Dating the Brassicaceae specialist Thecaphora thlaspeos

Plants are colonized and interact with a huge variety of microorganisms that form the plant microbiome. This multi-organismal playground comprises opportunistic, plant-beneficial and pathogenic microbes that co-exist and interact with each other and their host. Understanding the molecular and evolutionary complexity of such interaction networks under changing abiotic conditions is a challenging task. Progress in that direction will bring us closer to stable applications of microbial communities for crop improvement. To date, suitable model systems are scarce. Therefore at the beginning of CEPLAS, we announced for suitable candidates and got a promising response from the smut fungus Thecaphora thlaspeos.

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Researchers working in plant-microbiome interactions with a profound interest in the molecular and evolutionary complexity of inter-species cross-talk, plant nutrition and crop protection are looking for an easy-going fungus that is genetically tractable and infects model plants to build a long-term relationship in the lab.

Response from Thecaphora thlaspeos:

Dear researchers,
I am a smut fungus adapted to Brassicaceae hosts and infect at least 15 host species including Arabis hirsuta, the perennial model plants Arabis alpina and Arabidopsis lyrata, and also Cardamine spps. (Vanky et al., 2008), a plant genus that is used to study the evolution of plant development (Hay et al., 2014). In my hosts I establish a long-lived systemic infection along the vasculature of both, roots and shoots and I’m able to overwinter in my perennial hosts. At the end of my sexual cycle I produce single spores in the siliques of my hosts partially or completely replacing seeds (Vanky et al., 2008). Since I am related to the well-established model pathogen of grasses Ustilago maydis, you will be able to take advantage of the advanced genetic tools and methods of smut fungi and apply them to Brassicaceae model systems.
I would love to join your lab and have a good researcher taking care of me.

Bests, Thecaphora thlaspeos

Dear Thecaphora thlaspeos,
We think you could be a perfect synthetic symbiont to study host-microbe and microbe-microbe interactions. If you agree, we would like to meet you in the field, collect spores and then bring you to the lab to observe how you infect plants. Your relative U. maydis is already with us in the lab. So, using our experience from U. maydis we would like to cultivate your yeast-like form, sequence and genetically manipulate your genome.
If we get on well, there are many more things we could do in the future. Let us know where to meet!
Best, The researcher team

Dear researchers,
Meeting in the field is a good idea. There are several places in Germany where you will find me on Arabis hirsuta. Feel free to sequence my genome. There might be interesting surprises. I guess you need to know a few more things about me (Frantzeskakis et al., 2017):

  • I can infect roots and shoots, and inside the plant I grow to the vasculature to spread throughout the whole plant. You will only see me in the siliques as spores.
  • I am economic and only germinate when I sense that there are germinating plant seeds around. They have such nice signals in roots and leaves.
  • After germination, I do not grow in a yeast form, but you can grow me as filamentous cultures.
  • My mating types are similar to U. maydis and I can mate, but I am very private about these things.
  • In the lab, you can make me enter your favourite model plant Arabidopsis thaliana.

I hope I made you curious enough to realize my potential!
Bests, T. thlaspeos

Dear T. thlaspeos,
You are quite a smut fungus! Your genome tells me you are very similar to U. maydis, but then you behave so differently! Now we are really curious to compare your infection biology to other smuts!
And please let us know

  • How do you interact with the plant microbiome?
  • How can you grow in the plant as an endophyte for such a long time? You need nutrients. How come the plant does not miss them? Do you affect photosynthesis as U. maydis does in maize?
  • And what about your other relatives the potato smut T. solani (Andrade et al., 2004) and the peanut smut T. frezii (Conforto et al., 2013)? Can you tell us how to develop effective defence strategies for crop protection?

We feel this is the beginning of a long-lasting research relationship!
Let’s tell everybody!
Your researcher team

Contributed by Dr. Ronny Kellner (Max Planck Institute for Plant Breeding Research
) and Dr. Vera Göhre (Institute of Microbiology, Heinrich-Heine-Universität Düsseldorf
)
Figure by Jörn Aschenbroich (Institute of Microbiology, Heinrich-Heine-Universität Düsseldorf
)

Planter’s Punch

Under the heading Planter’s Punch we present each month one special aspect of the CEPLAS research programme. All contributions are prepared by our young researchers.

Further Reading

Andrade, O., Munoz, G., Galdames, R., Duran, P., and Honorato, R. 2004. Characterization, In Vitro Culture, and Molecular Analysis of Thecaphora solani, the Causal Agent of Potato Smut. Phytopathology 94:875-882. [Abstract]

Conforto, C., Cazón, I., Fernández, F.D., Marinelli, A., Oddino, C., and Rago, A.M. 2013. Molecular sequence data of Thecaphora frezii affecting peanut crops in Argentina. Eur J Plant Pathol 137:663-666. [Abstract]

Frantzeskakis, L., Courville, K.J., Pluecker, L., Kellner, R., Kruse, J., Brachmann, A., Feldbrügge, M., and Göhre, V. 2017. The plant-dependent life cycle of Thecaphora thlaspeos: a smut fungus adapted to Brassicaceae. Molecular Plant-Microbe Interactions. [Abstract]

Hay, A.S., Pieper, B., Cooke, E., Mandáková, T., Cartolano, M., Tattersall, A.D., Ioio, R.D., McGowan, S.J., Barkoulas, M., Galinha, C., Rast, M.I., Hofhuis, H., Then, C., Plieske, J., Ganal, M., Mott, R., Martinez-Garcia, J.F., Carine, M.A., Scotland, R.W., Gan, X., Filatov, D.A., Lysak, M.A., and Tsiantis, M. 2014. Cardamine hirsuta: A versatile genetic system for comparative studies. Plant J 78:1-15. [Abstract]

Vanky, K., Lutz, M., and Bauer, R. 2008. About the genus Thecaphora (Glomosporiaceae) and its new synonyms. Mycol Prog 7:31-39. [Abstract]

Heinrich Heine University
University of Cologne
Max Planck Institute for Plant Breeding Research
Forschungszentrum Jülich