A3
Evolution and Ecology

Domestication-driven metaorganism evolution of wheat

Plants are colonized by a wide diversity of microbes including both eukaryotic and prokaryotic species. Accumulating evidence shows that the plant-associated microbiota plays a role in plant adaptation to various environmental conditions and disease resistance. Given future demands to secure increased food production, there is an urgent need to develop sustainable crop production strategies, and it is therefore essential to understand the role of plant-associated microbiota in plant health.

Here we aim to study microbiota function and interactions of fungal and bacterial species associated with domesticated and wild wheat, Triticum spp. We hypothesize that plant domestication, entailing strong direction selection and a modification of the plant environment, has altered the ability of plants to assemble and sustain microbial communities.

Our research combines expertise on plant domestication and its evolutionary consequences on plant-associated fungi (A3.1, PI Stukenbrock) with expertise on bacterial evolutionary genomics (A3.2, PI Dagan). Our research addresses evolutionary and ecological aspects of wheat-microbiome interactions.

In the A3.1 subproject we study the microbiome resilience in healthy and diseased plants. In resistant wheat, pathogen infection confers the production of antimicrobial compounds that are tolerated by resilient microbes. Our objectives in A3.1 are to identify and characterize microbial species including fungi and bacteria that are resilient to perturbation by a fungal foliar pathogen, Zymoseptoria tritici.
In the second phase, we will further investigate microbe-plant interactions during disease and immune responses with the specific aims to
1) identify adaptations of resilient microbes using experimental and computational approaches, and
2) elucidate the functional importance of vertically transmitted seed-borne microbiota as well as microbes that are resilient to abiotic stress responses in plant tissues.
The research will specifically focus on fungal partners of the wheat microbiome, and will compare the diversity and function of resilient microbes in wild and domesticated wheat species.

In the A3.2 subproject we study bacterial adaptation to colonization of the wheat habitat, in order to elucidate main stages in the life-cycle of seed-borne bacteria along developmental stages of the wheat host. The research in A3.2 is focused on one member of the wheat microbiota – Pantoea agglomerans. This enterobacterium is described in the literature as growth promoting and with anti-fungal activity. The first funding period was used for the establishment of a system for planned experiments on bacterial colonization dynamics within the wheat root. Using our system we estimated the root carrying capacity and examined priority effects during the root colonization.
In the second funding phase, the objectives of A3.2 are to:
1) test the function of putative wheat-associated ‘lifestyle’ genes;
2) pinpoint specific genetic adaptations in the evolution of a wheat-associated lifestyle using an experimental evolution approach;
3) study seed colonization dynamics upon flowering; and
4) examine possible direct interactions of Pantoea and fungal pathogens within the host (collaboration with A3.1, Stukenbrock).
Our results are expected to elucidate microbial traits that are essential for vertically transmitted bacteria in the wheat microbiome.

Overall, the A3 project will help to identify adaptations of bacteria and fungi to plant symbiosis. It will specifically assess the consequences of plant domestication and resulting changes in the microbiota. It will be one of the first projects to characterize resilience of the plant microbiome upon disease-induced disturbance. It will similarly be one of the first to dissect the evolution and genetic mechanisms of plant colonization by environmental bacteria.

A3
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Related Publications

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2020
A3

Seed-derived microbial colonization of wild emmer and domesticated bread wheat (Triticum dicoccoides and T. aestivum) seedlings shows pronounced differences in overall diversity and composition

Özkurt E, Hassani MA, Sesiz U, Künzel S, Dagan T, Özkan H, H. Stukenbrock E (2020) mBio. 11(6): e02637-20. doi: 10.1128/mBio.02637-20

2020
A3

Ecological assembly processes of the bacterial and fungal microbiota of wild and domesticated wheat species

Hassani MA, Özkurt E, Franzenburg S, H Stukenbrock E (2020) Phytobiomes Journal. 4(3):217-224. doi: 10.1094/PBIOMES-01-20-0001-SC
2020
A2
A3

A fungal pathogen induces systemic susceptibility and systemic shifts in wheat metabolome and microbiome composition

Seybold H, Demetrowitsch TJ, Hassani M A, Szymczak S, Reim E, Haueisen J, Lübbers L, Rühlemann M, Franke A, Schwarz k, H. Stukenbrock E (2020) Nature Communications. 11(1):1910. doi: 10.1038/s41467-020-15633-x

2019
A3
A4
B2
C1
C2
INF

Advancing our functional understanding of host–microbiota interactions: a need for new types of studies

He J, Lange J, Marinos G, Bathia J, Harris D, Soluch R, Vaibhvi V, Deines P, Hassani MA, Wagner K-S, Zapien‐Campos R, Jaspers C, Sommer F (2019) BioEssays, 1900211 (1-5). doi: 10.1002/bies.201900211

 

2019
A1
A2
A3
B1
B2
C1
C2
INF
Z3

Comparative analysis of amplicon and metagenomic sequencing methods reveals key features in the evolution of animal metaorganisms

Rausch P, Rühlemann M, Hermes BM, Doms S, Dagan T, Dierking K, Domin H, Fraune S, von Frieling J, Hentschel U, Heinsen F-A, Höppner M, Jahn MT, Jaspers C, Kissoyan KAB, Langfeldt D, Rehman A, Reusch TBH, Roeder T, Schmitz RA, Schulenburg H, Soluch R, Sommer F, Stukenbrock E, Weiland-Bräuer N, Rosenstiel P, Franke A, Bosch T, Baines JF (2019) Microbiome, doi: 10.1186/s40168-019-0743-1

2019
A3

Interactions and coadaptation in plant metaorganisms

Hassani MA, Özkurt E, Seybold H, Dagan T, Stukenbrock EH (2019) Annu Rev Phytopathol. 57: 483-503. doi: 10.1146/annurev-phyto-082718-100008

2019
A3
C3

Currency, Exchange, and Inheritance in the Evolution of Symbiosis

Wein T, Romero Picazo D, Blow F, Woehle C, Jami E, Reusch TBH, Martin WF, Dagan T (2019) Trends in Microbiology doi: 10.1016/j.tim.2019.05.010

2019
A3

Nutzpflanzen nachhaltig vor Krankheiten schützen?

Seybold H, Haueisen J, H Stukenbrock E (2019) BIOspektrum, 25:3, 254-257, doi: 10.1007/s12268-019-1037-7

2018
A3
INF

The genomic rate of adaptation in the fungal wheat pathogen Zymoseptoria tritici

Grandaubert J, Dutheil JY, Stukenbrock EH (2019) Evolution Letters, 

 

2018
A1
A2
A3
A4
B1
B2
C1
C3
Z1
Z2

Metaorganisms in extreme environments: do microbes play a role in organismal adaptation?

Bang C, Dagan T, Deines P, Dubilier N, Duschl W J, Fraune S, Hentschel U, Hirt H, Hülter N, Lachnit T, Picazo D, Galan P L, Pogoreutz C, Rädecker N, Saad M M, Schmitz R A, Schulenburg H, Voolstra C R, Weiland-Bräuer N, Ziegler M, Bosch T C G (2018); Zoology, doi: 10.1016/j.zool.2018.02.004

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