Natural genetic variation and incipient speciation (Weigel)

A key question in biology is how organisms adapt to their environment, which eventually leads to the invention of new structures or organs. Many developmental biologists are trying to answer this question by comparing complex structures between distantly related taxa. The difficulties inherent in such an approach were already apparent to Darwin: “To suppose that the eye with all its inimitable contrivances … could have been formed by natural selection, seems, I freely confess, absurd to the highest degree.” An alternative to the study of macroevolutionary events is to investigate variation that occurs within a species or between sister species that can still interbreed.

One of the models that is used in the department to address such questions is phenotypic variation among different strains of Arabidopsis thaliana. The geographical distribution of A. thaliana includes much of the Northern hemisphere, and plants can be found in very different habitats. We have, for example, documented extensive variation in the time to flowering, and have been using forward genetics to identify the responsible loci (e.g., Balasubramanian et al., 2006). We have also been looking at other traits, and in the course of these studies, we discovered the first example of a naturally occurring genetic defect associated with a triplet repeat expansion outside humans (Sureshkumar et al., Science 2009).

To enable the more rapid discovery of functionally relevant variation, we conducted a few years ago a collaboration with Perlegen Sciences to discover a large fraction of common SNPs in 19 wild strains of Arabidopsis thaliana, using array-based whole-genome variation scans (Clark et al., 2007). This work was the basis for the development of a 250k SNP chip. This chip is currently being used by our collaborators to type hundreds of strains, which sets the stage for genome-wide association studies in A. thaliana.

As a next step, we have embarked on more extensive genome sequencing using Illumina's Solexa technology. The lab is a leader in the use of short read sequencing, and we have recently released the SHORE analysis tool for the analysis of such data (Ossowski et al., 2008). We have initiated a 1001 Genomes Project for A. thaliana; see the project website for more information.

Finally, we have discovered multiple cases of gene-flow barriers between wild strains of A. thaliana. Fertilization, hybrid zygote formation and germination of F1 plants are normal at either 16°C or 23°C. At 23°C, F1 hybrid seedlings continue to develop normally, but at 16°C they progressively suffer severe growth defects and are infertile. Our results show that this is caused by dominant interaction of gene products from two unlinked loci, with each parent contributing one incompatible allele at one of the loci. This conforms to predictions of the Bateson-Dobzhansky-Muller model for evolution of post-zygotic isolation. The underlying mechanism is autoimmunity, in which another genome is mistaken as pathogenic (Bomblies et al., 2007).

Key publications

• Balasubramanian , S., Sureshkumar, S., Agrawal, M., Michael, T. P., Wessinger, C., Maloof, J., Clark, R., Warthmann, N., Chory, J., and Weigel, D. (2006) The PHYTOCHROME C photoreceptor gene mediates natural variation in flowering and growth responses of Arabidopsis thaliana. Nature Genetics 38, 711-715.

• Bomblies, K., Lempe, J., Epple, P., Warthmann, N., Lanz, C., Dangl, J. L., and Weigel, D. (2007) Autoimmune response as a mechanism for a Bateson-Dobzhansky-Muller-type incompatibility syndrome in plants. PLoS Biol. 5, e236.

• Clark, R. M., Schweikert, G., Ossowski, S., Zeller, G., Shinn, P., Rätsch, G., Warthmann, N., Fu, G., Hinds, D., Chen, H.-M., Frazer, K., Toomajian, C., Hu, T. T., Huson, D. H., Schölkopf, B., Nordborg, M., Ecker, J. R., and Weigel, D. (2007) Common sequence polymorphisms shaping genetic diversity in Arabidopsis thaliana. Science 317, 338-342.

• Ossowski, S., Schneeberger, K., Clark, R. M., Lanz, C., and Weigel, D. (2008) Sequencing of natural strains of Arabidopsis thaliana with short reads. Genome Res. 18, 2024-2033.
• Sureshkumar, S., Todesco, M., Schneeberger, K., Harilal, R., Balasubramanian, S., and Weigel, D. (2009) A genetic defect caused by a triplet repeat expansion in Arabidopsis thaliana. Science 323, 1060-1063.

Personnel

Dr. Detlef Weigel weigel@weigelworld.org

Director

Helena Boldt

Ph.D. student

Dr. Jun Cao

Postdoctoral fellow

Dr. Eunyoung Chae

Postdoctoral fellow

Dr. Yalong Guo

Postdoctoral fellow

Jörg Hagmann

Ph.D. student

Dr. Sang-tae Kim

Postdoctoral fellow

Dr. Yasushi Kobayashi

Postdoctoral fellow

Dr. Roosa Laitinen

Postdoctoral fellow

Stephan Ossowski

Ph.D. student (also Small RNA group)

Felix Ott

Ph.D. student

Dr. Patrice Salome

Postdoctoral fellow

Dr. Lisa Smith

Postdoctoral fellow (also Small RNA group)

Korbinian Schneeberger

Ph.D. student

Marco Todesco

Ph.D. student (also Small RNA group)

Norman Warthmann

Ph.D. student

Georg Zeller

Ph.D. student (with B. Schölkopf, MPI for Biological Cybernetics, and G. Rätsch, FML) 

Collaborators

Dr. Justin Borevitz

University of Chicago, US

Dr. Joanne Chory

Salk Institute, California, US

Dr. Joe Ecker

Salk Institute, California, US

Dr. Daniel Huson

University Tübingen

Dr. Magnus Nordborg

University of South California, US

Dr. Gunnar Rätsch

Friedrich Miescher Laboratory, Tübingen

Dr. Bernhard Schölkopf

Max Planck Institute for Biological Cybernetics, Tübingen