New paper: Unearthing diversity in fungal dark matter

To be born an orchid is a most unlikely thing. First your parents must be pollinated, which is difficult. Orchids are both rare, and rarely pollinated due to the bizarre and dishonest means by which they go about attracting pollinators. Added to that, orchids often rely on a single species of pollinator to do the job.

Let’s say, however, that your orchid parents do manage to achieve fertilization. Your orchid mother will produce many thousands of tiny dust-like seed, which will be jettisoned into the wind. Unlike most seeds, you have no maternal energy investment to power your germination and first days as a seedling. Instead, you must rely on blind luck to land you within reaching distance of a strand of soil fungus. This fungus is the wet nurse to bring you into the world, invading the seed coat and hooking the young orchid up to a network of fungal strands that pervade the soil. Tapping into this network provides you with the first sips of carbohydrate and nutrient you need in order to build your first green leaf and begin to stand on your own roots. But it is not enough to land near any fungus. Many orchid species require fungal partnership with a specific species of fungus for this to occur at all. Multiplied together, it is a wonder that orchids ever overcome these odds to propagate themselves into the next generation.

The southwest of Western Australia is rightly famous as a global biodiversity hotspot. The area is particularly rich in orchids, and the spider orchids (Caladenia) are some of the most impressive and diverse of the region’s main orchid groups. In 1967, University of Adelaide researcher John Warcup discovered in association with Caladenia a new genus of fungi. Today those fungi are called Serendipita, and although we have known of them for around 60 years, there have been less than a handful of species discovered and described.

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The spider orchid Caladenia arenicola was one of those sampled in the study

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White spider orchid (Caladenia splendens)

Ubiquitous yet invisible

Although related to mushrooms, Serendipita fungi have not been observed producing the conspicuous spore-bearing fruit bodies we usually use to find and identify them. This makes them largely invisible, and I have therefore never observed them in the wild. Despite that, recent research using DNA sequencing has found them to be absolutely everywhere. Inside all kinds of plants, outside all kinds of plants, and distributed from the equator to Antarctica. It is clear then that there must be a hidden biodiversity of these species siting, waiting to be discovered.

My study took a wide sample of southwest WA spider orchid samples and assayed them for the presence of Serendipita fungi. We then sequenced the DNA of all the fungi we found, and used a new analytical technique for dividing that DNA sequence diversity into units that are probably species. This is currently the only way to sensibly identify Serendipita fungi, as they all look completely alike and do not produce spores in the lab.

We found a total of eight species of Serendipita fungi, including the original species discovered by Warcup back in the 60s. These came from a total of 18 species of orchid. At some sites where we sampled multiple orchid species, we found six species of Serendipita, meaning that the fungi were as diverse as the orchids!

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Lying just below the soil horizon, that swollen, yellow stem bit is called the “collar”, and its where all spider orchids keep their fungus.

Untapped agricultural potential?

Although we have chosen to study these Serendipita in association with orchids, their wide host association has got other researchers interested in their role in plant health and application to agriculture. For example, Warcup’s species and one other have been used in experiments (and patent applications) showing inoculation with Serendipita results in profound benefits for the host plant, including:

  • Increased plant weight in maize, poplar, parsley, tobacco, barley, wheat, switchgrass and Arabidopsis
  • Enhanced grain yield in barley
  • Accelerated plant development in barley
  • Greater seed set, increased growth and faster flowering time in tobacco
  • Increased wheat yield in poor soils
  • Improved nutrient uptake in chickpea and lentil
  • Improved salinity tolerance in barley
  • Enhanced protection against root and stem pathogens in barley
  • Improved resistance to stem pathogens in tomato
  • Stronger defense response against mildew leaf pathogen in barley
  • Increased essential oil content in fennel and thyme
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Figure 7 from Ray and Craven (2016): Root growth in winter wheat in Serendipita vermifera inoculated plants (left) versus control (right)

These proven benefits make Serendipita a potentially powerful tool to enhance plant productivity and stress tolerance in crops. Furthermore, application of Serendipita fungi could be an organic alternative permitting growers to lower the application of unsustainable and ecologically harmful synthetic fertilizers. Our knowledge of plant-Serendipita associations in the wild suggests that these relationships are more prevalent in nutrient poor soils such as those in southwest WA. They are probably one factor that allows our plant diversity to thrive in such weathered, poor soils. This means that species of fungi that have evolved with the nutrient poor soils (like those discovered in this paper) might be untapped tools to enhance agriculture taking place in those very same soils.

 

(Erratum: This story was edited to replace the figure attributed to Ray and Craven (2016). The first image I used was one showing Arabidopsis capability for mycorrhizal association. Arabidopsis is typically thought to be a non-mycorrhizal plant, which is why this is interesting. The image however showed slower growth in the mycorrhizal treatment. A related Serendipita has been shown to enhance root growth in Arabidopsis however. I have now updated the post with a more appropriate image of root growth gains in wheat. Thanks to Pawel Waryszak (@PWaryszak) for pointing this out.)

 

My study:

Whitehead, M. R., Catullo, R. A., Ruibal, M., Dixon, K. W., Peakall, R., & Linde, C. C. (2017). Evaluating multilocus Bayesian species delimitation for discovery of cryptic mycorrhizal diversity. Fungal Ecology, 26, 74-84.

Further reading:

Weiß, M., Sýkorová, Z., Garnica, S., Riess, K., Martos, F., Krause, C., … & Redecker, D. (2011). Sebacinales everywhere: previously overlooked ubiquitous fungal endophytes. Plos one, 6(2), e16793.

Weiß, M., Waller, F., Zuccaro, A., & Selosse, M. A. (2016). Sebacinales–one thousand and one interactions with land plants. New Phytologist, 211(1), 20-40.

Ray, P., & Craven, K. D. (2016). Sebacinavermifera: a unique root symbiont with vast agronomic potential. World Journal of Microbiology and Biotechnology, 32(1), 16.

Bokati, D., & Craven, K. D. (2016). The cryptic Sebacinales: An obscure but ubiquitous group of root symbionts comes to light. Fungal Ecology, 22, 115-119.

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Australia’s sexual swindlers.

Seduction. Pollination. Deception.

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I recently wrote an article for Wildlife Australia about Australian sexually deceptive orchids, their evolutionary biology, and historical and current research about them. You can download and read the article here: PDF. Thanks to Carol Booth for her collaboration and editorial guidance.

The latest of Australia’s sexually deceptive orchids that I have seen (below) are Caleana major, the Flying Duck orchid (left), and a spider orchid Caladenia clavigera (right). Both were photographed last week in Brisbane Ranges NP, Victoria.

Flowering this year is one of the best seasons of recent times both east and west of the country. So if you’re in Australia, don’t miss the chance to get out bush and enjoy it.

Sex, lies and pollination. Australia’s remarkable sexual swindlers.

Article reposted from original publication with The Territories.

Rather than luring its pollinator with the promise of food this flower uses an equally, if not more, powerful motivator: sex.

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In shades of dusky green and claret red, the bird orchid’s subdued palette hints at its alternative lifestyle. The usual strategy for flowers attempting to catch the compound eye of a passing insect is to advertise proudly. Petals are used as panels for saturated colour, assembled en masse into conspicuous aggregate displays exuding exotic scents. In this way, nectar-filled flowers loudly broadcast the promise of their reward to entice would be pollinators into servicing them.

 

A deviant among flowering plants, the bird orchid eschews these typical hallmarks of floral advertisement. Crouched modestly on the forest floors of eastern Australia, its stature belies its status as one of the supreme specialists amongst the world’s flowering plants. Like those other showy flowers, the bird orchid needs the service of a pollinator from time to time, however unlike most other flowers, it attracts its pollinator without the payment of any reward. The orchid flower in fact completely lacks nectar.

 

Rather than luring its pollinator with the promise of food this flower uses an equally, if not more, powerful motivator: sex. Undetectable to human senses, the orchid’s advertisement is a precise chemical mimicry of a female wasp’s sex pheromone. This is targeted marketing at its finest, as the use of a signature sex pheromone ensures that the orchid attracts only males of a specific species of wasp.

 

Skimming by on wide zig-zagging flights, the wasps are interminably attracted when the ruse takes hold. They alight onto the flower with fervor, probing and hunting for the mate that their senses scream must be there. Bucking back into the column of the flower (the reproductive parts of an orchid flower are fused in this special structure), they make contact with the anthers and a large packet of pollen is deposited on them. The wasp disengages eventually and leaves, but soon, elsewhere, he will catch on the breeze the smell of a mate, and if fooled again, fulfill his role as duped courier for an orchid’s reproductive ends.

 

Called “sexual deception”, this mode of pollination was noticed by Darwin and his contemporaries in an age in which Europe’s natural sciences were in full bloom. It was a naturalist in Blackburn, Victoria however, who was first to discover the phenomenon outside Europe. In 1927, Edith Coleman had turned her great capacity for observation of the natural world to a peculiar native orchid. Resembling more flesh than flower, Cryptostylis, known also as “tongue-orchids” had caught her attention for its magnetic allure to a specific kind of wasp. Through her observations, Coleman was able to discern that male wasps were being attracted to the flower in order to copulate with it. An experiment through a window showed scent to be the primary attractant, and Coleman even observed the ejaculate remaining after having been visited by clearly convinced wasps. She wrote up her notes in a series of papers for the Victorian Naturalist and Transactions of the Royal Society for Entomology, which made quite a splash with the best of botany at the time.

 

We now know this was the tip of the iceberg. Australia is not only home to tongue orchids, but hosts a diverse array of other sexually deceptive orchids including the spider orchids, elbow orchids, hammer orchids, dragon orchids, greenhoods, duck orchids, hare orchids, beard orchids, bird orchids, and the list goes on. Harbouring over 50% of the world’s known examples of sexually deceptive pollination, Australia is certainly the world’s hotspot for this unusual phenomenon. Remarkably, we have several hundred species that employ this unique brand of pollinator attraction, and what is more remarkable, the evidence points to at least six different independent evolutionary occurrences in the Australian orchid family tree. To our eyes, sexual deception seems like a freaky, unlikely strategy and its repeated independent incidence through Australia’s evolutionary history is therefore a startling paradox.

 

Although the reliance on a single species of pollinator for pollination seems precarious, studies have demonstrated that sexual deception comes with the advantage of promoting healthy breeding for our native orchids. In nectar-bearing plants, foraging insects will frequently move between flowers on the same plant and between neighbouring plants. Called “optimal foraging”, exhausting local nectar supplies in a patch before putting energy into finding a new buffet makes economic sense for a nectar-feeding insect. Sexual deception however, has been shown to drive pollinators far from the flower after being fooled, so that pollen escapes the local neighbourhood. As a plant, your neighbours are likely to be related to you, thus deception is a way of ensuring offspring quality by avoiding breeding with your relatives.

 

Another factor supporting the profusion of our sexually deceptive species is Australia’s immense diversity of insects to fool. Although there are examples of gnat and ant sexual deception systems, wasps are the most commonly targeted pollinator for our orchids. Incredibly, we are only now beginning to uncover the immense hidden diversity of Australian wasps. For example, a recent study in a small patch of bush near Margaret River uncovered 28 species of wasps, most of which were previously unknown to science. With each of these species most likely having their own private sex-pheromone cocktail, there is seemingly a kaleidoscope of chemical communication channels available for different orchids to exploit.

 

Despite our deepening understanding of the natural history of sexual deception, its repeated occurrence in Australia remains a true puzzle.

 

Try the Atlas of Living Australia’s region search to discover which orchids (Plant family: Orchidaceae) live near you. [Link: http://biocache.ala.org.au/explore/your-area%5D

New article: The Territories

The Territories is Heath Killen’s new project. The site blends stories of Australia’s natural and cultural history under a unique aesthetic. I encourage you to check it out.

I was happy to make a recent contribution to The Territories, a story and photo gallery about Australia’s abundance of deceptive orchids:

“Sex, Lies and Pollination”

Rather than luring its pollinator with the promise of food this flower uses an equally, if not more, powerful motivator: sex. Undetectable to human senses, the orchid’s advertisement is a precise chemical mimicry of a female wasp’s sex pheromone. This is targeted marketing at its finest, as the use of a signature sex pheromone ensures that the orchid attracts only males of a specific species of wasp.

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