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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