles away.

How did BHL manage to find yermo among the 51,749,439 pages held in the collection? It was magic!!! No, not really … sorry. But it’s just as cool as magic. As texts are processed, scientific names are extracted from each page using Global Names Recognition and Discovery (GNRD), a taxonomic name recognition algorithm. GNRD provides an open and global-names-based infrastructure to index, organize and manage biodiversity data. Like BHL, GNRD aims for easy public access, with the goal of spurring widespread and innovative use of biodiversity data. A noble goal indeed!

So if you’re in need of biodiversity literature, especially if it’s old or rare or otherwise difficult to access, pay a visit to the BHL. Adventure and discovery start here. And if you’re looking for a good time, browse the always-interesting BHL blog (warning: you'd better have plenty of time on your hands).
Above, Coffea arabica was the first coffee species to be cultivated, and still accounts for most of world's coffee production (from Köhler's Medizinal-Pflanzen; see The Berry that Changed the World). Below, Miss C.H. Lippincott Flower Seeds catalog cover (1900), from Leading Ladies in the World of Seeds (you can view over 11,000 seed and nursery catalogs in the BHL collection!).