When Plants Parasitise Fungi: myco-heterotrophy

Deep down on the forest floor, sunlight is the scarcest of all resources for plants. They struggle to reach it, lianas and vines climbing up to reach the top and seedlings exploit a gap in the canopy to shoot up and out-compete other plants. But some species have evolved a way to do without sunlight entirely. These plants don't photosynthesise at all. They have no (or very few non-functional) chloroplasts and so lack the green colouration associated with plants.

Instead, they "steal" the carbon they require from fungi, and frequently, indirectly through fungi from other plants. Plants that parasitise fungi are called myco-trophic (myco=fungal, trophic=relating to feeding or nutrition).

The Australian orchid, Rhizanthella gardneri, does not photosynthesise, but
relies on its fungal host for nutrients and carbon.
Photo: Bert Wells, WA Government Recovery Plan.

80% of land plant families are mycorrhizal, having a symbiotic relationship with fungi. Normally, the relationship is mutualistic, with the plant providing the fungus with energy by way of carbon products from photosynthesis, and the fungus supplying the plant with nutrients from the soil such as nitrogen and phosphorous; see (a) in figure below. Species such as the orchid Rhizanthella gardneri, above, "cheat" on this relationship, taking both nutrients and carbon from the host mycorrhizae; see (b). Because many mycorrhizal fungi and their hosts are generalists, sometimes an entire underground network of hyphae from a single fungus connects multiple individual plants of different species. So while the "cheater" parasitises the fungus, its ultimate hosts are the other mutualistic plants in the network, with the fungus acting as a bridge.

Of course, sometimes fungi are pests of plants and take nutrients away from the plant. In (c) we see how that works. Carbon and nutrients are obtained by a pathogenic fungus. But here, the tables are turned. Another plant is parasitising the parasitic fungus. It's an epiparasite: the parasite of a parasite.

So far, the process is relatively straightforward. The parasitic plant is simply exploiting mechanisms that have evolved many times in plant evolution, the elegant, microscopic interaction of plant root cells and fungal hyphae. It's an example of how mutualisms can be unstable, able to switch to parasitism as environmental pressures alter. As with much in biology, it represents the ongoing "arms race" that occurs between species competing for resources.

The fourth mode (d), is a little understood but quite extraordinary relationship: the recruitment by a plant of a fungal host that is normally free-living. In this case, the fungi is saprotrophic: it obtains its nutrients by digesting dead plant material, such as logs.

© Margaret Morgan

Saprotrophic fungi are a common sight in forests and woodlands. Their fruiting bodies (the "mushrooms") are frequently seen growing out of dead logs or leaf litter, but most of the organism is beneath the surface, masses of filamentous hyphae exuding enzymes to break down the organic material. 

Mycena galericulata, a saprotrophic fungus growing on a dead log.
Image (CC) by Dan Molter, Wikimedia.  

The Asian orchid Gastrodia confusa, below, has recently been found to be an example of myco-heterotrophy of a saprotroph, gaining its carbon and nutrients from a Mycena species (Ogura-Tsujita et al. 2009).

Gastrodia confusa, Taiwan. Image © JJ-Merry. Reproduced with permission. 

For many years, it has been assumed that plants in this genus were themselves saprophytes, gaining nutrients directly from decaying organic matter. Indeed, this claim is still made. Molecular studies employing isotopes of carbon and nutrients have now shown that in this species at least, the fungal host is playing an essential role. Gastrodia species are broadly distributed from Africa and India, to South-East Asia, Australia and Pacific islands. Three species are endemic to New South Wales. It would be fascinating to establish whether in these species myco-heterotrophy is also occurring. 

I'd bet good money that it is.

_____________________________________________

This post is adapted from a scientific poster I made for BIOL341 Parasitology, a unit at Macquarie University convened by Dr Michelle Power.

Special thanks to JJ-Merry for permission to include his image of Gastrodia confusa. There are very few images of this species online, and most are his work. His excellent photography of South-East Asian tropical plants can be found here. 

References:

Bidartondo, MI 2005, 'The evolutionary ecology of myco-heterotrophy', New Phytologist, vol. 167, no. 2, pp. 335-52.

Bidartondo, MI, Redecker, D, Hijri, I, Wiemken, A, Bruns, TD, Dominguez, L, Sérsic, A, Leake, JR, Read, DJ 2002, 'Epiparasitic plants specialized on arbuscular mycorrhizal fungi', Nature, vol. 419, no. 6905, pp. 389-92.

Hibbett, DS 2002, 'When good relationships go bad', Nature, vol. 419, no. 6905, p. 345.

Kikuchi, G, Higuchi, M, Yoshimura, H, Morota, T, Suzuki, A 2008, 'In vitro symbiosis between Gastrodia elata Blume (Orchidaceae) and Armillaria Kummer (Tricholomataceae) species isolated from the orchid tuber', Journal of Japanese Botany, vol. 83, no. 2, p. 77.

Leake, JR 2005, 'Plants parasitic on fungi: unearthing the fungi in myco-heterotrophs and debunking the 'saprophytic' plant myth', Mycologist, vol. 19, no. 3, pp. 113-22.

Merckx, V, Bidartondo, MI , Hynson, NA 2009, 'Myco-heterotrophy: when fungi host plants', Annals of botany, vol. 104, no. 7, pp. 1255-61.

Ogura-Tsujita, Y, Gebauer, G, Hashimoto, T, Umata, H, Yukawa, T 2009, 'Evidence for novel and specialized mycorrhizal parasitism: the orchid Gastrodia confusa gains carbon from saprotrophic Mycena', Proceedings of the Royal Society B: Biological Sciences, vol. 276, no. 1657, pp. 761-7.

Adventures in a subtropical rainforest: Part 4

The next of this series of posts on Bulburin National Park will look at some lichen I observed in the rainforest. Bryophytes and lichens have long fascinated me, possibly because once you look closely, they themselves can look like intricate forests of great complexity and beauty. The moisture level of rainforests allows them to flourish there.

This enormous Ficus sp. is covered with an array of lichens of various hues. Lichens are the result of a symbiosis between a fungus and an algae. The algae provides sugars produced by photosynthesis, and in return, the fungi supply the algae with nutrients it extracts from the substrate--in these cases, the bark of the tree.

Next post: Mosses.

The Evolution of Chloroplasts: endosymbiosis and horizontal gene transfer

Chloroplasts are the machines of life, upon which we heterotrophs (organisms which can't create their own food, but instead rely on eating other organisms) depend. Their evolution massively transformed the earth itself, changing the air by dramatically increasing atmospheric oxygen essential for animal life, and providing an energy source.

Micrograph of the cells of a moss species, Plagiomnium.

The round green organelles are chloroplasts. [Source]

All green plants contain chloroplasts, amazing molecular machines which use carbon dioxide, water and photons from sunlight to create sugar and oxygen. The oxygen, so precious to us, is in fact a mere waste product of the reaction. This is the process called photosynthesis:

The story of how plants evolved the ability to perform this chemical feat begins around 3.6 billion years ago. That was before multicellular organisms appeared, and indeed, before eukaryotic cells evolved. (A eukaryotic cell is one with a membrane-bounded nucleus (containing DNA) and various organelles performing specialised functions.) The only living organisms that existed were the prokaryotes, which were much less complex. Prokaryotes have a very different type of DNA structure. Instead of being wrapped around histones in the familiar X-shaped chromosomal form, they are circular. 

One type of prokaryote, cyanobacteria, developed the capacity to use energy from the sun to power its metabolic needs. We see the ancient remains of these early autotrophs today, in the form of stromatolites, layered, fossilised structures like these at Lake Thetis in Western Australia:

                                      [Source]

The ability to use sunlight as a means to make their own food provided photosynthesising prokaryotes with a huge competitive advantage, and they rapidly populated the earth's oceans and lakes. The oxygen they emitted as a waste product led to what's known as the Great Oxidation Event, around 2.4 billion years ago. We can see evidence of this event in rocks from the era. Here is sedimentary rock containing black-banded ironstone, showing the oxidation of iron.

                                    [Source]

About 2.7 billion years ago, another remarkable change was occurring: the evolution of eukaryotic cells. This entailed the process of endosymbiosis [Gk: endon "within", syn "together" and biosis "living".] In endosymbiosis, one organism engulfs another and incorporates it into its own body or cells. It's important to remember that this takes place by invagination: think of pushing your finger into the side of an inflated balloon. Your finger is surrounded by both its own external membrane (your skin) as well as the membrane of the balloon itself. Now imagine (and sorry, the metaphor gets a bit gross at this point!) that your finger falls off and the balloon seals itself up again. Now your finger is inside the balloon, wrapped in a double membrane. That endosymbionts evolved by this process is evidenced by the fact that they have a double membrane, including their own original form that resembles the ancestral bacterial surface. 

Below is a graphic I've put together to show the two crucial stages in the incorporation of photosynthesising prokaryotes into proto-eukaryotic cells, leading to a true eukaryotic cell with both a mitochondrion and a chloroplast. 

Although only green plants possess chloroplasts in their cells, all animal and plant cells have mitochondria, a specialised organelle that oxidises (burns) sugar and provides energy for cells to work.

Note that the DNA of the proteobacterium and the cyanobacterium are circular, compared with the condensed nucleus of the proto-eukaryotic cell. This structure continues down the lineage. Mitochondria and chloroplasts have their own, circular DNA that replicates independently from the DNA in the cell's nucleus. 

The first organisms resulting from the endosymbiosis of cyanobacteria were the green algae, the direct ancestors of all modern plants.

Chloroplasts, able to perform feats well beyond human technology--the efficient splitting of water into hydrogen and oxygen, and the synthesis of sugars from water and carbon dioxide to chemically store energy--are extremely complex structures. A crucial protein in the creation of sugar (during the Calvin Cycle phase of photosynthesis) is Ribulose-1,5-biphosphate carboxylase oxygenase, commonly known as RuBisCO.

Over the course of plant evolution since the original endosymbiotic events, interactions have occurred between genes in the chloroplasts, nucleii and mitochondria. Some genes have disappeared because they are redundant to the organism (both doing the same work in synthesising proteins), and others have physically moved from one organelle to another. The latter process is known as horizontal (or lateral) gene transfer (HGT). Thus, in RuBisCO, some of the protein chains are synthesised by the DNA in the nucleus (nDNA), while others are synthesised by the DNA in the chloroplasts (cDNA). In an astoundingly intricate dance, the cellular machines work together to create what is one of the most important organic molecules on earth. Without it, we and all the other animals on earth wouldn't be here.

Before I finish this rather long post (and if you're still reading, thank you!), I just wanted to mention the mysterious case of the klepto-plast slug.

                                   [Source]

This gorgeous creature is Elysia chlorotica, the Green Sea Slug. And it photosynthesises! Just think about that for a moment. An animal capable of making its own food by using light from the sun. Wouldn't you love to be able to do that? It'd certainly solve the global energy crisis, but perhaps a green hue wouldn't suit everyone's taste.

The Green Sea Slug eats algae, and incorporates the algal chloroplasts into the spaces between its own cells. It differs, however, from the endosymbiosis of plant chloroplasts, because in this case there is no horizontal gene transfer. Once the algae in the slug die, that's it. The slug needs to eat more to keep photosynthesising. It's tempting to think that this might be an evolutionary stage towards a truly autotrophic animal, but apparently too much damage is done to the chloroplasts as they travels through the gut of the slug, and the chloroplasts can no longer replicate themselves. 

Pity. 

This post was adapted from a genetics seminar I recently gave as part of my studies. If you'd like to read more on the topics raised, here's some further reading:

Archibald, J.M. & Keeling, P.J. (2002) Recycled plastids: a 'green revolution' in eukaryotic evolution. Trends Genet 18:11:577-584.

Delwiche, C.F. (1999) Tracing the thread of plastid diversity through the tapestry of life. The American Naturalist 154 Supplement:S165-S177.

Gould, S.B., Waller, R.F. & McFadden (2008) Plastid Evolution. Annu. Rev. Plant Biol. 59:491-517.

Keeling, P.J. & Palmer, J.D. (2008) Horizontal gene transfer in eukaryotic evolution. Nature Reviews: Genetics 9:606-618.

Keeling, P.J. (2009) Role of horizontal gene transfer in the evolution of photosynthetic eukaryotes and their plastids, in Gogarten, M.B. et al. (eds.) Horizontal Gene Transfer: Genomics in Flux, vol. 532: 501-515.

Martin, W. & Schnarrenberger, C. (1997) The evolution of the Calvin cycle from prokaryotic to eukaryotic chromosomes: a case study of functional redundancy in ancient pathways through endosymbiosis. Curr Genet 32:1-18

Smith, A.M. et al.(2010) Plant Biology, Garland Science, New York.

Taiz, L. & Zeiger, E. (2006) Plant Physiology, Sinauer Associates, Sunderland, MA U.S.A.

UPDATE: This post was featured in the May 2010 edition of Blog Carnival of Evolution, this month hosted by the official blog for Springer Verlag's journal, Evolution: Education and Outreach! I feel chuffed. 

FURTHER UPDATE: This post also won the 3 Quarks Daily 2010 Prize in Science "Charmed Quark" award. Which makes me exceeding happy.

Geeky Stuff Round-up: Ecopsychology, The Evil Weed, Aphids, and Photosynthesis.

I confess that one of my pleasures as I read each day's feeds from various science blogs and news sites is to post sundry bits on Facebook. I figure that if I've found it interesting, others will too. A couple of my friends on Facebook have asked me if I provide these links elsewhere. The answer was no, but there seemed no good reason why I shouldn't do exactly that.

So here's the first in a series of occasional posts on what's caught my fancy lately. I hope you find them fascinating too!